Immune function during pregnancy varies between ecologically distinct populations

Abstract

<jats:title>Abstract</jats:title> <jats:sec> <jats:title>Background and objectives</jats:title> <jats:p>Among placental mammals, females undergo immunological shifts during pregnancy to accommodate the fetus (i.e. fetal tolerance). Fetal tolerance has primarily been characterized within post-industrial populations experiencing evolutionarily novel conditions (e.g. reduced pathogen exposure), which may shape maternal response to fetal antigens. This study investigates how ecological conditions affect maternal immune status during pregnancy by comparing the direction and magnitude of immunological changes associated with each trimester among the Tsimane (a subsistence population subjected to high pathogen load) and women in the United States.</jats:p> </jats:sec> <jats:sec> <jats:title>Methodology</jats:title> <jats:p>Data from the Tsimane Health and Life History Project (N = 935) and the National Health and Nutrition Examination Survey (N = 1395) were used to estimate population-specific effects of trimester on differential leukocyte count and C-reactive protein (CRP), a marker of systemic inflammation.</jats:p> </jats:sec> <jats:sec> <jats:title>Results</jats:title> <jats:p>In both populations, pregnancy was associated with increased neutrophil prevalence, reduced lymphocyte and eosinophil count, and elevated CRP. Compared to their US counterparts, pregnant Tsimane women exhibited elevated lymphocyte and eosinophil counts, fewer neutrophils and monocytes, and lower CRP. Total leukocyte count remained high and unchanged among pregnant Tsimane women while pregnant US women exhibited substantially elevated counts, resulting in overlapping leukocyte prevalence among all third-trimester individuals.</jats:p> </jats:sec> <jats:sec> <jats:title>Conclusions and implications</jats:title> <jats:p>Our findings indicate that ecological conditions shape non-pregnant immune baselines and the magnitude of immunological shifts during pregnancy via developmental constraints and current trade-offs. Future research should investigate how such flexibility impacts maternal health and disease susceptibility, particularly the degree to which chronic pathogen exposure might dampen inflammatory response to fetal antigens.</jats:p> </jats:sec> <jats:sec> <jats:title>Lay Summary</jats:title> <jats:p>This study compares immunological changes associated with pregnancy between the Tsimane (an Amazonian subsistence population) and individuals in the United States. Results suggest that while pregnancy enhances non-specific defenses and dampens both antigen-specific immunity and parasite/allergy response, ecological conditions strongly influence immune baselines and the magnitude of shifts during gestation.</jats:p> </jats:sec>

Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane forager-horticulturalists

“…We included body mass index (BMI) and age as covariates in all models, and included a pregnancy covariate for women (0/1) [ 44 ]. The small number of pregnant women ( n = 6) precluded a trimester-level analysis [ 45 ]. We included only STHs with >10% prevalence across the sample set.…”

Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane hunter-horticulturalists

“…We included body mass index (BMI) and age as covariates in all models, and, in the female specific models, included a covariate for pregnancy (0/1) [47]. While previous research in the Tsimane has shown differences in immune function by trimester, the small number of pregnant women (n=6) in this study precluded a trimester-level analysis [48]. We included in our models only STHs with a prevalence of over 10% across our sample set.…”

“…Because of the lack of standard health surveillance in the region, we are unable to know for certain if study participants had previously been exposed to H1N1, which would shape the interpretation of our results. We know that immunological changes during pregnancy vary by trimester [48], but our low sample size of pregnant women precluded a trimester-level analysis. We also did not include children in our analyses and thus cannot assess the role of early life exposure in this relationship.…”

Hematological and CD4+ T- cell count reference interval for pregnant women attending antenatal care at Hawassa University Comprehensive Specialized Hospital, Hawassa Southern Ethiopia

“…Pregnancy is a state characterized by profound hematological changes, and regulated inflammation which is consistently marked by a rise in the total number of circulating leukocytes, primarily due to the increase of neutrophils and monocytes. These phagocytic cells can also induce inflammatory activation and strengthen resistance to extracellular infections, but are also associated with the etiology of autoimmune diseases [ 14 ].…”

“…Immunity in pregnancy is physiologically compromised and may affect the CD 4 + cell count, as lower CD 4 + cell count has been reported in pregnant compared with non-pregnant females [ 15 ]. On the other hand, total lymphocyte counts are consistently reduced during pregnancy, primarily due to fewer circulating cytotoxic lymphocytes capable of directly recognizing and targeting fetal antigens [ 14 ]. On the contrary CD4 T cells, the proliferation of regulatory lymphocytes is increased [ 16 ].…”