Effect of Chronic Social Stress on Prenatal Transfer of Antitetanus Immunity in Captive Breeding Rhesus Macaques (Macaca mulatta)

Abstract

Because tetanus can cause significant morbidity and mortality in NHP, colonywide vaccination with tetanus toxoid is recommended for outdoor breeding colonies of rhesus macaques, with primary immunizations commonly given to infants at 6 mo of age followed by booster vaccines every 10 y. Maternal antibodies are thought to offer protective immunity to infants younger than 6 mo. However, historical colony data from the Yerkes National Primate Research Center show a higher incidence of tetanus among infants (≤ 6 mo old) born to subordinate dams. Whether this higher incidence of infantile tetanus is due to a higher incidence of trauma among subordinate animals or is a stress-induced impairment of maternal antibody protection is unknown. Studies in other NHP species suggest that chronic exposure to social stressors interferes with the receptor-mediated transplacental transfer of IgG. Therefore, the primary aim of this study was to determine whether chronic stress associated with social subordination impairs prenatal transfer of antitetanus immunity in breeding female rhesus macaques. Subjects included 26 high- and 26 low-ranking adult female rhesus macaques that were nearly 5 or 10 y after their initial immunization and their nonimmunized infants. We hypothesized that infants born to subordinate dams that were nearly 10 y after immunization would have the lowest infant-to-dam antibody ratios and thus would be at greatest risk for infection. Results revealed no significant intergroup differences in infant antitetanus IgG levels. However, infant-to-dam IgG ratios against tetanus were significantly lower among subordinate animals compared with dominant macaques, after accounting for the number of years since the dam's initial vaccination. In addition, higher maternal hair cortisol levels predicted lower infantto-dam tetanus toxoid IgG ratios. Together, these findings suggest that chronic social stress in female rhesus macaques may hamper the prenatal transfer of antitetanus immunity to offspring.

Maternal Mental Disorders and Pediatric Infectious Diseases

“…5 In macaques, maternal stress impairs the transplacental transfer of IgG antibodies. 6 Mental disorders are also associated with preterm birth, low birthweight and small-for-gestational age birth, 2,7,10 adverse birth outcomes associated with lower levels of maternal IgG. 5,8 When we excluded these children from the analysis, associations weakened mostly for preterm birth, suggesting that gestational length and immaturity may be more important than growth-related pathways.…”

“…5 Animal studies suggest that maternal stress hampers transplacental transfer of IgG antibodies. 6 Depression and stress are risk factors for prematurity and low birthweight, 2,7 birth outcomes associated with reduced transfer of IgG antibodies. 5,8 Mental disorders may additionally affect breast-feeding and childcare, furthering the risk of infection.…”

Utility of Automated Feeding Data to Detect Social Instability in a Captive Breeding Colony of Rhesus Macaques (Macaca mulatta): A Case Study of Intrafamily Aggression

“…Social rank data of each family were available in colony records and determined by the frequency of submissive behavior and aggression received by nonfamilial group mates. 40 Matrilineal coefficient of relatedness was based on genetic data available at the time of the fighting incident.…”

Neonatal Immune System Ontogeny: The Role of Maternal Microbiota and Associated Factors. How Might the Non-Human Primate Model Enlighten the Path?

“…Gestational stress has a negative impact in fetus growth, weight, development, immunity, and cognitive function in infant rhesus primates (Macaca mulatta) [22,23]. In rhesus macaques, chronic stress also impairs prenatal transfer of antibodies to the fetus [24]. In addition, gestational stress alters colonization in the infant primate that possesses a reduced abundance of Lactobacillus and Bifidobacterium compared to infant primates from undisturbed mothers [25].…”