Hidden Consequences of Living in a Wormy World: Nematode-Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 Th2) over a type 1 Th1) response, impairing the host\u27s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown. We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild

Mutualism or Parasitism? Using a Phylogenetic Approach to Characterize the Oxpecker-Ungulate Relationship

With their striking predilection for perching on African ungulates and eating their ticks, yellow-billed (Buphagus africanus) and red-billed oxpeckers (B. erythrorhynchus) represent one of the few potentially mutualistic relationships among vertebrates. The nature of the oxpecker–ungulate relationship remains uncertain, however, because oxpeckers are known to consume ungulate tissues, suggesting that the relationship between oxpeckers and ungulates may also be parasitic. To examine this issue further, we obtained data on oxpecker preferences for different ungulate species, the abundance of ticks on these ungulates, and ungulate hide thickness. In support of the mutualism hypothesis, we found that both species of oxpeckers prefer ungulate hosts that harbor a higher abundance of ticks. We found no evidence that hide thickness—a measure of the potential for parasitism by oxpeckers—predicts oxpecker preferences for different ungulate species. Oxpeckers also prefer larger-bodied ungulates, possibly because larger animals have more ticks, provide a more stable platform upon which to forage, or support more oxpeckers feeding simultaneously. However, the preference for ungulates with greater tick abundance was independent of host body mass. These results support the hypothesis that the relationship between oxpeckers and ungulates is primarily mutualistic.Human Evolutionary Biolog

Hidden Consequences of Living in a Wormy World: Nematode‐Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co-occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown.We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild

Complex Tissue Regeneration in Mammals Is Associated with Reduced Inflammatory Cytokines and an Influx of T Cells

While mammals tend to repair injuries, other adult vertebrates like salamanders and fish regenerate damaged tissue. One prominent hypothesis offered to explain an inability to regenerate complex tissue in mammals is a bias during healing toward strong adaptive immunity and inflammatory responses. Here we directly test this hypothesis by characterizing part of the immune response during regeneration in spiny mice (Acomys cahirinus and Acomys percivali) vs. fibrotic repair in Mus musculus. By directly quantifying cytokines during tissue healing, we found that fibrotic repair was associated with a greater release of pro-inflammatory cytokines (i.e., IL-6, CCL2, and CXCL1) during acute inflammation in the wound microenvironment. However, reducing inflammation via COX-2 inhibition was not sufficient to reduce fibrosis or induce a regenerative response, suggesting that inflammatory strength does not control how an injury heals. Although regeneration was associated with lower concentrations of many inflammatory markers, we measured a comparatively larger influx of T cells into regenerating ear tissue and detected a local increase in the T cell associated cytokines IL-12 and IL-17 during the proliferative phase of regeneration. Taken together, our data demonstrate that a strong adaptive immune response is not antagonistic to regeneration and that other mechanisms likely explain the distribution of regenerative ability in vertebrates

Evaluation of the Sensitivity and Specificity of an Enzyme-Linked Immunosorbent Assay for Diagnosing Brucellosis in African Buffalo (Syncerus caffer)

Brucellosis is a disease of veterinary and public health importance worldwide. In sub- Saharan Africa, where this disease has been detected in several free-ranging wildlife species, successful disease control may be dependent on accurate detection in wildlife reservoirs, including African buffalo (Syncerus caffer). This study estimates the sensitivity and specificity of a commercial enzyme-linked immunosorbent assay (IDEXX, Brucellosis Serum Ab Test) for brucellosis based on a dataset of 571 serum samples from 258 buffalo located within the Kruger National Park, South Africa. We defined a pseudo-gold standard test result as those buffalo that were consistently positive or negative on two additional serological tests, namely the rose bengal test (RBT) and the complement fixation test (CFT). The ELISA’s cut-off value was selected using receiver operating characteristics (ROC) analysis, the pseudo-gold standard, and a threshold criterion that maximizes the total sensitivity and specificity. Then, we estimated the sensitivity and specificity of all three tests using Bayesian inference and latent class analysis. We estimated the ELISA to have a sensitivity of 0.928 (95% BCI from 0.869-0.974) and specificity of 0.870 (95% BCI from 0.836-0.900). Compared to the ELISA, the RBT had a higher estimated sensitivity of 0.986 (95% BCI from 0.928- 0.999), and both the RBT and CFT had higher specificities, estimated to be 0.992 (95% BCI from 0.971 to 0.996) and 0.998 (95% BCI from 0.992 to 0.999), respectively. Therefore, this study shows that no single serological test perfectly diagnosed infection. However, after adjustment of cut-off values for South African conditions, the IDEXX Brucellosis Serum Ab Test may be a valuable additional screening test for brucellosis in Kruger National Park’s African buffalo.This is an author's peer-reviewed final manuscript, as accepted by the publisher. The published article is copyrighted by the Wildlife Disease Association and can be found at: http://www.jwildlifedis.org/,This research was approved by Kruger National Park’s Scientific Services committee and by Oregon State University and University of Georgia IACUC (Protocol numbers OSU: 3822; UGA: A201010-190-A1).Keywords: Bayesian, Sensitivity, Enzyme linked immunosorbent assay, Brucellosis, Latent data, African buffalo, Specificit

Hidden Consequences of Living in a Wormy World:Nematode-Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co-occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown.We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild

Context-dependent survival, fecundity and predicted population-level consequences of brucellosis in African buffalo

1. Chronic infections may have negative impacts on wildlife populations, yet their effects are difficult to detect in the absence of long-term population monitoring. Brucella abortus, the bacteria responsible for bovine brucellosis, causes chronic infections and abortions in wild and domestic ungulates, but its impact on population dynamics is not well understood. 2. We report infection patterns and fitness correlates of bovine brucellosis in African buffalo based on (1) 7 years of cross-sectional disease surveys and (2) a 4-year longitudinal study in Kruger National Park (KNP), South Africa. We then used a matrix population model to translate these observed patterns into predicted population-level effects. 3. Annual brucellosis seroprevalence ranged from 8·7% (95% CI = 1·8–15·6) to 47·6% (95% CI = 35·1–60·1) increased with age until adulthood (>6) and varied by location within KNP. Animals were on average in worse condition after testing positive for brucellosis (F = −5·074, P < 0·0001), and infection was associated with a 2·0 (95% CI = 1·1–3·7) fold increase in mortality (χ² = 2·039, P = 0·036). Buffalo in low body condition were associated with lower reproductive success (F = 2·683, P = 0·034), but there was no association between brucellosis and pregnancy or being observed with a calf. For the range of body condition scores observed in the population, the model-predicted growth rate was λ = 1·11 (95% CI = 1·02–1·21) in herds without brucellosis and λ = 1·00 (95% CI = 0·85–1·16) when brucellosis seroprevalence was 30%. Our results suggest that brucellosis infection can potentially result in reduced population growth rates, but because these effects varied with demographic and environmental conditions, they may remain unseen without intensive, longitudinal monitoring.Keywords: disease ecology, Brucella abortus, population growth, bacteria, chronic disease, African buffalo, conservation biolog

Context-dependent survival, fecundity and predicted population-level consequences of brucellosis in African buffalo

1. Chronic infections may have negative impacts on wildlife populations, yet their effects are difficult to detect in the absence of long-term population monitoring. Brucella abortus, the bacteria responsible for bovine brucellosis, causes chronic infections and abortions in wild and domestic ungulates, but its impact on population dynamics is not well understood. 2. We report infection patterns and fitness correlates of bovine brucellosis in African buffalo based on (1) 7 years of cross-sectional disease surveys and (2) a 4-year longitudinal study in Kruger National Park (KNP), South Africa. We then used a matrix population model to translate these observed patterns into predicted population-level effects. 3. Annual brucellosis seroprevalence ranged from 8·7% (95% CI = 1·8–15·6) to 47·6% (95% CI = 35·1–60·1) increased with age until adulthood (>6) and varied by location within KNP. Animals were on average in worse condition after testing positive for brucellosis (F = −5·074, P < 0·0001), and infection was associated with a 2·0 (95% CI = 1·1–3·7) fold increase in mortality (χ2 = 2·039, P = 0·036). Buffalo in low body condition were associated with lower reproductive success (F = 2·683, P = 0·034), but there was no association between brucellosis and pregnancy or being observed with a calf. 4. For the range of body condition scores observed in the population, the model-predicted growth rate was λ = 1·11 (95% CI = 1·02–1·21) in herds without brucellosis and λ = 1·00 (95% CI = 0·85–1·16) when brucellosis seroprevalence was 30%. 5. Our results suggest that brucellosis infection can potentially result in reduced population growth rates, but because these effects varied with demographic and environmental conditions, they may remain unseen without intensive, longitudinal monitoring.To the best of our knowledge, one or more authors of this paper were federal employees when contributing to this work. This is the publisher’s final pdf. The published article is copyrighted by The Authors and the British Ecological Society. It is published by John Wiley & Sons, Inc., and can be found at: https://doi.org/10.1111/1365-2656.1235

Co-infection best predicts respiratory viral infection in a wild host

1. The dynamics of directly transmitted pathogens in natural populations are likely to result from the combined effects of host traits, pathogen biology, and interactions among pathogens within a host. Discovering how these factors work in concert to shape variation in pathogen dynamics in natural host–multi-pathogen systems is fundamental to understanding population health. 2. Here, we describe temporal variation in incidence and then elucidate the effect of hosts trait, season and pathogen co-occurrence on host infection risk using one of the most comprehensive studies of co-infection in a wild population: a suite of seven directly transmitted viral and bacterial respiratory infections from a 4-year study of 200 free-ranging African buffalo Syncerus caffer. 3. Incidence of upper respiratory infections was common throughout the study—five out of the seven pathogens appeared to be consistently circulating throughout our study population. One pathogen exhibited clear outbreak dynamics in our final study year and another was rarely detected. 4. Co-infection was also common in this system: The strongest indicator of pathogen occurrence for respiratory viruses was in fact the presence of other viral respiratory infections. Host traits had minimal effects on odds of pathogen occurrence but did modify pathogen–pathogen associations. In contrast, only season predicted bacterial pathogen occurrence. 5. Though a combination of environmental, behavioural, and physiological factors work together to shape disease dynamics, we found pathogen associations best determined infection risk. Our study demonstrates that, in the absence of very fine-scale data, the intricate changes among these factors are best represented by co-infection.National Science Foundation Ecology of Infectious Disease; National Science Foundation; National Institute of Health; University of Pretoria; USDA-NSF-NIH-BBRSC Ecology and Evolution of Infectious Disease Program and Achievement Rewards for College Scientists Foundation.http://wileyonlinelibrary.com/journal/jane2021-11-24am2021Veterinary Tropical Disease