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Comparative Study
. 2016;55(3):277-90.

Effect of Indoor Compared with Outdoor Location during Gestation on the Incidence of Diarrhea in Indoor-Reared Rhesus Macaques (Macaca mulatta)

Hanie A Elfenbein  1 , Laura Del Rosso  2 , Brenda McCowan  1 , John P Capitanio  3
Affiliations
Comparative Study

Effect of Indoor Compared with Outdoor Location during Gestation on the Incidence of Diarrhea in Indoor-Reared Rhesus Macaques (Macaca mulatta)

Hanie A Elfenbein et al. J Am Assoc Lab Anim Sci. 2016.

Abstract

Behavior and health, including the incidence of chronic idiopathic diarrhea, can vary widely among NHP reared indoors. We hypothesized that factors during gestation account for some of the variability in chronic diarrhea risk that cannot be explained by postnatal environment, genes, or known physiologic deficits. We hypothesized that, among macaques reared indoors postnatally, outdoor housing during gestation (when the dam engaged with a large, species-typical social group) would be protective against diarrhea as compared with gestation experienced in an indoor setting. We also hypothesized that exposure to routine husbandry and veterinary care in utero would increase diarrhea rates in offspring. We built models to test the influence of specific events during pregnancy as well as their interactions with anxiety-related genotype as a way of understanding gene×environment interaction on the development of diarrhea in indoor-reared rhesus macaques. Although previous reports have suggested that rearing by the mother in an indoor environment is preferable to nursery rearing, we found that whether gestation occurred indoors (in single or pair housing) or outdoors (in a large social group) better explained the variability in diarrhea rate in our study population of indoor-reared macaques. Furthermore, the diarrhea incidence was associated with nervous temperament and serotonin transporter promoter genotype. Several significant interactions indicated that some of these effects were specific to subsets of animals. Our results demonstrate that the prenatal environment can have unexpected lasting health consequences.

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Figures

Figure 1.
Figure 1.
The hypothalamic–pituitary–adrenal (HPA) axis is an important regulatory system (green solid arrows) for cortisol, a hormone involved in the stress response as well as metabolism, inflammation, and other important homeostatic functions. The HPA axis operates through negative feedback (red dashed arrows), which may be blunted or sensitized due to chronic stress during development.
Figure 2.
Figure 2.
Description of variables.
Figure 3.
Figure 3.
Breakdown of subject pool. (A) Rearing type and gestation location. To be classified as gestated indoors, at least 75% of the duration of the pregnancy was spent indoors; otherwise the offspring was classified as outdoor gestated. Postnatally, all infants in this study were reared indoors, either by their mother or in the nursery. (B) Reasons for animals exiting the study. Alive, alive at end of study period (that is, ‘aged out’ of cohort); died or culled, macaque died or was culled for medical reasons; project, macaque was assigned to an active project and thus removed from the cohort; shipped, macaque was sent to another facility and thus lost to follow-up. A macaque's stint in the study population varied between animals and was included in all models.
Figure 4.
Figure 4.
Mean number of episodes of diarrhea according to rearing type (mother, reared indoors by mother; nursery, reared indoors in nursery) or gestation location. *, P < 0.01; bar, SE.
Figure 5.
Figure 5.
Number of diarrhea episodes in male and female macaques according to the presence (filled symbols) or absence (open symbols) of the serotonin transporter short allele. *, Interaction effect (P < 0.05); bar, SE.
Figure 6.
Figure 6.
Mean number of diarrhea episodes according to (A) the sex of the macaque and presence (black) or absence (gray) of the low-expression MAOA allele, (B) the gestation location (indoor, hashed; outdoor, open) and MAOA genotype, and (C) gestation location and sex of animal. Because the gene is sex-linked, male macaques have only a single allele (either high or low expression). Bar, SE; interaction effect, P < 0.05.
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