Evaluating Stress during Pregnancy: Do We Have the Right Conceptions and the Correct Tools to Assess It?

Table 1

Stress during pregnancy, cortisol levels, and its association with pregnancy outcome. Adverse outcome of stress for the pregnancy was reviewed in the latest bibliography in order to know the type of association that stress causes on pregnancy and the type of mood disorder (anxiety and depression) which were the tools applied to assess stress during pregnancy. In italics the adverse outcomes related to stress and depression are shown, while in bold those adverse outcomes among anxiety or the combination of the mood disorders are shown. On the psychometric test column the double asterisks show those studies in which an inventory of stress was used. From [12–17] those researches used on animal models to study the prenatal stress long term effects on the offspring are obtained. Besides this table shows the studies assessing physiological stress with cortisol measurements; different tools were found along the studies and different trimester of gestation.

Reference	Stress and adverse pregnancy outcome		Association with cortisol		Type of adverse outcome	Mood variables	Tools assessing stress; Psychometric test/biomarkers	Gestational age	Studies with human or animal
	Yes	No	Yes	No
[15] Huizink et al. (2002)	X				Infant temperament at 3 and 8 months of age	Stress	Stress: perceived stress and pregnancy anxiety; Infant: direct observation and by parent report		Human
[23] DiPietro et al. (2002)	X				Fetal motor activity	Stress	Affect Intensity Measure, Daily Stress Inventory, Pregnancy Experience Scale; Fetal heart rate, fetal movement		Humans
[1] De Weerth et al. (2003)	X				Premature birth	Stress			Humans
[2] Sandman et al. (2006)	X				Preterm birth (19 weeks of gestation)	Hormonal stress	CRH and plasma cortisol		Human
[3] Nepomnaschy et al. (2006)	X		X		Spontaneous miscarriages	Hormonal stress	Cortisol in urine		Human
[4] Grandi et al. (2008)	X				Preterm birth	Stress	Focus group and psychosociocultural interview		Human
[5] Lobel et al., (2008)	X				Preterm birth	Pregnancy specific stress	Prenatal Distress Questionnaire, Prenatal Life Events Scale, State Anxiety Subscale of the State-Trait Personality Inventory, Prenatal Health Behaviors Scale		Humans
[7] Kramer et al. (2009)		X		X	Preterm birth	Stress	Perceived Stress Scale, Pregnancy-Related Anxiety by Dunkel-Schetter, Rosenberg Self-Esteem Scale, Life Orientation Test, Center; for Epidemiologic Studies Depression; CRH, placental histopathology and maternal hair cortisol		Human
[26] Salacz et al. (2012)	X			X	Anxiety and depression	Feelings of distress	Beck Depression Inventory, State-Trait Anxiety Inventory, Perceived Stress Scale, a Likert-like scale for fear of delivery, a structured interview to assess health and socioeconomic status Plasma cortisol		Human
[27] Buss et al. (2012)	X		X		Emotional problems in children	Hormonal stress	Child Behavior Checklist; Cortisol in saliva	15 weeks of gestation	Human
[14] Butler et al. (2002)	X				Fetal programming, neurological disorders, psychiatric disorders, and metabolic and cardiovascular problems	Stress	Glucocorticoid		Animals
[28] Van den Hove et al. (2005)		X			Anxiety and depressive-like behavior in the offspring	Stress	The open field test, the home cage emergence test, and the Forced Swim Test (offspring); Plasma corticosterone (pregnancy)		Animals
[29] Kraszpulski et al. (2006)	X				Differences in amygdalar nuclei, suggesting that this may predispose to fear related behaviors such anxiety	Stress			Animals
[30] Yang et al. (2006)	X				Altering synaptic plasticity and enhancing the effects of acute stress on synaptic plasticity in the hippocampus, which may be the mechanism for the impaired spatial learning and memory in young rat offspring	Stress	Morris water maze		Animals
[31] Pawluski et al. (2011)	X				Increased anxiety-like behavior, decreased; depressive-like behavior, and lower corticosterone levels	Stress	Elevated Zero Maze (anxiety), Forced Swim Test (depression)		Animals
[18] Howerton and Bale (2012)	X				The male offspring displayed anhedonia and increased sensitivity to selective serotonin reuptake inhibitor; treatment. Long term alterations in central corticotropin-releasing factor (CRF) and glucocorticoid receptor (GR) expression, as well as; increased hypothalamic-pituitary-adrenal (HPA) axis responsivity, were present in these mice and likely contributed to an elevated; stress sensitivity	Stress	Comparisons between placental PCR array and epigenetic analyses		Animal
[32] Brunton and Russell (2008)	X				Low weigh and hyperinsulinaemic at 6 months of age following oral glucose load in the female and high blood glucose in adult males	Stress			Animals
[33] Orr et al. (2007)	X				Preterm birth	Anxiety	Prenatal Social Environment Inventory		Human
[7] Kramer et al. (2009)	X				Preterm birth	Anxiety	Perceived Stress Scale, Pregnancy-Related Anxiety by Dunkel-Schetter, Rosenberg Self-Esteem Scale, Life Orientation Test, Center for Epidemiologic Studies Depression; CRH, placental histopathology and maternal hair cortisol		Human
[34] Romo-González et al. (2012)	X				Pregnancy complications, hypertension, and preterm birth	Anxiety	State-Trait Anxiety Inventory; Serum cortisol, estradiol, and progesterone		Human
[34] Romo-González et al. (2012)		X			Low birth weight	Anxiety	State-Trait Anxiety Inventory; Serum cortisol, estradiol, and progesterone		Human
[35] Steer et al. (1992)	X				Preterm birth and low birth weight	Depression	Beck Depression Inventory		Human
[9] Field et al. (2004)	X				Preterm birth and low birthweight; The newborn’s biochemistry (except for epinephrine) was higher than the maternal biochemistry	Depression	Urine cortisol, norepinephrine, serotonin, epinephrine, and dopamine		Human
[36] Diego et al. (2009)	X				Preterm birth and low birth weight	Depression	Structured Clinical Interview for DSM-IV Axis I Disorders, The Center for Epidemiological Studies Depression Scale; Urine cortisol	18 weeks of gestation	Human
[37] Hompes et al. (2012)	X		X	X	Low birth weight	Depression	Anxiety and depression; Basal cortisol	Only first trimester but not third trimester	Human
[38] Wadhwa et al. (1993)	X				Birth weight and gestational age at birth	Stress and anxiety	Perceived Stress Scale, Hopkins Symptom Checklist, an instrument; assessing maternal fears and anxiety related to the; health of the baby, toward the labor and delivery process,; and confidence in the obstetrician and other; health care providers,; 1- and 5-minute Apgar scores		Human
[39] Brouwers et al. (2001)	X				Child development (three weeks postpartum and after 2 years)	Stress and anxiety	State-Trait Anxiety Inventory; Neonatal Behavioral Assessment Scale; Bayle Scales of Infant Development	32 weeks of gestation	Human
[40] Rieger et al. (2004)	X				Child development (three weeks postpartum and after 2 years)	Stress and anxiety	Neonatal Behavioral Assessment Scale		Human
[6] Harville  et al. (2009)	X			X	Preeclampsia	Stress and anxiety	Perceived Stress, state-trait anxiety coping style, life events, social support, and pregnancy specific anxiety; Plasma cortisol and CRH		Human
[41] Davis and Sandman (2010)	X		X	X	Elevated concentration of cortisol early in gestation was associated with a slower rate of; development over the first postnatal year and lower scores on the mental development index of the; BSID at 12 months; Elevated levels of maternal cortisol late; in gestation were associated with accelerated development over the first year and higher scores on the BSID; Elevated levels of maternal pregnancy specific anxiety early in pregnancy were independently associated with lower scores on the BSID at 12 months	Stress and anxiety	Bayle Scales of Infant Development (BSID), Mental Development Index and Psychomotor Development Index; Salivary cortisol	Only first trimester but not third trimester	Human
[42] Paarlberg et al. (1999)	X				Low birth weight	Stress and depression	Daily stressors, psychological and mental well-being		Human
[43] Davis et al. (2004)	X				Infant negative behavioral reactivity	Anxiety and depression	State-Trait Anxiety Inventory and Center for Epidemiological Studies Depression Inventory; Harvard Infant Behavioral Reactivity Protocol	32 weeks of gestation and 8 weeks after delivery	Human
[44] Pimentel (2007)	X				Urinary infection (anxiety), preterm birth (depression), and preeclampsia (family dysfunction)	Anxiety and depression	Test Goldberg (anxiety and depression) and APGAR scale (Appearance, Pulse, Grimace, Activity, Respiration)		Human
[8] Diego et al. (2006)	X		X		Low fetal weight	Stress, depression, and anxiety	Daily hassles, Center for Epidemiologic Studies Depression, and State-Trait Anxiety Inventory Scales; Urine cortisol and norepinephrine	Half of gestation	Human
[12] Vianna et al. (2011)	X				Preeclampsia	Stress, depression, and anxiety	Testing through in vitro proliferation assays; Testing through in vivo approaches		Humans
[45] Ruiz et al. (2003)				X	Stress	Plasma cortisol	Perceived Stress Scale	All gestational period	Human
[46] Sarkar et al. (2007)			X		Stress	Plasma cortisol and amniotic fluid	Not specified	17 to 18 weeks onwards	Human
[47] Buske- Kirschbaum et al. (2007)			X		Stress in preterm birth children	Salivary cortisol	Psychological Stress Test		Human
[48] Entringer et al. (2010)			X		Stress	Blood pressure, heart rate, and salivary cortisol	Trier Social Stress Test (TSST),; Perceived Stress Scale, and Center for Epidemiological Studies Depression Scale	Only first trimester but not third trimester	Human
[49] Kaasen et al. (2012)				X	Stress	Salivary and serum cortisol	Impact of Event Scale, General Health Questionnaire, and Edinburgh Postnatal Depression Scale	12–32 weeks of gestation	Human
[50] Voegtline et al. (2013)				X	Stress and well-being	Salivary cortisol	Spielberger Trait Anxiety Scales, Center for Epidemiologic Survey Depression Scale, Pregnancy Experiences Scale, World Health Organization Well-being Index Five	Second half of gestation	Human