Effect of Pregnancy and Age on Alopecia in Adult Female Baboons (Papio hamadryas spp)

Abstract

Alopecia occurs frequently in captive populations of nonhuman primates. Because multiple factors can play a role in alopecia, a better understanding of its etiology will help identify potential welfare concerns. The purpose of this study was to investigate risk factors for alopecia in a breeding colony of baboons with a focus on pregnancy and age. Alopecia was scored on a scale of 0 (no alopecia) to 5 (severe alopecia) in 253 female baboons during routine physicals. The subjects ranged in age from 4 to 23 y (Mean = 9.6) and were categorized as pregnant (n = 83), nursing (n = 60) or control (n = 110). Resulting alopecia scores were combined into 2 categories (mild = 0 or 1; moderate = 2 or 3); no animals scored a 4 or 5. Significantly more pregnant females had moderate alopecia than did control females. There was no effect of age on alopecia. An unexpected outcome was that among nursing females, more of those with female infants had moderate alopecia than did those with male infants. The impact of the infant’s sex on alopecia may be due to sex differences in maternal contact or maternal investment. This information adds to our understanding of alopecia risk factors in captive nonhuman primates.

Alopecia, or hair loss, is frequently reported to occur in captive populations of nonhuman primates (NHP). The degree and pattern of hair loss can vary from small, localized patches to large bare areas covering most of the body. Although hair-plucking is often the default diagnosis,³⁷ alopecia is a multifaceted condition that is affected by a variety of both intrinsic and environmental variables including species, sex, age, social rank, pregnancy, housing, season, behavior, stress, hormonal changes, nutritional deficits, infection, and parasites.^{5,6,9,10,12-14,21,25,28,30-33,37-41,43,47-49,53,56,60,62} Because coat quality and alopecia can be impacted by multiple factors, identification of potential causes can be challenging.

Hair undergoes cyclic regrowth that is typically viewed as recurring phases: the anagen, catagen, and telogen phases, followed by hair shedding.^15,20,44,49 The anagen phase is the active growth phase involving cell renewal. The duration of this phase can determine hair length.^{15,20,44,50,51} In humans, hair grows at a rate of approximately 0.65 to 2.2 cm/mo.³⁵ Catagen is the degradation phase during which the hair follicle undergoes a form of programmed cell death, is shortened in length and reduced in volume.^15,20,50 The telogen phase is the resting phase during which the hair shaft matures into a club hair under which a new germ layer develops.^15,50 This is followed by hair shedding.^15,20,49 In humans, most of an individual’s hair (approximately 60% to 90%) is in the anagen phase, approximately 5% to 35% is in the telogen phase, and the remaining percentages are in the catagen and hair shedding phases.^{15,20,44,50,51}

Telogen effluvium is a disorder characterized by significant hair shedding resulting from a disruption of the hair cycle and excessive loss of telogen hairs.³⁶ Different functional types of telogen effluvium range from chronic to acute and can be influenced by factors such as a major illness, high fever, physiologic stress, drug use, or malnutrition.^20,36,52 In women, telogen effluvium is also associated with pregnancy.^17,20,45 In the later stage of pregnancy, the percentage of hairs in the telogen phase can increase to 30% to 50%,^44,51 followed by accelerated diffuse hair shedding.⁴⁴ Hair loss resulting from postpartum telogen effluvium can begin approximately 1 to 5 mo after delivery and can last approximately 2 to 6 mo.^15,17,45,54 Although the duration and location of postpartum alopecia can vary,⁵⁴ the hair cycle eventually returns to normal.⁴⁴

As with humans, NHP can also experience hair loss during and after pregnancy. In rhesus monkeys (Macaca mulatta), hair loss was observed throughout the gestation and perinatal periods, becoming most pronounced during the final months of pregnancy and into the month after parturition.^6,13,14 Overall, pregnant females were significantly more likely to have alopecia than were nonpregnant females.^6,40,41 Regrowth occurs shortly after parturition,¹³ with one study reporting only a moderate difference in coat condition between postpartum females and control females that were not pregnant or nursing.⁴⁰ However, not all females experience hair loss during pregnancy or the perinatal period. Such differences in hair loss may be due in part to differences in maternal investment (i.e., the provision of resources to offspring at some cost to the parent) during pregnancy.¹⁴ To our knowledge, genetic effects on alopecia have not been investigated.

Hair loss has also been associated with aging. In humans, scalp hair density and mean anagen growth rate gradually decrease with age.⁵⁸ Female pattern hair loss, characterized by diffuse hair thinning over the scalp, increases with advancing age,⁵⁷ while the hair density, diameter, and tensile strength decrease.^29,42 In NHP, hair coat condition also tends to worsen with age;^{6,12,38,49,56} some studies have reported that monkeys with alopecia were often significantly older than those without alopecia.^25,31 Older animals also had an increase in the percentage of hairs in the telogen phase, which is a pattern of hair loss that is characteristic of chronic telogen effluvium.²⁵ One study comparing geriatric (mean age = 25.4 y) and adult (mean age = 9.8 y) rhesus monkeys reported that the older monkeys had higher frequencies of skin abnormalities (for example, scaling, wrinkling, laxity of the skin) as well as alopecia.²⁶ However, in other studies, hair coat quality did not change linearly with age,^32,62 and still others reported either no effect of age on alopecia^37,59 or higher levels of alopecia in the younger animals.⁴¹

Hair loss is readily apparent, and its persistence may result in management or clinical responses that are not consistent with animal wellbeing.⁴ Therefore, a better understanding of the etiology of alopecia in captive NHP will help to identify welfare concerns. Because alopecia commonly occurs in pregnant women and NHPs,^{6,13,14,17,20,40,44,45,51} the purpose of this study is to further assess the incidence of alopecia in NHP during pregnancy. Due to its association with alopecia, age is also included as a variable. Much of the research on alopecia in NHP has focused on macaque monkeys.^{5,6,10,12-14,21,30-33,37-40,47,48,53,56,60,62} Even though baboons are commonly used as models in a wide range of research areas,¹¹ less is known about alopecia in these animals.⁴¹ Therefore, this study assesses animals from the genus Papio to attain a broader perspective of the impact of pregnancy and age on alopecia. We predict that both age and pregnancy will have an impact on hair loss.

Materials and Methods

Subjects.

This study evaluated adult female olive baboons (Papio hamadryas anubis) and olive/yellow baboons (P. h. cynocephalus) crosses (n = 253). The subjects ranged in age from 4 to 23 y (mean = 9.6 y). Of the 253 subjects, 83 were pregnant, 60 had nursing infants, and 110 were neither pregnant nor nursing (controls). The gestation period in baboons lasts approximately 6 mo.^2,19,61

Housing.

The subjects were socially housed in 35 groups consisting of one adult male, 5 to 13 adult females, and their associated offspring. They were housed in outdoor enclosures measuring approximately 6 × 9 m, containing heated indoor access measuring approximately 6 × 3 m, as well as perches, hanging barrels, and various enrichment items. The subjects were fed Purina 5 LEO biscuits (Purina Mills, Gray Summit, MO) 2 times per day. Their diet was supplemented with fruit, vegetables, grains, and cereals. The facility is accredited by AAALAC International, and the animals were maintained in accordance with the Guide for the Care and Use of Laboratory Animals.²⁷ The research was approved by the Texas Biomedical Research Institute’s Institutional Animal Care and Use Committee and complied with the laws and regulations of the United States Animal Welfare Act.

Procedures.

Assessments were conducted opportunistically when the animals were sedated for routine physical examinations that were performed between March 2018 and February 2019. The pregnant females were sampled at an average of 80 d prior to delivery (range: 7 to 170 d). Nursing females were sampled at an average of 120 d postpartum (range: 12 to 306 d). Alopecia was scored on a scale of 0 to 5 using the “rule of nines” method, with 0 being no alopecia and 5 being severe alopecia.³ Each animal was scored once. A single observer scored all of the animals. The date of parturition and sex of the fetus (pregnant females) or infant (nursing females) were obtained from the animal records.

Data analysis.

The majority of the baboons had an alopecia score of 1 or 2, with few having scores of 0 or 3, and none having a score of 4 or 5 (Figure 1). Therefore, the subjects were consolidated into 2 alopecia categories: mild (score of 0 or 1) and moderate (score of 2 or 3) for further analyses. Statistics were conducted with SYSTAT 13 (SYSTAT Software, Chicago, IL). Statistical significance was based on a P-value of < 0.05.

Figure 1.

Overall alopecia scores

A χ² test was used to examine study group (pregnant, nursing, control) differences in alopecia levels (mild, moderate). Because age was not normally distributed in the study groups, a nonparametric Kruskal–Wallis H test was used to examine study group differences in age, and a Mann–Whitney U test was used to compare alopecia level (mild, moderate) with age.

Because research has shown that hair loss in rhesus monkeys is most pronounced during the final months of pregnancy, with hair growing back postpartum,^6,13,14 logistic regressions were conducted separately on the pregnant and nursing study groups to further assess the effect of pregnancy on mild or moderate alopecia levels. Variables specific to the 2 study groups included days prior to birth (pregnant females) and days postpartum (nursing females). Additional group-specific variables included sex of the fetus (pregnant females) and sex of the infant (nursing females). For the logistic regressions, the group-specific variables and their interactions were initially entered into each model. A backward elimination procedure was used to determine the “best-fit” model. Variables were assessed for their contribution to the model by evaluating the change in total variance accounted for (R squared) when that term was removed. Terms with the highest P values were removed first.

Results

Across Groups.

Alopecia scores were significantly different across study groups (χ²(2,253) = 10.960, P < 0.005). A significantly larger proportion of pregnant females had moderate alopecia as compared to control females (χ²(1,193) = 10.993, P < 0.005). Moderate alopecia was not significantly different between nursing and control females (χ²(1,170) = 3.120, P < 0.10; Figure 2). There was no significant difference in age across study groups (H(2) = 1.994, P > 0.30) and there was no effect of age on alopecia level (U = 5,879, P > 0.80).

Figure 2.

A comparison of alopecia across groups

Within Groups.

Sex of the infant was associated with greater alopecia in nursing females. Significantly more mothers that were nursing female infants had moderate alopecia (40%) in comparison to those that were nursing male infants (13%; b = –1.466, P < 0.05). No other predictors were significant.

Discussion

This study supports previous findings that alopecia is a common condition in healthy, pregnant, nonhuman primates.^{5,13,14,40,41} Although the percentage of pregnant baboons with moderate alopecia (36%) was lower than that reported in pregnant rhesus macaques (63%),⁴⁰ significantly more pregnant baboons had moderate alopecia in comparison to nonpregnant animals. This result supports previous findings of higher levels of hair loss in pregnant or postpartum human and nonhuman primates.^{6,13-15,17,20,40,41,44,45,51,54} The baboons in the present study may be experiencing a form of pregnancy-related telogen effluvium. However, the hair gradually grows back postpartum, as observed in the nursing females whose percentage with moderate alopecia was not significantly different from that of nonpregnant controls.

In contrast, age did not contribute to alopecia levels. This finding contradicts previous studies reporting that alopecia typically increases with age in both humans^29,42,57,58 and NHPs.^{6,12,38,49,56} The broad age range of animals sampled in the current study (4 to 23 y) should have been sufficient for detecting an age effect. These data suggest that baboons maintain their hair coat as they age. A previous study on baboon alopecia reported that younger animals were more likely to experience hair loss than were older animals.⁴¹ However, the age range in that study included both juveniles as young as 2 to 3 y of age and males. These 2 differences may influence the relationship between age and alopecia in baboons.

A surprising finding in this study is that the infant’s sex influences alopecia. A greater proportion of mothers nursing female infants had moderate alopecia as compared with those nursing male infants. However, the sex of the fetus did not affect alopecia in pregnant females, suggesting that the effect of infant sex on alopecia occurs postpartum. Postpartum alopecia could be due to the friction and rubbing of the hair when infants are in physical contact with their mothers, either causing additional alopecia or restricting postpartum regrowth. In this case, differences in alopecia based on the infant’s sex may be due to sex differences in maternal contact. Often male infants have less contact with their mothers than do female infants, as reported in captive Japanese macaques (Macaca fuscata)¹⁶ and captive baboons.⁷ Similarly, in wild baboons, mothers of male infants were more tolerant of infant independence than were mothers of female infants.⁴⁶ Male infants were also more active and had more infant-initiated changes in mother-infant contact.⁴⁶ However, this male-biased separation was not reported in all studies. In captive hamadryas baboons (Papio hamadryas hamadryas), mothers broke contact with their female infants more often than with their male infants²² and sex differences in separation from the mother was not observed in captive rhesus macaques¹⁴ or wild yellow baboons.¹

Alternatively, differences in maternal alopecia based on the infant’s sex could be due to differential maternal investment. For example, in alopecic rhesus monkey mothers, hair cortisol concentrations (indicators of stress) in pregnancy were positively correlated with infant birth weight, infant growth rate, and milk yield volume; this association was not present in mothers without alopecia.¹⁴ Maternal investment can be measured by variables such as infant birth weight, infant growth weight, milk production, milk content, and interbirth interval.^{8,14,18,23,24,34,55} Although some studies reported no infant sex differences in birth or growth weight in captive macaque monkeys,^34,55 other studies reported that male rhesus infants weighed significantly more than females at birth, with relative weight increasing during the first year,⁸ suggesting that in this case maternal investment was directed toward male offspring. In contrast, other studies reported that rhesus monkey mothers rearing daughters had higher calcium concentrations in milk than did mothers rearing sons²⁴ and in low-ranking mothers, daughters made more nipple contacts, suggesting that female infants were obtaining more milk.¹⁸ However, one study reported that although rhesus monkey mothers of females produced more milk, mothers of sons produced milk of higher energy density; therefore, available milk energy was the same for sons and daughters.²³ Another indicator of maternal investment is interbirth interval, or the timing between subsequent births. Although studies of macaque monkeys reported no overall differences in interbirth interval,^18,55 low-ranking mothers raising female infants typically did not give birth the following year; this did not occur in high-ranking mothers or mothers with sons.^18,34 These results suggest that raising female infants can be more costly, at least in low-ranking mothers. Due to colony management procedures, maternal rank, natural interbirth interval, and infant birth weight and growth rates are not known for the animals in the present study. However, these important variables should be assessed in future studies.

In conclusion, our study found that pregnancy was a risk factor for alopecia in captive baboons. However, in our population, age did not contribute to alopecia, which may be unique to baboons. Moderate alopecia was shown to be more common in mothers with female infants than in those with male infants. This difference could be due, in part, to greater contact with female infants or to increased maternal investment directed toward daughters. The current study focused on pregnancy as a risk factor for alopecia, but another useful study would be to examine whether alopecia in baboons correlates with measures of welfare, such as indicators of stress. Future research in this area could be useful for evaluation of animal wellbeing.