FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Front Vet Sci / Exploring Histoplasma species seroprevalence and risk factor...
Frontiers in veterinary science2024; 11; 1444887; doi: 10.3389/fvets.2024.1444887

Exploring Histoplasma species seroprevalence and risk factors for seropositivity in The Gambia’s working equid population: Baseline analysis of the Tackling Histoplasmosis project dataset.

Abstract: Exposure rates to species, the causative agent of equine epizootic lymphangitis (EL), are unknown amongst working equids in The Gambia. The primary aims of this study were to estimate anti- antibody seroprevalence in the equid population in rural The Gambia and to explore risk factors for seropositivity. Unassigned: A nationwide cross-sectional study was conducted (February-July 2022), representing baseline measurements of a longitudinal cohort study. Horses ( 463) and donkeys ( = 92) without EL signs were recruited in 18 study sites. Following informed owner consent, equid clinical and management data were recorded. Blood samples were collected by jugular venepuncture, and sera were subject to the IMMY Latex Agglutination test (LAT). Seropositivity risk factors were explored by multi-level, multivariable logistic regression analysis. Study site and household variance were described using a latent-variable approach. Whole blood DNA extractions were subject to nested ITS-PCR to detect var. (HCF), and agreement with LAT results was measured using Cohen's kappa statistic. Unassigned: Anti- antibody seroprevalence in horses and donkeys was 79.9% [95% confidence interval (CI) 76.0-83.5%] and 46.7% (95% CI 36.3-57.4%), respectively. In , two multivariable models explained the maximum amount of data variability. Model 1 demonstrated increased odds of seropositivity in mares [odds ratio (OR) = 2.90 95% CI 1.70-4.95,  < 0.001] and decreased odds in horses <2.5 years (OR = 0.46 95% CI 0.22-0.95,  = 0.04; reference: ≥4.5 years). Model 2 demonstrated increased odds in horses recruited during the rainy season (OR = 2.03 95% CI 1.08-3.84,  = 0.03) and those owned by farmers reporting previous EL in their equids (OR = 1.87 95% CI 1.04-3.37,  = 0.04). Decreased odds were measured in horses <2.5 years (OR = 0.37 95% CI 0.18-0.78,  = 0.01) and horses reported to transport firewood (OR = 0.45 95% CI 0.28-0.74,  = 0.001). On multivariable analysis of , decreased odds of seropositivity were demonstrated amongst donkeys owned by households which also owned horses (OR = 0.23 95% CI 0.06-0.85,  = 0.03). HCF infection prevalence in horses and donkeys was 22.0% ( = 102/463, 95% CI 18.3-26.1%) and 5.4% ( = 5/92, 95% CI 1.8-12.2%), respectively. No significant agreement was measured between LAT and nested ITS-PCR results ( < 0.00). Unassigned: High spp. exposure was demonstrated amongst equids in The Gambia. Investigation of risk factors, including equid husbandry and management strategies, as well as geoclimatic variations, is warranted. Outcomes may inform sustainable and equitable EL control strategies in The Gambia and comparable settings worldwide.
Copyright © 2024 Cornell, Fye, Nyassi, Ceesay, Jallow, Langendonk, Wootton, Pinchbeck and Scantlebury.
Get Full Text
Publication Date: 2024-09-19 PubMed ID: 39364262PubMed Central: PMC11446873DOI: 10.3389/fvets.2024.1444887Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article examines the prevalence and risk factors of Histoplasma species exposure among working horses and donkeys in The Gambia. It found that a high percentage of these animals have been exposed to this agent of equine epizootic lymphangitis (EL), with certain risk factors playing a crucial role. Uncovering these aspects can help develop effective disease control strategies.

Study Design and Methodology

  • The research employed a nationwide cross-sectional study, conducted from February to July 2022. The data collected serves as the baseline measurements for a forthcoming longitudinal cohort study.
  • The sample size comprised 463 horses and 92 donkeys from 18 different study sites, with all animals showing no EL signs. All owners gave informed consent before the study commenced.
  • The researchers collected blood samples and recorded clinical and management data for each animal. The blood samples underwent the IMMY Latex Agglutination test for testing Histoplasma antibody presence.
  • Risk factors to seropositivity were explored using multi-level, multivariable logistic regression analysis.
  • Additionally, whole blood DNA extractions were subject to nested ITS-PCR to detect Histoplasma Capsulatum Fungus (HCF), and agreement with the Latex Agglutination test results was measured.

Results and Findings

  • The findings revealed a Histoplasma antibody seroprevalence of 79.9% in horses and 46.7% in donkeys.
  • The study identified several risk factors influencing seropositivity—age, gender, season of recruitment, owner’s history of equine lymphangitis, and the type of work these animals perform. For instance, mares, older horses, horses recruited during the rainy season, and those owned by farmers with a previous EL history in their equids were found to have higher rates of seropositivity. The transport of firewood reduced the odds of seropositivity in horses.
  • A lower seropositivity rate was observed in donkeys owned by households that also owned horses.
  • The results from the study also showed an HCF infection prevalence of 22.0% in horses and 5.4% in donkeys, with no significant agreement dialogued between the Latex Agglutination test and nested ITS-PCR results.

Implications

  • The high seroprevalence of Histoplasma species among working equids in The Gambia highlights the importance of further investigation into risk factors such as animal management strategies, and the effect of geoclimatic variations.
  • The findings of this study could help guide the development of sustainable and equitable equine lymphangitis control strategies, not only in The Gambia but also in other regions across the globe with similar situations.

Cite This Article

APA
Cornell TR, Fye BL, Nyassi E, Ceesay F, Jallow M, Langendonk RF, Wootton DG, Pinchbeck G, Scantlebury CE. (2024). Exploring Histoplasma species seroprevalence and risk factors for seropositivity in The Gambia’s working equid population: Baseline analysis of the Tackling Histoplasmosis project dataset. Front Vet Sci, 11, 1444887. https://doi.org/10.3389/fvets.2024.1444887

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 11
Pages: 1444887
PII: 1444887

Researcher Affiliations

Cornell, Tessa Rose
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Fye, Biram Laity
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Nyassi, Edrisa
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Ceesay, Fatou
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Jallow, Mahmud
  • Department of Livestock Services (DLS), Ministry of Agriculture, Livestock and Food Security, Abuko, Gambia.
Langendonk, R Frèdi
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Wootton, Dan G
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
  • NIHR Health Protection Research Unit in Emerging and Zoonotic Diseases, University of Liverpool, Liverpool, United Kingdom.
Pinchbeck, Gina
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.
Scantlebury, Claire Elizabeth
  • Institute of Infection, Veterinary, and Ecological Sciences (IVES), University of Liverpool, Liverpool, United Kingdom.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 66 references
  1. Allan FK. A landscaping analysis of working equid population numbers in LMICs, with policy recommendations.. (2021).
  2. The Brooke, Food and Agriculture Organization of the United Nations (FAO). The role, impact and welfare of working (traction and transport) animals.. Animal Production and Health Report 2014.
  3. Grace DC, Diall O, Saville K, Warboys D, Ward P, Wild I. The global contributions of working equids to sustainable agriculture and livelihoods in agenda 2030.. EcoHealth (2022) 19:342.
    doi: 10.1007/s10393-022-01613-8pmc: PMC9434516pubmed: 36048298google scholar: lookup
  4. Bekele M, Leggese G, Teshome W, Nahom W, Anteneh K, Tewodros T. Socioeconomic impact of epizootic lymphangitis in cart mules in Bahir Dar City, north West Ethiopia.. Proceedings of the 7th International Colloquium on Working Equids 2014 pp. 10–15.
  5. Scantlebury CE, Zerfu A, Pinchbeck GP, Reed K, Gebreab F, Aklilu N. Participatory appraisal of the impact of epizootic lymphangitis in Ethiopia.. Prev Vet Med (2015) 120:265–76.
    doi: 10.1016/j.prevetmed.2015.03.012pubmed: 25980831google scholar: lookup
  6. Nigatu A, Abebaw Z. Socioeconomic impact of epizootic Lymphangitis (EL) on horse-drawn taxi business in Central Ethiopia.. The 6th international colloquium on working equids: Learning from others 2010 pp. 83–86.
  7. Robertson E, Abera C, Wood K, Deressa K, Mesfin S, Scantlebury C. Striving towards access to essential medicines for human and animal health; a situational analysis of access to and use of antifungal medications for histoplasmosis in Ethiopia.. PLoS One (2023) 18:e0278964.
    doi: 10.1371/journal.pone.0278964pmc: PMC9997978pubmed: 36893127google scholar: lookup
  8. Jones K. Epizootic lymphangitis: the impact on subsistence economies and animal welfare.. Vet J (2006) 172:402–4.
    doi: 10.1016/j.tvjl.2006.06.003pubmed: 16899380google scholar: lookup
  9. Richer FJC. La Lymphangite épizootique: revue générale de la maladie et observations cliniques en République du Sénégal.. These Ecole Nationale Veterinaire d’Alfort 1977.
  10. Abdullahi AS, Abdullahi B, Bale US, Sackey AKB, Musa GA, Babashani C. Detection and clinical manifestation of epizootic Lymphangitis in horses in Zaria and Kontagora emirates, Nigeria.. Savannah Vet J (2019) 2:7–12.
    doi: 10.36759/svj.2018.029google scholar: lookup
  11. Fisher LWS, Ceesay A, Jallow D, Hawkes SF, Showering A, Kane Y. Validation of a real-time polymerase chain reaction for the detection and quantification of the nucleic acid of Histoplasma from equine clinical samples.. Microbiol Spectr (2024) 12:e03100-23.
    doi: 10.1128/spectrum.03100-23pmc: PMC10986522pubmed: 38411051google scholar: lookup
  12. Hadush B, Ameni G, Medhin G. Equine histoplasmosis: treatment trial in cart horses in Central Ethiopia.. Trop Anim Health Prod (2008) 40:407–11.
    doi: 10.1007/s11250-007-9099-9pubmed: 18575967google scholar: lookup
  13. WOAH. Terrestrial Manual. Chapter 3.6.4. Epizootic Lymphangitis.. (2018).
  14. Scantlebury C, Reed K. Epizootic Lymphangitis. Review chapter. Infectious diseases of the horse 2009.
  15. Duguma BE, Tesfaye T, Kassaye A, Kassa A, Blakeway SJ. Control and prevention of epizootic Lymphangitis in mules: an integrated community-based intervention, Bahir Dar, Ethiopia.. Front Vet Sci (2021) 8:648267.
    doi: 10.3389/fvets.2021.648267pmc: PMC8632952pubmed: 34869708google scholar: lookup
  16. World Health Organization. WHO fungal priority pathogens list to guide research, development and public health action.. (2022).
  17. Dos Santos B, Langoni H, da Silva RC, Menozzi BD, Bosco S De MG, Paiz LM. Molecular detection of Histoplasma capsulatum in insectivorous and frugivorous bats in Southeastern Brazil.. Med Mycol (2018) 56:937–40.
    doi: 10.1093/mmy/myx138pubmed: 29294049google scholar: lookup
  18. Gugnani HC, Muotoe-Okafor FA, Kaufman L, Dupont B. A natural focus of Histoplasma capsulatum var. duboisii is a bat cave.. Mycopathologia (1994) 127:151–7.
    doi: 10.1007/BF01102915pubmed: 7808510google scholar: lookup
  19. Denton JF, DiSalvo AF. The isolation of Histoplasma capsulatum, Cryptococcus neoformans and Blastomyces dermatitidis from the same natural site.. Sabouraudia (1979) 17:193–5.
    doi: 10.1080/00362177985380281pubmed: 394361google scholar: lookup
  20. Department of Livestock Services Ministry of Agriculture. The Gambia National Livestock Census 2016.. 2016.
  21. Endebu B, Roger F. Comparative studies on the occurrence and distribution of epizootic Lymphangitis and ulcerative Lymphangitis in Ethiopia.. Int J Appl Res Vet Med (2003).
  22. Thrusfield M. Veterinary epidemiology.. 4th ed. (2018).
  23. Brooke T. The working equid veterinary manual - chapter 10: The teeth - ageing and a practical approach to dentistry.. (2013).
  24. IMMY. LA-Coccidioides, LA-Histoplasma, and LA-Sporothrix antibody systems.. IMMY Packag Inser (2018).
  25. QIAGEN. DNeasy Blood & Tissue Handbook.. (2020).
  26. Scantlebury CE, Pinchbeck GL, Loughnane P, Aklilu N, Ashine T, Stringer AP. Development and evaluation of a molecular diagnostic method for rapid detection of Histoplasma capsulatum var. farciminosum, the causative agent of epizootic Lymphangitis, in equine clinical samples.. J Clin Microbiol (2016) 54.
    doi: 10.1128/JCM.00896-16pmc: PMC5121390pubmed: 27707938google scholar: lookup
  27. Epitools. Estimated true prevalence and predictive values from survey testing.. (2021).
  28. Mathewos M, Bukero R, Endale H, Mekbib B, Giday W, Mekore D. Study on prevalence and associated risk factors of epizootic lymphangitis in equine in Nagele Arsi town, southeastern Ethiopia.. Res Vet Sci (2023) 161:80–5.
    doi: 10.1016/j.rvsc.2023.06.008pubmed: 37327692google scholar: lookup
  29. Hosmer DW, Lemeshow S. Model-building strategies and methods for logistic regression. Applied logistic regression 2nd ed. (2000) 91–128.
  30. Goldstein H, Browne W, Rasbash J. Partitioning variation in multilevel models.. Underst Stat (2002) 1:223–31.
    doi: 10.1207/S15328031US0104_02pubmed: 0google scholar: lookup
  31. Altman D. Practical statistics for medical research.. (1999).
  32. World Organisation for Animal Health (WOAH). WAHIS - country dashboard: disease situation.. (2023).
  33. Ashraf N, Kubat RC, Poplin V, Adenis AA, Denning DW, Wright L. Re-drawing the maps for endemic mycoses.. Mycopathologia (2020) 185:843–65.
    doi: 10.1007/s11046-020-00431-2pmc: PMC7416457pubmed: 32040709google scholar: lookup
  34. Taylor ML, del Rocío Reyes-Montes M, Estrada-Bárcenas DA, Zancopé-Oliveira RM, Rodríguez-Arellanes G, Ramírez JA. Considerations about the geographic distribution of Histoplasma species.. Appl Environ Microbiol (2022) 88:e0201021.
    doi: 10.1128/aem.02010-21pmc: PMC9004366pubmed: 35262368google scholar: lookup
  35. Chandler JW, Smith TK, Newberry WM, Chin TDY, Kirkpatrickt CH. Immunology of the mycoses. II. Characterization of the immunoglobulin and antibody responses in histoplasmosis.. J Infect Dis (1969) 119:247–54.
    doi: 10.1093/infdis/119.3.247pubmed: 4181002google scholar: lookup
  36. Wheat LJ, Kohler RB, French MLV, Garten M, Kleiman M, Zimmerman SE. Immunoglobulin M and G Histoplasmal antibody response in histoplasmosis.. Am J Respir Dis (1983) 128:65–70.
    pubmed: 6408962
  37. Gabal MA, Khalifa K. Study on the immune response and serological diagnosis of equine histoplasmosis (epizootic lymphangitis).. Zentralblatt fur Vet B (1983) 30:317–21.
    doi: 10.1111/j.1439-0450.1983.tb01850.xpubmed: 6613411google scholar: lookup
  38. Molla AM, Temesgen Jemberu W, Fentahun T. Prevalence and risk factors of epizootic lymphangitis in cart pulling horses and mules in central and South Gondar zones, Amhara region, Ethiopia.. Heliyon (2022) 8:e09939.
    doi: 10.1016/j.heliyon.2022.e09939pmc: PMC9343934pubmed: 35928106google scholar: lookup
  39. Abdela MG, Teshale S, Gobena MM, Zewde A, Jaleta H, Gumi B. Epidemiology of epizootic Lymphangitis among carthorses in Ethiopia.. Front Vet Sci (2021) 8:762937.
    doi: 10.3389/fvets.2021.762937pmc: PMC8713507pubmed: 34970614google scholar: lookup
  40. Ameni G, Terefe W. A cross-sectional study of epizootic lymphangitis in cart-mules in western Ethiopia.. Prev Vet Med (2004) 66:93–9.
    doi: 10.1016/j.prevetmed.2004.09.008pubmed: 15579337google scholar: lookup
  41. Hadush B, Michaelay M, Menghistu HT, Abebe N, Genzebu AT, Bitsue HK. Epidemiology of epizootic lymphangitis of carthorses in northern Ethiopia using conventional diagnostic methods and nested polymerase chain reaction.. BMC Vet Res (2020) 16:1–7.
    doi: 10.1186/s12917-020-02582-2pmc: PMC7541241pubmed: 33028302google scholar: lookup
  42. Kauffman CA. Histoplasmosis: a clinical and laboratory update.. Clin Microbiol Rev (2007) 20:115–32.
    doi: 10.1128/CMR.00027-06pmc: PMC1797635pubmed: 17223625google scholar: lookup
  43. Paya CV, Roberts GD, Cockerill FR. Transient Fungemia in acute pulmonary histoplasmosis: detection by new blood-culturing techniques.. J Infect Dis (2023) 156:313–5.
    doi: 10.1093/infdis/156.2.313pubmed: 3298456google scholar: lookup
  44. Whitt SP, Koch GA, Fender B, Ratnasamy N, Everett ED. Histoplasmosis in pregnancy: case series and report of Transplacental transmission.. Arch Intern Med (2004) 164:454–8.
    doi: 10.1001/archinte.164.4.454pubmed: 14980998google scholar: lookup
  45. Damasceno LS, Almeida AMB, Aguiar BDO, Muniz MDM, Almeida MDA, Zancopé-Oliveira RM. Postpartum histoplasmosis in an HIV-negative woman: a case report and phylogenetic characterization by internal transcribed spacer region analysis.. Rev Soc Bras Med Trop (2020) 53:e20190364.
    doi: 10.1590/0037-8682-0364-2019pmc: PMC7083345pubmed: 31994667google scholar: lookup
  46. Mitku M, Assefa A, Abrhaley A. Prevalence, associated risk factors and socioeconomic impact of epizootic lymphangitis (EL) in carthorses in and around Gondar town.. J Am Sci (2018) 14:77–83.
    doi: 10.7537/marsjas140218.10google scholar: lookup
  47. Ameni G. Epidemiology of equine histoplasmosis (epizootic lymphangitis) in carthorses in Ethiopia.. Vet J (2006) 172:160–5.
    doi: 10.1016/j.tvjl.2005.02.025pubmed: 16772141google scholar: lookup
  48. Muthee K, Duguma L, Nzyoka J, Minang P. Ecosystem-based adaptation practices as a nature-based solution to promote water-energy-food nexus balance.. Sustain For (2021) 13:1–17.
    doi: 10.3390/sጃ1142google scholar: lookup
  49. Gabal MA, Hennager S. Study on the survival of Histoplasma Farciminosum in the environment/Experimentelle Untersuchungen zur Lebensfähigkeit von Histoplasma Farciminosum.. Mycoses (1983) 26:481–7.
    doi: 10.1111/j.1439-0507.1983.tb03243.xpubmed: 6646170google scholar: lookup
  50. Zeidberg LD, Ajello L. Environmental factors influencing the occurrence of Histoplasma capsulatum and Microsporum gypseum in soil.. J Bacteriol (1954) 68:156–9.
    doi: 10.1128/jb.68.2.156-159.1954pmc: PMC357359pubmed: 13183922google scholar: lookup
  51. Mahvi TA. Factors governing the epidemiology of Histoplasma capsulatum in soil.. Mycopathotogica Mycol Appl (1970) 41:167–76.
    pubmed: 5535367
  52. Zeidberg LD, Ajello L, Webster RH. Physical and chemical factors in relation to Histoplasma capsulatum in soil.. Science (1955) 80:122.
    pubmed: 14385817
  53. Cornell TR, Conteh B, Drammeh L, Jeffang F, Sallah E, Kijera A. Histoplasma seropositivity and environmental risk factors for exposure in a general population in Upper River region, the Gambia: a cross-sectional study.. One Heal (2024) 18:100717.
    doi: 10.1016/j.onehlt.2024.100717pmc: PMC10992707pubmed: 38576541google scholar: lookup
  54. Powell RK, Bell NJ, Abreha T, Asmamaw K, Bekelle H, Dawit T. Cutaneous histoplasmosis in 13 Ethiopian donkeys.. Vet Rec (2006) 158:836–7.
    doi: 10.1136/vr.158.24.836pubmed: 16782861google scholar: lookup
  55. Awad FI. Studies on epizootic Lymphangitis in the Sudan.. J Comp Pathol Ther (1960) 70:457–63.
    doi: 10.1016/S0368-1742(60)80043-4pubmed: 13685309google scholar: lookup
  56. Pallin W. A treatise on epizootic Lymphangitis.. 2nd ed. (1904).
  57. Bartlett PC, Weeks RJ, Ajello L. Decontamination of a Histoplasma capsulatum-infested bird roost in Illinois.. Arch Environ Health (1982) 37:221–3.
    pubmed: 7114902
  58. Tosh FE, Weeks RJ, Pfeiffer FR, Hendricks SL, Greer DL, Chin TDY. The use of formalin to kill Histoplasma capsulatum at an epidemic site.. Am J Epidemiol (1967) 85:259–65.
    doi: 10.1093/oxfordjournals.aje.a120689pubmed: 6067016google scholar: lookup
  59. Oliveira dos Santos P, Messias Rodrigues A, Ferreira Fernandes G, Marques H, da Silva S, Burger E. Immunodiagnosis of Paracoccidioidomycosis due to Paracoccidioides brasiliensis using a latex test: detection of specific antibody anti-gp43 and specific antigen gp43.. PLoS Negl Trop Dis (2015) 9:e0003516.
    doi: 10.1371/journal.pntd.0003516pmc: PMC4334539pubmed: 25679976google scholar: lookup
  60. Thompson EM, Ellert J, Peters LLW, Ajdukiewicz A, Mabey D. Histoplasma duboisii infection of bone.. Br J Radiol (1981) 54:518–21.
    doi: 10.1259/0007-1285-54-642-518pubmed: 7237032google scholar: lookup
  61. Mabey DCW, Ajdukiewicz AB, Hay RJ. Treatment of African histoplasmosis with ketoconazole.. Trans R Soc Trop Med Hyg (1983) 77:219–20.
    pubmed: 6306875
  62. Rivron RP, Evans EG. Enlarged cervical lymph node due to African histoplasmosis.. J Laryngol Otol (1988) 102:945–6.
    doi: 10.1017/S0022215100106887pubmed: 3199018google scholar: lookup
  63. Matta M, Farah FS. North American blastomycosis. Report of a case encountered in Lebanon and probably originating in Gambia.. Dermatologica (1973) 146:346–9.
    pubmed: 4127045
  64. Armitage EP, Senghore E, Darboe S, Barry M, Camara J, Bah S. High burden and seasonal variation of paediatric scabies and pyoderma prevalence in the Gambia: a cross-sectional study.. PLoS Negl Trop Dis (2019) 13:e0007801.
    doi: 10.1371/journal.pntd.0007801pmc: PMC6812840pubmed: 31609963google scholar: lookup
  65. Turner PC, Moore SE, Hall AJ, Prentice AM, Wild CP. Modification of immune function through exposure to dietary aflatoxin in Gambian children.. Environ Health Perspect (2003) 111:5753.
    doi: 10.1289/ehp.5753pmc: PMC1241353pubmed: 12573908google scholar: lookup
  66. Molla AM, Fentahun T, Jemberu WT. Estimating the economic impact and assessing owners’ knowledge and practices of epizootic Lymphangitis in equine cart animals in central and South Gondar zones, Amhara region, Ethiopia.. Front Vet Sci (2021) 8:673442.
    doi: 10.3389/fvets.2021.673442pmc: PMC8245057pubmed: 34222399google scholar: lookup

Citations

This article has been cited 0 times.
Subscribe to our newsletter
Join 99,030 horse owners like you who receive our email updates on horse health and nutrition.