{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,11]],"date-time":"2026-06-11T11:29:41Z","timestamp":1781177381725,"version":"3.54.1"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,8,2]],"date-time":"2025-08-02T00:00:00Z","timestamp":1754092800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,8,2]],"date-time":"2025-08-02T00:00:00Z","timestamp":1754092800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100002386","name":"Cairo University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100002386","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Equine habronemiasis, caused by\u00a0<jats:italic>Habronema<\/jats:italic> (<jats:italic>H.<\/jats:italic>) <jats:italic>muscae<\/jats:italic>,\u00a0<jats:italic>H. microstoma<\/jats:italic>, and\u00a0<jats:italic>Draschia megastoma<\/jats:italic>, is a parasitic disease that presents in both gastric and cutaneous forms. Conventional diagnostic methods often lack sensitivity due to intermittent egg shedding and nonspecific clinical signs. This study aimed to enhance diagnostic accuracy by integrating molecular identification, oxidative stress profiling, and cytokine gene expression analysis.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Methods<\/jats:title>\n            <jats:p>A total of 100 horses from a private farm in Giza, Egypt, were clinically examined for signs of habronemiasis. Fecal and skin samples were examined using parasitological techniques alongside polymerase chain reaction (PCR) targeting the mitochondrial cytochrome c oxidase subunit I (COXI) gene. The serum levels of oxidative stress biomarkers, including malondialdehyde (MDA), superoxide dismutase (SOD), glutathione (GSH), and total antioxidant capacity (TAC), were quantified. Additionally, the expression of cytokines (interferon-gamma (<jats:italic>IFN-\u03b3<\/jats:italic>), tumor necrosis factor-alpha (<jats:italic>TNF-\u03b1<\/jats:italic>),\u00a0interleukin 1 beta (<jats:italic>IL-1\u03b2<\/jats:italic>) and interleukin-6 (<jats:italic>IL-6<\/jats:italic>))was assessed via real-time PCR.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>\n              <jats:italic>Habronema<\/jats:italic>\u00a0spp. eggs were detected in 62% of fecal samples, with molecular analysis confirming\u00a0<jats:italic>H. muscae<\/jats:italic>\u00a0as the predominant species. Infected horses exhibited significantly elevated oxidative stress markers compared with those in healthy controls. Cytokine gene expression analysis demonstrated a marked upregulation of proinflammatory markers, indicating a Th1-dominated immune response.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusions<\/jats:title>\n            <jats:p>This study underscores the value of molecular diagnostics combined with immunological profiling for the detection and characterization of equine habronemiasis. The integration of oxidative stress and cytokine biomarkers provides important insights into host\u2013pathogen interactions and may contribute to the development of improved diagnostic and therapeutic strategies.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Graphical Abstract<\/jats:title>\n          <\/jats:sec>","DOI":"10.1186\/s13071-025-06970-1","type":"journal-article","created":{"date-parts":[[2025,8,2]],"date-time":"2025-08-02T14:00:56Z","timestamp":1754143256000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Innovative diagnostic strategies for equine habronemiasis: exploring molecular identification, gene expression, and oxidative stress markers"],"prefix":"10.1186","volume":"18","author":[{"given":"Mai A.","family":"Salem","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sohila M.","family":"El-Gameel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed S.","family":"Kamel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eslam M.","family":"Elsamman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reem M.","family":"Ramadan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,8,2]]},"reference":[{"key":"6970_CR1","doi-asserted-by":"publisher","first-page":"4299","DOI":"10.1007\/s00436-016-5212-1","volume":"115","author":"K Morsy","year":"2016","unstructured":"Morsy K, Bashtar AR, Al Quraishy S, Adel S. Description of two equine nematodes, Parascaris equorum and Habronema microstoma from the domestic horse in Egypt. Parasitol Res. 2016;115:4299\u2013306.","journal-title":"Parasitol Res"},{"key":"6970_CR2","doi-asserted-by":"publisher","DOI":"10.3389\/fvets.2020.00358","volume":"7","author":"A Barlaam","year":"2020","unstructured":"Barlaam A, Traversa D, Papini R, Giangaspero A. Habronematidosis in equids: current status, advances, future challenges. Front Vet Sci. 2020;7:358.","journal-title":"Front Vet Sci"},{"key":"6970_CR3","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/j.jevs.2013.06.004","volume":"34","author":"DG Pugh","year":"2014","unstructured":"Pugh DG, Hu XP, Blagburn B. Habronemiasis: biology, signs, diagnosis, treatment and prevention of the nematodes and vector flies. J Equine Vet Sci. 2014;34:241\u20138.","journal-title":"J Equine Vet Sci"},{"key":"6970_CR4","doi-asserted-by":"publisher","first-page":"4439","DOI":"10.1007\/s00436-014-4123-2","volume":"113","author":"E Rakhshandehroo","year":"2014","unstructured":"Rakhshandehroo E, Sharifiyazdi H, Shayegh H, Ahmadi A. Molecular and morphological comparison of two different types of Habronema muscae in horse. Parasitol Res. 2014;113:4439\u201345.","journal-title":"Parasitol Res"},{"key":"6970_CR5","doi-asserted-by":"publisher","DOI":"10.1016\/j.rvsc.2024.105525","volume":"184","author":"LC Calixto-Vega","year":"2025","unstructured":"Calixto-Vega LC, Castro-Mesa AF, Mart\u00ednez-Aranzales JR. Gastric habronematidosis in mules: gastroscopy and histopathology-based diagnosis. Res Vet Sci. 2025;184:105525.","journal-title":"Res Vet Sci"},{"key":"6970_CR6","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1007\/s11230-017-9714-8","volume":"94","author":"R Jian","year":"2017","unstructured":"Jian R, Wang SW, Zhang WX, Zhang LP. Morphological and molecular identification of Habronema spp. (Nematoda: Habronematidae) from donkeys in Xinjiang, China, and notes on the taxonomical status of Habronema majus and H. microstoma. Syst Parasitol. 2017;94:511\u201325.","journal-title":"Syst Parasitol"},{"key":"6970_CR7","first-page":"100295","volume":"17","author":"CN Devi","year":"2019","unstructured":"Devi CN, Borthakur SK, Patra G, Singh NS, Tolenkhomba TC, Ravindran R, et al. Incidence of cutaneous habronemosis in Manipuri ponies in India. Vet Parasitol Reg Stud Rep. 2019;17:100295.","journal-title":"Vet Parasitol Reg Stud Rep"},{"key":"6970_CR8","doi-asserted-by":"publisher","first-page":"46","DOI":"10.58803\/fahn.v1i2.12","volume":"1","author":"D Forouzanpour","year":"2022","unstructured":"Forouzanpour D, Ostovari G, Mashhadi M, Dehghani H, Hajimohammadi A. Habronemiasis (equine summer sore) in an 8-year-old Arab horse. Farm Anim Health Nutr. 2022;1:46\u20139.","journal-title":"Farm Anim Health Nutr"},{"key":"6970_CR9","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.vetpar.2018.03.023","volume":"255","author":"W El-Deeb","year":"2018","unstructured":"El-Deeb W, Iacob O, Fayez M, Elgioushy M, Shawaf T, Ibrahim A. Acute phase proteins, interleukin-6, tumor necrosis factor, nitric oxide and oxidative stress markers in horses with cutaneous habronemosis under field condition. Vet Parasitol. 2018;255:20\u20135.","journal-title":"Vet Parasitol"},{"key":"6970_CR10","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.vetpar.2014.07.005","volume":"205","author":"B Esmaeilnejad","year":"2014","unstructured":"Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Malekinejad H, Jalilzadeh-Amin G, et al. Evaluation of antioxidant status, oxidative stress and serum trace mineral levels associated with Babesia ovis parasitemia in sheep. Vet Parasitol. 2014;205:38\u201345.","journal-title":"Vet Parasitol"},{"key":"6970_CR11","doi-asserted-by":"publisher","first-page":"761264","DOI":"10.1155\/2014\/761264","volume":"2014","author":"A Rahal","year":"2014","unstructured":"Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, et al. Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int. 2014;2014:761264.","journal-title":"Biomed Res Int"},{"key":"6970_CR12","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1177\/0192623309356453","volume":"38","author":"JE Klaunig","year":"2009","unstructured":"Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol. 2009;38:96\u2013109.","journal-title":"Toxicol Pathol"},{"key":"6970_CR13","doi-asserted-by":"publisher","first-page":"5351","DOI":"10.1182\/blood-2012-02-368076","volume":"119","author":"RJ Robb","year":"2012","unstructured":"Robb RJ, Hill GR. The interferon-dependent orchestration of innate and adaptive immunity after transplantation. Blood. 2012;119:5351\u20138.","journal-title":"Blood"},{"key":"6970_CR14","doi-asserted-by":"publisher","DOI":"10.1016\/j.rvsc.2023.105097","volume":"166","author":"MA Salem","year":"2024","unstructured":"Salem MA, Mahdy OA, Ramadan RM. Ultra-structure, genetic characterization and immunological approach of fish borne zoonotic trematodes (Family: Heterophyidae) of a redbelly tilapia. Res Vet Sci. 2024;166:105097.","journal-title":"Res Vet Sci"},{"key":"6970_CR15","doi-asserted-by":"publisher","DOI":"10.1016\/j.cimid.2020.101453","volume":"70","author":"E Mostafavi","year":"2020","unstructured":"Mostafavi E, Esmaeilnejad B, Abtahi Foroushani MS. Evaluation of cytokines and sialic acids contents in horses naturally infected with Theileria equi. Comp Immunol Microbiol Infect Dis. 2020;70:101453.","journal-title":"Comp Immunol Microbiol Infect Dis"},{"key":"6970_CR16","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1007\/s00436-008-1276-x","volume":"104","author":"R Iorio","year":"2008","unstructured":"Iorio R, \u0160lapeta J, Otranto D, Paoletti B, Giangaspero A, Traversa D. Phylogenetic relationships of Habronema microstoma and Habronema muscae (Spirurida: Habronematidae) within the order Spirurida inferred using mitochondrial cytochrome c oxidase subunit 1 (cox1) gene analysis. Parasitol Res. 2008;104:979\u201384.","journal-title":"Parasitol Res"},{"key":"6970_CR17","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1007\/s10493-024-00933-4","volume":"93","author":"RM Ramadan","year":"2024","unstructured":"Ramadan RM, Taha NM, Auda HM, Elsamman EM, El-Bahy MM, Salem MA. Molecular and immunological studies on Theileria equi and its vector in Egypt. Exp Appl Acarol. 2024;93:439\u201358.","journal-title":"Exp Appl Acarol"},{"key":"6970_CR18","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1186\/s13071-024-06564-3","volume":"17","author":"RM Ramadan","year":"2024","unstructured":"Ramadan RM, Bakr AF, Fouad E, Mohammed FF, Abdel-Wahab AM, Abdel-Maogood SZ, et al. Novel insights into antioxidant status, gene expression, and immunohistochemistry in an animal model infected with camel-derived Trypanosoma evansi and Theileria annulata. Parasit Vectors. 2024;17:474.","journal-title":"Parasit Vectors"},{"key":"6970_CR19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12917-025-04821-w","volume":"21","author":"RM Ramadan","year":"2025","unstructured":"Ramadan RM, Khalifa MM, Youssef FS, Fouad EA, Kamel M, El-Bahy MM, et al. A paradigm shift in trichinellosis management: curcumin\u2013olive oil nanocomposite\u2019s multi-faceted therapeutic approach. BMC Vet Res. 2025;21:1\u201313.","journal-title":"BMC Vet Res"},{"key":"6970_CR20","first-page":"101283","volume":"62","author":"FA Gamal","year":"2025","unstructured":"Gamal FA, Abdel-Wahab AM, Khalifa MM, Ramadan RM, Nassar AM. Incidence, genetic characterization and phylogenetic analysis of Cryptosporidium species infecting domestic pigeons (Columba livia domestica) in Egypt. Vet Parasitol Reg Stud Rep. 2025;62:101283.","journal-title":"Vet Parasitol Reg Stud Rep"},{"key":"6970_CR21","doi-asserted-by":"publisher","DOI":"10.1186\/s12917-024-04295-2","volume":"20","author":"MM Attia","year":"2024","unstructured":"Attia MM, Barsoum SS, Baghdadi HBA, Mahdy OA, El Gameel SM. Evaluation of different inflammatory markers during the infection of domestic cats (Felis catus) by Cystoisospora felis (Coccidia: Apicomplexa). BMC Vet Res. 2024;20:516.","journal-title":"BMC Vet Res"},{"key":"6970_CR22","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.ijvsm.2016.10.003","volume":"4","author":"NY Salem","year":"2016","unstructured":"Salem NY, Yehia SG, Farag HS, Elkhiat MA. Clinical, hemato-biochemical alterations and oxidant\u2013antioxidant biomarkers in Babesia-infected calves. Int J Vet Sci Med. 2016;4:17\u201322.","journal-title":"Int J Vet Sci Med"},{"key":"6970_CR23","doi-asserted-by":"publisher","first-page":"22026","DOI":"10.1038\/s41598-024-72433-9","volume":"14","author":"MA Salem","year":"2024","unstructured":"Salem MA, Taha NM, El-Bahy MM, Ramadan RM. Phylogenetic position of the pigeon mite, Ornithonyssus sylviarum, with amplification of its immunogenetic biomarkers in Egypt. Sci Rep. 2024;14:22026.","journal-title":"Sci Rep"},{"key":"6970_CR24","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method. Methods. 2001;25:402\u20138.","journal-title":"Methods"},{"key":"6970_CR25","doi-asserted-by":"publisher","DOI":"10.1186\/s12917-025-04616-z","volume":"21","author":"NM Taha","year":"2025","unstructured":"Taha NM, Salem MA, El-Saied MA, Mohammed FF, Kamel M, El-Bahy MM, et al. Multifaceted analysis of equine cystic echinococcosis: genotyping, immunopathology, and screening of repurposed drugs against E. equinus protoscolices. BMC Vet Res. 2025;21:178.","journal-title":"BMC Vet Res"},{"key":"6970_CR26","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0303702","volume":"19","author":"RM Ramadan","year":"2024","unstructured":"Ramadan RM, Mahdy OA, El-Saied MA, Mohammed FF, Salem MA. Novel insights into immune stress markers associated with myxosporeans gill infection in Nile tilapia. PLoS ONE. 2024;19:e0303702.","journal-title":"PLoS ONE"},{"key":"6970_CR27","doi-asserted-by":"publisher","first-page":"2173","DOI":"10.1016\/j.sjbs.2021.11.044","volume":"29","author":"MM Attia","year":"2022","unstructured":"Attia MM, Soliman SM, Salaeh NMK, Salem HM, Alkafafy M, Saad AM, et al. Evaluation of immune responses and oxidative stress in donkeys: immunological studies provoked by Parascaris equorum infection. Saudi J Biol Sci. 2022;29:2173\u20139.","journal-title":"Saudi J Biol Sci"},{"key":"6970_CR28","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1111\/evj.12280","volume":"47","author":"A Betancourt","year":"2014","unstructured":"Betancourt A, Lyons ET, Horohov DW. Characterisation of the inflammatory cytokine response to anthelmintic treatment in ponies. Equine Vet J. 2014;47:240\u20134.","journal-title":"Equine Vet J"},{"key":"6970_CR29","doi-asserted-by":"publisher","DOI":"10.1016\/j.exppara.2023.108650","volume":"255","author":"MM El-Bahy","year":"2023","unstructured":"El-Bahy MM, Kamel NO, Auda HM, Ramadan RM. A smart economic way to control camel parasites and improve camel production in Egypt. Exp Parasitol. 2023;255:108650.","journal-title":"Exp Parasitol"},{"key":"6970_CR30","first-page":"101025","volume":"51","author":"NM Taha","year":"2024","unstructured":"Taha NM, Sabry MA, El-Bahy MM, Ramadan RM. Awareness of parasitic zoonotic diseases among pet owners in Cairo, Egypt. Vet Parasitol Reg Stud Rep. 2024;51:101025.","journal-title":"Vet Parasitol Reg Stud Rep"},{"key":"6970_CR31","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/j.vetpar.2006.05.021","volume":"141","author":"D Traversa","year":"2006","unstructured":"Traversa D, Iorio R, Capelli G, Paoletti B, Bartolini R, Otranto D, et al. Molecular cross-sectional survey of gastric habronemosis in horses. Vet Parasitol. 2006;141:285\u201390.","journal-title":"Vet Parasitol"},{"key":"6970_CR32","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1208\/s12249-015-0405-y","volume":"17","author":"A Nazarizadeh","year":"2015","unstructured":"Nazarizadeh A, Asri-Rezaie S. Comparative study of antidiabetic activity and oxidative stress induced by zinc oxide nanoparticles and zinc sulfate in diabetic rats. AAPS PharmSciTech. 2015;17:834\u201343.","journal-title":"AAPS PharmSciTech"},{"key":"6970_CR33","doi-asserted-by":"publisher","first-page":"541571","DOI":"10.1155\/2012\/541571","volume":"2012","author":"C Maia","year":"2012","unstructured":"Maia C, Campino L. Cytokine and phenotypic cell profiles of Leishmania infantum infection in the dog. J Trop Med. 2012;2012:541571.","journal-title":"J Trop Med"},{"key":"6970_CR34","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2011.00002","volume":"2","author":"SJ Sasindran","year":"2011","unstructured":"Sasindran SJ, Torrelles JB. Mycobacterium tuberculosis infection and inflammation: what is beneficial for the host and for the bacterium? Front Microbiol. 2011;2:2.","journal-title":"Front Microbiol"},{"key":"6970_CR35","doi-asserted-by":"publisher","first-page":"1583","DOI":"10.1016\/j.joca.2012.08.008","volume":"20","author":"TN Ross","year":"2012","unstructured":"Ross TN, Kisiday JD, Hess T, McIlwraith CW. Evaluation of the inflammatory response in experimentally induced synovitis in the horse: a comparison of recombinant equine interleukin 1 beta and lipopolysaccharide. Osteoarthritis Cartilage. 2012;20:1583\u201390.","journal-title":"Osteoarthritis Cartilage"}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-025-06970-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13071-025-06970-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-025-06970-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,8]],"date-time":"2025-09-08T12:19:46Z","timestamp":1757333986000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/s13071-025-06970-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,2]]},"references-count":35,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["6970"],"URL":"https:\/\/doi.org\/10.1186\/s13071-025-06970-1","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,2]]},"assertion":[{"value":"16 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 July 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 August 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This study was conducted and approved in accordance with the guidelines of the Institutional Animal Care and Use Committee (IACUC-VET-CU-110520251130) of the Faculty of Veterinary Medicine, Cairo University.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"325"}}