{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T03:02:22Z","timestamp":1780628542618,"version":"3.54.1"},"reference-count":116,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T00:00:00Z","timestamp":1780012800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>Trypanosomiasis remains a major constraint to small ruminant production in sub-Saharan Africa, particularly among smallholder farmers. Although WAD goats are considered trypanotolerant because of their relatively low mortality during chronic infection, recent findings show that this survival is at the expense of reproductive efficiency. To back up this claim with scientific evidence, this review followed PRISMA guidelines and systematically searched PubMed, Scopus, and Web of Science for important studies published between January 1980 and February 2026. Search terms included African animal trypanosomiasis, Trypanosoma spp., WAD goats, reproductive dysfunction, trypanotolerance, oxidative stress, and hypothalamic\u2013pituitary\u2013gonadal axis. Of the 1245 retrieved articles, 14 met the inclusion criteria. Evidence from the included studies indicates that chronic trypanosome infection disrupts reproduction through interconnected mechanisms involving systemic inflammation, oxidative stress, endocrine imbalance, and impaired gonadal function. Available evidence suggests that T. brucei is frequently associated with ovarian dysfunction and embryonic loss, whereas T. congolense has been linked in some studies to uterine pathology and gestational reproductive disturbances. Female goats commonly exhibit irregular oestrous cycles, embryonic loss, and prolonged kidding intervals, while males develop impaired spermatogenesis, abnormal sperm morphology, and reduced testosterone levels. These reproductive impairments reduce kid output, milk yield, herd productivity, and household livelihood resilience. Integrated control strategies combining vector control, targeted chemotherapy, nutritional support, and selective breeding are essential for preserving both fertility and survival in trypanosome-endemic areas.<\/jats:p>","DOI":"10.3390\/vetsci13060535","type":"journal-article","created":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T14:38:42Z","timestamp":1780411122000},"page":"535","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Reproductive Impacts of African Animal Trypanosomiasis in West African Dwarf Goats\u2014Mechanistic Insights into Trypanotolerance Survival\u2013Fertility Trade-Off: A Systematic Review"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1495-824X","authenticated-orcid":false,"given":"Ugochinyere J.","family":"Njoga","sequence":"first","affiliation":[{"name":"Department of Veterinary Obstetrics and Reproductive Diseases, Faculty of Veterinary Medicine, University of Nigeria, Nsukka 410001, Nigeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2333-7584","authenticated-orcid":false,"given":"Emmanuel O.","family":"Njoga","sequence":"additional","affiliation":[{"name":"Department of Agriculture and Animal Health, College of Agriculture and Environmental Sciences, University of South Africa, Florida Science Campus, Roodepoort, Johannesburg 1709, South Africa"},{"name":"Department of Veterinary Public Health and Preventive Medicine, Faculty of Veterinary Medicine, University of Nigeria, Nsukka 410001, Nigeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Izuchukwu S.","family":"Ochiogu","sequence":"additional","affiliation":[{"name":"Department of Veterinary Obstetrics and Reproductive Diseases, Faculty of Veterinary Medicine, University of Nigeria, Nsukka 410001, Nigeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0780-7531","authenticated-orcid":false,"given":"John I.","family":"Ihedioha","sequence":"additional","affiliation":[{"name":"Department of Veterinary Pathology, Faculty of Veterinary Medicine, University of Nigeria, Nsukka 410001, Nigeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6810-4437","authenticated-orcid":false,"given":"James W.","family":"Oguttu","sequence":"additional","affiliation":[{"name":"Department of Agriculture and Animal Health, College of Agriculture and Environmental Sciences, University of South Africa, Florida Science Campus, Roodepoort, Johannesburg 1709, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,5,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1007\/s12571-024-01452-1","article-title":"Opportunities to improve goat production and food security in Botswana through forage nutrition and the use of supplemental feeds","volume":"16","author":"Cooke","year":"2024","journal-title":"Food Secur."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1007\/s11250-008-9267-6","article-title":"Physiological adaptation to the humid tropics with special reference to the West African Dwarf (WAD) goat","volume":"41","author":"Daramola","year":"2009","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1007\/BF02237927","article-title":"Some production traits of the West African Dwarf goat","volume":"13","author":"Oppong","year":"1981","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"35","DOI":"10.4102\/ojvr.v76i1.59","article-title":"Tsetse and Trypanosomosis in Africa: The Challenges, the Opportunities","volume":"76","author":"Ilemobade","year":"2009","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5984376","DOI":"10.1155\/2022\/5984376","article-title":"Prevalence and associated risk factors of African animal trypanosomosis in cattle in Lambwe, Kenya","volume":"2022","author":"Okello","year":"2022","journal-title":"J. Parasitol. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.vetpar.2016.05.003","article-title":"Combatting African animal trypanosomosis (AAT) in livestock: The potential role of trypanotolerance","volume":"225","author":"Yaro","year":"2016","journal-title":"Vet. Parasitol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.4102\/ojvr.v84i1.1412","article-title":"Differential virulence and tsetse fly transmissibility of Trypanosoma congolense and Trypanosoma brucei strains","volume":"84","author":"Gitonga","year":"2017","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"22683","DOI":"10.1038\/s41598-025-90112-1","article-title":"Epidemiology and economic impact of bovine trypanosomosis in Jawi District, Northwest Ethiopia","volume":"15","author":"Adane","year":"2025","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Venturelli, A., Tagliazucchi, L., Lima, C., Venuti, F., Malpezzi, G., Magoulas, G.E., Santarem, N., Calogeropoulou, T., Cordeiro-da-Silva, A., and Costi, M.P. (2022). Current treatments to control African trypanosomosis and One Health perspective. Microorganisms, 10.","DOI":"10.3390\/microorganisms10071298"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Kimeli, P., Mwacalimba, K., Tiernan, R., Mijten, E., Miroshnychenko, T., and Poulsen Nautrup, B. (2025). Important diseases of small ruminants in Sub-Saharan Africa: A review with a focus on current strategies for treatment and control in smallholder systems. Animals, 15.","DOI":"10.3390\/ani15050706"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Abro, Z., Kassie, M., Muriithi, B., Okal, M., Masiga, D., Wanda, G., Gis\u00e8le, O., Samuel, A., Nguertoum, E., and Nina, R.A. (2021). The potential economic benefits of controlling trypanosomosis using waterbuck repellent blend in sub-Saharan Africa. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0254558"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"11786302241274698","DOI":"10.1177\/11786302241274698","article-title":"Epidemiology and economic cost of trypanosomosis among smallholder cattle herders in Arba Minch and Zuria Districts, Gamo Zone, Ethiopia","volume":"18","author":"Tora","year":"2024","journal-title":"Environ. Health Insights"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1111\/1477-9552.12531","article-title":"Socioeconomic burden of trypanosomosis: Evidence from crop and livestock production in Ethiopia","volume":"74","author":"Abro","year":"2023","journal-title":"J. Agric. Econ."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Smetko, A., Soudre, A., Silbermayr, K., M\u00fcller, S., Brem, G., Hanotte, O., Boettcher, P.J., Stella, A., M\u00e9sz\u00e1ros, G., and Wurzinger, M. (2015). Trypanosomosis: Potential driver of selection in African cattle. Front. Genet., 6.","DOI":"10.3389\/fgene.2015.00137"},{"key":"ref_15","first-page":"5","article-title":"Reproductive disorders in African trypanosomiasis: A review","volume":"45","author":"Ikede","year":"1988","journal-title":"Acta Trop."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 statement: An updated guideline for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Njoga, E.O., Awoyomi, O.J., Onwumere-Idolor, O.S., Awoyomi, P.O., Ugochukwu, I.C.I., and Ozioko, S.N. (2022). Persisting vaccine hesitancy in Africa: The whys, global public health consequences and ways-out\u2014COVID-19 vaccination acceptance rates as case-in-point. Vaccines, 10.","DOI":"10.3390\/vaccines10111934"},{"key":"ref_18","first-page":"477","article-title":"Depression of ovarian function and plasma progesterone and estradiol-17\u03b2 in female goats chronically infected with Trypanosoma congolense","volume":"117","author":"Mutayoba","year":"1988","journal-title":"Acta Endocrinol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1016\/j.theriogenology.2004.02.007","article-title":"Effects of an experimental Trypanosoma congolense infection on the reproductive performance of West African Dwarf goats","volume":"62","author":"Faye","year":"2004","journal-title":"Theriogenology"},{"key":"ref_20","first-page":"189","article-title":"Sequential testicular and ovarian pathology in experimental Trypanosoma brucei infection in goats","volume":"164","author":"Adamu","year":"2009","journal-title":"Vet. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1196\/annals.1373.040","article-title":"Trypanosomosis in goats: Current status","volume":"1081","author":"Gutierrez","year":"2006","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.actatropica.2004.10.008","article-title":"Influence of an experimental Trypanosoma congolense infection and plane of nutrition on milk production and some biochemical parameters in West African Dwarf goats","volume":"93","author":"Faye","year":"2005","journal-title":"Acta Trop."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"154","DOI":"10.20506\/rst.17.1.1088","article-title":"Trypanotolerance, an option for sustainable livestock production in areas at risk from trypanosomosis","volume":"17","author":"Wissocq","year":"1998","journal-title":"Rev. Sci. Tech."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"194176","DOI":"10.1155\/2013\/194176","article-title":"Trypanosoma evansi and surra: A review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects","volume":"2013","author":"Desquesnes","year":"2013","journal-title":"BioMed Res. Int."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1111\/j.1365-3024.2010.01277.x","article-title":"Virulence in Trypanosoma congolense Savannah subgroup: A comparison between strains and transmission cycles","volume":"33","author":"Chitanga","year":"2011","journal-title":"Parasite Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1017\/S003118202000178X","article-title":"Parasitological and molecular detection of Trypanosoma spp. in cattle, goats and sheep in Somalia","volume":"147","author":"Ibrahim","year":"2020","journal-title":"Parasitology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2502","DOI":"10.14202\/vetworld.2020.2502-2507","article-title":"Frequency and diversity of trypanosomes in sheep and goats from Mongo County in South Gabon, Central Africa","volume":"13","author":"Maganga","year":"2020","journal-title":"Vet. World"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"295","DOI":"10.19182\/remvt.9091","article-title":"Prevalence of trypanosomosis in sheep and goats in a region of northern Nigeria","volume":"47","author":"Daniel","year":"1994","journal-title":"Rev. Elev. Med. Vet. Pays Trop."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.3923\/javaa.2010.2422.2426","article-title":"Prevalence of trypanosomosis in ruminants in parts of Abia State, Nigeria","volume":"9","author":"Ohaeri","year":"2010","journal-title":"J. Anim. Vet. Adv."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/S0361-9230(97)00305-5","article-title":"Plasma luteinizing hormone levels in response to gonadotropin-releasing hormone agonist and clonidine in Trypanosoma congolense-infected female goats","volume":"44","author":"Odongo","year":"1997","journal-title":"Brain Res. Bull."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1007\/BF02240384","article-title":"Trypanosomosis and reproduction: I. Effect of Trypanosoma vivax infection on the oestrous cycle and fertility in the ewe","volume":"26","author":"Elhassan","year":"1994","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/BF00430035","article-title":"The effects of experimental Trypanosoma evansi infection on fertility of male goats","volume":"15","author":"Ngeranwa","year":"1991","journal-title":"Vet. Res. Commun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1023\/A:1005133518092","article-title":"Reduced ovulatory and oestrous activity following Trypanosoma vivax infection in ruminants","volume":"31","author":"Obasi","year":"1999","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1186\/1297-9716-42-63","article-title":"Association of Trypanosoma vivax in extracellular sites with central nervous system lesions and changes in cerebrospinal fluid in experimentally infected goats","volume":"42","author":"Batista","year":"2011","journal-title":"Vet. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.vetpar.2007.04.005","article-title":"The comparative role of cattle, goats and pigs in the epidemiology of livestock trypanosomosis on the plateau of eastern Zambia","volume":"147","author":"Simukoko","year":"2007","journal-title":"Vet. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1007\/s11250-022-03367-5","article-title":"The detection of African trypanosomes in goats reared in tsetse-infested villages of Eastern Zambia","volume":"54","author":"Mulenga","year":"2022","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.cois.2014.07.003","article-title":"Trypanosome transmission dynamics in tsetse","volume":"3","author":"Aksoy","year":"2014","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.prevetmed.2013.10.024","article-title":"Mapping the economic benefits to livestock keepers from intervening against bovine trypanosomosis in Eastern Africa","volume":"113","author":"Shaw","year":"2014","journal-title":"Prev. Vet. Med."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Von Wissmann, B., Machila, N., Picozzi, K., F\u00e8vre, E.M., Bronsvoort, B.M.D., Handel, I.G., and Welburn, S.C. (2011). Factors associated with acquisition of human infective and animal infective trypanosome infections in domestic livestock in Western Kenya. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0000941"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.jcpa.2005.06.001","article-title":"Experimental Trypanosoma evansi infection in the goat. I. Clinical signs and clinical pathology","volume":"133","author":"Dargantes","year":"2005","journal-title":"J. Comp. Pathol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1186\/s13071-017-2411-2","article-title":"Molecular prevalence of trypanosome infections in cattle and tsetse flies in the Maasai Steppe, northern Tanzania","volume":"10","author":"Simwango","year":"2017","journal-title":"Parasites Vectors"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1186\/s13071-018-2801-0","article-title":"A meta-analysis of the prevalence of African animal trypanosomosis in Nigeria from 1960 to 2017","volume":"11","author":"Odeniran","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"20337","DOI":"10.1038\/s41598-023-47141-5","article-title":"Prevalence of African animal trypanosomiasis among livestock and domestic animals in Uganda: A systematic review and meta-regression analysis from 1980 to 2022","volume":"13","author":"Cecchi","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_44","unstructured":"Habeeb, M.A., Sadiq, M.B., and Oladipo, O.T. (2021). Prevalence of animal African trypanosomosis and species distribution in Nigeria: A scoping review. Animals, 11."},{"key":"ref_45","first-page":"45","article-title":"Trypanosoma vivax, T. congolense or T. brucei infection rates in Glossina morsitans when maintained in vitro on the blood of goat or calf","volume":"41","author":"Moloo","year":"1984","journal-title":"Acta Trop."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Choi, B., Vu, H.T., Vu, H.T., Radwanska, M., and Magez, S. (2024). Advances in the immunology of host\u2013parasite interactions in African trypanosomosis, including single-cell transcriptomics. Pathogens, 13.","DOI":"10.3390\/pathogens13030188"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Stijlemans, B., Caljon, G., Van Den Abbeele, J., Van Ginderachter, J.A., Magez, S., and De Trez, C. (2016). Immune evasion strategies of Trypanosoma brucei within the mammalian host: Progression to pathogenicity. Front. Immunol., 7.","DOI":"10.3389\/fimmu.2016.00233"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/1475-9292-4-5","article-title":"Detection of trypanosomes in small ruminants and pigs in western Kenya: Important reservoirs in the epidemiology of sleeping sickness?","volume":"4","author":"Njiru","year":"2005","journal-title":"Kinetoplastid Biol. Dis."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Ignatiuk, V.M., Sharova, V.S., and Zakharova, L.A. (2025). The role of cytokines in the development and functioning of the hypothalamic\u2013pituitary\u2013gonadal axis in mammals in normal and pathological conditions. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms262211057"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2428","DOI":"10.1128\/AAC.06386-11","article-title":"Induction of oxidative stress in Trypanosoma brucei by the antitrypanosomal dihydroquinoline OSU-40","volume":"56","author":"He","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Berean, D., Bogdan, L.M., Ciupe, S., and Cimpean, R. (2026). Hormonal and Non-Hormonal Estrus Synchronization in Sheep and Goats: Physiological Basis, Efficacy, and Practical Applications. Appl. Biosci., 5.","DOI":"10.3390\/applbiosci5020035"},{"key":"ref_52","first-page":"215","article-title":"Reproductive issues in small ruminants: A review","volume":"25","author":"Ali","year":"2019","journal-title":"Large Anim. Rev."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Raghupathy, R., and Szekeres-Bartho, J. (2022). Progesterone: A unique hormone with immunomodulatory roles in pregnancy. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23031333"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Shah, N.M., Lai, P.F., Imami, N., and Johnson, M.R. (2019). Progesterone-related immune modulation of pregnancy and labor. Front. Endocrinol., 10.","DOI":"10.3389\/fendo.2019.00198"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s13223-016-0113-5","article-title":"The role of cytokines in the pathogenesis and staging of Trypanosoma brucei rhodesiense sleeping sickness","volume":"12","author":"Kato","year":"2016","journal-title":"Allergy Asthma Clin. Immunol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.ogc.2014.10.003","article-title":"Progesterone and the luteal phase: A requisite to reproduction","volume":"42","author":"Mesen","year":"2015","journal-title":"Obstet. Gynecol. Clin. N. Am."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Bustamante-Andrade, J.A., Meza-Herrera, C.A., Rodr\u00edguez-Mart\u00ednez, R., Santos-Jimenez, Z., \u00c1ngel-Garc\u00eda, O., Gayt\u00e1n-Alem\u00e1n, L.R., Gutierrez-Guzman, U.N., Esquivel-Romo, A., and V\u00e9liz-Deras, F.G. (2021). Luteogenesis and embryo implantation are enhanced by exogenous hCG in goats subjected to an out-of-season fixed-time artificial insemination protocol. Biology, 10.","DOI":"10.3390\/biology10050429"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"5941","DOI":"10.3168\/jds.2015-10070","article-title":"The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants","volume":"99","author":"Spencer","year":"2016","journal-title":"J. Dairy Sci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1093\/biolre\/ioaf032","article-title":"Reactive oxygen and nitrogen species: Multifaceted regulators of ovarian activity","volume":"112","year":"2025","journal-title":"Biol. Reprod."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Jonczyk, A.W., Piotrowska-Tomala, K.K., and Skarzynski, D.J. (2019). Effects of prostaglandin F2\u03b1 (PGF2\u03b1) on cell-death pathways in the bovine corpus luteum (CL). BMC Vet. Res., 15.","DOI":"10.1186\/s12917-019-2167-3"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Wen, X., Liu, L., Li, S., Lin, P., Chen, H., Zhou, D., Tang, K., Wang, A., and Jin, Y. (2020). Prostaglandin F2\u03b1 induces goat corpus luteum regression via endoplasmic reticulum stress and autophagy. Front. Physiol., 11.","DOI":"10.3389\/fphys.2020.00868"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"31","DOI":"10.33549\/physiolres.935485","article-title":"Mechanisms of granulosa cell programmed cell death and follicular atresia in polycystic ovary syndrome","volume":"74","author":"Shen","year":"2025","journal-title":"Physiol. Res."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Song, J., Xiao, L., Zhang, Z., Wang, Y., Kouis, P., Rasmussen, L.J., and Dai, F. (2024). Effects of reactive oxygen species and mitochondrial dysfunction on reproductive aging. Front. Cell Dev. Biol., 12.","DOI":"10.3389\/fcell.2024.1347286"},{"key":"ref_64","first-page":"57","article-title":"Small ruminant production in West Africa: Traditional and improved practices for smallholder farmers","volume":"176","author":"Lebbie","year":"2019","journal-title":"Small Rumin. Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1007\/s11259-026-11188-2","article-title":"Effect of estrus synchronization\/induction in ouled djellal ewes using combinations of melatonin, gnrh, and prostaglandin f2\u03b1 on fertility parameters","volume":"50","author":"Mehallaine","year":"2026","journal-title":"Vet. Res. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/0093-691X(94)90373-Q","article-title":"Reproductive disorders caused by animal Trypanosomosis: A review","volume":"42","author":"Sekoni","year":"1994","journal-title":"Theriogenology"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.pt.2008.12.004","article-title":"Trypanotolerance in small ruminants of sub-Saharan Africa","volume":"25","author":"Geerts","year":"2009","journal-title":"Trends Parasitol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.anireprosci.2012.01.011","article-title":"Hormonal control of reproduction in small ruminants","volume":"130","author":"Abecia","year":"2012","journal-title":"Anim. Reprod. Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1071\/RD04037","article-title":"New treatments associated with timed artificial insemination in small ruminants","volume":"16","author":"Menchaca","year":"2004","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_70","first-page":"108827","article-title":"Interplay between endocrine disorders and liver dysfunction: Mechanisms of damage and therapeutic approaches","volume":"31","author":"Torre","year":"2025","journal-title":"World J. Gastroenterol."},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Lanser, L., Fuchs, D., Kurz, K., and Weiss, G. (2021). Physiology and inflammation-driven pathophysiology of iron homeostasis\u2014Mechanistic insights into anemia of inflammation and its treatment. Nutrients, 13.","DOI":"10.3390\/nu13113732"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"402","DOI":"10.21451\/1984-3143-AR2019-0041","article-title":"Pre-TAI protocol strategies to increase reproductive efficiency in beef and dairy cows","volume":"16","author":"Sales","year":"2019","journal-title":"Anim. Reprod."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Hamad, M.N.M., Albadrani, G.M., Ghazwani, A.A., Abdelmola, A., Suliman, R.S., Mahjaf, G.M., Fahmy, S.A., Badi, S., Yassin, H.M., and Othman, G.A. (2025). Assessment of cytokines TNF-\u03b1, IFN-\u03b3, TGF-\u03b21, and IL-10 in malaria patients of the River Nile State, Sudan. BMC Immunol., 26.","DOI":"10.1186\/s12865-025-00753-0"},{"key":"ref_74","unstructured":"Luckins, A.G., Llewelyn, C., Munro, C.D., and Murray, M. (1986). Effects of Pathogenic Trypanosomes on the Mammalian Reproductive System, IAEA."},{"key":"ref_75","first-page":"e82579","article-title":"Chronic inflammation: A multidisciplinary analysis of shared pathways in autoimmune, infectious, and degenerative diseases","volume":"17","author":"Yacine","year":"2025","journal-title":"Cureus"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Przygrodzka, E., Plewes, M.R., and Davis, J.S. (2021). Luteinizing hormone regulation of inter-organelle communication and fate of the corpus luteum. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22189972"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Abedel-Majed, M.A., Romereim, S.M., Davis, J.S., and Cupp, A.S. (2019). Perturbations in lineage specification of granulosa and theca cells may alter corpus luteum formation and function. Front. Endocrinol., 10.","DOI":"10.3389\/fendo.2019.00832"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"63","DOI":"10.12717\/DR.2025.29.3.63","article-title":"The steroidogenic acute regulatory (STAR) gene: Anatomy, expression, and roles","volume":"29","author":"Lim","year":"2025","journal-title":"Dev. Reprod."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"5080843","DOI":"10.1155\/2019\/5080843","article-title":"Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis","volume":"2019","author":"Su","year":"2019","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Almansa-Ordonez, A., Bellido, R., Vassena, R., Barragan, M., and Zambelli, F. (2020). Oxidative stress in reproduction: A mitochondrial perspective. Biology, 9.","DOI":"10.3390\/biology9090269"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1186\/s43556-025-00338-8","article-title":"ROS homeostasis in cell fate, pathophysiology, and therapeutic interventions","volume":"6","author":"Chen","year":"2025","journal-title":"Mol. Biomed."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/s40104-025-01241-6","article-title":"Mechanisms of programmed cell death in livestock follicular development and atresia: A review","volume":"16","author":"Han","year":"2025","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"10166","DOI":"10.1074\/jbc.M111.293274","article-title":"Follicle-stimulating hormone regulates pro-apoptotic protein BimEL-induced porcine granulosa cell apoptosis","volume":"287","author":"Wang","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Zhang, T., Lin, M., Wang, C., and Zhou, J. (2025). Mechanisms of follicular atresia: Focus on apoptosis, autophagy, and ferroptosis. Front. Endocrinol., 16.","DOI":"10.3389\/fendo.2025.1603467"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Liu, S., Jia, Y., Meng, S., Luo, Y., Yang, Q., and Pan, Z. (2023). Mechanisms of and potential medications for oxidative stress in ovarian granulosa cells: A review. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24119205"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1186\/s43556-025-00321-3","article-title":"Cholesterol metabolism: Molecular mechanisms, biological functions, diseases, and therapeutic targets","volume":"6","author":"Cui","year":"2025","journal-title":"Mol. Biomed."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"109521","DOI":"10.1016\/j.steroids.2024.109521","article-title":"Expression of pregnenolone-synthesizing enzymes CYP11A1 and CYP1B1 in the human, rat, and mouse brain","volume":"212","author":"Lin","year":"2024","journal-title":"Steroids"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/s12929-024-01017-6","article-title":"A matter of new life and cell death: Programmed cell death in the mammalian ovary","volume":"31","author":"Chesnokov","year":"2024","journal-title":"J. Biomed. Sci."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"112420","DOI":"10.1016\/j.mce.2024.112420","article-title":"Luteal fibroblasts produce prostaglandins in response to IL-1\u03b2 in a MAPK-mediated manner","volume":"596","author":"Monaco","year":"2025","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_90","first-page":"109","article-title":"Glucocorticoids, stress, and fertility","volume":"35","author":"Whirledge","year":"2010","journal-title":"Minerva Endocrinol."},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Aitken, R.J., Drevet, J.R., Moazamian, A., and Gharagozloo, P. (2022). Male infertility and oxidative stress: A focus on the underlying mechanisms. Antioxidants, 11.","DOI":"10.3390\/antiox11020306"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1080\/10495398.2013.790824","article-title":"Comparative messenger RNA expression of FSH\u03b2, LH\u03b2, FSHR, LHR, and ER\u03b2 in high and low prolific goat breeds","volume":"24","author":"Zi","year":"2013","journal-title":"Anim. Biotechnol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"25310","DOI":"10.18632\/oncotarget.15813","article-title":"Oxidative stress-induced apoptosis in granulosa cells involves JNK, p53 and Puma","volume":"8","author":"Yang","year":"2017","journal-title":"Oncotarget"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"687","DOI":"10.33549\/physiolres.934421","article-title":"Follicle-stimulating hormone inhibits the expression of p53 up-regulated modulator of apoptosis induced by reactive oxygen species through PI3K\/Akt in mouse granulosa cells","volume":"69","author":"Shi","year":"2020","journal-title":"Physiol. Res."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Ibrahim, A., Engku Ismail, E.H., Irwan Khoo, M., Yusuf, L., Nik Hussain, N.H., Mat Zin, A.A., Noordin, L., Abdullah, S., Mahdy, Z.A., and Nik Lah, N.A.Z. (2026). Impaired implantation as a major upstream pathway of preeclampsia: A narrative synthesis of mechanistic, epidemiological and biomarker evidence. Front. Reprod. Health, 7.","DOI":"10.3389\/frph.2025.1743504"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Parker, J., O\u2019Brien, C., Uppal, T., and Tremellen, K. (2025). Molecular impact of metabolic and endocrine disturbance on endometrial function in polycystic ovary syndrome. Int. J. Mol. Sci., 26.","DOI":"10.20944\/preprints202509.1235.v1"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Abdul Hafizz, A.M.H., Mohd Mokthar, N., Zin, R.R.M., Mongan, N.P., Mamat Yusof, M.N., Kampan, N.C., Chew, K.T., and Shafiee, M.N. (2025). Insulin-like growth factor 1 (IGF-1) and its isoforms: Insights into the mechanisms of endometrial cancer. Cancers, 17.","DOI":"10.3390\/cancers17010129"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1007\/s11357-016-9943-9","article-title":"IGF-1 deficiency in a critical period early in life influences the vascular aging phenotype in mice by altering miRNA-mediated post-transcriptional gene regulation","volume":"38","author":"Tarantini","year":"2016","journal-title":"Age"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Kasprzak, A. (2021). Insulin-like growth factor 1 (IGF-1) signaling in glucose metabolism in colorectal cancer. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22126434"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1080\/10253890290027912","article-title":"Stress and reproduction: Central mechanisms and sex differences in non-rodent species","volume":"5","author":"Tilbrook","year":"2002","journal-title":"Stress"},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Oberbauer, A.M. (2013). The regulation of IGF-1 gene transcription and splicing during development and aging. Front. Endocrinol., 4.","DOI":"10.3389\/fendo.2013.00039"},{"key":"ref_102","doi-asserted-by":"crossref","unstructured":"Ranisavljevic, N., Huberlant, S., Montagut, M., Alonzo, P.M., Darn\u00e9, B., Languille, S., Anahory, T., and C\u00e9drin-Durnerin, I. (2022). Low luteal serum progesterone levels are associated with lower ongoing pregnancy and live birth rates in ART: Systematic review and meta-analyses. Front. Endocrinol., 13.","DOI":"10.3389\/fendo.2022.892753"},{"key":"ref_103","doi-asserted-by":"crossref","unstructured":"Lee, S.-H., and Lee, S. (2021). Prostaglandin F2 Alpha Triggers the Disruption of Cell Adhesion with Cytokeratin and Vimentin in Bovine Luteal Theca Cells. Animals, 11.","DOI":"10.3390\/ani11041073"},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Arrebola, F.A., Torres-Martell, R., Gonz\u00e1lez-Casquet, O., Meza-Herrera, C.A., and P\u00e9rez-Mar\u00edn, C.C. (2022). Periovulatory hormonal profiles after estrus induction and conception rate by fixed-time artificial insemination in Payoya goats during the anestrous season. Animals, 12.","DOI":"10.3390\/ani12202853"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0378-4320(00)00172-X","article-title":"Disruption of spermatogenesis in boars sub-clinically infected with Trypanosoma brucei brucei","volume":"63","author":"Omeke","year":"2000","journal-title":"Anim. Reprod. Sci."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"537","DOI":"10.5455\/javar.2020.g451","article-title":"Changes of reproductive indices of the testis due to Trypanosoma evansi infection in dromedary bulls (Camelus dromedarius)","volume":"7","author":"Amin","year":"2020","journal-title":"J. Adv. Vet. Anim. Res."},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Abdel-Hakeem, S.S., Megahed, G., Al-Hakami, A.M., Tolba, M.E.M., and Karar, Y.F.M. (2025). Impact of trypanosomosis on male camel infertility. Front. Vet. Sci., 11.","DOI":"10.3389\/fvets.2024.1506532"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.theriogenology.2021.04.015","article-title":"Vitamin E and selenium supplementation synergistically alleviate the injury induced by hydrogen peroxide in bovine granulosa cells","volume":"170","author":"Wang","year":"2021","journal-title":"Theriogenology"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s12958-018-0323-4","article-title":"Role of L-carnitine in female infertility","volume":"16","author":"Agarwal","year":"2018","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Dutta, S., Sengupta, P., Slama, P., and Roychoudhury, S. (2021). Oxidative stress, testicular inflammatory pathways, and male reproduction. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms221810043"},{"key":"ref_111","doi-asserted-by":"crossref","unstructured":"Monageng, E., Offor, U., Takalani, N.B., Mohlala, K., and Opuwari, C.S. (2023). A review on the impact of oxidative stress and medicinal plants on Leydig cells. Antioxidants, 12.","DOI":"10.3390\/antiox12081559"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"1302","DOI":"10.1111\/andr.13772","article-title":"Immunoregulation and male reproductive function: Impacts and mechanistic insights into inflammation","volume":"13","author":"Ma","year":"2025","journal-title":"Andrology"},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Zhou, J., Hu, S., Ouyang, Y., Kong, Y., and Liu, M. (2025). Immunometabolism and male reproductive function: Linking inflammation, oxidative stress, and declining fertility. Front. Immunol., 16.","DOI":"10.3389\/fimmu.2025.1736492"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"17562872221105017","DOI":"10.1177\/17562872221105017","article-title":"Understanding and managing the suppression of spermatogenesis caused by testosterone replacement therapy and anabolic-androgenic steroids","volume":"14","author":"Desai","year":"2022","journal-title":"Ther. Adv. Urol."},{"key":"ref_115","doi-asserted-by":"crossref","unstructured":"Lei, T., Yang, Y., and Yang, W.X. (2025). Luteinizing hormone regulates testosterone production, Leydig cell proliferation, differentiation, and circadian rhythm during spermatogenesis. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26083548"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s12958-024-01333-4","article-title":"The role of luteinizing hormone activity in spermatogenesis: From physiology to clinical practice","volume":"23","author":"Esteves","year":"2025","journal-title":"Reprod. Biol. Endocrinol."}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/13\/6\/535\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T02:27:09Z","timestamp":1780626429000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/13\/6\/535"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,29]]},"references-count":116,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["vetsci13060535"],"URL":"https:\/\/doi.org\/10.3390\/vetsci13060535","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,29]]}}}