Schneider-Crease, I. et al. Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population. PLoS Negl Trop Dis 11, e0005709 (2017).
Google Scholar
Schneider-Crease, I. et al. Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate. Funct. Ecol. 34, 1898–1906 (2020).
Google Scholar
Gillespie, T. R. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 27, 1129 (2006).
Google Scholar
Budischak, S. A., Hoberg, E. P., Abrams, A., Jolles, A. E. & Ezenwa, V. O. A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts. Mol. Ecol. Resour. 15, 1112–1119 (2015).
Google Scholar
Ghalehnoei, H., Bagheri, A., Fakhar, M. & Mishan, M. A. Circulatory microRNAs: promising non-invasive prognostic and diagnostic biomarkers for parasitic infections. Eur. J. Clin. Microbiol. Infect. Dis. 39, 395–402 (2020).
Google Scholar
Hing, S., Narayan, E. J., Andrew Thompson, R. C. & Godfrey, S. S. The relationship between physiological stress and wildlife disease: consequences for health and conservation. Wildl Res. 43, 51–60 (2016).
Google Scholar
Kersey, D. C. & Dehnhard, M. The use of noninvasive and minimally invasive methods in endocrinology for threatened mammalian species conservation. Gen. Comp. Endocrinol. 203, 296–306 (2014).
Google Scholar
Behringer, V. & Deschner, T. Non-invasive monitoring of physiological markers in primates. Horm. Behav. 91, 3–18 (2017).
Google Scholar
Higham, J. P., Stahl-Hennig, C. & Heistermann, M. Urinary suPAR: A non-invasive biomarker of infection and tissue inflammation for use in studies of large free-ranging mammals. R Soc Open Sci. 7, 191825 (2020).
Google Scholar
Heistermann, M. & Higham, J. P. Urinary neopterin, a non-invasive marker of mammalian cellular immune activation, is highly stable under field conditions. Sci Rep. 5, 16308 (2015).
Google Scholar
Higham, J. P. et al. Evaluating noninvasive markers of nonhuman primate immune activation and inflammation. Am. J. Phys. Anthropol. 158, 673–684 (2015).
Google Scholar
Behringer, V. et al. Elevated neopterin levels in wild, healthy chimpanzees indicate constant investment in unspecific immune system. BMC Zool. 4, 1–7 (2019).
Google Scholar
Dibakou, S. E., Basset, D., Souza, A., Charpentier, M. & Huchard, E. Determinants of variations in fecal neopterin in free-ranging mandrills. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00368 (2019).
Google Scholar
Löhrich, T., Behringer, V., Wittig, R. M., Deschner, T. & Leendertz, F. H. The use of neopterin as a noninvasive marker in monitoring diseases in wild chimpanzees. EcoHealth 15, 792–803 (2018).
Google Scholar
Behringer, V., Stevens, J. M. G., Leendertz, F. H., Hohmann, G. & Deschner, T. Validation of a method for the assessment of urinary neopterin levels to monitor health status in nonhuman primate species. Front Physiol. 8, 51 (2017).
Google Scholar
Negrey, J. D., Behringer, V., Langergraber, K. E. & Deschner, T. Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status. Sci. Rep. 11, 9298 (2021).
Google Scholar
Behringer, V. et al. Cell-mediated immune ontogeny is affected by sex but not environmental context in a long-lived primate species. Front. Ecol. Evol. 9, 272 (2021).
Google Scholar
Müller, N., Heistermann, M., Strube, C., Schülke, O. & Ostner, J. Age, but not anthelmintic treatment, is associated with urinary neopterin levels in semi-free ranging Barbary macaques. Sci. Rep. 7, 41973 (2017).
Google Scholar
Dibakou, S. E. et al. Ecological, parasitological and individual determinants of plasma neopterin levels in a natural mandrill population. Int. J. Parasitol. Parasites Wildl. 11, 198–206 (2020).
Google Scholar
Eisenhut, M. Neopterin in diagnosis and monitoring of infectious diseases. J. Biomark. 2013, 196432 (2013).
Google Scholar
Franceschi, C. & Campisi, J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol. A Biol. Sci. Med Sci. 69(Suppl 1), S4–9 (2014).
Google Scholar
Basha, S., Surendran, N. & Pichichero, M. Immune responses in neonates. Expert. Rev. Clin. Immunol. 10, 1171–1184 (2014).
Google Scholar
Werner, E. R. et al. Determination of neopterin in serum and urine. Clin. Chem. 33, 62–66 (1987).
Google Scholar
Lucore, J. M., Marshall, A. J., Brosnan, S. F. & Benítez, M. E. Validating urinary neopterin as a biomarker of immune response in captive and wild capuchin monkeys. Front. Vet. Sci. 9, 918036. https://doi.org/10.3389/fvets.2022.918036 (2022).
Google Scholar
Berdowska, A. & Zwirska-Korczala, K. Neopterin measurement in clinical diagnosis. J. Clin. Pharm. Ther. 26, 319–329 (2001).
Google Scholar
Denz, H. et al. Value of urinary neopterin in the differential diagnosis of bacterial and viral infections. Klin. Wochenschr. 68, 218–222 (1990).
Google Scholar
Reibnegger, G. et al. Urinary neopterin reflects clinical activity in patients with rheumatoid arthritis. Arthritis Rheum. 29, 1063–1070 (1986).
Google Scholar
Huber, C. et al. Immune response-associated production of neopterin. Release from macrophages primarily under control of interferon-gamma. J. Exp. Med. 160, 310–316 (1984).
Google Scholar
Horak, E., Gassner, I., Sölder, B., Wachter, H. & Fuchs, D. Neopterin levels and pulmonary tuberculosis in infants. Lung 176, 337–344 (1998).
Google Scholar
Fendrich, C. et al. Urinary neopterin concentrations in rhesus monkeys after infection with simian immunodeficiency virus (SIVmac 251). AIDS 3, 305–307 (1989).
Google Scholar
Chan, C. P. Y. et al. Detection of serum neopterin for early assessment of dengue virus infection. J. Infect. 53, 152–158 (2006).
Google Scholar
Wu, D. F., Behringer, V., Wittig, R. M., Leendertz, F. H. & Deschner, T. Urinary neopterin levels increase and predict survival during a respiratory outbreak in wild chimpanzees (Taï National Park, Côte d’Ivoire). Sci. Rep. 8, 13346 (2018).
Google Scholar
Maizels, R. M. & McSorley, H. J. Regulation of the host immune system by helminth parasites. J. Allergy Clin. Immunol. 138, 666–675 (2016).
Google Scholar
Maizels, R. M. & Yazdanbakhsh, M. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733–744 (2003).
Google Scholar
Yazdanbakhsh, M., Kremsner, P. G. & van Ree, R. Allergy, parasites, and the hygiene hypothesis. Science 296, 490–494 (2002).
Google Scholar
Faz-López, B., Morales-Montor, J. & Terrazas, L. I. Role of macrophages in the repair process during the tissue migrating and resident helminth infections. Biomed. Res. Int. 2016, 8634603 (2016).
Google Scholar
Garcia, H. H., Rodriguez, S., Friedland, J. S. Cysticercosis Working Group in Peru. Immunology of Taenia solium taeniasis and human cysticercosis. Parasite Immunol. 36, 388–396. https://doi.org/10.1111/pim.12126 (2014)
Google Scholar
Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65–74 (2016).
Google Scholar
Schneider-Crease, I. A., Griffin, R. H., Gomery, M. A., Bergman, T. J. & Beehner, J. C. High mortality associated with tapeworm parasitism in geladas (Theropithecus gelada) in the Simien Mountains National Park, Ethiopia. Am. J. Primatol. https://doi.org/10.1002/ajp.22684 (2017).
Google Scholar
Nguyen, N. et al. Fitness impacts of tapeworm parasitism on wild gelada monkeys at Guassa, Ethiopia. Am. J. Primatol. 77, 579–594 (2015).
Google Scholar
Schneider-Crease, I. A. et al. Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane forager-horticulturalists. Evol. Med. Public Health 9, 349–359 (2021).
Google Scholar
Roberts, E. K., Lu, A., Bergman, T. J. & Beehner, J. C. Female reproductive parameters in wild geladas (Theropithecus gelada). Int. J. Primatol. 38, 1–20 (2017).
Google Scholar
Beehner, J. C. et al. Corrigendum to “Testosterone related to age and life-history stages in male baboons and geladas” [Horm. Behav. 56/4 (2009) 472-480]. Horm Behav. 80, 149 (2016).
Google Scholar
Erb, R. E., Tillson, S. A., Hodgen, G. D. & Plotka, E. D. Urinary creatinine as an index compound for estimating rate of excretion of steroids in the domestic sow. J. Anim. Sci. 30, 79–85 (1970).
Google Scholar
Tinsley Johnson, E., Snyder-Mackler, N., Lu, A., Bergman, T. J. & Beehner, J. C. Social and ecological drivers of reproductive seasonality in geladas. Behav. Ecol. 29, 574–588 (2018).
Google Scholar
Kaushik, S. & Kaur, J. Effect of chronic cold stress on intestinal epithelial cell proliferation and inflammation in rats. Stress 8, 191–197 (2005).
Google Scholar
Jarvey, J. C., Low, B. S., Pappano, D. J. & Bergman, T. J. Graminivory and fallback foods: annual diet profile of geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. Int. J. Primatol. https://doi.org/10.1007/s10764-018-0018-x (2018).
Google Scholar
Gowda, C., Hadley, C. & Aiello, A. E. The association between food insecurity and inflammation in the US adult population. Am. J. Public Health. 102, 1579–1586 (2012).
Google Scholar
Becker, D. J. et al. Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence. J. Anim. Ecol. 89, 972–995 (2020).
Google Scholar
Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1, 1–7 (2014).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2021. https://www.R-project.org/.
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).
Google Scholar
Simon, A. K., Hollander, G. A. & McMichael, A. Evolution of the immune system in humans from infancy to old age. Proc. Biol. Sci. 282, 20143085 (2015).
Heinonen, S. et al. Infant immune response to respiratory viral infections. Immunol. Allergy Clin. North Am. 39, 361–376 (2019).
Google Scholar
Teran, R. et al. Immune system development during early childhood in tropical Latin America: Evidence for the age-dependent down regulation of the innate immune response. Clin. Immunol. 138, 299–310 (2011).
Google Scholar
van de Pol, M. & Verhulst, S. Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am. Nat. 167, 766–773 (2006).
Google Scholar
Furman, D. et al. Chronic inflammation in the etiology of disease across the life span. Nat. Med. 25, 1822–1832 (2019).
Google Scholar
Petrovsky, N., McNair, P. & Harrison, L. C. Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 10, 307–312 (1998).
Google Scholar
Lasselin, J., Rehman, J.-U., Åkerstedt, T., Lekander, M. & Axelsson, J. Effect of long-term sleep restriction and subsequent recovery sleep on the diurnal rhythms of white blood cell subpopulations. Brain Behav. Immun. 47, 93–99 (2015).
Google Scholar
Auzéby, A., Bogdan, A., Krosi, Z. & Touitou, Y. Time-dependence of urinary neopterin, a marker of cellular immune activity. Clin Chem. 34, 1866–1867 (1988).
Google Scholar
Ansari, A. & Williams, J. F. The eosinophilic response of the rat to infection with Taenia taeniaeformis. J. Parasitol. 62, 728–736 (1976).
Google Scholar
Schneider-Crease, I. A., Snyder-Mackler, N., Jarvey, J. C. & Bergman, T. J. Molecular identification of Taenia serialis coenurosis in a wild Ethiopian gelada (Theropithecus gelada). Vet. Parasitol. 198, 240–243 (2013).
Google Scholar
Terrazas, L. I., Bojalil, R., Govezensky, T. & Larralde, C. Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps). J. Parasitol. 84, 74–81 (1998).
Google Scholar
Toenjes, S. A., Spolski, R. J., Mooney, K. A. & Kuhn, R. E. The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/Th2-type response. Parasitology 118(Pt 6), 623–633 (1999).
Google Scholar
Gaze, S. et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 8, e1002520 (2012).
Google Scholar
Johnston, M. J. G., MacDonald, J. A. & McKay, D. M. Parasitic helminths: a pharmacopeia of anti-inflammatory molecules. Parasitology 136, 125–147 (2009).
Google Scholar
Cortés, A., Muñoz-Antoli, C., Esteban, J. G. & Toledo, R. Th2 and Th1 responses: Clear and hidden sides of immunity against intestinal helminths. Trends Parasitol. 33, 678–693 (2017).
Google Scholar
White, M. P. J., McManus, C. M. & Maizels, R. M. Regulatory T-cells in helminth infection: induction, function and therapeutic potential. Immunology 160, 248–260 (2020).
Google Scholar
Maizels, R. M. & Holland, M. J. Parasite immunity: Pathways for expelling intestinal helminths. Curr Biol. 8, R711–R714 (1998).
Google Scholar
Zhang, D. & Frenette, P. S. Cross talk between neutrophils and the microbiota. Blood 133, 2168–2177 (2019).
Google Scholar
Wang, J., Chen, W.-D. & Wang, Y.-D. The relationship between gut microbiota and inflammatory diseases: The role of macrophages. Front. Microbiol. 11, 1065 (2020).
Google Scholar
Pallikkuth, S. et al. Age associated microbiome and microbial metabolites modulation and its association with systemic inflammation in a rhesus macaque model. Front. Immunol. 12, 748397 (2021).
Google Scholar
Pierce, Z. et al. The infant gut microbiome is associated with stool markers of macrophage and neutrophil activity. FASEB J. 30, 668–9 (2016).
Levast, B. et al. Impact on the gut microbiota of intensive and prolonged antimicrobial therapy in patients with bone and joint infection. Front. Med. https://doi.org/10.3389/fmed.2021.586875 (2021).
Google Scholar
Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).
Google Scholar
Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).
Google Scholar
Libertucci, J. & Young, V. B. The role of the microbiota in infectious diseases. Nat. Microbiol. 4, 35–45 (2019).
Google Scholar
Huttenhower, C. et al. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).
Google Scholar
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).
Google Scholar
Blaser, M. J. & Falkow, S. What are the consequences of the disappearing human microbiota?. Nat. Rev. Microbiol. 7, 887–894 (2009).
Google Scholar
Brown, E. M., Kenny, D. J. & Xavier, R. J. Gut microbiota regulation of T cells during inflammation and autoimmunity. Annu. Rev. Immunol. 37, 599–624 (2019).
Google Scholar
Gollwitzer, E. S. & Marsland, B. J. Impact of early-life exposures on immune maturation and susceptibility to disease. Trends Immunol. 36, 684–696 (2015).
Google Scholar
Ravi, A. et al. Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients. Microbial. Genomics https://doi.org/10.1099/mgen.0.000293 (2019).
McLaren, M. R. & Callahan, B. J. Pathogen resistance may be the principal evolutionary advantage provided by the microbiome. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190592 (2020).
Google Scholar
Ragonnaud, E. & Biragyn, A. Gut microbiota as the key controllers of “healthy” aging of elderly people. Immun Ageing 18, 2 (2021).
Google Scholar
Wilmanski, T. et al. Gut microbiome pattern reflects healthy ageing and predicts survival in humans. Nat. Metab. 3, 274–286 (2021).
Google Scholar
Cattadori, I. M. et al. Impact of helminth infections and nutritional constraints on the small intestine microbiota. PLoS ONE 11, e0159770 (2016).
Google Scholar
Houlden, A. et al. Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome: Effects reversed by pathogen clearance. PLoS ONE 10, e0125945 (2015).
Google Scholar
Holm, J. B. et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS ONE 10, e0125495 (2015).
Google Scholar
Peachey, L. E., Jenkins, T. P. & Cantacessi, C. This gut ain’t big enough for both of us. Or is it? Helminth–microbiota interactions in veterinary species. Trends Parasitol. 33, 619–632 (2017).
Google Scholar
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