Maternal Parasitic Infections Research Articles

Impact of helminth infections during pregnancy on maternal and newborn Vitamin D and on birth outcomes

Poor birth outcomes in low- and middle income countries are associated with maternal vitamin D deficiency and chronic helminth infections. Here, we investigated whether maternal Schistosoma haematobium affects maternal or cord vitamin D status as well as birth outcomes. In a prospective cross-sectional study of pregnant women conducted in Lambaréné, Gabon, we diagnosed maternal parasitic infections in blood, urine and stool. At delivery we measured vitamin D in maternal and cord blood. S. haematobium, soil-transmitted helminths, and microfilariae were found at prevalences of 30.2%, 13.0%, and 8.8%, respectively. Insufficient vitamin D and calcium levels were found in 28% and 15% of mothers, and in 11.5% and 1.5% of newborns. Mothers with adequate vitamin D had lower risk of low birthweight babies (aOR = 0.11, 95% CI 0.02–0.52, p = 0.01), whilst offspring of primipars had low cord vitamin D levels, and low vitamin D levels increased the risk of maternal inflammation. Maternal filariasis was associated with low calcium levels, but other helminth infections affected neither vitamin D nor calcium levels in either mothers or newborns. Healthy birth outcomes require maintenance of adequate vitamin D and calcium levels. Chronic maternal helminth infections do not disrupt those levels in a semi-rural setting in sub-Saharan Africa.

Maternal Infection and altered fetal immune programming.

Abstract The maternal-fetal interface involves complex and balanced interactions between mother and fetus, which support the development of the fetal immune system. While we know maternal helminth infection during pregnancy is known to disrupt this relationship and affect neonatal immune development, the fundamental mechanisms that drive fetal immune programming is not completely understood. To further examine how maternal parasitic infection influences offspring immunity, we established a model in which female mice prior to mating are infected with the persistent mouse intestinal helminth, Heligmosomoides polygyrus (HP). One week after infection, female mice are mated, and the progeny are aged to adulthood. The offspring are then challenged with influenza virus. Intriguingly, we found that offspring born from mothers with HP infections were less susceptible to influenza challenge than offspring born from uninfected mothers. This data implies that the effects of maternal helminth infection are long lasting, and potentially involve fetal programming during the early development of the immune system.

Вплив перенесених паразитарних інфекцій під час вагітності на імунну систему плода (огляд літератури)

Transmission of infections during pregnancy is known to alter the development and functioning of the fetus immune system, resulting in an inadequate immune response to common childhood infections and immunizations. Although it is a developing and actively researched topic, maternal parasitic infections remain poorly understood. Millions of women of reproductive age are currently at risk of parasite infection, while many pregnant, chronically infected women are excluded from mass drug administration due in part to a lack of resources, as well as fear of unknown adverse fetal outcomes. infection, there is no clear mechanism for understanding how maternal infection reprograms offspring immunity. Purpose - to determine the currently studied mechanisms of the influence of parasitic infections transmitted during pregnancy on the immune system of the fetus and to describe the possible effects of these influence in the long term on the health of children. Conclusions. The study of maternal parasitic infections is a rapidly developing field. Although infant mortality rates are declining, areas with endemic parasites still have the highest infant mortality rates. As antiparasitic therapy is not always curable, there is a critical need to understand the effects of maternal infection on offspring immune development. Due to the increased risk of immune alteration due to maternal inflammation and reduced passive antibody transmission, maternal parasitic infections and their mechanism of adverse immunomodulation must be uncovered to improve vaccination regimens and reduce childhood morbidity in endemic regions. No conflict of interests was declared by the author.

Altered Offspring Immunity in Maternal Parasitic Infections.

Maternal infection during pregnancy is known to alter the development and function of offspring's immune system, leading to inappropriate immune responses to common childhood infections and immunizations. Although this is an expanding field, maternal parasitic infections remain understudied. Millions of women of reproductive age are currently at risk for parasitic infection, whereas many pregnant, chronically infected women are excluded from mass drug administration due partially to a lack of resources, as well as fear of unknown adverse fetal developmental outcomes. In areas endemic for multiple parasitic infections, such as sub-Saharan Africa, there are increased rates of morbidity and mortality for various infections during early childhood in comparison with nonendemic areas. Despite evidence supporting similar immunomodulatory effects between various parasite species, there is no clear mechanistic understanding of how maternal infection reprograms offspring immunity. This brief review will compare the effects of selected maternal parasitic infections on offspring immunity.

The relationship between Toxoplasma gondii infection in mothers and neonate’s gender

Background The secondary sex ratio can be affected by various factors such as stress, immunosuppression, and age of parents in addition to mother infectious disease (Maternal infections). Toxoplasmosis is one of the critical maternal parasitic infections during pregnancy. Besides the complications of the acute form of the disease, hormonal shifts, and even alterations in the secondary sex ratio can be induced by the manipulative activity of the chronic form of the disease. Therefore, this study aimed to evaluate the correlation between Toxoplasma gondii infection in mothers and neonate’s gender. Methods In this case-control study, 137 seropositive mothers to Anti-Toxoplasma IgG(case) was compared to 137 age-matched subject Toxoplasma-seronegative mothers(control) in terms of their neonate’s gender. These individuals were randomly selected based on exclusions and inclusions criteria of the study from among 2014 mothers who had been tested for Toxoplasma infection during pregnancy from 2015 to 2018 in Shiraz, Iran. Results From a total of 2014 studied pregnant mothers, 326 (16.2%) mothers were seropositive to anti-Toxoplasma IgG, and 1688 (83.8%) were negative for IgG. It was found that the numbers of female and male neonates were 136 (45.48%) and 163 (54.51%) in the control group whereas, they were 165 (49.84%) and 166 (50.15%) in the case group, respectively. The sex ratio was 1.006:1 in Toxoplasma-seropositive and 1.2:1 in Toxoplasma-seronegative mothers. The number of male and females offsprings indicated a significant difference in Toxoplasma-seronegative mothers (54.5%, p = .015). Moreover, comparing the number of males and females between the two randomly selected groups showed that female gender is significantly more than male gender in seropositive mothers to Toxoplasma (54.8%, p = .014), which means that of 301 females, 165 offspring were born to seropositive mothers. No significant difference was observed for the sex ratio of aborted fetuses between groups. However, in the Toxoplasma-seropositive group, the sex ratio of aborted fetuses showed that the aborted male fetuses were significantly higher in number. (31 male vs 13 female, p < .001). Conclusion Comprehensively, a significant relationship was found between chronic Toxoplasma infection and secondary sex ratio. However, it is suggested that this relationship be investigated in further studies as well as an animal study.

Factors associated with early childhood stunted growth in a 2012\u20132015 birth cohort monitored in the rural Msambweni area of coastal Kenya: a cross-sectional study

BackgroundChronic malnutrition, often measured as stunted growth, is an understudied global health problem. Though poor nutritional intake has been linked to stunted growth, there is evidence suggesting environmental exposures may have a significant role in its occurrence. Here, we characterize the non-nutritional prenatal and postnatal factors that contribute to early childhood stunted growth in rural coastal Kenya.MethodsOverall, 232 women and 244 children from a 2012–2015 maternal-child cohort in Msambweni, Kenya were included. Women were tested for parasitic infections during the prenatal period and at the time of delivery. Children were tested for parasitic infections and assessed for stunted growth using height-for-age Z-scores (HAZ) at 6-month intervals after birth. Socioeconomic status (SES) was evaluated using both a simplified water, asset, maternal education, and income (WAMI) index and a principal component analysis (PCA) asset score. Multivariate logistic regression analysis was used to determine the relative influence of prenatal and postnatal factors on the occurrence of stunted growth.ResultsOf the 244 children (ages 6–37 months), 60 (25%) were stunted at the study endpoint. 179 mothers (77%) had at least one parasitic infection during pregnancy and 94 children (38%) had at least one parasitic infection during the study period. There was no significant association between maternal parasitic infection and child stunted growth (p = 1.00). SES as determined using the WAMI index was not associated with HAZ in linear regression analysis (p = 0.307), however, the PCA asset score was (p = 0.048). Multivariate logistic regression analysis identified low birth weight (AOR: 3.24, 95% CI: [1.38, 7.57]) and child parasitic infectious disease burden (AOR: 1.41, 95% CI: [1.05, 1.95]) as independent predictors of stunted growth, though no significant association was identified with PCA asset score (AOR: 0.98, 95% CI: [0.88, 1.10]).ConclusionsStunted growth remains highly prevalent in rural Kenya, with low birth weight and child parasitic infectious disease burden demonstrated to be significantly associated with this indicator of chronic malnutrition. These results emphasize the multifaceted nature of stunted growth and the need to address both the prenatal and postnatal environmental factors that contribute to this problem.

Maternal malaria but not schistosomiasis is associated with a higher risk of febrile infection in infant during the first 3 months of life: A mother-child cohort in Benin

BackgroundMalaria and schistosomiasis represent two of the most prevalent and disabling parasitic infections in developing countries. Few studies have evaluated the effect of maternal schistosomiasis and malaria in the peri-conceptional period on infant’s risk of infection.MethodsIn Benin, women were followed from the preconception period until delivery. Subsequently, their children were followed from birth to 3 months of age. Pre-pregnancy malaria, malaria in pregnancy (MiP)—determined monthly using a thick blood smear—and urinary schistosomiasis—determined once before pregnancy and once at delivery using urine filtration—were the main maternal exposures. Infant’s febrile infection (fever with respiratory, gastrointestinal and/or cutaneous clinical signs anytime during follow-up) was the main outcome. In a secondary analysis, we checked the relation of malaria and schistosomiasis with infant’s hemoglobin (Hb) concentration. Both effects were separately assessed using logistic/mixed linear regression models.ResultsThe prevalence of MiP was 35.7% with 10.8% occurring during the 1st trimester, and the prevalence of schistosomiasis was 21.8%. From birth to 3 months, 25.3% of infants had at least one episode of febrile infection. In multivariate analysis, MiP, particularly malaria in the 1st trimester, was significantly associated with a higher risk of infant’s febrile infection (aOR = 4.99 [1.1; 22.6], p = 0.03). In secondary results, pre-pregnancy malaria and schistosomiasis were significantly associated with a lower infant’s Hb concentration during the first 3 months.ConclusionWe evidenced the deleterious effect of maternal parasitic infections on infant’s health. Our results argue in favor of the implementation of preventive strategies as early as in the peri-conception.

Parasitic infections during pregnancy need not affect infant antibody responses to early vaccination against Streptococcus pneumoniae, diphtheria, or Haemophilus influenzae type B.

BackgroundGlobally, vaccine-preventable diseases remain a significant cause of early childhood mortality despite concerted efforts to improve vaccine coverage. One reason for impaired protection may be the influence of prenatal exposure to parasitic antigens on the developing immune system. Prior research had shown a decrease in infant vaccine response after in utero parasite exposure among a maternal cohort without aggressive preventive treatment. This study investigated the effect of maternal parasitic infections on infant vaccination in a more recent setting of active anti-parasitic therapy.Methodology/Principal findingsFrom 2013–2015, 576 Kenyan women were tested in pregnancy for malaria, soil-transmitted helminths, filaria, and S. haematobium, with both acute and prophylactic antiparasitic therapies given. After birth, 567 infants received 10-valent S. pneumoniae conjugate vaccine and pentavalent vaccine for hepatitis B, pertussis, tetanus, H. influenzae type B (Hib) and C. diphtheriae toxoid (Dp-t) at 6, 10, and 14 weeks. Infant serum samples from birth, 10 and 14 weeks, and every six months until age three years, were analyzed using a multiplex bead assay to quantify IgG for Hib, Dp-t, and the ten pneumococcal serotypes. Antenatal parasitic prevalence was high; 461 women (80%) had at least one and 252 (43.6%) had two or more infections during their pregnancy, with the most common being malaria (44.6%), S. haematobium (43.9%), and hookworm (29.2%). Mixed models comparing influence of infection on antibody concentration revealed no effect of prenatal infection status for most vaccine outcomes. Prevalences of protective antibody concentrations after vaccination were similar among the prenatal exposure groups.Conclusions/SignificanceThese findings are in contrast with results from our prior cohort study performed when preventive anti-parasite treatment was less frequently given. The results suggest that the treatment of maternal infections in pregnancy may be able to moderate the previously observed effect of antenatal maternal infections on infant vaccine responses.

Parasitic Infections in Pregnancy Decrease Placental Transfer of Antipneumococcus Antibodies.

Many factors can influence maternal placental antibody transfer to the fetus, which confers important immune protection to the newborn infant. However, little is known about the effect of maternal parasitic infection on placental antibody transfer. To investigate this, we selected from a parent study of 576 pregnant Kenyan women four groups of women with term deliveries (≥37 weeks), including uninfected women (n = 30) and women with solo infections with malaria (n = 30), hookworm (n = 30), or schistosomiasis (n = 10). Maternal plasma at delivery and infant cord blood were tested via multiplex fluorescent bead assay for IgG against 10 pneumococcal serotypes (PnPs 1, 4, 5, 6B, 7F, 9V, 14, 18C, 19F, and 23F), diphtheria toxoid, and Haemophilus influenzae type B. Infants born to mothers with prenatal malaria, hookworm, or Schistosoma haematobium infections were associated with a significantly reduced ratio of maternal to infant cord blood antibody concentration for Streptococcus pneumoniae serotypes 1, 4, 5, 6B, 7F, 9V, and 18C compared to infants of uninfected mothers. Anti-diphtheria toxoid and anti-H. influenzae type B IgG ratios were not significantly different among infection groups. Prenatal parasitic infections decrease the transfer of maternal IgG antibodies to infants for several serotypes of S. pneumoniae.

Maternal Parasitic Infections Alter Infant Antibody Response to Pneumococcal Immunization

Maternal Parasitic Infections Alter Infant Antibody Response to Pneumococcal Immunization

Maternal body size influences offspring immune configuration in an oviparous snake

Like most ectothermic vertebrates, keelback snakes (Tropidonophis mairii) do not exhibit parental care. Thus, offspring must possess an immune system capable of dealing with challenges such as pathogens, without assistance from an attendant parent. We know very little about immune system characteristics of neonatal reptiles, including the magnitude of heritability and other maternal influences. To identify sources of variation in circulating white blood cell (WBC) concentrations and differentials, we examined blood smears from 246 hatchling snakes and their field-caught mothers. WBC concentrations were lower in hatchlings than in adults, and hatchlings had more basophils and fewer azurophils than adults. A hatchling keelback's WBC differential was also influenced by its sex and body size. Although hatchling WBC measures exhibited negligible heritability, they were strongly influenced by maternal body size and parasite infection (but not by maternal body condition, relative clutch mass or time in captivity). Larger mothers produced offspring with more azurophils and fewer lymphocytes. The mechanisms and consequences of WBC variation are currently unknown, but if these maternal effects enhance offspring fitness, the impact of maternal body size on reproductive success may be greater than expected simply from allometric increases in the numbers and sizes of progeny.

Endoparasite infection has both short- and long-term negative effects on reproductive success of female house sparrows, as revealed by faecal parasitic egg counts.

Parasites have the potential to severely reduce host reproductive success. However, the effects of endoparasites on reproductive success have not received the same amount of attention as the effects of parasites on host survival. We investigated the relationship between an avian endoparasite (gapeworm, Syngamus trachea) and both current and future reproductive success of female house sparrows (Passer domesticus) in a population on the coast of Helgeland, northern Norway. We found that the proportion of eggs in a nest that failed to develop into fledglings increased as the faecal parasitic egg count of the mothers increased. We also found that juvenile females with high numbers of parasitic eggs in their faeces had lower lifetime reproductive success as adults. However, we did not find a relationship between maternal parasite infection and clutch size or recruitment rate of offspring. To our knowledge this is the first study to find a relationship between reproductive success of an avian host and faecal egg count of an endoparasite. The present study indicates that infection by an endoparasite may be associated with lower individual reproductive success in both the short-term and long-term in a wild population of hosts.

A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance.

BackgroundTrans-generational effects of immune stimulation may have either adaptive (trans-generational immune priming) or non-adaptive (fitness costs) effects on offspring ability to fight pathogens.MethodsAnopheles coluzzii and its natural malaria parasite Plasmodium falciparum were used to test how maternal parasite infection affected offspring resistance to the same parasite species.ResultsDaughters of exposed mothers had similar qualitative resistance, as measured by their ability to prevent infection, relative to those of control mothers. However, maternal disease exposure altered offspring quantitative resistance, measured as the ability to limit parasite development, with mosquitoes of infected mothers suffering slightly increased parasite intensity compared to controls. In addition, quantitative resistance was minimal in offspring of highly infected mothers, and in offspring issued from eggs produced during the early infection phase.ConclusionsPlasmodium falciparum infection in An. coluzzii can have trans-generational costs, lowering quantitative resistance in offspring of infected mothers. Malaria-exposed mosquitoes might heavily invest in immune defences and thereby produce lower quality offspring that are poorly resistant.Electronic supplementary materialThe online version of this article (doi:10.1186/1475-2875-13-442) contains supplementary material, which is available to authorized users.

Association of In Utero Sensitization to Schistosoma haematobium with Enhanced Cord Blood IgE and Increased Frequencies of CD5– B Cells in African Newborns

This study investigated in utero priming as a consequence of maternal parasitic infections. Cord blood plasma samples of 63 African newborns were assessed by enzyme-linked immunosorbent assay for their content of total and schistosome-specific or filaria-specific IgE and IgG4. The frequencies of lymphocyte phenotypes in cord blood were also determined by using flow cytometry, and were compared with those of European newborns. We found significantly increased schistosome soluble egg antigen (SEA)-specific IgE in cord plasma of those born to mothers with schistosome infections and correlations between fetal and maternal SEA-specific and filaria antigen-specific IgE. These data are evidence for in utero priming of the fetal immune system to maternal helminth infections. Furthermore, we show significantly enhanced percentages of CD5- B cells in African newborns cord blood compared with Europeans, which is consistent with earlier maturation of the African fetal immune system.

GENETİK, ÇEVRESEL VE KÜLTÜREL ETMENLERİN IŞIĞINDA ANEMİ: BAZI ESKİ ANADOLU TOPLULUKLARINDAN ÖRNEKLER

GENETİK, ÇEVRESEL VE KÜLTÜREL ETMENLERİN IŞIĞINDA ANEMİ: BAZI ESKİ ANADOLU TOPLULUKLARINDAN ÖRNEKLER

Persistent effects of maternal parasitic infection on offspring fitness: implications for adaptive reproductive strategies when parasitized

1 Maternal effects on offspring phenotype may represent adaptive strategies to optimize maternal or offspring fitness given the maternal environment. The effect of maternal parasitic infection on offspring phenotype has been largely ignored, despite the potential for such effects to be components of a maternal reproductive strategy. In addition, the persistence and fitness consequences of maternal effects are understudied, particularly with respect to research on maternal parasitic infection. 2 Deer mice (Peromyscus maniculatus) increase reproductive output by weaning heavier offspring when infected with a schistosome parasite (Schistosomatium douthitti). Here, I examine the persistence of maternal effects on offspring phenotype and evaluate potential consequences of maternal parasitic infection for offspring lifetime fitness. 3 Offspring of parasitized females are born heavier, and this mass advantage persists in sons until adulthood. Because adult body mass is known to influence adult reproductive success in deer mice, parasitized mothers would have produced sons of higher reproductive success. 4 Neither maternal infection nor offspring mass influenced adult son aggression. Survival was enhanced for heavier offspring post-weaning. 5 The production of heavier offspring by parasitized females, therefore, led to increased offspring fitness through enhanced survival and potentially reproductive success. The resultant increase in current maternal reproductive success in response to possible infection-induced decreases in future reproductive opportunities supports the hypothesis that infected females trade-off between current and future reproduction.

The intestinal nematode Trichuris arvicolae affects the fecundity of its host, the common vole Microtus arvalis

Parasites have detrimental effects on host fitness. Consequently, they play a major role for host population dynamics. In this study, we investigated experimentally the impact of the nematode Trichuris arvicolae on the reproduction of its host, the common vole Microtus arvalis. Wild common voles were trapped in east of France and reared in standardized conditions before being experimentally infected. Infection with Trichuris arvicolae did not affect host consumption of food or water. Parasitized females gave birth to slightly less pups (mean 3.36 +/- 0.38) than unparasitized females (mean 3.60 +/- 0.40). Controlling for natal litter size using analysis of covariance (ANCOVA), T. arvicolae infection had a significant effect on the individual mass at birth, with pups from parasitized females having significantly lower mass (2.11 g +/- 0.01) than pups from unparasitized females (2.20 g +/- 0.01). Other measures of host reproductive outputs (time to first reproduction, mass of pups at weaning, litter survival) were not affected by maternal parasite infection. We discuss how these changes in M. arvalis reproductive investments associated with T. arvicolae infection must now be investigated in the context of physiological trade-offs.

Maternal Income-Generating Activities, Child Care, and Child Nutrition in Mali

Women in sub-Saharan Africa play a key role in household food security. The income-generating activities of mothers are postulated to be related to the nutritional status of children. The objective of the study was to examine whether maternal income-generating activities, maternal food production, and child care were determinants of the nutritional status of children in rural West Africa. The study hypotheses were that maternal income-generating activities and maternal food production are positively associated with children's dietary intake and anthropometry, and that maternal income-generating activities are not associated with child care. Data were collected from a cross-sectional sample of mother-child pairs on maternal time use, child anthropometry, maternal food production, dietary intake, parasitic infection, and household, maternal, and child determinants of child nutritional status. The children were 12 to 36 months of age and included breastfed and nonbreastfed children. Food intake was assessed by the 24-hour recall method. The data were analyzed by multivariate regression and controlled for confounding variables. Time spent by the mother in income-generating activities was negatively associated with children's animal protein intake and height-for-age (p < .05). Maternal cash crop production was positively associated with children's weight-for-height, whereas maternal staple food production was negatively associated with energy intake from non-breastmilk foods (p < .05). The negative relationships observed for children's animal protein intake and children's height-for-age were not mediated by any child-care variable. Maternal supervision of feeding was a positive predictor of children's animal protein intake. Giardia infection was negatively related to children's weight gain (p < .05). Own-account cash crop farming by mothers benefits children's nutrition. Maternal income-generating activities in the context of extended families, sibling caretaking, and prolonged breastfeeding do not adversely affect child care.

Intestinal nematode infection affects host life history and offspring susceptibility to parasitism

Summary The effects of experimental infection with a naturally occurring intestinal nematode (Heligmosomoides polygyrus, Dujardin 1845) on reproduction and on offspring growth, morphology and susceptibility to parasitism for wild‐derived house mice (Mus musculus, Linnaeus 1758) that were two to three generations captive‐born were examined. Parasitized females averaged 2·8 more pups per litter at weaning and, after adjusting for the effects of litter size on offspring mass, parasitized females had slightly larger offspring than unparasitized females (by 1–2%). Heligmosomoides polygyrus did not affect mean values of other measures of host reproductive output (time to first litter production, interlitter intervals, sex ratio, offspring loss from birth to weaning) but parasitized mice were more variable than unparasitized mice in the number of days to first litter production and for numbers of pups that died between birth and weaning. Offspring growth was not affected by either maternal parasite infection or direct parasite infection. Body mass of all pups at sexual maturity was equivalent but there were differences in body composition (fat mass, organ masses) between parasitized and unparasitized pups and between males and females. Only offspring from parasitized mothers cleared their own infection but for offspring that retained their infection there were no effects of either offspring sex or maternal parasite infection on infection intensity. These results clearly demonstrate that infection with an intestinal nematode affects host life history, primarily litter size but also offspring mass at weaning, and susceptibility of offspring to infection with the same parasite.

Effects of intestinal nematodes during lactation: consequences for host morphology, physiology and offspring mass.

Sublethal parasites are often assumed to have no detrimental effects on their host. However, the sublethal intestinal nematode Heligmosomoides polygyrus affects both the morphology and the physiology of its laboratory mouse (Mus musculus) host and therefore has the potential to affect host life history. The objectives of the present study were to determine (1) whether lactating and non-lactating mice responded similarly to experimental infection with H. polygyrus and (2) whether the changes in morphology and physiology that occurred with parasite infection affected host reproductive performance. Parasitized mice had greater whole body mass as a result of greater lean mass compared with unparasitized mice. Parasitized mice had larger organs (spleen, stomach, cecum and small intestine) and a diminished rate of glucose transport by the small intestine compared with unparasitized mice. Lactating mice had larger organs (liver, kidney, spleen, heart, stomach, large intestine, cecum and small intestine), lean mass and whole body mass, but a similar rate of glucose transport compared with virgin mice. Resting metabolism increased with lactation but not with parasitism. Lactating and non-lactating mice responded similarly to parasite infection for most measured variables. Production of large litters was followed by production of small litters for parasitized but not unparasitized females. After adjusting for parity and litter size, parasitized mothers produced female pups that were 6% smaller at weaning than female pups from unparasitized mothers, but there was no effect of maternal parasite infection on mass at weaning for male pups. Other measures of reproductive output were not affected by parasite infection.