Effect of Premature Birth on Psycho-biological Processes of Asults

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CHAPTER ONE

Little is known about the psychobiological processes of adults, at age 23, who

were born prematurely despite the fact that 1 out of every 9 infants is born too early

(Atzil, Hendler & Feldman, 2011; CDC, 2015; Mannisto, Vaarasmaki, Sipola –

Leppanen, Tikanmaki, Matinolli, Pesonen, Raikkonen, Jarvelin, Hovi, & Kajantie,

2015).   Compared to infants born at term, premature infants, face additional obstacles

of immature body systems and more neonatal stress, and are at risk for developmental

delay, and possible parental overprotection patterns (Clarke, Cooper & Creswell,

2013; Grunau, 2013; Kopp & Rethelyi, 2003; Pinquart, 2014).

Developmentally, in the United States, 23 year olds are expected to achieve

independence and form intimate relationships, yet there is limited knowledge about

their emotional intelligence and related psychobiological processes while more is

known about their stress levels, coping strategies, and emotional disorders (Clarke, et

al, 2013; Ingels, Glennie, Lauff, & Wirt, 2012; Pinquart, 2014; Simpson, 2009).

Intrapersonal, interpersonal, adaptability, stress management effectiveness, as well as

general emotional health are all involved in reaching adult developmental milestones

(Granger & Kivlighan, 2003; Simpson, 2009).   These important young adults

milestones require the ability to:  communicate effectively with others, be sensitive to

others, maintain emotional self-control, use both knowledge and experiences to cope,

manage stress, work and assume responsibilities (Arnett, 2013; Di Fabio & Saklofse,

2014; Simpson, 2009).

The abilities required to meet young adult developmental milestones are captured

in definitions of emotional intelligence (EI) and also incorporates the involvement of

the brain’s prefrontal cortex executive functioning which further evolves during this

time period (Kristensen, Parker, Taylor, Keefer, Kloosterman, & Summerfeldt, 2014;

Arnett, 2013; Davis & Humphrey, 2012; Armstrong, Galligan, & Critchley, 2011;

Lishner, Swim, Hong & Vitacco, 2011; Aldao, Nolen-Hoeksema & Schweizer, 2010;

Stuss, 2009; Tarasuik, Ciorciari & Stough, 2009; Ciarrochi, Deane & Anderson,

2000).   The Hypothalamic – Pituitary -Adrenal (HPA) Axis biological response to

stress and prefrontal cortex executive functioning abilities are theorized to be involved

with emotional intelligence (EI), functioning, stress, coping, and emotional health

(Frodl & Stuart, & Pretorius, 2007; Smith & Vale, 2006; Herman, Ostrander, Meuller

& Figueiredo, 2005).

Young adults who were born prematurely carry the consequences of their early

birth.   As infants, their immature physical systems were responding to ongoing

physical pain from neonatal medical procedures, a longer hospitalization and a

multitude of environmental stimuli with unstable and ineffective bodily system

responses (Grunau, 2002).   The foundations for brain growth and functioning and

what will become their usual stress response were being laid at this point in time and

will likely influence lifelong development including meeting young adult milestones.

However, there is a need for research examining the mechanisms of stress and its

relationship with adult emotional health outcome to assure the well being of young

adults and their attainment of developmental milestones (Mannisto, et al., 2015;

Simpson, 2009; Tarasuik, et al., 2009).   There is minimal research into emotional

health and its association with biological processes functioning existing to help in

identifying the precise timing and targets of health promoting interventions.

Theoretical Framework

The Developmental Origins of Health and Disease (DOHaD) theory of HPA

dysregulation postulates that the stress of prematurity and during early life critical

brain growth periods (i.e. formation completes during young adulthood) effects the

HPA Axis structure and functioning (Eiland & McEwen, 2012; Sullivan, Hawes,

Winchester & Miller, 2008; Barker, 2007; Miller, Chen & Zhou, 2007; De Boo &

Harding, 2006; Pujol, Vendrell, Junque, Marti-Vilalta, & Capdevila, 1993).   Stress

responses from the HPA axis are adaptive (allostasis) and if occur frequently,

particularly with prematurely born infants and their underdeveloped systems, will

result in injury or ‘”wear and tear” (allostatic load) on the body (McEwen, 2003 &

2006; McEwen & Seeman, 2006).   If the stress is ongoing or chronic than the “wear

and tear” on the body will result in illness (McEwen, 2003 & 2006 McEwen &

Seeman, 2006).   Cortisol is the primary HPA hormone and it can be measured

non-invasively and reliably in saliva (Helhammer, Wust, & Kudielka 2009;

Turner-Cobb, 2005; Granger & Kivlighan, 2003).   When the body is stressed, the

HPA axis releases higher levels of cortisol resulting in metabolic imbalances

involving blood sugar and insulin, higher blood pressure, faster heart rate, mood

changes, thyroid imbalances and weakened immunological responses (Bruyere, 2009).

A normal salivary cortisol stress reactivity response consists of a peak elevation

of salivary cortisol concentrations 10 minutes after the cessation of the test stressor

with a decrease to pre-stress levels approximately 90 minutes after the start of the test

(Kirschbaum, Pirke & Hellhammer, 1993).   In addition, heart rates peak during the

protocol’s stressful task and then drops to baseline once the stressor stops (Kirschaum,

Pirke, & Hellhammer, 1993).   In a recent study, prematurely born age 6 -10 years olds

were found to have an exaggerated cortisol response when faced with a social stressor

in a reliable laboratory paradigm, and more emotional and memory problems

(Quesada, Tristao, Pratesi & Wolf, 2014).    Biological stress responses (i.e. cortisol)

play a reciprocating role whether the stress is physical or psychological.

Psychological stress (i.e. social evaluation and the perception of uncontrollability in

the situation) activates the cortisol response (HPA Axis), which in turn effects the

physical systems.   Conversely physical stress activation (i.e. pain) of the cortisol

system (HPA Axis) is associated with psychological changes in affective and

cognitive processes (Smith & Vale, 2006; Dickerson & Kemeny, 2004).

This study uses a standardized, widely used and well-researched laboratory test

for inducing moderate psychobiological stress responses called the Trier Social Stress

Test (TSST), (Kudielka, Hellhammer & Kirschaum, 2010; Kirschbaum, Pirke,

Hellhammer, 1993).   In a meta-analysis of 208 laboratory stress studies, the TSST

was found to repeatedly induce changes in the concentration levels of cortisol (both

serum and saliva), as well as other major HPA Axis endocrines, and to significantly

cause an increase in heart rate (Kirschaum, 2010; Kudielka, Hellhammer &

Kirschaum, 2010).   Two key components of the TSST’s protocol are well studied and

known to be needed to induce a reliable and strong activation of the HPA Axis

measured in salivary cortisol.   The components are the psychological stress of the

threat of social evaluation, and the perception of uncontrollability in the situation

(Kirschbaum, 2010; Dickerson & Kemeny, 2004).   Over fifteen years of TSST

research has shown an increase by 50-300% over baseline in endocrine,

immunological and cardiovascular parameters (Kirschbaum, 2010).

Young adults born early with immature body systems may not just simply grow

out of it and catch up to those born full term (URI, 2011).   Subtle, minor and clear

differences in attention, hyperactivity, and emotional and socialization effectiveness

have been found during childhood and adolescence (Healy, 2010).   Guided by the

DOHaD theory, the developmental challenges of independent living at age 23 years

call for greater knowledge about how mechanisms of stress and capacity for response

are seen in former premature infants.   There is minimal research on 23-year-old

outcomes of stress, coping, emotional intelligence, emotional health, stress reactivity

responses and the progression of emotional disorders.   More knowledge about the

relationship of premature birth, the neuroendocrine stress response, self-reported

stress, coping and emotional intelligence will expand our understanding of the well

being of young adults and their attainment of developmental milestones. (Mannisto, et

al., 2015; Simpson, 2009; Tarasuik, et al., 2009).

Purpose

The Developmental Origins of Health and Disease (DOHaD) framework provides

the theoretical perspective for the proposed study.   DOHaD asserts that early prenatal

and neonatal stress seen in HPA axis function affects later health and behavior.   It

offers a mechanism to enable the understanding of salient young adult developmental

performance abilities.  This is a secondary analysis of a well- characterized cohort of

premature infants categorized by neonatal illness into four groups of prematurely born

infants (Appendix A Measurements) and one group of full-term infants (for a total of

5 groups) who were assessed at age 23 years in a research protocol, which included

measures of stress, coping, emotional intelligence, emotional health and

the Trier Social Stress Test.   The purpose of the study is to: 1. Compare the effect of

prematurity on stress, coping, emotional intelligence and emotional health at age 23

years.   2.   Examine the neuroendocrine functioning of the stress response and

the stress recovery period at age 23 years.   3.  Examine emotional health with HPA

Axis stress reactivity responses accommodating for prematurity and gender.   The

knowledge gained from this study can help to inform how neonatal stress of

prematurity effects young adult coping, emotional intelligence, physiological

responses, developmental milestones and emotional health at age 23 years in a sample

at risk for HPA dysfunction.   The results can help to identify who may be at risk, the

role of the neuroendocrine systems as an underlying mechanism, and suggest clinical

interventions to be taken to avoid risk factors and promote future adult health

outcomes (Rice, 2012; Kirschibaum. 2010; Sullivan, 2008).

Aims and Hypotheses

In a sample of young adults at age 23, former premature infants with a wide

variation in diagnoses of neonatal illnesses and a full term group, the aims of the

study, with related hypotheses are:

Aim 1.   Compare the effect of prematurity on stress, coping, emotional

intelligence and emotional health.

Hypothesis 1. Higher self-reported stress scores, higher use of avoidance

coping types, lower emotional intelligence scores and more emotional health

disorders will be found for the adults at age 23 years born prematurely

compared to the term-born adults.

Aim 2.   Compare the salivary cortisol response to social stress between premature

and term-born infants using stress paradigm of the Trier Social Stress Test

(TSST).

Hypothesis 2.   Adults at age 23 who were born prematurely will have a

prolonged stress recovery period of the TSST.

Aim 3. Examine the relationship between effect of emotional health and on the

stress recovery period of the TSST measured in salivary cortisol.

Hypothesis 3.   The stress recovery period for adults at age 23 years with

emotional health problems will be prolonged compared to adults without

emotional health problems when prematurity is controlled.

Summary

This study used a well-characterized, longitudinal sample of preterm and full term

born infants who have been followed from birth in a series of research studies.   The

study used neonatal data and self-report of stress, coping and emotional intelligence,

clinical diagnosis of emotional health, and neuroendocrine function during a social

stress paradigm at age 23 years in a secondary analysis.   The study is congruent with

the original, larger, study using the same theoretical framework and relevant variables

to examine self-reported stress, coping, emotional intelligence and emotional health

with the primary biomarker of HPA axis system, cortisol.   The overall aim of the

study is to examine self-reports of important emerging adult independent function with

neuroendocrine activity in the well-standardized social stress test, the TSST.   The

brain areas most affected by stress are the same areas involved in adapting to stress

and coping effectively (Compas, 2006).   Researching these integrated

psychobiological processes through multiple analyses will lead to further

understanding of how stress effects young adults emotional development (Compas,

2006).   This study has the potential to add relevant knowledge about salient

developmental characteristics, elements and competencies.   The following chapter (2)

provides the scientific literature in support of this study.   These include the DOHaD

theoretical framework and developmental milestones at age 23 years old of the

emerging adult who was prematurely born.   The use of secondary longitudinal data

for analysis will also be addressed.

CHAPTER TWO

Theoretical Background and Related Literature

In this chapter, selected theoretical perspectives for this study are delineated,

specifically the Developmental Origins of Health and Disease (DOHaD),

neuroendocrine function of the HPA Axis, and prematurity.   Age appropriate young

adult development at age 23 years will be described in relation to concepts of stress,

coping, emotional intelligence, and emotional health.   Prematurity effects compared

to the full term born for 23 year olds will be understood within a disease

developmental theory integrating both biological and psychosocial aspects.

The discussion will begin with a historical review of the DOHaD theory and the

contributions up until present time.   Included is a review of the construct development

of emotional intelligence and the relationship of DOHaD to stress, coping and

emotional health.

Theoretical Perspectives

The relatively new Developmental Origins of Health and Disease (DOHaD)

theory has gained scientific acceptance within the last thirty years (Wandhwa, Buss,

Entringer & Swanson, 2009).   DOHaD postulates that fetal and neonatal stressors

affect the neurological and endocrine systems adaptive responses, specifically the

hypothalamic-pituitary-adrenal (HPA) axis, which is essential for physical and

psychological growth (Barker & Thornburg, 2013; Carpenter, Gawuga, Tyrka, Lee,

Anderson, & Price, 2010; Wandhwa, et al., 2009; McEwen, 2003; Sapolosy, 2001).

The major stress pathway of the neurological system is the HPA Axis (Figure 1)

which releases cortisol.   Cortisol, the most dominant stress hormone that crosses the

blood – brain barrier, has the important function of adapting the body to both physical

and emotional stress responses (Bruyere, 2009).   Additionally cortisol is vital in the

regulation of blood vessel tone, the inflammatory response, stimulation of glucose

production, insulin, and metabolism (Bruyere, 2009).   HPA functioning is altered by

stress during structural growth periods resulting in permanent programming of early

life stress responses that contribute to disease formation later in life (Sullivan, Hawes,

Winchester & Miller, 2008).

Figure 1

 

                                              Hypothalamic-Pituitary-Adrenal Axis

Figure 1. Reprint by permission from Worth Publishers. “An Introduction to Brain and Behavior (5th Ed.)” by Bryan Kolb and Ian Q. Whishaw, 2016. Copyright 2016 by Worth Publishers. From: AN INTRODUCTION TO BRAIN AND BEHAVIOR 5E, by Bryan Kolb, et al, Copyright 2016 by Worth Publishers. Used by Permission of the publisher.

Premature birth (<37 weeks gestation) occurs at a rate of one out of every nine

births, is the leading cause of infant deaths and long-term neurological disabilities in

children (CDC, 2014).   The normal duration of pregnancy is 9 months (280 days)

with full term birth occurring at 40 weeks gestation (Taber’s, 2009).   Preterm birth,

either naturally or by cesarean section, is “arbitrarily defined as before 37 weeks”

(WHO, 2015; Johansson & Cnattigius, 2010).   Preterm birth can be further

subdivided into:  moderately premature (32-<37 weeks), very premature (28-32

weeks), and extremely premature (<28 weeks), (WHO, 2015).   The characteristics of

low birth weight and rates of fetal growth has also been used to define prematurity.

In preterm research studies, the combination of gestation weeks and birth weights are

used to avoid any misclassification especially with infants who have growth

restrictions (Johansson & Cnattigius, 2010).    Low birth weight is <2500g (5 lbs. & 8

oz.), very low birth weight is <1500g (3 lbs. & 4 oz.), and extremely low birth weight

is  <1000g (2 lbs. & 3 oz.), (Johansson & Cnattigius, 2010).

Surviving preterm born infants may have intellectual disabilities, neurological

problems, respiratory, visual, hearing and digestive problems (CDC, 2014; Martin &

Osterman, 2013).   Premature infants have experienced prenatal stress, often from

health risk factors in the mother and postnatal stress from months–long intensive

care in the Neonatal Intensive Care Unit (NICU).   These early stress experiences

evoke broad biological responses in the underdeveloped premature infant’s

neurophysiological systems including brain growth occurring during uterine

development (Phillips, 2001) and peak growth spurts well into the mid-twenties of

age (Epstein, 1986).   Thus, the premature infant’s neuroendocrine system is

frequently activated leading to the inductive development and empirical evidence in

support of DOHaD theory.

Historical Evidence and Perspectives

DOHaD evolved from Barker’s original “Fetal Origins Hypothesis” which

originated inductively from epidemiological studies. (Barker, 1990; 2004, 2007;

Barker & Thornburg, 2013; Wandhwa, et al., 2009; Gluckman & Hanson, 2007;

Reynolds, 2007; Hofman, Regan & Cutfield, 2006).    During this time period

multiple retrospective mortality and epidemiological studies from different countries

showed evidence that adult height and geographical differences were related to infant

mortality caused by heart disease (Barker, 1990, Barker, Erickson, Forsen, & Osmond,

2002; Phillips, 2001).   An influential study, consisting of 499 people at age 50 born

in England, revealed their current blood pressure measurements and hypertensive risk

factors were strongly related to the measurements of their hospital-recorded placenta

and birth weights (Barker & Osmond, 1986; Barker, 1990).   A lack of evidence was

found for the role of some commonly involved environmental variables in heart

disease, such as a high fat diet, and this finding prompted an alternative hypothesis

(Barker, 1995, 2007; Barker & Osmond, 1983).   As a result of this landmark study, a

paradigm shift representing a new conceptualization of disease causation occurred

(Barker, 2007).   This shift in scientific thinking about adult diseases, which was

defined as degenerative in nature and viewed as a result of gene and environmental

interactions, occurred and resulted in the inclusion of biological programming during

fetal and infant life (Barker, 1990) as a plausible explanation (Gordis, 2009).

Barker’s (1995) initial assumption was:  “ fetal under-nutrition in middle to late

gestation, which leads to disproportionate fetal growth, programs later coronary

 

heart disease (p 171)” lead to further studies from this hypothesis.  Later Barker

(2004) refined this to the hypothesis:

Cardiovascular disease and type 2 diabetes originate through developmental 

        plasticity, in response to undernutrition. As it is now known that growth during

       infancy and early childhood is also linked to later disease “developmental origins

       hypothesis’ is now preferred (p. 114).” 

Barker, defined a process of developmental plasticity as: “ a critical period when a

system is plastic and sensitive to the environment, followed by loss of plasticity and a

fixed functional capacity” (Barker, 2007, p 415).  According to Barker, developmental

plasticity also has three features:  1. The response will depend on the nature of the

environmental cue.   2. There are critical time periods for different systems when

changes will occur and these changes may be temporary or permanent.  3. Duration of

these critical time periods are different depending on the structure with the brain

periods longer.   These changes can be gross, substructure or functional.

The imbalance of fetal nutrients and oxygen was thought to result in an alteration

of not only metabolic yet endocrine functioning leading to smaller birth weights and a

variety of adult pathologies (Drake, Tang, & Nyirenda, 2007; Phillips, 2007; De Boo

& Harding, 2006, Gibson, Carney & Wales, 2006).   Despite the scientific acceptance

of this explanation, methodological issues surrounding the use of body measurement,

birth weight or gestation age, and studies designed without a well-characterized cohort

utilizing prenatal and adult health outcomes, as well as observational and prospective

designs, added to concerns about confounding variables (socioeconomic status, diet,

cigarette smoking, physical exercise and selection bias), statistical effect sizes

(attrition and statistical over adjustments) and publication bias (Skogen & Overland,

2012; Erickson, 2006; Godfrey, 2006).   A 2003 meta-analysis study addressing

publication bias relating to low birth weight and higher blood pressure found a weaker

association than initially determined yet maintained support for the fetal origins

hypothesis (Skogen & Overland, 2012).   Despite a weaker association found, while

addressing some of the common confounding variables as alternative explanations,

better research methodologies resulted and improved the replication of findings

(Gordis, 2009).

Further studies from a variety of countries designed to control for confounding

variables supported the association between low birth weights as a fetal antecedent to

diseases (Barker & Bagby, 2005; Vohr, Wright, Dusick, Mele, Verter, Steichen,

Simon, Wilson, Broyles, Bauer, Delaney-Black, Yolton, Fleisher, Papile & Kaplan,

2000).   At the same time debates occurred focusing on the idea that the only

important applicable time period for DOHaD was during pregnancy and the theory

was useful in explaining only cardiovascular diseases (Gluckman & Hanson, 2006;

Godfrey, 2006).   Indeed, DOHaD flourished in explaining cardiovascular risk (Bryan

& Hindmarsh, 2006).   Later, researchers significantly correlated low birth weight with

increased risk in a number of diseases that are part of the metabolic syndrome

(Hofman, Regan & Cutfield, 2006) such as truncal (middle body) obesity,

hypercholesterolemia, atherosclerosis, coronary artery disease, insulin resistant

diabetes mellitus, cardiomyopathy, congestive heart failure, autoimmune disease,

anxiety, depression, chronic pain and headache (Fricchione, 2015).   Replicable cross

sectional studies of relationships between disease formations with metabolic illnesses

supported further study of the HPA axis associations.

The results from a retrospective longitudinal study of Helsinki, Finland male

adults, gave credence to the findings that smaller infants have a higher rate of

cardiovascular disease for men in adulthood (Ericksson, Forsen, Tuomilehto, Osmond

& Barker, 2001, Godfrey, 2006).  The sample size consisted of 4,630 men born in

Helsinki (1934-44) and utilized child welfare clinic medical health records with

multiple time points of childhood through adult weight recordings, height

measurements and hospital admissions for coronary heart disease (Ericksson, et al.,

2001).   Overall, low birth weight was associated with heart disease, low weight gain

was associated with an increased risk of heart disease and rapid weight gain after age 6

was associated with further risk (Ericksson, et al., 2001).   As a result of this study,

determining what changes occurred in prenatal growth and those that occurred later

lead to focusing on the interactions of both prenatal and postnatal environments in the

development of adulthood cardiovascular diseases (Ericksson, 2006; Godfrey, 2006).

Concurrently animal researchers showed that exposure of rats during pregnancy

and after birthing, along with their offspring, to a variety of stressors resulted in

elevated stress-induced cortisol levels in the off-spring and disease development

(Phillips, 2001).   This study added a “dose-response” relationship, or intensity and

timing of the exposure of stressors to the DOHaD research literature.   Animal studies,

pinpointed the HPA Axis response to stressors introduced during critical times of rat

brain growth, that occurred after birth and produced permanent changes in the animals

HPA Axis response (Matthew, 2002; Phillips, 2001).   As mentioned earlier, in

humans, critical brain growth occurs during uterine development (Phillips, 2001) and

continues with peak growth spurts well into the mid-twenties of age (Epstein, 1986).

Sterling and Eyer in 1988 coined the word “allostasis” (Sterling & Schulkin,

2004) based on research with monkeys while studying high blood pressure.   Allostasis

was now a new paradigm to explain arousal pathology and replaced homeostasis

conceptually.   Allostasis involves regulation by: varying parameters and variations in

anticipated demands.  A new core assumption now was that physiology is sensitive to

social relations.   Allostasis also depended on higher-level brain functioning, other

then basic physiological automatic responses, and involved prefrontal cortex

regulation.   Anticipatory regulation for anxiety and satisfaction was found to rely on

the prefrontal cortex through neuronal mechanisms.

McEwen, in 1989, further developed these principles through “allostatic load” and

is credited with the advancement of the theory by publishing research findings related

to human autonomic, central nervous system, endocrine and immune system activity

(Sterling & Schulkin, 2004).    McEwen (2006) implicated stress to an event as an

individual biological response factor in the development of a disease.   In addition to

acute stress events, McEwen defined the effects of general “wear and tear” (p 367) on

the body as allostatic load that targets the HPA Axis, releasing an end product of

cortisol and can lead to the development of adulthood diseases (McEwen, 2003 &

2006).

The main hypothesis of the DOHaD theory, involves one sensitive brain area of

prenatal and postnatal development occurring in adulthood disease development by

resetting the glucocorticoid endocrines, which is the Hypothalamic-Pituitary –Adrenal

(HPA) Axis (Sloboda, Newnham, Moss and Challis, 2006).   McEwen (2008) further

delineated this dimension of the theory by postulating that stress hormones have a

central effect in health and disease by providing protective, damaging and mediating

effects.

These mediating stress effects can be from a physical, psychological, emotional,

cognitive, intellectual, major life events, environmental or social/caring interactions.

Biologically, individuals can either adapt to acute stress (allostasis) or become

overloaded (allostatic load) with chronic stress resulting in pathophysiological changes

(McEwen & Seeman, 2006).   See Figure 2.

Figure 2

Stress Response and Development of Allostatic Load

nfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Figure 2. Reprinted by permission from Macmillan Publishers Ltd;

Neuropsychopharmacology, 2000, by B., McEwen, Allostasis and allostatic load: Implications for neuropsychopharmacology, Neuropsychopharmacology, 22, 108-124. Copyright 2000 by Nature Publishing Group.

The brain is viewed as not only the controller of the stress response yet conversely

as the target (Rubinow, 2006).   The HPA Axis as programmed is effected by the

totality of lifelong stressors (cumulative risk) and negative effects on the brain and

body (allostasis/allostatic load) leading to the long-term consequences of adulthood

disease (Manzanares, Monseny, Ortega, Montalvo, Franch, Gutierrez-Zotes,

Reynolds, Walker, Vilella & Labad, 2014; McEwen, 2012, Sullivan, et al., 2008).    In

other words, the adaptability to a stressor or anxiety rather than the initial reaction will

predict long-term outcomes and allostatic load becomes the unifying concept between

cumulative risk and HPA dysregulation (Manzanares, et al, 2014; McEwen, 2012,

Sullivan, et al., 2008).

McEwen did initially base his theory on the idea of homeostasis, which

conceptually is a bodily system that is stable and unchanging (Dictionary.com, 2015)

and postulated there is an optimal level and ideal set point (McEwen, 2004).   This

explanation evolved to include the idea of variation (allo) of levels and set points

achieving a balance in the total system (Dictionary.com, 2015).   McEwen points out:

Homeostasis is about adjusting this level while allostasis is about the brain

coordinating body-wide changes to achieve stability through change (McEwen, 1998

& 2004).   Thus adaptation in a central concept of the theory.   Stressors, according to

McEwen result in experiences that are either acute or chronic.   Acute stress is the

“fight or flight” response or those responses resulting from major life events.   Chronic

stress is defined as the accumulation of minor and daily stresses.

There are four types of allostatic load (Figure 3):  normal, repeated, lack of

adaptation and inadequate (McEwen, 2000 & 2007).   Endocrine and metabolic

Figure 3

 Four Types of Allostatic Load

nfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

“Four types of allostatic load are illustrated. The top panel illustrates the normal allostatic response, in which a response is initiated by a stressor, sustained for an appropriate interval, and then turned off. The remaining panels illustrate four conditions that lead to allostatic load: 1) Repeated “hits” from multiple novel stressors; 2) Lack of adaptation; 3) Prolonged response due to delayed shut down; and 4) inadequate response that leads to compensatory hyperactivity of other mediators, e.g., inadequate secretion of glucocorticoid, resulting in increased levels of cytokines that are normally counter-regulated by glucocorticoids). Figure drawn by Dr. Firdaus Dhabhar, Rockefeller University.” 

Figure 3. Reprinted by permission from Macmillan Publishers Ltd; Neuropsychopharmacology, 2000, by B., McEwen, Allostasis and allostatic load: Implications for neuropsychopharmacology, Neuropsychopharmacology, 22, 108-124.

Copyright 2000 by Nature Publishing Group.

responses protect the body from allostatic load in the short term through homeostatic

adaptation called allostasis.   Chronic stressors or allostatic load, whether physical,

psychological or a combination, result in structural brain changes that effect our

physiological and behavioral responses and lead to the development of adulthood

diseases (Ewen, 2003 & 2006).

The stress experience or the stress response that the individual has to a potential

stressor, is the focal point (McEwen, 1998) and added to “Barker hypothesis” of

prenatal stage development, the future time determinants of adulthood diseases

(Skogen & Overland, 2012).   Stress as defined by McEwen is a “state of real or

 

perceived threat to homeostasis” and stressors are “aversive stimuli” while

 

“maintaining homeostasis through activation of complex responses involving the

 

endocrine, nervous and immune system” is the stress response (McEwen, 2006).  

 

Luthar, Cicchetti and Becker, 2000, are clearer in their definition of the stress

response, as a dynamic equilibrium, meaning an ability to sway and not as a fixed or

static state.   When a good adjustment is achieved across different domains of the

stress response, in the face of significant adversity, then “resiliency” is achieved

(Luthar, Cicchetti & Becker, 2000; Ficchione, 2015).   Thus, the capacity to maintain

allostasis while challenged by mental and physical aversive stimuli to well being,

constitutes resiliency (Ficchione, 2015).   One Mind Body Medicine equation

(hypothesis) is formulated as (Ficchione, 2015):

Stress (Allostatic Loading)     = Selective Vulnerability: Propensity to physical and

Resiliency Factors             mental illness

Ficchione (2015) defines resiliency factors as: “relaxation response, mindfulness;

 

social support/prosociality; cognitive skills; positive psychology; spirituality;

 

exercise; nutrition; healthy habits”.

According to McEwen (1998) there are two factors that determine the individuals

stress response:  how the situation is perceived and the individuals’ general state of

health (determined by genetics, behavior and lifestyle choice), (See Figure 2).

Matthews (2002) added that the timing and intensity of the aversive event and/or an

intervention also effects HPA axis development and functioning.   This focus on later

stress experiences added environmental triggers to critical or sensitive growth time

periods as a second possible causal pathway to disease suggesting the involvement of

more than one critical time period (Skogen & Overlad, 2012).   Stressors, occurring

prenatally result in adaptive changes within the HPA-Axis, become permanently

programmed, and impact health during adult life (Reynolds, 2013; Sullivan, Hawes,

Winchester & Miller, 2008; Barker, 2007) while later environmental triggers and

responses add to the allostatic load depending on coordination with sensitive growth

time periods (Skogen & Overland, 2012).

The body’s stress response helps individuals adapt to a problem and marshal the

resources to respond which includes releasing response coordinating hormones.   A

unifying and central relationship is if the stress response is activated too frequently or

under utilized then the stress-response itself can be more harmful than the stressor and

this concept is called allostatic load (McEwen, 1998 & 2004).   There has been

controversy over the labeling of this phenomenon yet the underlying concept has not

been challenged.  McEwen (2004) does identify features of some stress processes that

do not change in order to help and adds those processes that do vary in the context of

life cycles, individual experience and responses to the physical and social environment

(McEwen & Wingfield, 2010).   The challenge, according to McEwen, in the

definition is that allostasis adds to homeostasis a focus on how individuals have access

to bodily resources to respond to problems with the environment (McEwen, 2004).

Welberg and Seckl, 2001, found that stress during pregnancy could permanently

alter behavioral and/or physiological reactivity to stressors (Sullivan, et al, 2008).

The authors extensively reviewed available research of epidemiological, animal

biological, human biological, anxiety, cognition, neural mechanisms, under-nutrition,

interactions with postnatal environments and glucocorticoid studies.   In terms of HPA

function, the evidence showed:

“Birth weight correlates closely with HPA measures from infancy (206), through

       adolescence and young adulthood (207) to old age (208). These data suggest that

       low birth weight associates with both increased basal and ACTH-stimulated

       cortisol levels (207, 209). Taken as a whole, these findings are compatible with

 

       the hypothesis that fetal overexposure to glucocorticoids whether exogenous DEX

 

       or endogenous cortisol may underlie at least in part the connection between the

      prenatal environment and adult stress-related and behavioral disorders (Welberg

& Secki, 2001, p 123).”

As this evidence became available another shift in thinking about adulthood

disease formation occurred and became widely accepted by the scientific community

(Skogen & Overland, 2012; Salonen, Kajantie, Osmond, Forsen, Yliharsila, Paile-

Hyvarinen, Arker & Eriksson, 2011; Gluckman & Hanson, 2006; Godfrey, 2006).

The scientific community was now in consensus that relevant life periods are on a

continuum that includes during pregnancy, infancy and throughout the life span

(Gluckman & Hanson, 2006; Godfrey, 2006).    The focus of the theory was now

based on two main assumptions.   The first assumption is early life events that occur

during periods of critical biological growth partially determine future adulthood

disease development and secondly, this has implications for both disease development

and promotion of health (Gluckman & Hanson, 2006; Godfrey, 2006).    DOHaD

theory research then branched into three major areas of interest: 1.  Maternal, fetal and

postnatal nutrition, 2.  Preterm birth and, 3.  Epigenetics (or gene modification),

(Wadhwa, et al., 2009; Waterland & Michels, 2007).

DOHaD theory has been applied to a variety of diseases and health concerns:

behavioral, cancer, cognitive, diabetes, metabolic, muscular, neurological,

psychological and respiratory (Barker & Thornburg, 2013; Gluckman & Hanson,

2007; Hofman, Regan & Cutfield, 2006; Barker, 2005 & 2004).   The theory is widely

used in behavioral medicine and specifically with interventions directed at reducing

stress responses (Benson, 2015).    Researchers are also exploring the effects of

stressors, as measured by cortisol levels and magnetic resonance imaging, with major

psychiatric disorders such as post-traumatic stress disorders, anxiety responses, stress

responses, cognitive functioning, eating disorders, childhood disorders, personality,

long-term effects of child abuse, psychosis and addictions (Nosarti, Murray & Hack,

2010).   Indeed, anxiety, an autonomic nervous system response triggered by HPA

functioning, is a general symptom of stress and co-occurs with other psychiatric

disorders, especially depressive disorders (APA, 2000).

 

Theory Analysis

DOHaD a relatively new theory addressing the origins of adulthood disease is

widely accepted, utilized in clinical interventions and research studies.   Originating

from epidemiological study results DOHaD has developed into a major disease

causation theory.   The original theory was intended to explain one aspect of disease

causality and to be applicable to multiple diseases including those “future entitles yet

 

unknown” (Barker, 2007).   Extending the original Fetal Origins Hypothesis, beyond

the initial hypothesis of environmental influences during pregnancy has an effect on

later development, expanded the perspective beyond biological determinism (Skogen

& Overland, 2013).   The addition of stress responses through further refinement of

the HPA Axis dysregulation hypothesis, multiple critical time periods and life span

influences took into consideration the role of other causal issues.   In addition to

physical stressors, an individual’s perception of stress as threatening or uncontrollable

has been shown to activate the HPA axis as well as coping styles choices affects on

later life stress-related disease development (Figure 4).    The continued development

along this thinking moved DOHaD to a fuller life course perspective with multiple

causal factors including emotional health (individual perceptions of stress interpreted

as threatening or not) environmental (such as parenting) and for some the addition of

the biological bases of mammalian evolutionary attachment (social influences)

perspectives (Skogen & Overland, 2013; Fricchione, 2011).

DOHaD theory defines a plausible biological temporal relationship between

disease formation and the role of the HPA axis.   Research results show an association,

of a dose-response relationship of intensity and timing of stressors, and replication of

Figure 4

The Cardiovascular Toll of Stress (Emotional and Physical Stressors, HPA Axis &

 

Health)

Figure 4. Reproduced with permission of Lancet Publishing Group; Brotman, D.J., Golden, S. H., & Wittstein, I.S. (2007) The cardiovascular toll of stress, The Lancet,

370, 1089a1100.

findings in specificity to stress-related illness, although the majority of research

in the United States, has been at discrete time periods in a person or population’s life.

DOHaD theory states the necessary condition of structural and functional changes

prenatally and whether any of this is irreversible remains to be seen (Skogen &

Overland, 2012).   Some common confounding variables as alternative explanations

have been addressed and the national government (National Institute of Health) has

prioritized the use of longitudinal studies to address the complexities of what factors

(NIHR, 2015), may or may not be sufficient or necessary for disorders.

Literature recommendations for further research focus on utilizing regression

modeling statistical strategies to address:  the association between the two variables of

early exposure and adult outcomes, intermediate exposures, the interaction between

the early exposure and intermediate variables and to what degree the intermediate

variable is related to disease outcome (Skogen & Overland, 2012).   Research into the

effects of stress experiences on HPA Axis development, function and dysregulation

also requires addressing the roles of birth term, gender and social inequalities as

confounding moderating variables (Matthew, 2002; Sapolsky, 2009).   The renewed

interest in DOHaD theory is leading researchers into areas of study that promise to

identify risks and protective mechanisms; locate periods of transitions into pathology,

develop preventive and possibly corrective interventions to intervene in the

progression of disease pathologies over the course of a lifetime (McEwen &

Wingfield, 2002; Sullivan, Hawes, Winchester & Miller, 2008; Ben-Sholmo & Kuh,

2002).

Socioeconomic Status (SES)

Many socioeconomic status (SES) factors are associated with low birth weight,

coronary heart disease, under nutrition, low literacy rates and health disparities

(Senterfitt, Long, Shih, & Teutsch 2013; Baber, Muzaffer, Khan, Imdad, 2010).

Social and economic factors are considered the largest single predictor of health

outcomes and influencer of health behaviors (Senterfitt, et al., 2013).   Disparities

between countries in preterm birth weights have been partly explained by differences

in SES (Johansson & Cnattigus, 2010).   Multiple studies have found that the lower

the social, education, and economic position the higher the unhealthy behaviors (i.e.,

smoking, physical inactivity) and inability to engage in healthy behaviors (Senterfitt,

et al., 2013).

The World Health Organization (WHO, 2015) includes determinants of SES

consisting of:  the physical environment, the person’s individual characteristics and

behaviors (including how they “deal with life’s stresses and challenge, (p 1)”, social

support networks, genetics, available health services and gender.   Additionally, a

WHO (2003) sponsored study, found middle-class office workers and lower ranking

staff has more disease and die earlier than higher positioned workers.   The WHO

report (Wilkinson & Marmot, 2003) focuses on ten main areas of what is known:

1.  Life expectancy and shorter life spans occur further down the social ladder.

2.  Stressful circumstances lead to worry, anxiety, inability to cope that is damaging to

health.   3.  Foundations are laid in childhood: “slow growth and poor emotional

 

support raise the lifetime risk of poor physical health and reduce physical, cognitive

 

and emotional function in adulthood, (p 14)”.   4.  Poor life quality shortens lives.

5.  Stressful workplaces increase the risk of disease.   6.  Health risks of

unemployment increases the rates of premature death.   7.  Supportive relationships

contribute to health.   8.  Individuals addictions to alcohol, drugs and tobacco numb

difficult conditions and lead to downward mobility.   9.  Healthy food is a political

issue.   10.  People’s dependence on cars has increased resulting in less walking and

social contact and more traffic accidents and air pollution.

One of the earliest criticisms of the interpretations from DOHaD studies is the

the confounder of SES could explain results used to support the theory (James,

Nelson, Ralph, & Leather, 1997; Skogen & Overland, 2012).   James, et al, (1997)

found lower socio- economic groups have more premature and low weight births,

more illnesses, more risk factors and less nutritional diets.   The DOHaD theory

emphasizes that chronic exposure to stress mediators of the HPA Axis and the

sympathetic nervous system effects multiple organs resulting in disease (Dowd,

Simanek & Alello, 2009) although SES confounding variables in earlier studies were

not adequately controlled or interpreted.

Allostatic load has been used to explain part of the association between SES,

health and disease.   Lupien, King, Meaney, & McEwen (2001), as one goal of three,

explored the possibility that because lower SES status involved higher stress and

fewer coping resources then morning salivary cortisol levels would differ from other

SES groups.   The cross-sectional experimental design study, utilized 307 children

from a school setting, with 6 age groups (6-16 years old) and two categories (low and

high) of SES.   Overall findings showed that lower SES in children related to higher

cortisol levels with the impact of SES on cortisol absent after transition to high school.

The authors identified four possible social explanatory factors of:  changing status,

influence of peers, influence of youth culture, and resilience.

In contrast a systematic review of the literature, extending up until June of 2009,

on SES and biomarkers of physiological systems, was conducted by Dowd, et al.,

(2009) to address SES, cortisol levels and indirect measures of allostatic load.   A total

of 26 studies met the inclusion criteria of reported associations between an indicator of

SES and cortisol, and/or allostatic load.   Fourteen of these studies utilized salivary

cortisol secretions.   The findings overall were mixed with little evidence that lower

cortisol related to lower SES and lower SES related to higher allostatic load

measurements.   Overall, the authors found more studies with no associations of

cortisol to SES than the intuitive finding of lower SES associated with higher cortisol

levels.   The unexpected findings were attributed to differences in the nature of this

relationship or inconstancies in measurements and analysis of both cortisol and SES.

Standardization of cortisol procedures and analysis, variations in SES indicators used,

and the exclusion of subjects using stimulators of cortisol such as smoking, were

major recommendations for future research.   Although the review focused on cortisol

level daily patterns and indirect measurements of allostatic load, both laboratory stress

induced and dexamethasone challenges, were felt to provide more controls for

research on the differences of SES on HPA function.

Pluobidis, Benova, Grundy & Layton, 2014, identified four major hypotheses

from the literature about the associations between SES and later life health:  1.  Early

life SES directly effects later life health.   2.  Early life SES indirectly effects later life

SES.  3.  Early life and later life SES effects health through accumulation of risk.

4.  Early life health indirectly effects later life health via later life SES.   A sample of

aged 50-53 years was taken from an English longitudinal study on aging.   Multiple

measurements of early life and later life SES, health, and fibrinogen levels (indicator

of aging) were obtained.   The four major hypotheses were compared through

statistical modeling.   In general, results found early life SES extends directly until the

beginning of old age and predicts health at age 65 and older yet fibrinogen levels will

vary.

Co-existing with SES are social risk factors defined as (Msall, Sullivan & Park,

2010):  “suboptimal home and community environment, poverty, domestic violence,

 

drug addictions, crime, hunger, and poor quality housing (p 224).”   The conditions

of low SES along with access to care issues, coping with multiple adversities,

helplessness and low self-esteem; contribute to the risk of preterm births (p 225)

along with ethnicity, family history, maternal characteristics, multiple pregnancies and

air pollution (Johansson & Cnattigius, 2010; Msall, Sullivan & Park, 2010).

Low SES is consistently associated with poor health and disease yet how this gets

translated into biological risk is uncertain and studies have shown inconsistent and at

time weak results (Pluobidis, Benova, Grundy & Layton, 2014; Senterfitt, Long, Shih,

& Teutsch 2013; Baber, Muzaffer, Khan, Imdad, 2010; Dowd, Simanek & Alello,

2009; Wilkinson & Marmot, 2003; Lupien, King, Meaney, & McEwen, 2001).

Methodological issues in past studies have helped confound the influence of SES and

effected some interpretations of DOHaD theory evidence.

In this study, participants’ selection criteria at birth, as designed in the original

research, involved representation from all SES groups in each variable of birth

status (preterm and full-term born) to control for this effect.   Additionally later SES

status at age 23 was assessed for possible individual differences and SES group

variations from the prenatal time period.   Multiple measures of SES status, in addition

to income, were used and included standardized instruments, education level,

occupation level categorization and neighborhood ratings (Farrington, 1991).

Race and Ethnicity

The Center for Disease Control (CDC) found differences in preterm birth by race

and ethnicity and statistically analyzed the relevant differences, using percentages, and

z tests at the 95% confidence level (Martin & Osterman, 2013).   The percentage

results were:  1.  Black infant preterm birth rate (17.1%) was 60% higher than for

White infants (10.8%).   American Indian/Alaska Native (13.6%) and Hispanic

(11.8%) preterm birth rates were higher than White infants.    2.  Black infants had

double the early preterm birth rate (6.1%) than Whites, 25% higher than Hispanics

(Reagan & Salsberry, 2005), and other ethnicities (2.9%).   3.  Black infants were

40% “more likely to be born late preterm than White infants with Hispanic infants

 

more often than White infants, (Martins & Osterman, 2013).”

Reagen and Salsberry (2005) studied the health disparities of preterm births

among Blacks, Hispanics, and Whites focusing on social contexts of neighborhood

disadvantage and cumulative exposure to income inequality while controlling for

individual risk factors.   Neighborhood poverty and housing vacancy rates increased

the rates of premature births for Blacks while income inequality directly effected only

Hispanics (Reagan & Salsberry, 2005).   Not withstanding these findings, the close

relationship of social risk factors from low SES to ethnicity (Msall, Sullivan & Park,

2010) confounds the separation of SES from ethnicity effects.   Likewise, other

epidemiological studies have shown, that among the multiple causes for spontaneous

preterm births, being a member of the Black race, is also a risk factor (Goldberg,

Culhane, Iams & Romero, 2008).

Mustillo, Krieger, Gunderson, et al., 2004, found self-reported experiences of

racial discrimination by Black women were related to premature birth weights and

may contribute to disparities in perinatal health between races (Black 50%: White

5%).    One landmark study accounting for social disparities, showed that even college

educated Black women have an increase rate of premature births when compared to

White college educated women (Schoendorf, Hogue, Klieinman, et al., 1992).   In past

racial and ethnic disparities research, studies have separated their focus on either the

social construct of race or the biological processes (Kramer & Hogue, 2009).

A systematic review of the research literature, in 2009, focused on integrating the

racial biological and social patterning of premature births, with the expressed purpose

of  ‘understanding the etiology of black-white racial disparities in preterm birth

 

(Kramer & Hogue, 2009, p 85)”.   Over 1,459 citations were reviewed spanning from

1960-2009.   Studies utilizing ultrasound-based measurements and data cleaning

 

methodology approaches that decreased misclassification were utilized.   Conceptual

framework reviews lead to 3 primary biological pathways mediating the racial

disparities in preterm birth:  placental dysfunction, HPA dysfunction and

maternal-fetalinflammation.   Pre and peri-conceptual maternal health as well as

genetic and epigenic pathways studies were included in the review.   Overall the

researchers found evidence to support socially patterned maternal stress as a cause of

racial disparities.   The identification of few studies addressing genetics and the

challenges of controlling for multiple causal explanations prompted the authors’

suggestions for future research.   The suggestions included incorporating biological

markers into socially focused preterm birth studies as well as improved

epidemiological design studies.

In this secondary analysis longitudinal study, the original racial and ethnic

composition of the sampling is predominately White and reflective of the population

and geographical location in Southeastern New England from 1985 to 1989 (Sullivan,

et al., 2008).   The homogenous composition of this study population will be

applicable to the White racial group and not reflect the disparities inherent between

Black and Hispanic populations.   The identification of the White racial group preterm

health outcomes from 1985-1989 may contribute to further knowledge of health

advances made since that time period and could possibly be utilized to compare the

associated magnitude of racial disparities today.

 

Gender

Globally, males are slightly more likely to be born prematurely than females

(Katz, Lee, Kozuki, et al, 2013).   Decades of past research have shown males born

prematurely have higher mortality and morbidity and the phenomena is often referred

to as “male disadvantage” (Brothwood, Wolke, Gamsu, Benson & Cooper, 1986;

Stevenson, Verter, Fanaroff, et al., 2000; Banga, Barche, Singh, Sheehan &

Vasylyeva, 2015).   The confirmed risks of high blood pressure and placenta

abnormalities to the pregnant mother carrying a male fetus is thought to occur

secondary to sex differentiation hormones in utero and at conception (Katz, Lee,

Kozuki, et al., 2013, Ingemarsson, 2003).   Moreover, Sweden national figures show

death rates are higher for males by 55- 60% when born between 23 and 32 gestational

weeks (Ingemarsson, 2003).   Immediate complications of respiratory distress

syndrome are greater for prematurely born males and cognitive recovery after

intracranial hemorrhage is less when compared to premature females (Imaemarsson,

2003).   Similarly, in the United States, males are also more likely than females

(OR = 1.21; 95% CI: 1.02 – 1.42) to be born at 33 to 36 weeks (McGregor, Leff,

Orleans & Baron, 1992).   To put it another way, if a male and female are born at

the same prematurely gestational age then male infants risk becoming more seriously

ill than females (SMFM, 2015).

While prematurity survival rates have increased, the prematurely born at 25 weeks

will develop disabilities (1:10) such as lung disease, cerebral palsy, blindness or

deafness;  50% disabilities; and more commonly cognitive and neurological

impairments (Banga, Barche, Singh, Sheehan & Vasylyeva, 2015).   A retrospective

chart review of 160 (male 59% and female 41%) pediatric records at a Texas clinic

focused on children and adolescents born prematurely and any gender differences in

medical diagnoses.   The sample consisted primarily of White (39.2%) and Hispanic

(38.0%) races born prematurely and between 10 and 21 years old at the time of the

chart review.   Gestational ages were divided into two groups of 32-37 weeks and

< 32 weeks with birth weight divided into 7 groupings ranging from extremely low

birth weight to large for gestational age.   The incidence of neonatal complications

between genders was assessed according to:  jaundice, metabolic complications,

respiratory distress syndrome, sepsis, intracranial hemorrhage and hypertension.

Long-term morbidities included ICD-9 diagnoses of: asthma, allergic rhinitis, cardiac

defects, behavioral issues, developmental delays, growth delay and kidney anomaly

and diseases.   Even though, more preterm born males were at weights appropriate for

their gestational age, the study found males had a higher incidence of neonate

complications especially:  jaundice (63.1 vs. 36.8%; p = 0.02), metabolic issues

(64.2% vs. 35.7%, p = 0 .03), and respiratory distress syndrome (60.5% vs. 39.4%,

 p = 0.02),  (Banga, Barche, Singh, et al., 2015).   In contrast, prematurely born

females weights were primarily small for gestational age.   No differentiation between

genders for neonatal diagnoses of intracranial hemorrhage, sepsis or hypertension

were identified.   The only significant gender difference in long-term morbidities

found was notably in behavioral issues for males and mostly diagnosed with attention

deficit hyperactivity disorder (6% vs. 2%; p < 0.01), (Banga, Barche, Singh, et al.,

2015).

The prematurely born female chances of survival are higher than males yet Black

prematurely born females, weighing about 2.2 pounds or less, have a higher rate of

survival than their White peers (UF, 2006).   Researchers (UF, 2006) who studied

vital statistics from Florida, between the years of 1996 and 2000 utilizing records of

5,076 babies born in the state, found females at lower birth rates faired better with

Black females fairing better overall.   Although the researchers are yet unable to

explain why this racial and gender phenomena exists it is known that female

premature babies in general have more developed lungs than males (UF, 2006).

Finally, there are a few decades of history of the vulnerability of preterm males

over preterm females for increased mortality and morbidity.   Studies have shown

despite advancements in preterm neonate care this phenomenon continues to exist as a

risk to full term pregnancy and neonatal complications with male births.   A few

endocrine and biological adaptation explanations have been proposed without any

known etiology of this gender-related health disparity (Banga, Barche, Singh, et al.,

2015).    In this study, overall gender differences as well as gender and birth status

interaction are analyzed to identify the direction and strength of this effect (Baron

& Kenny, 1986).

Prematurity and Development at Age 23 as Emerging Adults

       Multiple factors including SES, race, gender, environment and lifestyles, to

mention a few, influence the health and the formation of physical diseases and

emotional health in all adults.   The prematurely born Age 23 emerging adult

entered this world with the disadvantage of multiple immature bodily systems.

Additionally, as has been previously stated, human brain growth occurs during uterine

development (Phillips, 2007), the newborn’s central nervous system (CNS) evolves

rapidly and peak growth spurts continue well into the mid-twenties of age (Epstein,

1986) resulting in multiple sensitive time periods of critical influence.   In preterm

infants who require extensive neonatal intensive care, it is possible that the HPA Axis

is repeatedly activated which may result in permanent programming of early life

responses (Maniam, Antoniadis, & Morris, 2014; Reynolds, 2013; Sullivan, Hawes,

Winchester & Miller, 2008).   Routine medical procedures activate the newborns

stress response system to react and moderate levels of endocrine hormones have been

found (Jensen, Beijers, Riksen-Walravan & de Weerth, 2010) that contributes to

alterations within the HPA Axis or fetal programing from cell death, and failed or

delayed responses of the central nervous system (CNS),  (Sullivan, Hawes, Winchester

& Miller, 2008).   See Figure 5

Figure 5

Prematurity, Postnatal Stress and HPA Function

Figure 5. Reprinted by permission Mary. C. Sullivan. 2008-2013. In “Risk and

protection in trajectories of preterm infants: Birth to adulthood (Grant # NIH R01

NR003695-14).”  Bethesda, MD, National Institutes of Health, National Institute of

Nursing Research.

Structural differences in the brains of premature low birth weight infants with

alterations continuing into adulthood have been found by researchers (Nostarti,

Murray & Hack, 2012).   Measurements of brain pathology using a variety of

biomarkers, such as salivary cortisol levels as an endocrine marker of the HPA Axis

activation is in wide use and may serve as a transitional marker for psychological

pathology (Turner-Cobb, 2005).

Feldman, Weller, Sirota & Eidelman (2002) in Israel, studied the effects of

mother to infant (or Kangaroo Care) skin-to-skin contact on both prematurely and

full term born infants.   Specifically they examined “infants’ capacity to regulate sleep

 

and wake states, organize behavior, regulate negative emotions, modulate arousal,

 

coordinate attention to mother and an object, and sustain effortful exploration of the

 

environment (p 194)”.   The infants born prematurely showed an abnormal response

to stimuli and often could not inhibit reactions.   Three theoretical perspectives were

included:  There is unique time windows for input required for optimal development

of the central nervous system and behavioral organization.   Sensory development is

sequential and lastly maternal proximity organizes sleep, rest and behavior inhibition.

A prematurely born group with intervention (n = 73) and a matched control group

(n  = 73) without intervention was used.   Pre and post interventions as well as

multiple time point measurements were used.   The premature infants who received

skin-to-skin contact from the mother were found to benefit by improved behavior

organization and emotional regulation when they reached full term.   Hence, self

regulation and the ability to adjust behaviors to the situation is a challenge to the

preterm infant, requires environmental control and sets up regulation parameters

overtime (M.C. Sullivan, personal communication, November 11, 2014).

Affect regulation of emotional experiences to serve a purpose or goal

contribute to meeting developmental milestones and adult maturation while emotional

influences on decision-making have been found during adolescent to contribute to

behavioral (alcohol and nicotine dependence), emotional and clinical disorders (Dahl,

2001).   Prematurely born children are at increased risk for behavioral and emotional

health problems along with associated psychiatric disorders especially anxiety,

depression, inattention and social difficulties (Johnson & Marlow, 2011;

Strang-Karlsson, 2011).    Children born at extreme prematurity have been found to

experience a 50-70% higher rate of attention and behavioral problems in school

despite normal IQ scores (Lynn, Cuskelly, O’Callaghan & Gray, 2011).   Even

children born near term  (34-35 weeks gestation) have a 36% increased risk for

developmental delay or disability at kindergarten age (Rabin, 2009).   Preterm born

17-year-old late adolescents have a higher percentage of psychological problems

when compared to the United States national age-related statistics (NIMH, 2007a  &

2007b; ADAA, 2007):  11% with ADHD compared to 3-5%; 12.1 % diagnosed with

depression compared to 5%;  9.8% diagnosed with anxiety disorders compared to

3.1%  (Sullivan, 2008).   Thus, prematurity is associated with behavioral and

emotional health issues, as well as, psychiatric disorders from preschool through

adolescence age, and have risk for continued problems in adulthood.

Miller, Sullivan, Hawes & Marks (2009), reported on their prospective,

longitudinal sample of 186 children, at age 12, grouped into four preterm perinatal

morbidity groups (healthy preterm without medical or neurological illness, medical

preterm with clinical illness but without neurological abnormality, neurological

preterm with severe illness and small for gestational age preterm with or without

medical problems) and healthy full-term comparison group.   A variety of biological,

social and physical environmental factors were measured utilizing a battery of tests

and neonatal medical data sources.   Differences for neurological status, motor status

and health at age 12 were significant with abnormal high rates in the four preterm

groups compared to the full term group.   Total health outcomes of the four preterm

groups were 3.4 times more likely than term births to have overall abnormal health

status at age 12.

A secondary analysis of this data (Wright & Sullivan, 2011) demonstrated that

prematurity measured by birth weight was associated with childhood psychiatric

symptoms at age 12.   Additionally, the mother’s perception of their premature child’s

vulnerability and psychiatric symptoms correlated positively at ages 4, 8, and 12.

Sullivan, Msall & Miller, (2012), found a higher percentage than the United

States’ statistics for psychological problems in their age 17 cohort of the study related

to attention deficit hyperactive disorder (ADHD), depression and anxiety.   This

prospective study reported on the same cohort at age 17 consisting of 215 infants born

between 1985-1989 with preterm birth weights <1850 grams and grouped by neonatal

morbidity then compared them with a full term group.   Outcomes of functioning and

disability included body functions, body structures, activities and participation.

Contextual factors were identified according to the World Health Organization

International Classification of Functioning (The ICF Model, WHO, 2002).   At age 17,

180 of the 215 adolescents, completed the standardized assessment process that

analyzed health, neurological, chronic conditions, psychological, environmental-

socioeconomic, personal-neonatal morbidity and gender status.   Overall results

indicated that physical long-term effects of prematurity were not only confined to

infants with very low or extremely low birth weight but also included small for

gestational age and preterm infants without neonatal complications.  Higher

percentages of psychological problems, 11% ADHD (4.1%), 12.1% (5-8%)

depression, and 9.8% (3.1%) anxiety disorders were found.

Emerging Adults

The age period between 18-25 years old is now termed the period of “emerging

adulthood” due to cultural delays in reaching developmental milestones (Arnett,

2013).   In the past, these ages were considered part of young adulthood, when the

taking on of adult roles were not delayed.   Emerging adulthood, is now a separate

category in the life span characterized by:  identity exploration, instability, self-focus,

feeling in-between adolescence and adulthood and feeling hopeful about future

possibilities (Arnett, 2013).   More importantly, emerging adults do not exist in all

cultures and only exist in cultures (middle income) that allow the putting off of adult

roles and responsibilities (Arnett, 2013).

Recent national behavioral trends in transitioning into adulthood have shown

delays in traditional major life events such as age at marriage and parenthood,

instability of residence, higher rates of enrollment in college education and a decline

in emerging adults working for pay (Ingels, Glennie & Lauff, 2012; Arnett, 2013).

Arnett (2000 & 2013) characterizes the self-views of emerging adults, in addition to

not perceiving themselves as an adolescent or an adult, as also not fully accepting

responsibility and not making independent decisions.   This may be especially difficult

for those who were born prematurely.    In addition during the transition from

adolescence (ages 10-18) into emerging adulthood (ages 18-25) extensive related

endocrine system changes occur and influence bodily processes (Arnett, 2013).   This

turbulence in endocrine hormones, involving all brain structures, adds to the life

experiences influencing brain growth and emotional health.   An emerging adult born

premature may not have the flexibility or adaptability of the HPA axis responses to

achieve allostasis and resiliency.

Globally emerging adults are experiencing life as less meaningful and health

professionals are increasingly concerned about emerging adults negative behavioral

choices to deal with stress as a way of coping (Hutchinson, Stuart & Pretorius, 2007).

American adolescents and emerging adults have a higher rate of risk behaviors than

other countries (Arnett, 2013).   Additionally, emerging adult college students were

more likely than older students to become angry or hostile about negative life events

instead of becoming more anxious and depressed (Jackson & Finney, 2002).

Emerging adults born premature who may have physical difficulties, learning

problems and limitations in social skills have an additional level of coping complexity

during this developmental period (Sullivan, 2008).   Considering these challenges at

age 23, it may be expected that prematurely born emerging adults will have difficulty

coping with adult stressors.

During emerging adulthood, exploration and changes occur that often lead to

lasting life choices (Arnett, 2000) with stressors, coping styles and neurophysiological

responses of these life choices effecting overall health (Lovallo, 2005; Somerfield &

McCrae, 2000).   Differences in stress exposure, appraisals of stress and coping styles

have been identified in adults with immune system disorders, cardiovascular,

depression disorders, and include a variety of physical and mental diseases (Cohen et

al, 2007; McEwen, Gray & Nasca, 2015; Segerstrom & Miller, 2004).    Anxious

adults with comorbid depression have been found to use more emotion oriented

coping than individuals without a comorbid diagnosis (Man, Dugan, & Rector, 2012).

The role of avoidance coping has been associated with the generation of stress that a

decade later leads to depressive symptoms (Holahan, Moos, Holahan, Brennan &

Schutte, 2005).

Given that higher percentages of psychological problems were found at the age 17

original study time point of both gestationally small and premature infants and that

growth of the brain was not fully completed, then obtaining stress, coping, emotional

intelligence and emotional health measurements by examining the age 23 cohort will

provide additional developmental data.

Stress and Coping

Multiple definitions of stress and stressors exist and are often criticized as being

“circular, formless or varied (Aldwin, 2009)”.   Indeed, stress is defined according to

each multiple discipline perspectives and applied to divergent topics (Aldwin, 2009).

Stress definitions have also been classified as:  a response (Styles:  physiological), a

stimulus (Holmes & Rahe:  adaption to life events), a transaction (Lazarus &

Folkman:  appraisals and coping), a dynamic process, state-like or trait-like and

acute or chronic (Rice, 2012; Lyons 2012; Butler, 1993).

Acute and chronic psychological stress in this study are defined by the DOHaD

theory.   Acute stress is characterized by the ‘fight or flight” response and is short term

with transient over arousal, gastrointestinal symptoms, muscular problems and

combinations of the three stress emotions of anger or irritability, anxiety or depression

(Miller & Smith, 2015).   The American Psychological Association (2015) also

defines an “episodic acute stress” characterized by an “individual always in chaos, in

 

a hurry, full of nervous energy and type A personalities.”   Chronic stress, is the daily

wear and tear of allostatic load and can lead to “suicide, violence, heart attack, and

 

stoke (Miller & Smith, 2015)”.

Related to types of stress are the Diagnostic and Statistical Manual of Mental

Disorders, 5th Edition (DSM-5; APA, 2013) broad definition of anxiety disorders.

Anxiety disorders have “features of excessive fears, anxiety and related behavioral

disturbances (p 189)”.   “Fear is the emotional response to real or perceived

imminent threat, resulting in arousal of the flight or fight response, and anxiety is the

 

anticipation of the future (p 189),(APA, 2013).”

Measuring stressors is often done by checklists and interviews (Gutman &

Nemeroff, 2011).   A number of functional tests of HPA activity have been developed

including the dexamethasone (DST) suppression test, the corticotrophin-releasing

factor (CRF) stimulation test and the combined (DEX/CRF) test.   These tests are

invasively administered or use oral administration (Gutman & Nemeroff, 2011).   The

Trier Social Stress Test (TSST) a reliable non-invasive psychological challenge test

was developed to test HPA axis reactivity to psychological stressors (Gutman &

Nemeroff, 2011).    A standardized laboratory protocol involves a 10-minute public

speech and a mental arithmetic test.   The TSST combines both uncontrollability and

evaluative threat, which are the conditions of DOHaD theory to activate the HPA axis

response (Kudiela, 2008).   As a result the response to TSST is both physiological and

psychological including increased anxiety and negative mood (Kirschbaum, 2010).

TSST testing has shown that total plasma cortisol levels are overall higher in

elderly women when compared to elderly men (mean age 67.3 years), younger men

and women (mean age 23.5 years) and without any differences in the patterns of

reactivity (Kudielka, Buske-Kirschbaum, Hellhammer & Kirschbaum, 2004).

Schommer, et al., (2003) found habituation to psychosocial stressors unchanged

overtime even if an individual was found to be a “high” or “low” cortisol responder to

the TSST.   Meaning, that the cortisol response to stress pattern remains uniform when

activated with repeated stress.    Additionally differences in cortisol response to TSST

have been found in many psychological disorders (McGirr, Daiaconu, Berlim,

Pruessner, Sable, Cabot & Turecki, 2010).

Maltreated female youths (ages 12-16 year) show a different cortisol pattern in

response to the TSST (McMillan, et al., 2009).   Youth without a history of

maltreatment showed an increase of cortisol followed by a gradual decline, in contrast

to youths with a history of maltreatment, who showed no increase in cortisol in

response to the TSST and no decline.   Emerging adults, at age 23, who were born

preterm are expected to have a pattern of salivary cortisol response of little to no

increase and little to no decline after exposure to the TSST.   Total cortisol levels may

vary in comparison to the full term born by being higher.

Lazarus and Folkman’s enduring model (Carver, 2011) of psychological stress

and coping responses focuses on the process between the person, environment, their

appraisal of and context of the event and is consistent with DOHaD theory (Lazarus,

1999; Park & Folkman, 1997).   Psychological stress is what happens when a person

is defeated in obtaining their goal commitment, intention or values (Lazarus, 1999).

Stress mediating processes include coping responses defined as problem and emotion

focused resulting from the primary and/or secondary appraisals used and are

considered psychologically effective if they work for the individual (Lazarus, 1999).

Moos and Holahan, (2003), added dispositional (inclined to cope) factors resulting

in two orientations:  focus and method of coping.   The focus is either approach or

avoidance while the methods of coping are cognitive and behavioral (Billings &

Moos, 1981; Moos, 1995; Moos & Holahan, 2003).   Approach coping is defined as

problem solving attempts to deal with and resolve stressors while avoidance coping

is defined as emotion focused attempts to avoid dealing with, thinking about, and

managing emotions associated with the stressor (Moos & Holahan, 2003).

Combining the focus and methods of coping results in eight coping subset styles listed

in Table 1 and defined in Table 2, and are measurable with standardized self-report

instruments.

Moos and Holahan’s definition of coping is one of three models (Aldwin, 2009;

Rice, 2012).   Two of the three other models explaining coping are:  the environmental

system, addressing ongoing life stressor and social resources, and the personal system

involving individual demographics (Rice, 2012).   The third model, transactional,

incorporates personal and contextual factors of the stress situation with coping skills

that affects the psychosocial functioning and maturation at the individual’s next stage

of development (Rice, 2012).   Determinants of coping responses are the types and the

severity of the stress, social resources and demographics (Rice, 2012).   Gender, age,

education, SES, cognitive abilities, problem-solving skills and personal control or

regulation will effect both the focus and method of coping.

Table 1

Coping Styles

 

Type of Coping            Approach Coping                             Avoidance Coping

_____________________________________________________________________________________________

Cognitive                     Logical Analysis                              Cognitive Avoidance

Positive Reappraisal                         Acceptance/Resignation

_____________________________________________________________________________________________

Behavioral                   Seeking Guidance and Support        Seeking Alternative Rewards

Problem Solving                               Emotion Discharge

____________________________________________________________________________________________

Table 1. From “Dispositional and Contextual Perspectives on Coping:  Toward an Integrative Framework,” by R. H. Moos and C. J. Holahan, 2003, Journal of Clinical

Psychology, 59 (12), p.1391. Copyright 2003 Wiley Periodicals, Inc.  Adapted with permission.

Table 2

Definitions of Coping Styles (Moos & Holahan, 2003)

___________________________________________________________________

COGNITIVE APPROACH COPING          Combination of logical analysis and

positive appraisal strategies

Logical Analysis                                         Attention to one aspect of the situation

Utilizing past experiences

Thinking about possible actions and their

consequences

Positive Appraisal                                       Accepting situation and restructuring it in

a favorable way

_____________________________________________________________________

BEHAVIORAL APPROACH COPING     Dealing directly with situation through

concrete actions

Seeking Guidance and Support                  Seeking guidance and support from others

Problem Solving                                         Actions derived from the approach

strategy, and organized information about

the problem along with the allocation of

resources, monitoring progress and

                                                                     evaluating results (Cherry, 2013)

COGNITIVE AVOIDANCE COPING       Combination of cognitive avoidance and

acceptance or resignation.

Cognitive Avoidance                                 Minimizing or denying the situation and/or

consequences

Acceptance/Resignation                            Accepting the situation and/or

consequences and deciding it cannot be

altered.

____________________________________________________________________

BEHAVIORAL AVOIDANCE                  Involves seeking alternative rewards,

venting feelings and/or engaging in risky

behaviors.

Seeking Alternative Rewards                    Replacing loses with involvement in new

activities resulting in an alternative source

of satisfaction

Emotional Discharge                                 Openly venting feelings of anger and

frustration

Behaviors that temporarily reduce tension

involving acting impulsively and/or doing

something risky

_____________________________________________________________________

Table 2. From “Dispositional and Contextual Perspectives on Coping:  Toward an Integrative Framework,” by R. H. Moos and C. J. Holahan, 2003, Journal of Clinical

Psychology, 59(12), p.1391. Copyright 2003 Wiley Periodicals, Inc.  Adapted with permission.

Gender Differences in Stress and Coping

       The American Psychological Association  (APA, 2010) reports differences in the

way males and females react to, manage, and view their ability to deal with stress.   In

general:  females report more stress than males (especially married females), more

physical symptoms of stress, and identify money and economy more often as sources

of stress while males report work more often as a source (APA, 2010).

Matud (2004) examined stress and coping differences between genders and found

outcomes consistent with decades of past research.   There were no significant

differences in life event frequencies experienced between genders, yet females

reported life events as more negative (p = <0.05), less controllable (p =<0.01) and

also reported more chronic stress (p = <0.01) than males.   The major stressors for

females were family and health related while males’ stressors were focused on

relationships, finances and work events.   Females utilized emotional and avoidance

coping styles more frequently while males used less emotional coping (p < 0.001).

Females experienced more psychological distress (p < 0.001) and somatic symptoms

(p = <0.001) than males.

Tamres, Janicki and Helgeson  (2002) in their meta-analysis of gender coping

differences reviewed 50 English language empirical studies between the years of

1990-2000, with actual stressor measurements rather than hypothetical situations, to

examine coping responses.   The authors categorized the studies’ definitions of

coping behaviors into problem-focused and emotional-focused with avoidance,

approach-based and other components.   Females showed a wider repertoire of types

of coping behaviors with higher usage of most types than males.   Significantly,

females used more verbal, social support seeking, ruminating and positive self -talk

than males.   A few differences between genders were found with females more often

than males using avoidance responses for coping with other’s health stressors while

males used avoidance responses for coping with relationship stressors.

Gender differences in coping patterns at emerging adulthood (ages 18-25 years)

have been found to reflect established cultural qualities (Davis, Burleson &

Krusewski, 2011; Kim & Sasaki, 2014) with endorsement of masculinity as a

significant predictor in problem-oriented coping (Lipinska-Grobelny, 2011).   A

recent decline in female gender depressive symptoms in emerging adults is thought to

be associated with greater autonomy and empowerment (Frye & Liem, 2011) although

in general, females had been found to have higher emotional coping than men (Durm

& Glaze, 2002).

DOHaD, Stress and Coping

DOHaD theory focuses on the HPA Axis physiological and biochemical

mechanisms and how these interact, as well as, the resultant effects on higher nervous

system processes such as behaviors, cognitions and emotions.   Importantly, DOHaD

theory defines stress as a real or perceived threat (physical or psychological), a

stressor as an aversive stimuli and the stress response as the activation of numerous

complex body systems through the HPA axis.   Accordingly, stress, coping responses

and affective states are thought to influence physical pathology by direct and indirect

Figure 6

Relationship of Hippocampus to HPA Axis

Macintosh HD:private:var:folders:xg:3yg_dxzx3c55v048jg5r8lpw0000gn:T:TemporaryItems:nn0309-241-F2.jpg

Figure 6. Reprinted by permission from Macmillan Publishers, Ltd: Nature Neuroscience, “How Adversity Gets Under the Skin” by Steven E Hyman,2009, Nature Neuroscience, 12, 241-243. Copyright 2009 by Macmillan Publishers, Ltd.

influences on the biological processes and behavioral responses with the HPA Axis

seen as the gateway (Cohen, Janiki-Deverts & Miller, 2007; Heindel & Vandenberg,

2015; Lovallo, 2005; Somerfield & McCrea, 2000).   The roles of allostasis and

allostatic load above all, is the link provided as a mediator of the accommodation to

the stressor, being that system-wide physiological changes are made and the HPA

Axis interconnects with other brain areas including the prefrontal cortex (PFC) to fit or

adapt to the situation (McEwen, Nasca & Gray, 2015; McEwen, 1998, Ganzel, Morris

& Werthington, 2010), (See Figure 6).   Figure 5 illustrates  “the HPA axis under the

excitatory control of the amygdala and inhibitory control of the hippocampus (Hyman,

2009)”.

Importantly, studies of individuals experienced in meditation, show related

inverse changes in functional brain imagery and mapping of brain activity (Hoffman,

et al., 1982).   When relaxation increases, heart rate, blood pressure and hippocampus

signal activity decreases (Hoffman et al.,1982).   Individuals with years of meditation

experience also show thickening of the frontal cortex of the brain (Lazar, et al., 2005).

The researchers think genomic charges are taking place from meditation relaxation

since, in addition to sympathetic nervous system responses, chemical changes related

to gene changes had been identified.   The gene changes are believed to be a

counterpart of the stress reduction response (Dusek, et al., 2008).

The resultant system-wide and HPA-Axis responses to stress (appraisal of threat)

and the stressor (aversive stimuli) allows for the inclusion of appraisal, cognition and

emotional states as key elements of the stress process.   Hence, DOHaD theory

advances an integrated model of stress through multilevel biomedical and

psychosocial models of stress (Ganzel, Morris, & Wethington, 2011).   Inherent in

dealing with stress are the efforts to manage the potential and threatening aspects of

the situation or circumstances, whether physical or psychological, and any detrimental

consequences to health (Moradi, Pishva, Ehsan, Hadadi, & Pouladi, 2011).

Psychologically, coping is defined as changing cognitively and behaviorally to mange

internal or external demands that extend beyond the persons existing resources

(Lazarus & Folkman, 1984).

Emotional Intelligence

A variety of emotional intelligence definitions were found in a systematic

literature review, using the keywords  “emotional intelligence”, from the Cumulative

Index of Nursing and Allied Health Literature (CINAHL), Cochrane Library,

ProQuest Dissertations, PubMed and the Web of Science.   The majority of

publications were from the disciplines of psychology and business with proliferation

of the topic in psychology beginning in the early 2000’s (Matthews, Zeider & Roberts,

2004).   Recently, the nursing literature on EI has shown an interest in the

epistemology, application to educational and the professional competences uses of the

construct (Por, Barriball, Fitzpatrick & Roberts, 2011; Akerjordet & Severinsson,

2010; Smith, Profette-McGrath & Cummings, 2009; Freshwater & Stickley, 2004;

McQueen, 2004).   A large body of literature exists in the business arena where EI is

extensively used in hiring, employee assessments, promotions and education of

managers (Ashkanasy, Ashton-James, & Jordan, 2004; Freedman, 2010).

One aspect of EI in which all agree is the involvement of an emotional awareness

of self and others and emotional regulation or management (Armstrong, Galligan, &

Critchly, 2011; Matthews, Zeider & Roberts, 2007 & 2004; Bar-On & Parker, 2000).

A broad common definition of EI is the capacity to identify, process and manage

emotions to contribute to a successful life (Armstrong, Galligan, & Critchly, 2011).

Emotional regulation is used interchangeably with emotional management and is

defined as the conscious or unconscious control of emotion, mood, and affect that is

most commonly achieved through coping strategies (Kowalczyk, 2015; Thompson,

1994).   The construct of EI developed out of the research on intelligence to bridge a

gap in the role of emotions and is widely used today in education and business settings

(Mayer, Salovey, & Caruso, 2004).

Multiple studies have indicated a relationship between stress, coping styles, EI

and emotional health (Por, Barriball, Fitzpatrick & Roberts, 2011; Tricky, Far hall,

Wertheim, Hinch & Ong, 2011; Ciarrochi, et al., 2002; Gerits, Derkson, Verbruggen

& Katzo, 2005).   Studies have found that individuals with high EI report less

perceived stress, have better health and report feelings of well being (Ciarrochi, et al.,

2002; Hertel, Schutz & Lammers, 2009; Pau and Croucher, 2003).   Individuals with

low EI reported more stress and difficulties with coping (Gohm 2005; Schutte,

Malouff, Thorsteinsson, Bhullar, & Rooke, 2007).    Cirrochi, Deane & Anderson,

2000, found stress associated with higher reports of depression, hopelessness, and

suicide ideation in college students (N = 302) with high emotional perception scores

and found more suicide ideation in college students who scored low in managing

others emotions.

The reciprocal relationships between stress, coping and the hippocampus and how

it relates to emotional intelligence warrants further investigation as recent studies are

finding smaller hippocampal volumes in individuals with long-term Post Traumatic

Stress Disorders (PTSD), (Woodward, et l., 2006), (See Figure 6).   Impairment has

been found in fear responses of individuals with PTSD involving dysfunctional

activation of the HPA Axis and especially within the ventromedial prefrontal cortex

(Milad et al., 2009).   EI can predict health functioning as well as distress and

traumatic stress (Singh & Sharma, 2012).   Additionally, oxidation of cells occurs

from psychosocial stress and reflects an increase in cell aging (Fricchione, 2015).

Singh and Sharma (2012) also found high levels of salivary cortisol improve coping

strategies in individuals with high EI while Tang, et al., (2007) found a significant

decrease in stress-related cortisol with 5 days of 20-minute meditation improving

attention and self-regulation.

Infants born prematurely have a variety of health impairments and a prevalence of

neurodevelopmental disabilities in general (Allen, Cristoalo & Kim, 2011).   Attention

issues and ineffective executive functioning has been found in premature low birth

weight infants suggesting that regulation of these functions in the cerebral cortex may

have been impaired (Kessenich, 2003).   This area of the brain is also utilized in

regulating emotions, interpreting and organizing information for responses which

influences the level of an individuals’ EI (Contrada & Baum, 2011).   Premature

emerging adults who may have perinatal injury and experienced sensitive time periods

of stress effecting the HPA Axis, then are exposed to increasing vulnerabilities to

stress, coping, and allostatic load during this time period, may have responses that

negatively effect EI (Allen, Cristofalo & Kim 2011; Hack, 2009; Ozer &

Benet-Martinez, 2006).   EI studies of emerging adults, ages 18-25 years old, are

scarce and the majority of studies are cross-sectional with mixed adult age ranges of

the participants.   Current measurement of the abilities to lead a successful life often

are functional and relate to developmental milestones determined by age-appropriate

roles, succeeding in schoolwork, succeeding in the work environment, social

maneuverability and forming intimate relationships to mention a few (Sullivan, Msall,

& Miller, 2012).   Given the identified vulnerabilities of prematurely born infants then

measuring and describing EI in this population at age 23, including gender differences,

may lead to further understanding of possible predictive functions, critical time

periods of risk, protective factors and types of effective clinical interventions.   “What

 

is not known is what are the long-term outcomes for adults who were born

 

prematurely and how does stress, biology, caregiving and social factors over a

 

lifetime effect the developing premature born infant? (Sullivan, 2008-2013)”.

EI Theoretical Perspectives

Historically, the modern origins of EI can be traced back to John Dewey (1902)

“moral motive” and then Thorndike’s 1902 conceptualization of “social intelligence”,

which at a rudimentary level, involves the ability to understand and mange other

people while getting along socially (Cantor, 2000; Zeidner, Matthews & Roberts,

2009).   Social intelligence was later eclipsed by interest in EI that included

differentiating between cognitive, emotional and other factors.   EI began to capture

scientific interest in academic journals during the early 1990’s through publications by

Mayer and Salovey’s model as a way of joining emotions to intelligence studies

(Mayer, Salovey & Caruso, 2000).   Culturally, Goleman popularized EI in the 1995

publication of the book Emotional Intelligence that integrated emotions with

intelligence.   The importance of both emotion and reason intuitively appealed to the

public and some in the scientific community (Matthews, Zeider and Roberts, 2004).

Although the scientific community is studying EI there is not agreement on whether it

is a scientific endeavor or if there is a science of EI (Zeidner, Matthews & Roberts,

2009).   A discussion of the theories, measurements, and applications of EI to this

controversy follow.

The term EI is used in three ways (Mayer, Salvey, & Carusi, 2000):  1.  The

popular meaning is that reason and emotion can be personally integrated and an

individual can achieve self-improvement.   2.  To describe personality traits through

connecting parts of the mind to life outcomes from mental mechanisms, models of

self, and self-relevant and general traits.   3.  To define a set of abilities dealing with

processing emotional information.   Three theorists have influenced the development

of EI knowledge, the use in practice, and research across multiple disciplines:   Daniel

Goleman, Mayer & Salovey, and Raven Bar-On  (Smith, Profetto-McGrath &

Cummings, 2009).

Goleman’s theories developed from the business sector and popularized the

concept of EI through use of work competency measures that covered a broad range of

personality measures (Mayer, Salovey & Caruso, 2004).   EI to Goleman consist of

five parts: “ knowing emotions, managing emotions, motivating oneself, recognizing

 

emotions in others, and handling relationships, (Goldman, Boyatzis and Hay Group,

2005).”   The five parts have been divided into 25 different competencies and include

mapping of these competencies.   Goleman’s model is a combination of theoretical

concepts and construct derived from multiple psychological perspectives resulting in a

popular, trait and ability mixed model.   The model has wide spread popular appeal

and is viewed as over inclusive by some in the scientific community.   Goleman,

Boyatzis and Hay Group (2005) developed the self-report, Emotional and Social

Competency Inventory (ESCI), to assess the emotional and social competencies of

outstanding leaders and provided guideline for using the ESCI.   Courses and

certifications in EI are also available.    Extensive construct and validity studies within

business organizations worldwide have been conducted.   Overall, reliability has

shown high internal consistency with limited evidence for test-retest reliability.   EI

has good construct validity with a variety of personality constructs (Wolf, 2005).

Mayer, Salovey & Carusso, 2000, ability model views EI as operating across both

cognition and emotional systems as a “unitary intelligence “ (Mayer, Salovey &

Carusso, 2000; DeFabio & Saklofske, 2014).   Emphasis is on EI as a “concept of an

intelligence that processes and benefits from emotion” and is composed of “mental

 

abilities, skills or capacities”.   The unifying system has 4 branches:  emotional

perception (perceive, attend, decipher and express), emotional integration (uses

cognitive system), emotional understanding (understanding and reasoning) and

emotional management (flexible guidelines to mange emotions).   EI is conceptualized

as a mental ability and measured with objective tasks.   The Mayer-Salovey-Caruso

Emotional Intelligence Test (MSCIET) measures EI by having the individual perform

tasks and solve emotional problems in 4 areas:  perceiving emotions, facilitating

thought, understanding emotions and managing emotions (Mayer, Salovery & Caruso,

2004b).   The original measurement had criticisms relating to scoring and reliability

and a second version addressing some of these issues are now in use (Mayer, Salovey,

Caruso & Sitrenious, 2001).

       Bar-On, 1997, generally classified as a trait model and by some others as a

mixed model defines EI as an “array of non-cognitive capacities, competences and

 

skills that influence one’s ability to succeed in coping with environmental demands

 

and pressures” (Bar-On, 1997; DiFabio & Saklofse,2014; Por, Barriball, Fitzpatrick

& Roberts, 2011).   Bar-On and Parker (2000) view the key elements of EI as stress

management and the ability to adapt.   The self-report trait EI, in this study, was

assessed with the Bar-On EQ-I.   The 133 likert-like item questionnaire provides a

total EI score (M = 100, SD = 15), and five composite scores for the principle

dimensions with 15 related content scale scores (Bar-On, 2002 & 2006; Di Fabio &

Saklofske, 2014; De Weerdt & Rossi, 2012).   The five composite score areas are:

intrapersonal, interpersonal, adaptability, stress management and happiness (Bar-On,

2002 & 2006; Di Fabio & Saklofske, 2014; De Weerdt & Rossi, 2012).   The 15

content scale scores are:  emotional self-awareness, assertiveness, self-regard,

self-actualization, independence, empathy, interpersonal relationship, social

responsibility, problem solving, reality testing, flexibility, stress tolerance, impulse

control, happiness and optimism (Bar-On, 2002 & 2006; Di Fabio & Saklofske, 2014;

De Weerdt & Rossi, 2012).   The model evolved from personality psychology and is

measured through a standardized self-report test that assessesself-perceptions rather

than actual abilities (Mayer, Salovey, & Carusso, 2000).   Studies show the EQi has a

significantly stronger association with mental health than other measures  (Gohm

2005; Schutte, Malouff, Thorsteinsson, Bhullar, & Rooke, 2007).   Raven Bar-On

EQi test is used in this study to assess EI, stress management, adaptability and general

mood.

A major issue and controversy with EI definitions is they vary so determining

what processes, behaviors and outcomes are related makes operationalization of the

construct difficult if not possible and limits hypothesis testing (Bar-On & Parker,

2000).   A construct is deliberately and consciously invented or adapted for a specific

purpose and identifies what meets inclusion or exclusion by categorization (Mishra,

2013; WSU, 2013).   In addition, constructs serve as an indirect link between the

abstraction defined and observed manifestations, in contrast to concepts which are

directly linked with observation (WSU, 2013).   Construct validity includes assessing

the test content, response processes, internal structure, association with other variables

and consequences of its use (Furr & Bacharach, 2014).   Construct validity in EI is, at

best questionable, as definitions of EI measurements are based on multiple theories

and not on an accurate and agreed upon representation of the entire domain (Stough,

Saklofske, & Parker, 2009).   As with many constructs in the social sciences, face

validity and content validity refers to the scores derived from each test item and not

the test, and is often also an issue with other social science constructs (Stough,

Saklofske, & Parker, 2009).   Conceptualization of EI on face validity is appealing yet

construct validity across measurements has not been achieved.   Research has shown

that ability based and self-reported trait EI tests are not correlated yet differing models

of trait self-reported EI were found to be correlated despite describing similar and not

identical constructs (DiFaboe & Saklofske, 2015).   EI developed from personality

theories and maybe redundant with personality constructs (Stough, Saklofske &

Parker, 2009).

DiFabeo & Saklofske, 2014, administered a battery of eight tests to assess

emotional intelligence (including Raven Bar-On), self-evaluating, resilience, and life

satisfaction, to 164 Italian high school students, and utilized multiple regression for

the data analysis.   Significant results were found for the ‘Big 5” personality factors

followed by trait self-reported emotional intelligence tests as the most predictive of

self-evaluation, resilience and life satisfaction.   An equally significant finding, was

the higher the self-reported trait EI score then the more positive, in control, able to

deal with adversity and emotional resources available were perceived by the

individual.

Summary

In summary, the construct of EI, is primarily based on personality theories, and

measurements lack construct validity across tests.   On the other hand, EI theories are

used in business, educational and health settings, and are capturing components or

factors related to success in dealing with stress, coping, emotional management and

getting along with others socially.   The Bar-On EQi, captures emotional and

psychological functioning, fits with DOHaD theory, and was utilized in this study to

assess the emotional development of emerging adults and any differences between the

prematurely and full term born.   Although definitions of EI vary and a unified

construct validity has not been achieved, EI is in wide use, and the appeal may be the

ability to capture assessments of traits of a mature personality as demonstrated in the

study above conducted by DiFabeo & Saklofske (2014).   Additionally, emotional

intelligence scores level off and usually without further gain in adulthood, and this

could be related to personality development theories (Garner, Qualter, & Whitely,

2011).   Thus, the measurement of EI at early or emerging adulthood is very relevant.

The Daily Hassles Questionnaire will provide a standardized measure of usual

life stress events.   Moos & Billings (1981) determinates of coping styles provides the

coping types and strategies used by an individual in stressful events, and carried over

from any previous stressful experiences while fitting conceptually with EI (Moradi,

Pishva, Ehsan, et al., 2011.   Bar-On and Parker (2000) view the key elements of EI as

stress management and the ability to adapt.   Elements from each of these

perspectives, a long with coping strategies and stress responses have been implicated

in health issues.

Emotional Health

Health, well-being, mental health and quality of life are similar concepts, which

include biology and the individual’s psychological state, to utilize goal directed

behaviors and involve multiple causal networks (CDC, 2013).   Emotional health is

defined as an individual   “adjusting to new situations and achieving the desired

 

outcomes”   (GUCCHD, 2016).   Higher emotional intelligence maybe related to better

emotional health and is linked to aspects of better psychosocial functioning (Schutte,

Malouff, Thorsteinnsson, Bhuller & Rooke, 2007).   Drug use, being bullied and

violence are a few of the behavioral risk factors that threaten emerging adults

emotional health globally (Lister, Merrill, Vance, West, Hall & Crookston, 2015;

Orleans, 2008).   There is a range of emotional behavior dependent on an individual’s

adaptation to stress and coping style, resulting in effects on feelings of well-being,

functioning and health behaviors (Glanz & Schwartz, 2008).

Childhood physical and emotional abuse is related to childhood psychiatric

disorders and also effects cortisol (HPA) stress reactivity (MacMillan, Tanka, Duku,

Vaillancourt & Boyle, 2013; MacMillan, et al., 2009).   Children and adolescents

mental health, according to the CDC (Perou, et al., 2013) is characterized by meeting

developmental and emotional milestones, social development, effective coping skills,

and being able to function at home, school and other areas of their life.   A similar

definition of emotional health exists for emerging adults (Arnett, 2013).   A number of

studies of emerging adults show their identified markers of transition are:  “accepting

 

responsibilities for oneself, making independent decisions and becoming financially

independent  (Arnett, 2013; Nelson, 2003).”   Additionally, social and emotional

loneliness is common and often used for self-reflection and mood management

(Arnett, 2013).   High EI scores were associated social functioning, mental health, and

vitality (Rey & Extremera, 2013).   EI has been found to have a moderate positive

relationship with coping styles and buffered stress in work situations (Gujral, 2013).

Health experts have agreed that most physical problems begin in the early teens

through the early 20’s and relate this to behavior patterns developed during this time

period (Arnett, 2013).   As a result, these patterns of behavior, become established

and effect adulthood responses.   Health educational programs, directed at risky

behaviors have shown mixed results (Arnett, 2013).   Effective psychosocial

protective factors have been identified, such as exercise that improves mood, weakens

the stress response and is thought to promote neurogenesis, while reinterpreting

negative stress stimuli through cognitive positive reframing involves memory, control

of emotion, and underlying neurobiology (Feder, Nestler & Charney, 2009).

Tsaousis & Nikolaou, 2005, through two studies (N = 365 & N = 212) with mean

age ranges of 25-36 years old measured:  1.  EI and general health in one group and

2.  EI, general health and health related behaviors (smoking, drinking, and exercise) in

another group.   EI was found to be negatively associated with poor general health,

negatively correlated with smoking and drinking and positively correlated with

exercise.

Burnett, et al., in 2011, conducted a meta-analysis of peer-reviewed research

article findings from 1995-2010.   The purpose was to look at “the prevalence of

 

psychiatric diagnoses in preterm and full-term children, adolescent and young adults.

(Burnett, 2011).”   Of 719 articles only 5 passed inclusion and exclusion criteria

resulting in 734 preterm and 634 full term (controls) individuals.   The study reported

high odds ratio of risk for anxiety, depression and other psychiatric disorders in the

prematurely born.

England’s young adults (between the ages of 18 and 25 years old) were found to

have resilience-related coping skills by utilizing social support when compared to

older adults (ages > 64 years old) who were more resilient and utilized emotional

regulation and problem solving (Gooding, Hurst, Johnson & Tarrier, 2011).   EI

research has shown an association with better health and is a plausible health predictor

(Martins, Ramalho & Morin, 2010;  Schutte, et al., 2007).

Adolescents with visible or invisible chronic health conditions (disabilities) were

found to do less well in several psychological study outcomes than adolescents

without disabilities (Wolman, Resnick, Harris, & Blum, 1994).   One similar invisible

condition is Alexithymia, broadly defined “as an inability to express one’s feelings

(Merriam-Webster Medical Dictionary, 2015)”.   Some researcher postulate this

condition is due to deficits in cognitive processing of emotions resulting in

undifferentiated poorly regulated emotions and representative of the opposite of

emotional intelligence (Velasco, Fernandez, Paez & Campos, 2006; Taylor, Bagby &

Parker, 1991).   Recent research developments have associated alexithymia with

maladaptive emotional regulation, low EI, reduced rapid eye movements, somatic

illness, and disease development (Taylor, 2000; Taylor, Bagby & Parker, 1991).

Given the potential for disabilities due to HPA axis, emotional dysregulation in

emerging adults born prematurely, coupled with previously mentioned higher

incidences of psychiatric disorders, then a range of developmental functioning,

well-being and psychopathologies are possible.   Indeed, if self-emotional regulation is

a part of EI, then the prematurely born are at risk for self-regulation and mental health

disorders especially Attention Deficit Hyperactive Disorder (ADHD), (Sullivan,

personal communication, November 11, 2014).

Summary

In this study measures for assessing stress responses, coping types, emotional

intelligence and emotional health are utilized.   The TSST provided physiological

responses by inducing a moderate stress situation along with salivary cortisol levels to

assess HPA regulation.   The DHS provided self-reports of everyday stress experiences

as representative of developmental milestones as well as stress magnitude scores in all

perinatal birth groups.   The Bar-On EQi (1997), total EQi score indicates the

emotional intelligence levels in the perinatal birth groups.  The ASR provides a

emotional health score for all participants.   Comparisons of emotional health and

stress reactivity of salivary cortisol levels determine if any differences between

perinatal birth groups exist.

HPA Axis and the Stress Response

The stress response consists of activation of two brain pathways triggered by the

hypothalamus.  The first pathway involves the autonomous nervous system and

release of epinephrine causing the physiological response of fight or flight.   This

pathway’s response is described by Selye’s theory of adaptation to stress definition of

immediate responses (Arnold & Kverno, 2009).

The second pathway involved in the stress response is the anterior HPA Axis.

Stress, directly and indirectly affects the HPA Axis, initiating the stress hormonal

response at the hippocampus level (Figure 7).   The primary hormone regulating this

axis is the glucocorticoid, cortisol (Edmunds & Mayhew, 2009).

The HPA Axis, consisting of the hypothalamus, pituitary and adrenal gland,

regulates cortisol secretion from the adrenal glands whenever we are stressed and

produces a physiological response (Bruyere, 2009).   Corticotrophin-releasing

hormone (CRH) from the hypothalamus acts as a chemical messenger to the pituitary

gland.   In turn the pituitary gland responds to the CRH and releases

adrenocorticotropic hormone (ACTH) into the blood stream.   The circulating ACTH

in the bloodstream reaches the adrenal gland that then produces and releases

cortisol.   The cortisol circulates in the bloodstream until the demand for it is met.

Physiologically, there is a cascade of effects including increased cardiac output, pupil

dilation, and shunting of blood from the digestive tract and kidneys to vital organs

ultimately resulting in decreased fluid loss, increased glucose, and decreased brain

nor-epinephrine.   Once the demand is satisfied the cortisol signals the pituitary to

stop producing ACTH.

Figure 7

Corticotropin Releasing Factor System

Figure 7. Reprinted with permission by Sage College. In W. Lovallo, (2005), Stress and health: Biological and psychological interactions (p 116). USA: Sage Publications. Copyright 2005 by Sage College.

The production of cortisol in the HPA axis is regulated through a negative feedback

loop system:

  1. Low serum cortisol levels activate the pituitary gland to release

adrenocorticotropic hormone or acetylcholine (ACTH).

  1. ACTH stimulates the adrenal cortex to increase cortisol.
  1. A high level of serum cortisol decreases ACTH production and results in a

decrease of cortisol production (Edmunds & Mayhew, 2009).

When the HPA Axis is functioning effectively the endocrine response will be

quick and adaptive.   If the HPA Axis is exposed to abnormal allostatic loads, defined

as repeated stress, lack of an adaptive response, or an inadequate response then

dysregulation occurs or allostasis is not achieved, resulting in variations in the cortisol

levels (Barker, 1990 & 2007).

Cortisol is the end product of the HPA Axis chemical transactions (de Weerth,

Zijl & Buitelaar, 2003).   Cortisol levels follow a circadian or diurnal pattern in normal

adults totaling a secretion level of 10 mg. a day (Edmund & Mayhew, 2009).   Cortisol

levels are highest in the early morning, peak 60 to 90 minutes after awakening, and are

lowest from evening to midnight (Edmund & Mayhew, 2009).

The processes involved in the HPA Axis negative feedback loop are complex and

influenced by a number of multifaceted variables.   The timing of sampling during

this process of cortisol circulation will affect the interpretation of results nonetheless

standardized timeline comparisons and interpretations are available for adults and

children (de Weerth, Zijl & Buitelaar, 2003).

      The cortisol feedback loop, also involves circulation to the frontal cortex and

limbic areas, which effects affective responses and past experiences (Lovallo, 2005).

Differences in the frontal-limbic system as part of the central cortisol feedback system

will in turn influence the differences in the stress response (Lovallo, 2005).

Summary

In summary, cortisol is a key stress response glucocorticoid within the HPA Axis

and prefrontal cortex negative feedback loop response.   Cortisol can be accurately

measured in the saliva as well as the blood, and patterns of responses are standardized.

Changes in HPA Axis responses may help identify periods of transition into disease

states.   Salivary cortisol, in this study, was measured to obtain the HPA stress

response pattern in a sample of former premature infants and a term born comparison

group at age 23 years.   The cortisol response was examined in association with

self-reported stress and coping patterns, as well as emotional intelligence and

emotional health.

HPA Axis Function in Prematurity

Prematurity rates in the United States contribute to national health care issues and

costs both in the short and long term.   The rate of premature birth for two and

one-half decades, from 1980-2006, increased by 20% (Martin, Osterman & Sutton,

2010).   Twelve percent of all births in 2010, were premature, totaling 523,033 births

for the year (CDC, 2010).   Currently the mortality rates for premature newborns with

low birth weights has decreased by around 2% due to newer preventative and

treatment approaches, but long-term morbidity remains (Child Trends Databank,

2011).   This decrease in mortality rates has increased the rates of immediate preterm

birth consequences such as:  adrenal insufficiency, intraventricular hemorrhage, patent

ductus arteriosus, respiratory distress syndrome, bronchopulmonary dysplasia,

necrotizing enterocolitis and retinopathy of prematurity (March of Dimes, 2008).

The long-term outcomes for these infants of decades of premature birth will

continue to influence social, educational, community, and family systems well into the

future.   Prematurity in general has multiple immediate birth-related health issues,

and requires continued vigilance throughout childhood (Saigal & Doyle, 2008;

Sullivan, et al., 2008; Hack, Taylor, Drotar, Schluchter, Carter, Andreias, et al.,

2005; Saigal, Burrows, Stoskopf, Rosenbaum, & Streiner, 2000).   More recently,

prematurity effects are proposed to contribute to the development of adulthood

illnesses (Hack, 2009; Saigal & Doyle, 2008).

In addition to the specific issues surrounding prematurity, the study of cortisol

levels as an indicator of the HPA Axis functioning in those born at term has

implications for application to health issues.   Identifying any difference between

premature and full term birth HPA Axis functioning by screening for alterations in

cortisol levels in combination with stress, coping, emotional intelligence and

emotional health measurements may identify vulnerable individuals of all birth group

types before expression of any variations (Dedovic, Duchesne, Dager & Pruessner,

2010).

Cortisol levels in newborns have been hard to standardize due the rapid shifting of

development, instability of the newborn system and brain volume growth of

15mL/week between 29 and 41 week’s gestation (Main, 2010).   No normal range of

preterm cortisol levels exist because of a variety of fluctuation in preterm and full term

physiological homeostasis (Ng, 2011).   There is agreement that around 1 year of age

preterm cortisol levels begin to stabilize into a pattern approximating the adult diurnal

cycle (de Weerth, Zijl & Buitelaar, 2003).   Under normal conditions, with full term

infants, cortisol levels reveal a circadian rhythm with the adult pattern of diurnal

decline from morning to evening at around 3 months of age (Turner-Cobb, 2005).

Attempts to collect salivary cortisol levels from newborns have met with issues of

lack of sufficient saliva quantity and concerns about interference of administered

sweet solutions (Morelius, Nelson & Theodorsson, 2004).   Morelius, Nelson

& Theodorson (2004), successfully obtained 113 preterm and term infant’s saliva

using less than a 10mL sample.   In combination with altering the detection limit of the

radio-immunoassay they were able to analyze very low concentrations of cortisol in

newborns without interference from oral glucose solutions.

Jansen, Beijers, Riksen & de Weerth (2010), analyzed 48 peer reviewed empirical

studies (1978-2008) providing pre and post stressor cortisol levels at various ages.

In the first 13 weeks or 3 months post-natal the mean cortisol reactivity effect to

painful stimuli was the highest and continued to decline with advancing infant age

groups (3 & 6 months, 6 & 12 months and 12 & 24 months).

Tollenaar, et al. (2010), obtained daily eye swab cortisol levels from 300 infants at

the ages of 6 weeks, 5 months and 12 months.   The infant’s cortisol levels declined

over the year however intra-individual variability was large and stabilized between 5

to 8 months.

Knowing that the newborn’s system, whether preterm or full term, is continuing to

evolve at a rapid pace, understanding the processing of a variety of stressors during

critical growth periods become paramount.   Prematurity is a stressor itself due to the

immaturity of the central nervous system and the neonatal course, which may include

neonatal illness and a long intensive care stay.   Routine medical procedures activate

the newborns stress response system to increase cortisol secretion.   Physical stressors

to the infants HPA Axis have resulted in subsequent moderate increases of cortisol

levels (Jansen, Beijers, Risken-Walraven & de Weerth, 2010).   The combination of

increased cortisol levels, contributing to cell death and a failed or delayed response of

the central nervous system (CNS) results in alterations within the HPA Axis or fetal

programming (Sullivan, Hawes, Winchester & Miller, 2008).

Sullivan, Hawes, Winchester and Miller (2008), define the immediate effects of

premature birth or neonatal programming and include individual differences such as

genetic, developmental and social/care giving, which influence the neonates

behavioral and neuroendocrine response (See Figure 8).   This response is heightened

Figure 8

Premature Birth:  Fetal/Neonatal Programming

Figure 8. Reprinted by permission Mary. C. Sullivan. 2008-2013. In “Risk and

protection in trajectories of preterm infants: Birth to adulthood (Grant # NIH R01

NR003695-14).”  Bethesda, MD, National Institutes of Health, National Institute of

Nursing Research.

or hypersensitive and contributes to the neonatal allostatic load.   Long-term

exposure to repeated negative developmental stress increases the allostatic load on the

HPA Axis and if not counteracted by positive or protect factors, such as mediated by

mother-child attachment security, then adult outcomes of disease occur.   Sullivan,

et al. (2008), attributes adulthood disease development to factors both positive and

negative, defined as cumulative risk and protection, which affect long-term outcomes

of functional, emotional, executive brain and work performance (See Figure 9).

In summary, early trauma with long term neurological consequences that are

dysfunctional, especially when paired with the proper timing of a stressor, at a critical

time in the development of a child, may result in health, emotional and behavioral

consequences exhibited in adulthood.

Figure 9

Cumulative Effects of Caregiving and Social Environments Over Time

 

Figure 9. Reprinted by permission Mary. C. Sullivan. 2008-2013. In “Risk and

protection in trajectories of preterm infants: Birth to adulthood (Grant # NIH R01

NR003695-14).”  Bethesda, MD, National Institutes of Health, National Institute of

Nursing Research.

HPA Axis Function in Stress and Anxiety

Anxiety is a complex response to a stressor that includes emotional, cognitive,

behavioral and physiological responses.   Diagnosed anxiety disorders, which last

longer than 6 months, affect 40 million adults age 18 and older each year (NIMH,

2009).   Anxiety disorders commonly occur with mental and physical illnesses, as well

as alcohol and substance abuse.   Individuals may complain of uneasiness, fearfulness

or nervousness, increased heart rate and increased respirations, to mention a few signs

and symptoms.

Walter Cannon’s well-known fight or flight response, further developed later by

Hans Selye, prepares the body to respond by increasing blood pressure, heart rate,

cardiac output and other responses as indicated in HPA functioning noted earlier

(Halter & Vascarolis, 2010).   If the individual’s underlying neurological functioning

or HPA Axis functioning is dysfunctional then mediating effects, positive and

negative or cumulative protective and risks factors, will effect this response according

to the DOHaD theory.   These mediating stress effects can be from a physical,

psychological, emotional, cognitive, intellectual, major life events, environmental and

social/caring interactions.

If the individual’s anxiety is transient and without dysfunction then no permanent

change will occur in the HPA Axis functioning    If there is an early trauma, such as

prematurity, with long term neurological consequences that are dysfunctional, paired

with the proper timing of the stressor during critical developmental periods of the

child, then the consequences will be evident in adulthood (Turner-Cobb, 2005).   In

other words, the adaptability to a stressor or anxiety rather than the initial reaction will

predict long-term outcomes.

What is known during childhood, is the relationship of low birth weight in

preterm births and subsequent psychopathology is coactive with psychiatric problems

but not necessarily medical problems (Nomura & Chemtob, 2007).   Additionally

directionality of cortisol levels in childhood is known and has been determined by

their behavior of engaging or withdrawing responses (Turner-Cobb, 2005).   Often a

child born prematurely will have a blunted cortisol response.   A blunted cortisol

response, is defined as a failed, less intense, less concentrated or delayed cortisol

response (Bruehl, Wolf, & Covit, 2009; Sullivan, et al, 2008).

Various adult studies exist that measure cortisol levels in a variety of

psychological pathologies, emergency situations, and anxiety reduction interventions

(Harvey, Nathens, Bandiera & LeBlance, 2010; Rapaport, Schettler & Bresse, 2010;

Yu, 2010).   At the other end of the life spectrum, Lanze, Mantella, Shi, et al., (2010),

report that researchers have found that one-third to one-half of elders develop

generalized anxiety disorder later in life, when aging neurological processes interfere

with brain cortex messages to the HPA Axis.

Although they are careful to report that multiple neurological pathways affect

health, the utilization of the selective serotonin re-uptake inhibitor drug escitalopram

was effective in symptom reduction and reducing cortisol levels in subjects that had

diurnal pretreatment cortisol levels above normal peak and daily total levels (Lanze,

Mantella, Shi, et al., 2010).

Elevation of cortisol levels in healthy adults has been found when the subject is

exposed to a standardized transient psychological stress test, the Trier Social Stress

Test (TSST) to trigger an acute anxiety or stress response.   If a stressor or anxiety

response is elicited then the corresponding standardized timed cortisol level responses

reflect this change.   A baseline diurnal cortisol level is obtained for comparison to the

stress induced cortisol response to measure reactivity of the HPA Axis.   This

psychological stress induced measurement is useful to look at the level of stress or

anxiety triggered (and the HPA Axis response) and the intensity level of the cortisol

release.

Stress, coping, emotional intelligence and emotional health differences have

been found in some studies with prematurely born children.   Given that the prefrontal

cortex and limbic system is part of the corticotropin releasing factor system, then

involvement of these structures and function effects will also influence emotional,

affective, appraisal and coping in the emerging adult (See Figure 10).

Summary

Structural differences in the brains of premature, low birth weight infants with

alterations continuing into adulthood have been found by researchers (Nostarti,

Murray& Hack, 2010).   The concept of allostatic load and research studies related to

DOHaD theory links (Sullivan, 2008-2013): “1.   Repeated infant stress responses to

 

prematurity and neonatal experiences with increased allostatic load.  2. The

 

cumulative effects of the social environments overtime with disease formation”.  

Measurements of brain pathology using a variety of biomarkers, such as magnetic

resonance imaging and free saliva cortisol levels, have yielded general structural and

functional data.   Salivary cortisol levels as a major endocrine marker of the HPA

activation is in wide use to measure stress responses, allostatic load, allostasis, health,

Figure 10

Stress, Coping, Prefrontal and Limbic System, HPA Axis, Cortisol, Emotional

 

Intelligence and Emotional Health

EMOTIONAL STRESSOR

|

APPRAISALS (Aversive)

|

_____________________________________________________________________                                                                      

 

                                 CORTISOL ___   ___   ___   ___   ___   ___   ___   ___   ___

                                               |                                         = Prefrontal Cortex &         |

   Limbic System:  Sensory

Cognitive & Memory          |

&

COPING                          |

    (Focus & Method)

|                                  |

|

= ANS ——–SNS                      |

Increase heart rate

|                                  |

|

|                                  |

= CORTISOL ___   ___   ___   ___

                    |

                    |

                    |

_____________________________________________________________________________________________

                                                                                                                       |

                                                                                                                       |

                                                                                  _____________________________________________

 

                                                                                        EMOTIONAL OUTCOMES

  • Emotional Intelligence
  • Emotional Health

                                                                                  _____________________________________________

 

 

Figure 10.  Adaptation from Dorine Felder with permission, (2003), “Schematic overview of the hypothalamic-pituitary-adrenal (HPA) axis. Stress activates the HPA-axis and thereby enhances the secretion of glucocorticoids from the adrenals”. CC BY-SA 4.0 (http://creativecommons.org/licenses/by-sa/4.0)], via Wikimedia Commons. Retrieved December 15, 2016.

disease and psychiatric pathology. (Turner-Cobb, 2005).   Salivary cortisol sampling

is non-invasive and easily, as well as, reliability measured.

The TSST, is another well established standardized protocol for provoking the

physiological and emotional stress responses in a laboratory setting for acute stress

reactions.   Measurements of TSST cortisol stress responses, in early adulthood (age

23) allows us to examine differences in HPA Axis functioning between former

premature and full term infants and prior to later adulthood and later aging process

interactions.

Emerging adults, at Age 23, have multiple intrapersonal, interpersonal and stress

adaptability reactions to master in order to reach developmental milestones and will

require effective emotional intelligence and emotional health.   Societal changes in

when emerging adults met the traditional milestone goals and the globally observed

increased risk-taking behaviors also warrant examining emerging adults coping styles.

Emerging adults coping styles to deal with stress will not only influence their current

emotional health yet will be carried with them into adulthood.   Stress, coping, the

cortisol stress response, emotional intelligence, and emotional health are all involved

in obtaining developmental milestones at Age 23 for emerging adults.   Results from

this study will inform us not solely of current emerging adults’ emotional health

status, yet also importantly, if there are any prematurity effects to address that

may point to risk for later adult disease.

Secondary Data Analysis

This secondary analysis is derived from the dataset of a prospective longitudinal

cohort designed study of preterm and full term infants:  Risk & Protection in

 

Trajectories of Preterm Infants:  Birth to Adulthood (Sullivan 2008-2013).   The

project received full IRB approval from the University of Rhode Island, Women &

Infants Hospital and Rhode Island Hospital.   The study also received a Certificate of

Confidentiality from the National Institutes of Health.   The subjects (N = 213) were

born at Women & Infant Hospital between 1985-1989 and continually followed at 9

time points in research studies:  1 month, 18 months, 30 months, age 4, age 8, age 12,

age 17 and age 23.   The sample retention rate at age 23 was 85% (N = 180).

The original researcher’s theoretical perspective was derived from DOHaD theory

and the purpose was to follow preterm (with ranges of gestational age and perinatal

morbidity) and full term born infants to age 23 to examine “the impact of prematurity,

medical history, and environments on achievements and deficits during young

 

adulthood (Sullivan, 2008)”.   The original study had 3 specific aims with related

hypotheses that focused on determining the effects, relationships, and outcomes of

young adults (age 23 years old) in terms of:  health (especially cardiovascular),

functional performance, emotional intelligence, executive function, work competence,

growth, neurological morbidities and psychological processes.   This secondary

analysis adds an in-depth subset analysis of findings related to stress, coping, EI,

emotional health and psychiatric disorders of the infant born prematurely at age 23

(Miller & Brewer, 2003).

Compatibility of the primary data with this secondary analysis is not an issue and

will still provide information on the differences over time between 23 year olds born

pre or full term (Miller & Brewer, 2003; Yea & Niemeier, 1996).   No data collection

expenses with be incurred in this secondary analysis study as did in the original

longitudinal study.   The first wave of the recruited participants did not change over

time and the retention rate (85%) and those lost to attrition at age 23 (15%) remained

less than 20% allowing confidence in interpreting the differences between birth groups

(Gordis, 2009; Miller & Brewer, 2003; Yea & Niemeier, 1996).

The initial cohort was well characterized and the study procedures and

measurements were standardized and well defined.   An “exposed” group of

prematurely born and a “non-exposed “ group of full term born infants comprised the

two comparison groups and were selected for birth status, neonatal illnesses, gender

and wide representation of socioeconomic status.   The original researchers followed

protocols without changes in research staff resulting in minimization of personnel

effects threatening the internal validity (Miller & Brewer, 2003; Menard, 2007).   As

with all longitudinal studies, all factors involved over time, are not captured yet the

original design accounted for common confounding variables associated with changes

in socioeconomic status between birth and age 23 and gender differences (Menard,

2007).

The two time points used in this secondary analysis add a distinctive period

over time and allow for identifying levels of stress adaptability, coping styles,

emotional intelligence levels and emotional health status (Singer & Willet, 2003).

Measurements included self-report, interview, observational coding, and standardized

protocols used over the course of the longitudinal study were age appropriate, and

minimized the effects of the setting and participants’ acclimation (Menard, 2007).

Furthermore, the current researcher had limited involved in the original research

nonetheless had access to the principal researchers for clarification, understanding and

information related to the study design, data, meaning and decision processes (Miller

& Brewer, 2003)

Ethical, confidentiality issues and use of the participants’ identity cleansed data

was addressed in the original study consent form at all time points and are not

accessible to this researcher (Miller & Brewer, 2003).   Notwithstanding the

availability of the original dataset, the selection and in-depth understanding of the

dependent variables required extensive analysis.   In addition, modeling analysis of

change variables is possible with this design (Singer & Willett, 2003).    What is

unique about this secondary analysis is it begins with the identified preterm and full

term birth groups before any manifestations of emotional issues and psychiatric

disorders develop and focus on the time point of the age 23 year old participants.

Summary

This study examined all dependent variables both alone and in combination that

may influence the prematurely born emerging adult in developing emotional health

issues.   Before the research plan for this study could be fully developed, a theoretical

and concept analysis of the Developmental of Health and Disease Theory, HPA Axis

functioning and Emotional Intelligence was done to clarify the concepts and constructs

and provide direction in measurement.   Issues in conducting a secondary analysis

were reviewed.   In Chapter 3 the secondary analysis and original study description,

sample characteristics, methodology, and data analysis plan to investigate any

differences in emotional health between the preterm and full term born emerging adult

is described.

CHAPTER 3

Methodology

This study is a secondary analysis of a larger longitudinal study aimed at

determining the effects of prematurity, risks and protective processes on adult

trajectories and health outcomes at age 23.   The original study’s theoretical

foundation is the Developmental Origins of Health and Disease (DOHaD) and the

variable measurements used are consistent with the purpose of this secondary analysis.

This secondary study is a descriptive correlational design of the effect of premature

birth and its relationship to stress, coping, emotional intelligence, emotional health and

the stress response of neuroendocrine functioning at age 23.   In this chapter, sample

and neonatal demographics, self-report measures of stress, coping and emotional

intelligence, assessment of emotional health, and timed measures of salivary cortisol

through a standardized laboratory social stress paradigm, the Trier Social Stress Test

(TSST) are defined.   The study procedures and data analysis plans are outlined.

Research Design

The University of Rhode Island, Office of Research Integrity, determined this

secondary data analysis, did not require Institutional Review Board (IRB) oversight:

# 910108-1 (See Appendix L).

Sample

The infant participants were born at Women’s and Infants Hospital in Rhode

Island between 1985-1989, continually followed in a series of research studies

supported by the National Institutes of Health (Lester, 1985; McGrath, 1989, 1994,

1998, 2003; Sullivan, 2008 – 2013.   The infant sample included 213 infants in a

5-group design of:  (1) full term healthy infants (FT), (2) preterm infants without

neonatal illness (HPT), (3) preterm infants with neonatal medical illnesses (MPT),

(4) preterm infants with neonatal neurological illness (NTG) and (5) preterm infants

with small for gestational age (SGA) with and without neonatal illness, (Sullivan,

2008-2013).   The original racial and ethnic composition of the 213 sampling,

consisted of 105 females and 108 males, and was reflective of the population and

geographical location in Southeastern New England from 1985 to 1989 (Sullivan,

2008-2013).   This original sampling included varied degrees of neonatal morbidity

in preterm birth.   The study maintained a 97% retention rate from age 4 to 23 years

(Sullivan, 2008-2013).    At age 23 years, 180 subjects were recruited for participation

in the 10th longitudinal follow-up study with a retention rate from birth of 85%, and

96% from the prior age point of 17 years.   Two time points, birth and age 23 years,

the 10th wave of this longitudinal study comprised the sample for this study.

The data (Appendix Measurements) utilized for this study will consist of neonatal

data from the original five groups and demographics.   Age 23 years data are, the

self-report measures of the Daily Hassles (DHS-R) for stress, Coping Response

Inventory (CRI-A) for coping styles, the Bar-On Emotional Quotient Inventory

(Bar-On EQi) for emotional intelligence, emotional health status from the Adult Self

Report (ASR) and salivary cortisol levels collected according to the established

protocol from the Trier Social Stress Test (TSST).

The neonatal sample inclusion and exclusion criteria as well as the characteristics

of 5-group design are well described (Sullivan, 2008-2013; Winchester, Sullivan,

Roberts & Granger, 2016).    For this study, inclusion criteria included the ability to

participate and complete the study protocol and measures.   Any 23-year old

participant with severe medical problems, such as cerebral palsy with wheelchair

assist, or low intelligence with or without physical limitations was excluded.   Females

who were pregnant, tested positive using urine pregnancy screening, or <8 weeks

post – partum were excluded from the original data collection.   Additionally any

23-year old young adult with positive urine testing for substance use was excluded.

Measurements

The following measurements are proposed for the current study.

Demographic Data

Demographic data included neonatal birth data at age 23 including the

Hollingshead Four Factor Index of Social Status (HH), (Holmes & Rahe, 1967).   HH

was used to estimate the socioeconomic status of unmarried individuals, female and

male heads of households and families (Hollingshead, 1977; Gottfried, 1985).   It is

widely used in medicine and public health to differentiate socioeconomic status

(Adams & Weakliem, 2011).   The four factors examined consist of:  education,

occupation, sex/gender and marital status that are used to derive a mathematical

estimate of social status (Hollingshead, 2011).

The occupation scale is scored between 1 and 9, nine being the most highly

regarded occupations and one being less highly regarded careers.   Examples of

occupations which would receive a score of nine are architects, lawyers and

physicians, while occupations that would earn a score of one are janitors, dishwashers

and personal attendants.   A seven-point scale is employed to determine educational

status.   A seven indicates the completion of a graduate degree or higher while a one

represents completion of less than a seventh grade education.   To acquire a social

status score the occupation score is multiplied by 5 and the education score is

multiplied by 3 (Hollingshead, 1977).   In families with two gainfully employed

persons the total score is divided by 2 to obtain a social status score.   The range of

computed social status scores (8-66) are then divided into five categories of:  lower

(8-19), lower-middle (20-29), middle (30-39), upper-middle (40-54) and upper

(55-66), (Hollingshead, 1975).

The Hollingshead Four Factor Index of Social Status is used as a benchmark to

compare other measures of socio-economic status (Adams, J., & Weakliem, D., 2011).

The Hollingshead reliability correlates with other indices of SES with ranges of

.73-.89 (Cirino, Chin, Sevcik, Wolf, Lovett & Morris (2002).   The social scores

achieved are considered the best valid measure of socioeconomic differentiation

available (Cassidy, Drotar, Ittenbach, Hottinger, Wray, Wernovsky, Newburger,

Mahoney, Mussatto, Cohen, & Marino, 2013; Adams, J., & Weakliem, D., 2011).

Stress

Stress (psychosocial) measurements include everyday and major life

experiences as captured by the Daily Hassles Scale-Revised (DHS–R).   The

DHS–R, developed by Kanner, Coyne, Schaefer & Lazarus, (1981), focuses on

everyday stressors instead of major stress life events and psychological and somatic

symptoms (Holm & Holroyd, 1992).   Measures of daily life hassles in 53 items (e.g.,

time alone, your spouse, your health) on a 4-point scale, ranging from “none or not

applicable” to a “great deal.”    The item scores are summed to give a score for the

overall severity of hassles, ranging from 0-159.   Internal consistency was .93-.97

over 2 years.   Mean day-to-day correlation was .77 and mean monthly correlation

was .82.   Daily hassles severity is related to depression, anxiety, PTSD and role

stress.   The DHS–R has been previously used in studies with preterm born children

(Msall & Park, 2008).

 

Coping

        The Coping Response Inventory-Adult Form (CRI–A) measured coping

responses, at Age 23 (Billing & Moss, 1981; Moos, 1995; Moss & Holahan, 2003).

The CRI-A form, developed by Rudolf Moos, is a 48-item self-report inventory

measuring cognitive and behavioral responses to stress.   It measures coping

orientation focus (approach or avoidance) and methods of coping used (cognitive or

behavioral)

The CRI–A is appropriate for use in both healthy adults 18 years of age and

older, and those with psychiatric, substance abuse and medical diagnoses.   The

instrument may be administered in structured interview or self- report format.   The

participants select and describe a recent stressor (within the last year) and use a

four-point scale varying from “not at all” to “fairly often” to rate their reliance on each

of the 48 coping items.   Eight types of approach and avoidance coping responses are

derived from the items.   Approach responses include logical analysis, positive

appraisal, seeking guidance and support, and problem solving.   Avoidance responses

include cognitive avoidance, acceptance or resignation, seeking alternative awards,

and emotional discharge.   Within each of the approach and avoidance responses, the

first two scales are representative of cognitive coping strategies and the third and

fourth scales of behavioral coping strategies (Moos, 1993).

Additionally, ten appraisal items assess if the stressor was expected, viewed as a threat or challenge, the perceived cause and if resolution has occurred.    Participants respond to questions aimed at examining the context of the stressor using a

four-point scale varying from “definitely no” to “definitely yes” (Moos, 1993).

The CRI-A is interpreted using T-scores, with possible T-scores ranging from 20 to 80 + with a mean of 50 and a standard deviation of 10.   A T-score of  < 34 is considerably below average and a score of  > 66 is considerably above average.   Internal consistencies range from 0.61 to 0.74 for males and 0.58 to 0.71 for females.    Cognitive avoidance internal consistency as measured by Cronbach’s alpha is .71 and emotional discharge is .60.   Avoidance coping “across time (1-year stability = .56;

6-year stability = .51) and across life domains (ie., interpersonal, health, and financial stressors), has been found to be stable (Holahan, Moos, Holahan, et al., 2005). “  Test-retests alphas showed moderate stability over 12 months (average

 r = 0.45 for males and 0.43 for females).  Content and face validity was built into the CRI-A by formulating definitions of specific domains, preparing items to fit the construct definitions, and selecting items that were conceptually and empirically related to a dimension.   Reliability and validity have been extensively researched and found to be adequate (Moos, 1993 & 2004).

Emotional Intelligence

 

       The Bar-On Emotional Quotient Inventory (Bar-On EQi) was used to

measure the emotional intelligence of all participants.   The Bar-On EQi is a

self-report measure of emotional and social behaviors and the participants potential

to deal with daily environmental demands and pressures (Bar-On, 2002 & 2006;

Sullivan, 2008).   It has been used world-wide in a variety of settings with diverse

populations and translated into 30 languages since being developed in the 1980’s

(Bar-On, 2006).   The Bar-On EQi contains 133 items, on a 4-point Likert-like

scale (ranging from very seldom to true), resulting in 5 composite scales and 15

subscales (Sullivan, 2008; Bar-On, 2006).      The 5 composite scales are:

intrapersonal, interpersonal, adaptability, stress management and general mood

(Bar-On, 2006)”.   The intrapersonal scale measures self-awareness and

self-expression as a composite assertiveness, independence and self-actualization

subscales.  The interpersonal scale measures social awareness and interpersonal

relationships as a composite score of the social responsibility and interpersonal

relationships (“the establishment of mutually satisfying relationships and relating well

 

with others”) scales (Bar-On, 2006).   Stress management measures emotional

management and regulation as a composite score of the stress tolerance and impulse

control subscales.   The adaptability score measures change management as a

composite score of the reality testing, flexibility and problem solving.   The general

mood composite score measuring self-motivation is derived from the subscales of

optimism and happiness.   Finally an overall total emotional quotient score is

generated.

The 133 items are rated on a five-point Likert-type scale with choices ranging

from “very seldom” or “not true” to “very often true” or “true”.   The raw scores are

converted into standard scores with a mean of 100 and standard deviation (SD) of 15.

The higher the score the more potential for effective emotional and social functioning

and the prediction for meeting daily demands and challenges (Bar-On, 2006).

The Bar-On EQi questionnaire has a built in validity correction factor that

adjusts for response bias.   Internal consistencies range from  .69 – .96 with all

composite scales correlate highly with the total EQ-I scores (.67 to .93), (Dawda &

Hart, 2000).   Test-retest reliability at six months ranges from .72 to .80 (Bar-On,

2006).   Ten subscales from a confirmatory factor analysis are the strongest measures

of the construct:  self-regard, interpersonal, impulse control, problem solving,

emotional self-control, “emotional self-awareness, flexibility, reality testing, stress

 

tolerance, assertiveness and empathy (Bar-On, 2006).”   The remaining 5 subscales

are facilitators of emotional and social intelligent behaviors:  independence,

self-actualization, social responsibility, optimism and happiness.  The Bar-On EQi

has been extensively researched and validated with evidence strongly supporting

construct, divergent, discriminant, criterion, and convergent and predictive validity.

Emotional Health

       The Adult Self-Report (ASR) was used to determine emotional health.   The ASR

for ages 18-59 is extensively researched and used widely in research studies for well

over twenty years (Achenbach, 2003).   The ASR assesses social competence and

behavior problems in adults ages 18-59.   The participant completes the ASR and

report their own functioning, problems and substance use.   It provides normative

scales for functioning, syndromes, substance use, internalizing, externalizing and total

problems (ASEBA, 2011).   The syndrome scales are then profiled to international

expertly derived Diagnostic and Statistical Manual of Mental Disorders Fourth

 

Edition Text Revision (DSM IV-TR) oriented scales (Archenbach, 2003).

The ASR (2003) is composed of data relating to friends, spouse or partner, family,

job, education and a list of self-descriptors.   The descriptor list contains 126 items

rated on a 3-point scale consisting of “ not true, somewhat, or sometimes true and

very true or often true”.   Raw scores are converted in t – scores are categorized into

clinical risk screening ratings of normal (t = <59), borderline (t = 60-63), and clinical

(t = 64 and above).   Classification parameters resulted in true positives

(sensitivity) = 80%;  true negative (specificity) = 95%;  false positives = 20%;  false

negatives = 5%.

Category scores are related to DSM IV-TR disorder criteria.   Internalizing

behaviors include anxiety, depression and withdrawn behaviors while externalizing

behaviors include aggression, rule breaking and intrusive behaviors.   The

DSM-oriented problem scales are depressive;  anxiety problems;  somatic;  avoidant

personality;  AD/H and antisocial personality.

Reliability is excellent:  1-week test-retest correlations were .80 – .90, 2 years

was .69 with none below .71.   Internal consistency range was  .78 – .85.  Discriminant

validity was demonstrated in the referred and non-referred samples and with

DSM IV-TR categories.

Stress Reactivity

     The stress reactivity responses were measured by the Trier Social Stress Test

(TSST).   The TSST, developed by Kirschbaum, is a standardized protocol for

inducing stress to subjects in studies and deliberately activates the HPA axis response

(Kirschbaum, 2010; Kirschbaum, Pirke & Hellhammer, 1993).   It was used in this

study to assess physiological reactivity to what the participant perceives as a

challenging situation which has the potential for being negatively judged by others

(Kudielka, 2008; Sullivan, 2008 – 2015).   In addition to invoking reports of negative

mood changes and increased anxiety, the HPA Axis response of endocrine,

immunological and other biological markers have been well documented (Stolerman,

2009).   It is widely used and involves a well-scripted task the participant is asked to

engage in hypothetically while others are evaluating their verbal response.   The task

consists of a brief preparation period (10 minutes), a test period where the participant

delivers a speech for a mock interview (5 minutes) and finally a period of calculating

mental arithmetic (5 minutes) in front of an audience.   While completing the tasks the

participants are also being video recorded to later assess their behaviors while under

stress.   In the original study their behavioral presentation will be evaluated according

to pre-established definition levels of:  humor, anxiety, non-verbal but otherwise

engaged, defensive, aggressive, scorn, frustration and distraught.

Salivary cortisol samples are collected at the following intervals:  prior to the task

(baseline), 15, 30, 45, 60, 75 and 90 minutes after the task has started (Sullivan,

2008-2013).   A mandatory part of the protocol is participants are debriefed after

completion of the test (Kirschbaum, 2010).   The TSST has been used with children,

adults, healthy subjects and clinical populations.   It is among one of the few tests that

assess both behavioral and psychobiological responses to situations that are perceived

as uncontrollable and socially threatening (Kudielka, 20008; Dickerson & Kemey,

2004).

HPA Axis Biomarker:  Salivary Cortisol

Salimetrics, Inc., Expanded Range High Sensitivity (ERHS) Salivary Cortisol

Enzymes Immunoassay Kit for research was used to collect samplings during the

TSST (Salimetrics, Inc., 2008).   Sensitivity and specificity of the Salivary Cortisol

Enzyme Immunoassay is excellent, as well as, a widely used solid technology, and the

“gold standard among researchers.   The laboratory procedures include duplicate

assays for each cortisol sample so that each saliva sample is tested twice on the assay

plate.   This renders two data points per sample and a mean for each sample tested in

duplicate.   Duplicate assays minimize the potential of with-in subject variability.

Each assay captures the full range of salivary cortisol levels (0.003 to 3.0 ug/dL) while

using only 25 uL of saliva per test (Salimetrics, Inc., 2008).   The lower limit of

sensitivity was determined by interpolating the mean minus 2 standard deviations

(SDs) for 10 sets of duplicates at 0 ug/dl standard.   For sensitivity, the minimal

concentration of cortisol that can be distinguished from 0 is < .003 ug/dL.   The

correlation between saliva (Salimetrics ERHS Salivary Cortisol EIA) and serum

(Diagnostic Systems Laboratory) was highly significant (r = .91, p = .0001).   During

testing, a potential hydrogen  (ph) indicator alerts if cortisol levels are artificially

inflated or lowered (< 3.5 or  > 9.0);  possible blood contamination is screened;  and

temperature is controlled.   Specificity of antiserum varies but is excellent.   The EIA

is accurate in diagnosis of Cushing Syndrome (Raff, Homan, & Skoner, 2003; Lucke,

Loucks & Berga, 2007).   Sensitivity/Specificity of 100 %/95 % was reported for

salivary cortisol to distinguish diagnosis of Cushing’s syndrome and obesity in an

age-matched sample of children (Castro, Elias, Martinelli, Antonnini, Santiago &

Moreira, 2000).   Various adult studies exist that measure cortisol levels in a variety of

psychological pathologies, emergency situations, and anxiety reduction interventions

(Harvey, Nathans, Bandiera & LeBlance, 2010; Rapaport, Schettler & Bresse, 2010).

In the primary study, a careful research protocol was followed.   A foam oral

swab was used to collect saliva and placed under the participant’s tongue for 2

minutes.   Approximately 1 mL. of saliva saturated the foam swab and then it was

inserted into a labeled collection tube and stored in a freezer.   The saliva samples

were placed into a cryostorage box with a minimum of 5 lbs. of dry ice and shipped

via Federal Express Priority for analysis by Salimetrics, Inc.   Samples were typically

submitted to Salimetrics quarterly (every 3 months) but more frequently when

necessary.   Shipping instructions according to www.salimetrics.com were followed.

Once analyzed, specimen data were entered into a spreadsheet by Salimetrics, Inc.

and reported to the Principal Investigator via e-mail in the form of an Excel file with

two values for each saliva sample and the mean in the form of a concentration (e.g.,

cortisol = 0.652 ug/dL).   Saliva samples were discarded according to Pennsylvania

Department of Environment Protection regulations 30 days after testing was

completed.   Data from the log were entered into MS Excel by study staff.   The only

identifier between the participant and the saliva sample was a predetermined label

provided by Salimetrics, Inc., who had no access to data to link the sample to the

participant.    It was the responsibility of the research staff to link the participant’s

unique identification number with the Salimetrics predetermined label.

Summary

Data for the proposed study include neonatal and demographic data from infancy

and self – report questionnaires, 8 sequential salivary cortisol samples from the TSST

standard laboratory protocol from the same participants at age 23 years.   The

measures are well developed with good psychometric values.   Questionnaire scoring

and subscale information are provided in the Appendix Measurements

Procedure

Researcher

In the study, the researchers were kept blinded to all identifying information

which was coded by the primary study staff.   The coded database was not associated

with identifying information.   The anonymous complete dataset for the study was

provided by the project director.

Recruitment

The infancy sample was recruited during the mother’s post-partum stay or during

the infant NICU stay.   The full term infants were identified during the post-partum

and in the same time frame as the preterm infants.   The criteria for recruitment were

neonatal diagnoses, birth weight < 1850 grams (4 pounds), maternal history (no

history of mental illness), and English as a primary language.   Parent(s) were then

invited to participate by research nurses.   Fewer than 10% of the parent(s) declined

participation.

Neonatal Group Criteria was:  (1) full term healthy infants (FT);  (2) preterm

infants without illness (healthy preterm group: HPT);  (3) preterm infants with medical

illness (bronchopulmonary dysplasia, respiratory distress syndrome, necrotizing

enterocolitis and sepsis: MPT);  (4) preterm infants with neurological illness

(meningitis, hydrocephalus, and grade 3 or 4 intraventricular hemorrhage:  NPT);  and

preterm infants who were small for gestational age (SGA).   Additionally specific

protocols for neonatal diagnostic labeling were used.   The range of premature infants

in weeks and grams were from 28.3 to 40 weeks gestational age and 1149 (2.5 lbs.) –

3420 (7.5 lbs.) grams in weight.   Socioeconomic status, incorporating both maternal

and paternal education and occupation, was measured with the Hollingshead Four

Factor Index.

Infants were followed in a series of research studies at ages 18 months, 30

months, 4 years, 8 years, 12 years, and 17 years.   At age 23, the original researchers

who had worked with the participants for more than 10 years, made recruitment

contact again.   Sample retention was high with 96% of the sample from age 17 years

and 85% of the birth sample participating at age 23 years.   The research protocol

included a home visit and hospital research laboratory visit.

Demographics

At age 23, demographic information was updated to include name, address, home

and cell telephone numbers, e-mail address, social security number, marital status,

education level/history, occupation/history, source(s) of financial support, lists of

people living in home, pregnancies (for female subjects) and number of children,

closet relative information, primary care provider information, and use of medical and

community support services.   The participant also filled out his or her own

Hollingshead Four Factor Index of Social Status.

       The Daily Hassles Scale-Revised (DHS-R), the Coping Response Inventory

(CRI-A), the Bar-On EQi and the Adult Self-Report (ASR) were administered to each

participant, as part of the larger study protocol of tests and questionnaires, during their

first laboratory visit.   Laboratory visits were scheduled according to standardized time

periods.   Each participant followed the same schedule or sequencing of

questionnaires, food breaks and examinations throughout the specified time period

allowing for consistency in protocol and comparison between participants.   This

battery of tests was administered after completion of the history and physical in a

small private room free from distractions.   The research assistants monitored, timed

and administrated the sequencing of tests according to study protocols.

TSST Protocol

The Trier Social Stress Test (TSST) followed standardized and extensive protocols

relating to timing during the day, timing with other testing and testing protocols.

Levels of cortisol are heightened in the morning and decline throughout the day.   To

reduce the potential of varied cortisol levels among subjects, administration of the

(TSST) was standardized to 1 pm for all participants.   Upon arrival the research nurse

(RN) greeted the participant, explained the laboratory protocol, confirmed consent and

addressed questions.   To avoid confounders in possible stimulation of the HPA axis,

the RN inquired about health-related limitations (colds, flu), physical activity,

smoking, medications, large meals, and hormonal treatments within the last 2 hours.

The RN had informed participants of these restrictions when the testing was

scheduled.   Participants were not informed in great detail about the exact procedure of

the TSST.   The RN inquired about the participant’s ideal occupation as this was

necessary information for the speech segment of the TSST protocol.   A baseline

salivary cortisol sample was collected 20 minutes after arrived (and the time noted)

followed by the TSST.

The participants were escorted to an assessment room and told there would be two

parts to this segment:  (1) mock job interview and (2) arithmetic problem.   All scripts

were followed verbatim.   For the mock job interview, the participant was instructed

by the researcher with a scripted standardized comment.   The participant was given

10 minutes to prepare for the interview and informed that no notes could be used and

they needed to make an impression on the committee (composed of 4 research

assistants) who would decide on the acceptance of the application.

The mock job interview was allowed 5 minutes, only one RA would talk and

direct the participant and the rest would be silent, with focused eye contact and a

serious demeanor that excluded any non-verbal encouragement.    A dummy video

camera was set up for the mock interview and the participant was asked to “please

 

step behind this line, and begin your speech.”   All research assistants followed

protocols for their roles, behavior, eye contact, facial expressions and speech.   If there

was a pause in the speech, then at 20-seconds the participant was told:  “You still have

 

time, please continue.”    Should there be another pause and the participant has

nothing to add then the RA will ask a standardized set of questions until the 5-minute

time period ended.   At the end of the job interview time the RA announces that the

second part of the test will begin and states it had nothing to do with the job interview.

The verbal instructions to the participant for the arithmetic test is also scripted and

in part includes:

“We ask you to count backwards to 0 in 13 number steps, starting at 1687.

       It is important to do it fast and correctly.   Should you miscalculate, you

      will be told to start again at 1687. Any questions? Please begin.”  

During this time the RA made notes on paper for errors in calculations.   If the

participant miscalculates, the RA will respond with “Error. 1687.”   After 5-minutes

of mental arithmetic, the RA stopped the TSST.

The second cortisol sample was collected 20 minutes after the TSST.   In the

interim, the RN conducted the health history interview.   After the collection of the

cortisol sample there was a break and then additional questionnaires were

administered and collected.   The third cortisol sample was collected after the

questionnaires were completed, approximately 30 minutes after the collection of the

second sample (50 minutes after the TSST).   The RN then begin the debriefing of the

TSST with:

     “The first thing I’d like to tell you is that the job interview speech and the

      arithmetic part were supposed to be difficult.   We did this to elicit a stressful

      situation for you.   When people encounter stressful events, their bodies respond

      with an accelerated heart rate and the body produces cortisol.  We will be

 

      measuring  your cortisol through your saliva.   We were not really recording

 

     audio or video for preverbal stress or behavioral analysis.   Also, the judge is

 

     actually one of our research assistants.   Let me introduce you to him/her.”

After, the debriefing, a healthy snack was given and further assessment inventories

were administered.   The physical examination followed and further salivary cortisol

samples were collected at 60, 75 and 90 minutes.

Summary

All measurements representative of the dependent and independent variables to be

utilized in this secondary analysis have been reviewed along with the original

study procedural protocols.   Use of this data, from the original measurements with

good psychometric prosperities, remains a strong fit to the aims of this study despite

the longevity of the original study design.

Analysis

All data was analyzed using the IBM SPSS Statistics Standard Grad Pack

(SPSS), Version 22 descriptive statistics.   The SPSS is used widely in social science

research to obtain descriptive statistics (mean, standard deviation, range), graphic

depiction, and hypothesis testing (Chi Square, ANOVA, ANCOVA, MANOVA and

MANCOVA.

First frequency statistics were performed for each variable. The frequency

and pattern of missing data were reviewed.   Missing data imputation was considered

when > 10 % data were missing.   Distribution skewness, kurtosis, box-plots were

examined and transformations considered when needed.   Correlations were examined

between all dependent variables.   Correlations > .80 were considered to behighly

correlated and decisions were made to use one variable (FGSE, 2016).   The

significance level wasp < = .05.   Analysis of Variance (ANOVA) was used to

determine any variations within and between the groups (LoBiondo-Wood & Haber,

2010) in all self-report variables.    AUCg was used with the cortisol endocrine data

as a measurement of hormonal output (Fekedulegn, et. al., 2007).   The AUCg is

the total area under the plotted curve of all the multivariate measurements and allows

for identification of the differences between the single measurements and the distance

of these measurements from ground (Spence, Cotton, Underwood & Duncan, 1976).

Measurements from ground (see Figure 11) take into consideration the distance from

zero instead of baseline data points and allows for total salivary cortisol response

comparisons between participants. (Fekedulegn, et. al., 2007).   Finally, the level of

effect power range recommended to reduce any Type I (is effect when there is

none) or II (no effect when there is) error at the 0.05 significance criterion is

0.80 – 0.95 (Lakens, 2013).   The study’s’ power was calculated at the 0.80

significance criteria.

Figure 11

Area Under the Curve with Respect to Ground (AUCg)

Macintosh HD:private:var:folders:xg:3yg_dxzx3c55v048jg5r8lpw0000gn:T:TemporaryItems:NP2016-3136743.004.jpg

Figure 11. From:   Catherine Raymond, Marie-France Marin, Anne Hand, Shireen Sindi, Robert-Paul Juster, and Sonia J. Lupien, “Salivary Cortisol Levels and Depressive Symptomatology in Consumers and Nonconsumers of Self-Help Books: A Pilot Study,” Neural Plasticity, vol. 2016, Article ID 3136743, 12 pages, 2016. Figure 4,p 9.  doi: 10.1155/2016/3136743 http://doi.org/10.1155/2016/3136743  Retrieved December 15, 2016.   This is an “open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.”

Aims and Hypotheses

Aim 1:  Compare effect of prematurity on stress, coping, emotional intelligence

and emotional health.   Compare independent categorical variable of birth groups with

the dependent continuous variables:  DHS summed scores ranging from 0-159 for

severity of stress, the CRI-A mean scores ranging from 20-80 + with M 50 (SD 10)

for avoidance coping, the Bar-On EQI total mean score of 100, (SD 15) for

emotional intelligence effectiveness and the ASR mean score of  > 60 for risk to

emotional health.

Hypothesis 1.   Higher self -reported stress scores, higher use of avoidance

coping styles, lower emotional intelligence scores and more emotional health

disorders will be found for the adults at age 23 years born prematurely compared to

the term-born adults.   Hypothesis 1 will be significant if DHS-R total scores are

higher, CRI-A avoidance t-scores are higher, EQi total scores are lower, and ASR

scores are higher for the premature groups.

Aim 2:  Compare the salivary cortisol response between premature and full-term

born infants in the social stress paradigm of the TSST.   Descriptive statistics

including line graphs by groups will be examined first.    Analysis of Variance

(ANOVA) will be used to determine differences in salivary cortisol responses as

measured by AUCg and at 6 sample times from the TSST paradigm at 15, 30, 45, 60,

75 and 90.

Hypothesis 2.   Adults at age 23 who were born prematurely will have a prolonged

stress recovery period for the TSST.   Hypothesis 2 will be significant if the AUCg

mean is higher during the stress recovery period for TSST in the prematurely born age

23 year old adult.

Aim 3. Examine the relationship between effect of emotional health and on the

stress recovery period of the TSST measured in salivary cortisol.   Three levels of

emotional health (normal > 59, borderline 60 – 63, and clinical > 64) as measured by

the ASR will be examined for the salivary cortisol samples across 6 sample times.

Descriptive statistics including graph lines by groups will be used followed by

ANCOVA where the effects of prematurity and gender will be controlled to

understand whether cortisol AUCg and slopes differ due to emotional health.

Hypothesis 3.  The stress recovery period for adults at age 23-years with

emotional health problems will be prolonged compared to adults without emotional

health problems (as determined by ASR t-scores) when prematurity is controlled.

Summary

The measurements used for this secondary analysis are consistent with the

aims of the primary study.   Measurements and procedures for all dependent and

independent variables were reviewed.   The measures have demonstrated good

psychometric properties.   In the original study, the research team developed and

trained on the procedure protocols.   Reliability between team members in the protocol

were consistently assessed and were >/= 90 %.   The design of this study allows for

correlational and multivariate modeling.   The use of neonatal data enables predictive

analysis.

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