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Investigation of the Vaginal and Clitoral Fungi in One-Humped Camels (Camelus Dromedarius) | ||
Iranian Journal of Veterinary Medicine | ||
مقاله 4، دوره 19، شماره 2، تیر 2025، صفحه 203-210 اصل مقاله (1.16 M) | ||
نوع مقاله: Original Articles | ||
شناسه دیجیتال (DOI): 10.32598/ijvm.19.2.1005423 | ||
نویسندگان | ||
Hosein Kochakzadeh Omran1؛ Massoud Talebkhan Garoussi* 1؛ Ali Reza Khosravi2؛ Jorgen Steen Agerholm3؛ Mehran Dabiri1 | ||
1Department of Theriogenology, Faculty of Veterinary Medicine, University of Tehran. Tehran, Iran. | ||
2Mycology Research Centre, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran. | ||
3Department of Veterinary Clinical Sciences, University of Copenhagen, Taastrup, Denmark. | ||
چکیده | ||
Background: Bacteria and fungi constitute crucial parts of the genital tract microenvironment and participate in mucosal homeostasis. While the genital tract microflora has been studied for several animal species, this is not true for the one-humped camel (Camelus dromedarius). Objectives: This survey aims to investigate the prevalence of vaginal and clitoral fungi in one-humped camels (C. dromedarius ) from different regions of Iran. Methods: Dairy camel farms were sampled in Khorasan Razavi, Semnan, Tehran, Qom, and Isfahan Provinces in central and northeast Iran. Two hundred and twenty paired samples were taken from the vaginal and clitoral mucosa of 110 camels and cultured on Sabouraud dextrose agar and CHROMagarTM Candida, followed by identification of cultured fungi. Data were analyzed using the Genmod procedure. Results: Six isolates were identified. Fungi were cultured and isolated from 31% of the camels. Cladosporium spp. and Aspergillus flavus were the most isolated prevalent. Aspergillus was the most frequently recovered species. The presence of fungi was evaluated in camels of different ages, but no correlation was observed (P>0.05). Conclusion: Fungal contamination of the camel's external organs of the reproductive system is very low compared to other domestic animals. It is likely due to the intrinsic immunity of one-humped camel (C. dromedarius). | ||
کلیدواژهها | ||
Aspergillus flavus؛ Camel؛ Clitoris؛ Cladosporium spp؛ Fungi؛ Vagina | ||
اصل مقاله | ||
Introduction
Materials and Methods
The fungi of the vaginal and clitoral mucosa seemed to be similar but varied between animals. No single species was consistently isolated from all or most camels. No correlation was found when analyzing the culture results (culture positive vs. negative) against the animals’ age (Table 3).
This survey showed that the amount of fungal contamination of external organs of the reproductive system in female camels is much lower than in mares (Azarvandi et al., 2017a, Azarvandi et al., 2017b). This may be due to the camel’s innate and general immune systems’ resistance to fungal infection.
Ali, A., Al-sobayil, F. A., Tharwat, M., Al-Hawas, A., & Ahmed, A. F. (2010). Causes of infertility in female camels (Camelus dromedarius) in middle of Saudi Arabia. Journal of Agricultural and Veterinary Sciences, Qassim University, 2(2), 59-66. [Link] Antoniassi, N. A., Juffo, G. D., Santos, A. S., Pescador, C. A., Ferreiro, L., & Driemeier, D. (2013). Geotrichum candidum as a possible cause of bovine abortion. Journal of Veterinary Diagnostic Investigation, 25(6), 795–797. [DOI:10.1177/1040638713508284] [PMID] Azarvandi, A., Talebkhan Garoussi, M., Khosravi, A., Hosseini, A., & Gharagozloo, F. (2017). Isolation and identification of molds flora in external genital tract of healthy mares. Journal of Veterinary Research, 72 (1), 103-110. [Link] Azarvandi, A., Khosravi, A. R., Shokri, H., Talebkhan Garoussi, M., Gharahgouzlou, F., & Vahedi, G., et al. (2017). Presence and distribution of yeasts in the reproductive tract of healthy female horses. Equine Veterinary Journal, 49(5), 614–617. [DOI:10.1111/evj.12657] [PMID] Chen, B. X., & Yuen, Z. X. (1984). Pregnancy diagnosis by rectal examination in the Bactrian camel. In: W. R. Cockrill (Ed.), The Camelid (pp. 399-406). (Scandinavian Institute of African Studies, Uppsala, Sweden. [Link] Cleff, M. B., Lima, A. P. D., Faria, R. O. D., Meinerz, A. R. M., Antunes, T. D. Á., & Araújo, F. B. D., et al. (2005). Isolation of Candida spp. from vaginal microbiota of healthy canine females during estrous cycle. Brazilian Journal of Microbiology, 36, 201-204. [DOI:10.1590/S1517-83822005000200018] Constable, P. D., Hinchcliff K. W., Done S. H., & Grunberg W. (2017). Veterinary medicine. A textbook of the diseases of cattle, horse, sheep, pigs and goats. Missouri: Saunders Elsevier. [Link] Dabiri, M., Garoussi, M. T., Mehrzad, J., Tajik, P., & Barin, A. (2021). The effects of cytopathic and non-cytopathic biotypes of bovine viral diarrhea virus on sperm vitality and viability of Holstein dairy bulls in vitro. Iranian Journal of Veterinary Medicine, 15(2), 197-206. [Link] Enany, M., Hanafi, M. S., El-Ged, A. G. F., El-Seedy, F. R., & Khalid, A. (1990). Microbiological studies on endometritis in she-camels in Egypt. Journal of the Egyptian Veterinary Medical Association, 50, 229-243. [Link] Fourichon, C., Seegers, H., & Malher, X. (2000). Effect of disease on reproduction in dairy cows: A meta-analysis. Theriogenology, 53(9), 1729–1759. [DOI:10.1016/S0093-691X(00)00311-3] [PMID] Garoussi, M. T., Eidi, S., & Mehravaran, M. (2016). Isolation and comparative investigation of vaginal mycoflora in feline population of urban and dairy cattle herds. Journal de Mycologie Medicale, 26(1), 22–27. [DOI:10.1016/j.mycmed.2015.10.013] [PMID] Garoussi, M. T., Khosrave, A. R., & Hovarashte, P. (2008). The survey of mycotic flora of uterine cows with reproductive disorders and h Journal of Veterinary Research, 63(1), 1, 7-10. [Link] Garoussi, M. T., Khosrave, A. R., & Havareshti, P. (2007). Mycoflora of cervicovaginal fluids in dairy cows with or without reproductive disorders. Mycopathologia, 164(2), 97–100. [DOI:10.1007/s11046-007-9031-x] [PMID] Heuwieser, W., Tenhagen, B. A., Tischer, M., Lühr, J., & Blum, H. (2000). Effect of three programmes for the treatment of endometritis on the reproductive performance of a dairy herd. The Veterinary Record, 146(12), 338–341. [DOI:10.1136/vr.146.12.338] [PMID] Hillson, S. (2005). Cambridge: Cambridge University Press.[Link] R. M. (2015). Bovine reproduction. New Jersey: Willy-Blackwell. [Link] Hosseinabadi, E., Talebkhan Garoussi1, M., Khosravi, A. R., Gharagozloo, F., Khoramian Toosi, B., & Moosakhani, F. (2022). Prevalence of prototheca and fungal contamination of bulk tank milk of industrial dairy cattle herds in Iran. Iranian Journal of Veterinary Medicine, 16(2), 155-165. [Link] Karstrup, C. C., Agerholm, J. S., Jensen, T. K., Swaro, L. R. V., Klitgaard, K., & Rasmussen, E. L., et al. (2017). Presence and localization of bacteria in the bovine endometrium postpartum using fluorescence in situ hybridization. Theriogenology, 92, 167–175. [DOI:10.1016/j.theriogenology.2017.01.026] [PMID] Khosravi, A. R., Eidi, S., Ziglari., T, & Bayat. T.M. (2008). Isolation and differentiation of malassezia pecies isolated from healthy and affected small animals, ear and skin. World Journal of Zoology, 3 (2), 77-80. [Link] Knudtson, W.U., Kirkbride, C.A., 1992. Fungi associated with bovine abortion in the northern plains states (USA). Journal of Veterinary Diagnostic Investigation 4, 181–185. [DOI: 10.1177/104063879200400211] [PMID] Merkt, H., Rath, D., Musa, B., & El-Naggar, M. A. (1990). Reproduction in camels. A review. Food and Agriculture Organization of the United Nations, 82, 19-21. [Link] Moradi, M. S., Kamkar, S., Sharifzadeh, A., Hassan, J., Shokri, H., & Abbasi, J. (2024). The in vitro effect of berberine sulfate and berberine chloride on the growth and aflatoxin production by aspergillus flavus and aspergillus parasiticus. Iranian Journal of Veterinary Medicine, 18(2), 223-232. [DOI:10.32598/IJVM.18.2.1005399] Mshelia, G. D., Okpaje, G., Voltaire, Y. A., & Egwu, G. O. (2014). Comparative studies on genital infections and antimicrobial susceptibility patterns of isolates from camels (Camelus dromedarius) and cows (Bos indicus) in Maiduguri, north-eastern Nigeria. SpringerPlus, 3, [DOI:10.1186/2193-1801-3-91] [PMID] Murase, H., Niwa, H., Katayama, Y., Sato, F., Hada, T., & Nambo, Y. (2015). A clinical case of equine fungal placentitis with reference to hormone profiles and ultrasonography. Journal of Equine Science, 26(4), 129–133. [DOI:10.1294/jes.26.129] [PMID] Noakes, D. E., Parkinson, T. J., & England, G C. W. (2019). Veterinary reproduction and obstetrics. Amsterdam: Elsevier. [Link] Orellana-Guerrero, D., Renaudin, C., Edwards, L., Rose, E., Aleman, M., & Moore, P. F., et al. (2019). Fungal placentitis caused by aspergillus terreus in a mare: Case report. Journal of Equine Veterinary Science, 83, [DOI:10.1016/j.jevs.2019.102799] [PMID] Pal, M. (2015). Growing role of fungi in mycotic abortion of domestic anima Journal of Bacteriology and Mycology, 2(1), 1009. [Link] Refaat, D., Ali, A., Saeed, E. M., Al-Sobayil, F., Al-Samri, A., & Elbehiry, A. (2020). Diagnostic evaluation of subclinical endometritis in dromedary camels. Animal Reproduction Science, 215, [DOI:10.1016/j.anireprosci.2020.106327] [PMID] Rebhun, C., & Guard, C. (1995). Diseases of dairy cattle. Pennsylvania: William & Wilkins. [Link] Różański, P., Ślaska, B., & Różańska, D. (2013). Current status of prevalence of yeast-like fungi in the environment of horses bred in Poland. Annals of Animal Science, 13(2), 365-374.[DOI:10.2478/aoas-2013-0016] Różański, P., Slaska, B., & Różańska, D. (2013). Prevalence of yeasts in English full blood mares. Mycopathologia, 175(3-4), 339–344. [DOI:10.1007/s11046-013-9615-6] [PMID] Shokri, H., Khosravi, A., Sharifzadeh, A., & Tootian, Z. (2010). Isolation and identification of yeast flora from genital tract in healthy female camels (Camelus dromedarius). Veterinary Microbiology, 144(1-2), 183–186. [DOI:10.1016/j.vetmic.2009.12.012] [PMID] Singh, G., Sidhu, S. S., Jand, S. K., & Singla, V. K. (1993). Mycoflora in uterine swabs of repeat breeder cows and buffaloes. Indian Journal of Animal Sciences, 63(5), 528-529. [Link] Sobel, J.D. (1988). Pathogenesis and epidemiology of vulvovaginal candidiasis. Annals of the New York Academy of Sciences, 544, 547–557. [DOI:10.1111/j.1749-6632.1988.tb40450.x] [PMID] Sugui, J. A., Kwon-Chung, K. J., Juvvadi, P. R., Latgé, J. P., & Steinbach, W. J. (2014). Aspergillus fumigatus and related species. Cold Spring Harbor Perspectives in Medicine, 5(2), a019786. [DOI:10.1101/cshperspect.a019786] [PMID] Tibary, A., Fite, C., Anouassi, A., & Sghiri, A. (2006). Infectious causes of reproductive loss in camelids. Theriogenology, 66(3), 633–647. [DOI:10.1016/j.theriogenology.2006.04.008] [PMID] Thrusfield, M., Christley, R., & Peter, H. B. (2018). Veterinary epidemiology. New Jersey: John Wiley & Sons Ltd. [DOI:10.1002/9781118280249] Youngquist, R. S., & Threlfall, W. R. (2006). Current therapy in large animal theriogenology. Amsterdam: Elsevier Health Sciences. [Link] | ||
مراجع | ||
Ali, A., Al-sobayil, F. A., Tharwat, M., Al-Hawas, A., & Ahmed, A. F. (2010). Causes of infertility in female camels (Camelus dromedarius) in middle of Saudi Arabia. Journal of Agricultural and Veterinary Sciences, Qassim University, 2(2), 59-66. [Link]
Antoniassi, N. A., Juffo, G. D., Santos, A. S., Pescador, C. A., Ferreiro, L., & Driemeier, D. (2013). Geotrichum candidum as a possible cause of bovine abortion. Journal of Veterinary Diagnostic Investigation, 25(6), 795–797. [DOI:10.1177/1040638713508284] [PMID]
Azarvandi, A., Talebkhan Garoussi, M., Khosravi, A., Hosseini, A., & Gharagozloo, F. (2017). Isolation and identification of molds flora in external genital tract of healthy mares. Journal of Veterinary Research, 72 (1), 103-110. [Link]
Azarvandi, A., Khosravi, A. R., Shokri, H., Talebkhan Garoussi, M., Gharahgouzlou, F., & Vahedi, G., et al. (2017). Presence and distribution of yeasts in the reproductive tract of healthy female horses. Equine Veterinary Journal, 49(5), 614–617. [DOI:10.1111/evj.12657] [PMID]
Chen, B. X., & Yuen, Z. X. (1984). Pregnancy diagnosis by rectal examination in the Bactrian camel. In: W. R. Cockrill (Ed.), The Camelid (pp. 399-406). (Scandinavian Institute of African Studies, Uppsala, Sweden. [Link]
Cleff, M. B., Lima, A. P. D., Faria, R. O. D., Meinerz, A. R. M., Antunes, T. D. Á., & Araújo, F. B. D., et al. (2005). Isolation of Candida spp. from vaginal microbiota of healthy canine females during estrous cycle. Brazilian Journal of Microbiology, 36, 201-204. [DOI:10.1590/S1517-83822005000200018]
Constable, P. D., Hinchcliff K. W., Done S. H., & Grunberg W. (2017). Veterinary medicine. A textbook of the diseases of cattle, horse, sheep, pigs and goats. Missouri: Saunders Elsevier. [Link]
Dabiri, M., Garoussi, M. T., Mehrzad, J., Tajik, P., & Barin, A. (2021). The effects of cytopathic and non-cytopathic biotypes of bovine viral diarrhea virus on sperm vitality and viability of Holstein dairy bulls in vitro. Iranian Journal of Veterinary Medicine, 15(2), 197-206. [Link]
Enany, M., Hanafi, M. S., El-Ged, A. G. F., El-Seedy, F. R., & Khalid, A. (1990). Microbiological studies on endometritis in she-camels in Egypt. Journal of the Egyptian Veterinary Medical Association, 50, 229-243. [Link]
Fourichon, C., Seegers, H., & Malher, X. (2000). Effect of disease on reproduction in dairy cows: A meta-analysis. Theriogenology, 53(9), 1729–1759. [DOI:10.1016/S0093-691X(00)00311-3] [PMID]
Garoussi, M. T., Eidi, S., & Mehravaran, M. (2016). Isolation and comparative investigation of vaginal mycoflora in feline population of urban and dairy cattle herds. Journal de Mycologie Medicale, 26(1), 22–27. [DOI:10.1016/j.mycmed.2015.10.013] [PMID]
Garoussi, M. T., Khosrave, A. R., & Hovarashte, P. (2008). The survey of mycotic flora of uterine cows with reproductive disorders and h Journal of Veterinary Research, 63(1), 1, 7-10. [Link]
Garoussi, M. T., Khosrave, A. R., & Havareshti, P. (2007). Mycoflora of cervicovaginal fluids in dairy cows with or without reproductive disorders. Mycopathologia, 164(2), 97–100. [DOI:10.1007/s11046-007-9031-x] [PMID]
Heuwieser, W., Tenhagen, B. A., Tischer, M., Lühr, J., & Blum, H. (2000). Effect of three programmes for the treatment of endometritis on the reproductive performance of a dairy herd. The Veterinary Record, 146(12), 338–341. [DOI:10.1136/vr.146.12.338] [PMID]
Hillson, S. (2005). Cambridge: Cambridge University Press.[Link]
R. M. (2015). Bovine reproduction. New Jersey: Willy-Blackwell. [Link]
Hosseinabadi, E., Talebkhan Garoussi1, M., Khosravi, A. R., Gharagozloo, F., Khoramian Toosi, B., & Moosakhani, F. (2022). Prevalence of prototheca and fungal contamination of bulk tank milk of industrial dairy cattle herds in Iran. Iranian Journal of Veterinary Medicine, 16(2), 155-165. [Link]
Karstrup, C. C., Agerholm, J. S., Jensen, T. K., Swaro, L. R. V., Klitgaard, K., & Rasmussen, E. L., et al. (2017). Presence and localization of bacteria in the bovine endometrium postpartum using fluorescence in situ hybridization. Theriogenology, 92, 167–175. [DOI:10.1016/j.theriogenology.2017.01.026] [PMID]
Khosravi, A. R., Eidi, S., Ziglari., T, & Bayat. T.M. (2008). Isolation and differentiation of malassezia pecies isolated from healthy and affected small animals, ear and skin. World Journal of Zoology, 3 (2), 77-80. [Link]
Knudtson, W.U., Kirkbride, C.A., 1992. Fungi associated with bovine abortion in the northern plains states (USA). Journal of Veterinary Diagnostic Investigation 4, 181–185. [DOI: 10.1177/104063879200400211] [PMID]
Merkt, H., Rath, D., Musa, B., & El-Naggar, M. A. (1990). Reproduction in camels. A review. Food and Agriculture Organization of the United Nations, 82, 19-21. [Link]
Moradi, M. S., Kamkar, S., Sharifzadeh, A., Hassan, J., Shokri, H., & Abbasi, J. (2024). The in vitro effect of berberine sulfate and berberine chloride on the growth and aflatoxin production by aspergillus flavus and aspergillus parasiticus. Iranian Journal of Veterinary Medicine, 18(2), 223-232. [DOI:10.32598/IJVM.18.2.1005399]
Mshelia, G. D., Okpaje, G., Voltaire, Y. A., & Egwu, G. O. (2014). Comparative studies on genital infections and antimicrobial susceptibility patterns of isolates from camels (Camelus dromedarius) and cows (Bos indicus) in Maiduguri, north-eastern Nigeria. SpringerPlus, 3, [DOI:10.1186/2193-1801-3-91] [PMID]
Murase, H., Niwa, H., Katayama, Y., Sato, F., Hada, T., & Nambo, Y. (2015). A clinical case of equine fungal placentitis with reference to hormone profiles and ultrasonography. Journal of Equine Science, 26(4), 129–133. [DOI:10.1294/jes.26.129] [PMID]
Noakes, D. E., Parkinson, T. J., & England, G C. W. (2019). Veterinary reproduction and obstetrics. Amsterdam: Elsevier. [Link]
Orellana-Guerrero, D., Renaudin, C., Edwards, L., Rose, E., Aleman, M., & Moore, P. F., et al. (2019). Fungal placentitis caused by aspergillus terreus in a mare: Case report. Journal of Equine Veterinary Science, 83, [DOI:10.1016/j.jevs.2019.102799] [PMID]
Pal, M. (2015). Growing role of fungi in mycotic abortion of domestic anima Journal of Bacteriology and Mycology, 2(1), 1009. [Link]
Refaat, D., Ali, A., Saeed, E. M., Al-Sobayil, F., Al-Samri, A., & Elbehiry, A. (2020). Diagnostic evaluation of subclinical endometritis in dromedary camels. Animal Reproduction Science, 215, [DOI:10.1016/j.anireprosci.2020.106327] [PMID]
Rebhun, C., & Guard, C. (1995). Diseases of dairy cattle. Pennsylvania: William & Wilkins. [Link]
Różański, P., Ślaska, B., & Różańska, D. (2013). Current status of prevalence of yeast-like fungi in the environment of horses bred in Poland. Annals of Animal Science, 13(2), 365-374.[DOI:10.2478/aoas-2013-0016]
Różański, P., Slaska, B., & Różańska, D. (2013). Prevalence of yeasts in English full blood mares. Mycopathologia, 175(3-4), 339–344. [DOI:10.1007/s11046-013-9615-6] [PMID]
Shokri, H., Khosravi, A., Sharifzadeh, A., & Tootian, Z. (2010). Isolation and identification of yeast flora from genital tract in healthy female camels (Camelus dromedarius). Veterinary Microbiology, 144(1-2), 183–186. [DOI:10.1016/j.vetmic.2009.12.012] [PMID]
Singh, G., Sidhu, S. S., Jand, S. K., & Singla, V. K. (1993). Mycoflora in uterine swabs of repeat breeder cows and buffaloes. Indian Journal of Animal Sciences, 63(5), 528-529. [Link]
Sobel, J.D. (1988). Pathogenesis and epidemiology of vulvovaginal candidiasis. Annals of the New York Academy of Sciences, 544, 547–557. [DOI:10.1111/j.1749-6632.1988.tb40450.x] [PMID]
Sugui, J. A., Kwon-Chung, K. J., Juvvadi, P. R., Latgé, J. P., & Steinbach, W. J. (2014). Aspergillus fumigatus and related species. Cold Spring Harbor Perspectives in Medicine, 5(2), a019786. [DOI:10.1101/cshperspect.a019786] [PMID]
Tibary, A., Fite, C., Anouassi, A., & Sghiri, A. (2006). Infectious causes of reproductive loss in camelids. Theriogenology, 66(3), 633–647. [DOI:10.1016/j.theriogenology.2006.04.008] [PMID]
Thrusfield, M., Christley, R., & Peter, H. B. (2018). Veterinary epidemiology. New Jersey: John Wiley & Sons Ltd. [DOI:10.1002/9781118280249]
Youngquist, R. S., & Threlfall, W. R. (2006). Current therapy in large animal theriogenology. Amsterdam: Elsevier Health Sciences. [Link] | ||
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