stress and reproductive failure_evolutionary approach

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S272

Stress and reproductive failure: An evolutionary approach with

applications to premature labor

Samuel K. Wasser, PhD

Seattle, Washington

This article takes an evolutionary approach to the study of reproductive failure, drawing attention to the im-

portance of reproductive failure among mammals as a means of t iming reproduction in response to a vari-

able environment.These concepts also apply to the diagnosis and treatment of prematurity, because before

the advent of modern medicine most premature births probably constituted failed reproduction. Problems in

the diagnosis and treatment of reproductive failure are described, with specific parallels drawn between the

diagnoses and treatments of infertility and prematurity. (Am J Obstet Gynecol 1999;180:S272-4.)

Key words: Infertility, preterm labor, stress

Studies attempting to show a causal relationship be-

tween psychosocial stress and infertility have had several

problems. First, investigators have often lumped all fertil-

ity disorders together.1 Because infertility is a multifacto-

rial entity, lumping all fertility disorders together is likely

to dilute the magnitude of the stress effect. A similar prob-

lem may result from studies of prematurity because of the

large number of potential causes for this condition.2

Second, many study designs examining the relationship

between stress and reproductive failure have been unable

to separate cause from effect.3-5 Infertile couples gener-

ally have emotional distress as a result of their infertility.

This results in a positive correlation between infertility and emotional distress, regardless of whether stress is a

cause or an effect. Again, the stressfulness of premature

birth causes similar design problems for retrospective

studies of prematurity. Third, not all stressors that induce

a stress response are necessarily relevant to reproductive

failure; some stressors may be more likely than others to

induce reproductive failure.6-8 Based on the classic work

of Selye,9 however, stress is commonly defined as a “spe-

cific syndrome that is nonspecifically induced.”

Wasser et al7 developed a study to address these design

problems in investigating the relationship between stress

and infertility that should also be relevant to studies of

prematurity. They assumed that all infertile women facestress resulting from their infertile condition. However,

infertility disorders mediated by the neuroendocrine sys-

tem, as opposed to more anatomic fertility disorders, were

argued to be most likely to result from psychosocial stress.

Most known forms of reproductive failure among mam-

mals in response to the environment appear to be medi-

ated through the neuroendocrine system, with little or no

clear anatomic component (eg, such functional abnor-

malities of the hypothalamic-pituitary-ovarian axis as sec-

ondary amenorrhea, luteal-phase deficiency, and hyper-

prolactinemia).8,10-15 In contrast, origins predominantly

anatomic in nature (eg, pelvic adhesions, proximal or dis-

tal tubal obstructions, tubal ligation, moderate to severe

endometriosis, and anatomic disorders of the cervix or

uterus) should be irrelevant to any adaptive reproductive

failure model because they tend to be irreversible without surgical intervention. These assumptions led to the pre-

dictions that infertile women with diagnosed neuro-

endocrine disorders would report higher levels of psycho-

social distress (distress beyond that induced by their

infertile condition) than would infertile women with

anatomic disorders. Moreover, if stress caused these neu-

roendocrine disorders, control subjects—women who do

not wish to become pregnant and therefore lack the stress

of being infertile but have the same neuroendocrine dis-

orders as women in the neuroendocrine infertility

group—also would report levels of psychosocial distress

significantly higher than seen in infertile women with

anatomic disorders. The 2 predictions generated by thishypothesis (those regarding differences between infertil-

ity groups and those regarding differences among infer-

tility groups and the control subjects) made tests of this

hypothesis particularly robust.

These expectations were supported by study results.

Patients with neuroendocrine infertility and control sub-

jects both reported significantly higher levels of stress

than did women with anatomic infertility disorders.

Moreover, the most salient stressors distinguishing these

diagnostic groups were those revolving around social en-

vironment.7

From the Division of Reproductive Endoc rinology, Depar tment of Obstetrics and Gynecology, University of Washington.Reprint requests: Samuel K. Wasser, PhD, Division of Reproductive Endoc rinology, Department of Obstetrics and Gynecology, PO Box 354693, University of Washington, Seattle, WA 98195.Copyright © 1999 by Mosby, Inc.0002-9378/99 $8.00 + 0 6/0/91055



Volume 180, Number 1, Part 3 Wasser S273 Am J Obstet Gynecol

Why should the environment play an important

role in reproductive failure?

Fifteen percent of couples are infertile,16 and >50% of

all conceptions spontaneously abort.17 Among all births,

7% are premature or of low birth weight infants (near

failures). These rates of reproductive failure may seem

high, yet they are comparable to those observed in a wide variety of mammals.11,18-21 What do differ, however, are

the explanations for these failure rates. Physicians typi-

cally view such failure in human beings as a pathology

that has little to do with the environment. Ecologists and

evolutionary biologists, on the other hand, argue that a

significant portion of the high reproductive failure rates

seen among mammals results from adaptive mechanisms

that evolved to safeguard the large mammalian invest-

ment in reproduction by controlling the timing of repro-

duction with respect to environmental hardship.6,11,20-22

For example, wild baboons breed year round but have a

distinct birth peak at the ecologically most optimal time

of the year23; females of high social status also conceive

more readily than do low-ranking females.14,15 These dif-

ferences occur in large part through physiologic mecha-

nisms that make successful implantation endocrinologi-

cally more difficult under predictably harsh conditions

(eg, suboptimal season or low social status).14,15

Accordingly, only the physically and socially healthiest of

nonpregnant and nonlactating adult female baboons are

able to conceive during these harsh times. Suppression is

maintained until reproductive conditions improve, limit-

ing the large investment in reproduction to conditions

under which the chances of success are greatest.23

Reproduction may be suppressed at all stages, from de-layed menses to ovulatory and pregnancy failure and may

include offspring death (including premature delivery,

abandonment, and infanticide). Such failures reportedly

occur in response to a wide variety of cues reflecting

harsh reproductive conditions in birds and mammals.

These include photoperiod (reflecting seasonal chan-

ges),19 body fat (reflecting nutritional status),24 embry-

onic or fetal malformations,25 and perceived stress result-

ing from aggression, social ostracism, or other life

pressures.6,12,13,21,26,27 Social pressures are among the

most consistently and dramatically observed stressors af-

fecting reproduction, particularly among highly social

species that breed throughout the year or have only a sin-gle dominant breeding pair.21 The stressfulness of social

pressures appears to stem from their enduring nature,

combined with the threat to survival from loss of social

support in socially living mammals. These views are con-

sistent with results of the Wasser et al7 stress and infertil-

ity study on women cited previously.

Several factors suggest that the adaptive reproductive

failure model also applies to human beings: (1) The adap-

tive value of physiologic mechanisms to conserve repro-

ductive effort is directly related to the amount of invest-

ment required for reproduction. Human reproduction

requires a relatively large amount of reproductive invest-

ment compared with that of other mammals because of

their long gestation and highly altricial (immature) sin-

gleton young. (2) The human pattern of reproductive

failure is quite similar to patterns observed among nu-

merous other mammals with respect to timing and failure

rates.11,14,15,17-21 (3) The same physiologic mechanismsthat commonly produce reproductive failure in response

to environmental stressors in mammals (eg, through the

hypothalamic-pituitary-ovarian axis11,14,15,19,20) also pro-

duce reproductive failure in women.7,8,12,27,28 (4) Human

beings evolved under social and ecologic conditions simi-

lar to those of other mammals that show stress-related re-

productive failure in response to social pressures.29-33 (5)

Human populations historically have been resource lim-

ited, and individuals appear to have regulated their re-

production and thus population growth in response to re-

source limitation.34-38 (6) Although the environment of

human evolutionary history has changed dramatically in

a relatively short time, many relevant factors (eg, parental

motivation to ensure an environment that promotes off-

spring survival, the importance of social living and status,

and the biologic mechanisms that evolved to respond to

these perceived environmental stressors) almost certainly

have remained in place.39,40 For these reasons Wasser et al

also expect the functionality of social relations between

key individuals in one’s social network (eg, parents,

spouse, close friends) to be salient stressors causing re-

productive failure in contemporary women.7

Clinical significance of the adaptive reproductive

failure model

The extent to which the adaptive reproductive failure

model applies to human beings reflects the likely effective-

ness of acute or long-term environmental therapy (eg, di-

etary, stress-reduction, and psychosocial therapies) as a

treatment for some forms of reproductive failure.

However, several factors have limited the acceptance of

psychosocial or other stress-reduction therapies compared

with a rapidly expanding biomedical technology: (1)

There are few data to challenge the general belief by physi-

cians that stress is not causally linked with reproductive

failure to a significant degree, making psychologic treat-

ment unproven and unattractive.41,42 (2) Psychosocial

problems tend to be more difficult for patients to acknowl-edge than biomedical problems. (3) Psychosocial therapy

is relatively more time consuming, and requires consider-

ably more personal effort on the part of the patient, than

most biomedical treatments (which are painted by the

media as a relatively rapid treatment for infertility). (4)

Gynecologists and obstetricians are not trained to diag-

nose psychologic problems or to provide psychologic ther-

apies. All these factors put pressure on physicians to rely

primarily on biomedical treatments for reproductive fail-

ure in this highly competitive field of practice. Despite our

vast knowledge of reproductive physiology, however, suc-



cess rates of these procedures remain quite low,43 and

treatment of prematurity is no exception to this rule.2,44

To the extent that natural reproductive filtering mech-

anisms exist, a purely biotechnologic approach may treat

only the physiologic symptoms that are suppressing a

woman’s fertility, without eliminating the stressors that

triggered the symptoms. Such patients may in turn faceelevated risks later on in the reproductive event for spon-

taneous abortion, premature birth,45 or production of in-

fants with birth defects.16,46,47 Demands of infant care on

an already stressed parent could also increase the proba-

bility of providing an emotionally and physically un-

healthy postnatal environment for the offspring.48-50 On

the other hand, biomedical treatment for reproductive

failure, in conjunction with diagnosis and appropriate

treatment of psychosocial stress when necessary, could

markedly improve overall reproductive outcomes (eg,

fertility, term gestation, and nurturing).

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