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Abstract
The aim of this study was to identify the preputial aerobic bacterial flora from bulls, rams and bucks and to determine their antimicrobial sensitivities. Preputial swabs were collected randomly from twenty each of clinically healthy post pubertal bulls, rams and bucks. Using standard bacteriological techniques, the following bacteria were identified; Escherichia coli (bulls 26.5%, rams 19.2% and buck 22.7%), Staphylococcus aureus (bulls 25.0 %, rams 26.0 % and bucks 24.2 %), Streptococcus (bulls 20.6%, rams 26.0 % and bucks 25.8%), Salmonella (bulls 14.7%), Shigella (rams 15.1% and bucks 15.2%) and Klebsiella (bulls 13.2%, rams 13.7 % and bucks 12.1%) species. There was no statistically significant difference (p>0.05) between the proportions of bacterial species and different animal species. In bulls, all bacterial isolates were susceptible to Ciprofloxacin (100%) and Levofloxacin (100%) while 60% of the bacterial isolates showed resistance to amoxicillin, ampiclox and streptomycin. In rams, all the bacterial isolates were susceptible to ciprofloxacin (100%) and gentamycin (100%) while 40% of bacterial isolates were resistant to chloramphenicol. In bucks, all bacterial isolates were susceptible to amoxicillin (100%), ampiclox (100%) and gentamycin (100%) while 20% bacterial isolates were resistant to streptomycin. This study shows that a few bacteria colonize the prepuce of ruminants in Maiduguri and there is need for preputial washing prior to breeding to reduce contamination of semen during natural mating or collection. Amoxiciillin, ampiclox, ciprofloxacin and gentamycin could be used as therapeutic agents to diseases that could be caused by the bacteria in prepuce of these animal species.
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References
- Adebowale, O., Makanjuola, M., Bankole, N., Olasoju, M., Alamu, A., Kperegbeyi, E., Oladejo, O., Fasanmi, O., Adeyemo, O. and Fasina, F.O. (2022). Multi-Drug-Resistant Escherichia coli, Biosecurity and Anti-Microbial Use in Live Bird Markets, Abeokuta, Nigeria. Antibiotics. 11,253. doi: 10.3390/antibiotics11020253. PMID: 35203856; PMCID: PMC8868421
- Ajala, O.O., Okunlade, A.O., Ogundare, O.F., Adekemi, A., Adeshoga, A., Afolabi, A.M. and Oludare, R.E. (2011). The Prevalence and identification of the bacteria associated with caprine vulvovaginitis in Ibadan. W Appl. Sci. J. 14, (8), 1115-1118.
- Akhter, S., Ansari, M.S., Andrabi, S.M.H., Ullah, N. and Qayyum, M., (2008). Effect of antibiotic in extender on bacterial and spermatozoal quality of cooled buffalo (Bubalus bubalis) bull semen. Reprod. Domest. Anim. 43: 272-278.
- Ayukekbong, J.A., Ntemgwa, M., and Atabe A.N. (2017). The threat of antimicrobial resistancein developing countries causes and control strategies. Antimicrob. Resist. Infect. Control. 15; 6: 47. doi:10.1186/s13756-017-0208-x. PMID:28515903; PMC5433038
- Bauer, A.W., Kirby, W.M.M., Sherris J.C. and Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. Amer J. Clin. Pathol. 36:493-496.
- Bukar-Kolo, Y. M. Amin J.D. and Zaria L.T. (2007). Bacterial Flora of the Gentalia of the Sahelian Doe in Maiduguri, Borno State Nigeria. Niger. Vet. J., 28(2), 60-62.
- Bukar-Kolo, Y.M., Peter I.D., Bukar, M.M., Muhammad, A.A. and Ayok, I.J. (2016). Prevalence and Antibiotic susceptibility of Aerobic Bacterial Flora of the Skin, Wound, and Anterior Vagina of Sheep, Goats and Dogs in Maiduguri, Nigeria. Alex. J. Vet. Sci.. 49(2): 6-12. doi: 10.5455/ajvs.218617
- Chander, A. and Raza, M.S. (2013). Antimicrobial susceptibility patterns of Pseudomonas aeruginosa clinical isolates at a tertiary care hospital in Kathmandu, Nepal. Asian J. Pharm. Clin. Res. 6: 235-238.
- Cowan, S.T. and Steel, E.J. (1993). Manual for identification of medical bacteria. Cambridge University press, London, 2nd edition, London, pp. 152-209.
- Eaglesome, M.D., Garcia, M.M. and Stewart, R.B. (1992). Microbial agents associated with bovine genital tract infections and semen. Part II. Haemophilus somnus, Mycoplasma spp and Ureaplasma sp, Chlamydia; pathogens and semen contaminants; treatment of bull semen with antimicrobial agents. Vet. Bulletin 62: 887e910.
- Economou, V. and Ghuosia, P. (2015). Agriculture and Food animals as a source of antimicrobial resistant bacteria. Infect. Drug Resist., 8, 49-61. doi: 10.2147/IDR.S55778. PMID: 25878509; PMCID: PMC4388096.
- Fache, M,. Guerin, B., Parez, M., Thibier, M.E (1985).tude quantitative de la flore bacte_rienne non pathoge_ne dans le sperme et la semence de taureau. Elev Insem. 207:13e8.
- Fatnassi, M., Padalino, B., Monaco, D., Khorchani, T., Lacalandra, G.M. and Ham-madi, M. (2014) Evaluation of sexual behavior of housed male camels (Camelus dromedarius) through female parades: Correlation with climatic parameters. Trop Anim. Hlth Prod.. 46: 313-321. doi: 10.1007/s11250-013-0489-x. Epub 2013 Oct 12. PMID: 24122649
- Givens, M.D. (2018). Review: Risks of disease transmission through semen in cattle. Animals, 12(1):165-171. https://doi.org/10.1017/S1751731118000708
- Gouletsou, P.G., Fthenakis, G.C., Tzora, A., Cripps, P.J. and Saratsis, P. (2006). Isolation of Arcanobacterium pyogenes from the scrotal skin and the prepuce of healthy rams or from rams with testicular abnormalities. Small Rum. Res. 63 (1-2) 177-182. https://doi.org/10.1016/j.smallrumres.2005.01.016
- Harada, K. and Asai, T. (2010) Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan. J Biomed. Biotech. 2010; 2010:180682. doi: 10.1155/2010/180682. Epub 2010 Jun 2. PMID: 20589071; PMCID: PMC2879543.
- Herrero, M., Grace, D., Njuki, J., Johnson, N., Enahoro, D., Silvestri, S., and Rufino, M.C. (2013). The roles of livestock in developing countries. Animal, 7(1), 3-18. https://doi.org/10.1017/S1751731112001954
- Holt, J.G., Kreig, N.R., Sneath, P.H.A., Sneath, J.T. and Williams, T.A. (1994). Bergey’s Manual of Determinative Bacteriology, (9th Edition), William and Wilkins Baltimore, 532-559.
- Igbinosa, E.O., Beshiru A., Igbinosa, I.H. and Okoh, A.I. (2022). Antimicrobial resistance and genetic characterisation of Salmonella enterica from retail poultry meats in Benin City, Nigeria. LWT. 114049. https://doi.org/10.1016/j.lwt.2022.114049
- Kabir, J., Umoh, V.J., Audu-Okoh, E., Umoh, U.J. and Kwaga, J.K.P. (2004). Veterinary drug use in poultry farms and determination of antimicrobial drug residues in commercial eggs and slaughtered chicken in Kaduna State, Nigeria. Food Cont, 15, 99–105. https://doi.org/10.1016/S0956-7135(03)00020-3
- Kabir, S.M.L. (2010). Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, Diagnosis, Control and Public Health Concerns. Int. J Environ. Res. Public Health, 7, 89–114. doi: 10.3390/ijerph7010089
- Kimera, Z.I., Mshana, S.E., Rweyemamu, M.M., Mboera, L.E. and Matee, I.N. (2020). Antimicrobial use and resistance in food-producing animals and environment: an African perspective. Antimicrob. Resist. Infect. Control. 9:37. https://doi.org/10.1186/s13756-020-0697-x
- Ma, F. Xu, S., Tang, Z., Li, Z. and Zhang, L. (2020). Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosafety Hlth., 3(1), 32–38. https://doi.org/10.1016/j.bsheal.2020.09.004
- Meena, G.S., Raina, V.S., Gupta, A.K., Mohanty, T.K., Bhakat, M., Abdullah, M. and Bishist, R. (2015). Effect of preputial washing on bacterial load and preservability of semen in Murrah buffalo bulls. Vet. World. 8(6): 798-803. doi: 10.14202/vetworld.2015.798-803.
- Mshelia, G.D., Bilal, V.T., Maina, V.A., Okon, K, Mamza, S.A., Peter, I.D. and Egwu, G.O. (2014). Microbiological studies on genital infections in slaughtered ewes from tropical arid zone of Nigeria. Sokoto J. Vet. Sci, 12:18-22. DOI:10.4314/sokjvs.v12i1.3
- Najee, H.B., Al-Shawii, A.M. and Abd-Al Rahman, L.Y. (2012). Bacterial contamination of imported bulls frozen semen. Al-Anbar J. Vet Sci.. 5(1): 54-62.
- Navya, M. (2012). Bacterial load in the neat, extended and frozen bull semen and its antibiogram. Msc. Bangalore, Karnataka Veterinary, Animal and Fisheries Sciences University, Bidar.
- Patel, H.V., Patel, R.K. and Chauhan, J.B. (2011). Biochemical properties of microbial load in frozen semen of cattle. Wayamba J. Anim Sci.ISSN :2012-578X; P118 - P121
- Peter, I.D., Bature, M., Mohammed, M.M., Stephen, J., Mustapha, A., Iliyasu, D., Naaya, I.U. and Wafar, E.S. (2023). Preputial Bacterial Flora and antibacterial Susceptibility in Camels in Maiduguri, North-eastern, Nigeria. J Sustain. Vet. Allied Sci, 4(2), 146-150. https://doi.org/10.54328/covm.josvas.2023.112
- Poole, K. (2005). Aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 49(2): 479-487. Doi: 10.1128/AAC.49.2.479-487.2005 PMCID: PMC547279 PMID: 15673721
- Romano, J.E., Zanoni, R.G., Mislei, B., Bucci, D., Mion, D. and Mari, G. (2022). Comparison between chlorhexidine and povidone-iodine solutions for flushing the preputial cavity on penile mucosa and semen bacterial counts in beef bulls. Theriogenol, 193:114-119. https://doi.org/10.1016/j.theriogenology.2022.09.012
- Rota, A., Calicchio, E., Nardoni, S., Fratini, F., Ebani, V.V., Sgorbini, M., Panzani, D., Camillo F.and Mancianti F. (2011). Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions. Theriogenol 76 464–470. https://doi.org/10.1016/j.theriogenology.2011.02.023
- Udoh, R.K. (1981). Geographical regions of Nigeria. Heinemann Education Books Ltd. Ibadan, 1-24.
- Wickware, C.L., Johnson T.A. and Koziol, J.H. (2020). Composition and diversity of the Preputial microbiota in healthy Bulls. Theriogenol, 145, 231-237. doi: 10.1016/j.theriogenology.2019.11.002. Epub 2019 Nov 5. PMID: 31732161.
- Yaniz, J.L., Marco-Aguado, M.A., Mateos, J.A. and Santolaria, P. (2010). Bacterial contamination of ram semen, antibiotic sensitivities, and effects on sperm quality during storage at 15°C. Anim. Reprod. Sci.1:142-149. doi: 10.1016/j.anireprosci.2010.08.006. Epub 2010 Aug 13. PMID: 20832206.
- Zaid, N.W. and Al-Zubaidy, I.A. (2009). The effect of natural mating on the bacterial population of the endogenous Ram. Al-Anbar J. Vet Sci.. Vol. 2(1):31-35.
References
Adebowale, O., Makanjuola, M., Bankole, N., Olasoju, M., Alamu, A., Kperegbeyi, E., Oladejo, O., Fasanmi, O., Adeyemo, O. and Fasina, F.O. (2022). Multi-Drug-Resistant Escherichia coli, Biosecurity and Anti-Microbial Use in Live Bird Markets, Abeokuta, Nigeria. Antibiotics. 11,253. doi: 10.3390/antibiotics11020253. PMID: 35203856; PMCID: PMC8868421
Ajala, O.O., Okunlade, A.O., Ogundare, O.F., Adekemi, A., Adeshoga, A., Afolabi, A.M. and Oludare, R.E. (2011). The Prevalence and identification of the bacteria associated with caprine vulvovaginitis in Ibadan. W Appl. Sci. J. 14, (8), 1115-1118.
Akhter, S., Ansari, M.S., Andrabi, S.M.H., Ullah, N. and Qayyum, M., (2008). Effect of antibiotic in extender on bacterial and spermatozoal quality of cooled buffalo (Bubalus bubalis) bull semen. Reprod. Domest. Anim. 43: 272-278.
Ayukekbong, J.A., Ntemgwa, M., and Atabe A.N. (2017). The threat of antimicrobial resistancein developing countries causes and control strategies. Antimicrob. Resist. Infect. Control. 15; 6: 47. doi:10.1186/s13756-017-0208-x. PMID:28515903; PMC5433038
Bauer, A.W., Kirby, W.M.M., Sherris J.C. and Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. Amer J. Clin. Pathol. 36:493-496.
Bukar-Kolo, Y. M. Amin J.D. and Zaria L.T. (2007). Bacterial Flora of the Gentalia of the Sahelian Doe in Maiduguri, Borno State Nigeria. Niger. Vet. J., 28(2), 60-62.
Bukar-Kolo, Y.M., Peter I.D., Bukar, M.M., Muhammad, A.A. and Ayok, I.J. (2016). Prevalence and Antibiotic susceptibility of Aerobic Bacterial Flora of the Skin, Wound, and Anterior Vagina of Sheep, Goats and Dogs in Maiduguri, Nigeria. Alex. J. Vet. Sci.. 49(2): 6-12. doi: 10.5455/ajvs.218617
Chander, A. and Raza, M.S. (2013). Antimicrobial susceptibility patterns of Pseudomonas aeruginosa clinical isolates at a tertiary care hospital in Kathmandu, Nepal. Asian J. Pharm. Clin. Res. 6: 235-238.
Cowan, S.T. and Steel, E.J. (1993). Manual for identification of medical bacteria. Cambridge University press, London, 2nd edition, London, pp. 152-209.
Eaglesome, M.D., Garcia, M.M. and Stewart, R.B. (1992). Microbial agents associated with bovine genital tract infections and semen. Part II. Haemophilus somnus, Mycoplasma spp and Ureaplasma sp, Chlamydia; pathogens and semen contaminants; treatment of bull semen with antimicrobial agents. Vet. Bulletin 62: 887e910.
Economou, V. and Ghuosia, P. (2015). Agriculture and Food animals as a source of antimicrobial resistant bacteria. Infect. Drug Resist., 8, 49-61. doi: 10.2147/IDR.S55778. PMID: 25878509; PMCID: PMC4388096.
Fache, M,. Guerin, B., Parez, M., Thibier, M.E (1985).tude quantitative de la flore bacte_rienne non pathoge_ne dans le sperme et la semence de taureau. Elev Insem. 207:13e8.
Fatnassi, M., Padalino, B., Monaco, D., Khorchani, T., Lacalandra, G.M. and Ham-madi, M. (2014) Evaluation of sexual behavior of housed male camels (Camelus dromedarius) through female parades: Correlation with climatic parameters. Trop Anim. Hlth Prod.. 46: 313-321. doi: 10.1007/s11250-013-0489-x. Epub 2013 Oct 12. PMID: 24122649
Givens, M.D. (2018). Review: Risks of disease transmission through semen in cattle. Animals, 12(1):165-171. https://doi.org/10.1017/S1751731118000708
Gouletsou, P.G., Fthenakis, G.C., Tzora, A., Cripps, P.J. and Saratsis, P. (2006). Isolation of Arcanobacterium pyogenes from the scrotal skin and the prepuce of healthy rams or from rams with testicular abnormalities. Small Rum. Res. 63 (1-2) 177-182. https://doi.org/10.1016/j.smallrumres.2005.01.016
Harada, K. and Asai, T. (2010) Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan. J Biomed. Biotech. 2010; 2010:180682. doi: 10.1155/2010/180682. Epub 2010 Jun 2. PMID: 20589071; PMCID: PMC2879543.
Herrero, M., Grace, D., Njuki, J., Johnson, N., Enahoro, D., Silvestri, S., and Rufino, M.C. (2013). The roles of livestock in developing countries. Animal, 7(1), 3-18. https://doi.org/10.1017/S1751731112001954
Holt, J.G., Kreig, N.R., Sneath, P.H.A., Sneath, J.T. and Williams, T.A. (1994). Bergey’s Manual of Determinative Bacteriology, (9th Edition), William and Wilkins Baltimore, 532-559.
Igbinosa, E.O., Beshiru A., Igbinosa, I.H. and Okoh, A.I. (2022). Antimicrobial resistance and genetic characterisation of Salmonella enterica from retail poultry meats in Benin City, Nigeria. LWT. 114049. https://doi.org/10.1016/j.lwt.2022.114049
Kabir, J., Umoh, V.J., Audu-Okoh, E., Umoh, U.J. and Kwaga, J.K.P. (2004). Veterinary drug use in poultry farms and determination of antimicrobial drug residues in commercial eggs and slaughtered chicken in Kaduna State, Nigeria. Food Cont, 15, 99–105. https://doi.org/10.1016/S0956-7135(03)00020-3
Kabir, S.M.L. (2010). Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, Diagnosis, Control and Public Health Concerns. Int. J Environ. Res. Public Health, 7, 89–114. doi: 10.3390/ijerph7010089
Kimera, Z.I., Mshana, S.E., Rweyemamu, M.M., Mboera, L.E. and Matee, I.N. (2020). Antimicrobial use and resistance in food-producing animals and environment: an African perspective. Antimicrob. Resist. Infect. Control. 9:37. https://doi.org/10.1186/s13756-020-0697-x
Ma, F. Xu, S., Tang, Z., Li, Z. and Zhang, L. (2020). Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosafety Hlth., 3(1), 32–38. https://doi.org/10.1016/j.bsheal.2020.09.004
Meena, G.S., Raina, V.S., Gupta, A.K., Mohanty, T.K., Bhakat, M., Abdullah, M. and Bishist, R. (2015). Effect of preputial washing on bacterial load and preservability of semen in Murrah buffalo bulls. Vet. World. 8(6): 798-803. doi: 10.14202/vetworld.2015.798-803.
Mshelia, G.D., Bilal, V.T., Maina, V.A., Okon, K, Mamza, S.A., Peter, I.D. and Egwu, G.O. (2014). Microbiological studies on genital infections in slaughtered ewes from tropical arid zone of Nigeria. Sokoto J. Vet. Sci, 12:18-22. DOI:10.4314/sokjvs.v12i1.3
Najee, H.B., Al-Shawii, A.M. and Abd-Al Rahman, L.Y. (2012). Bacterial contamination of imported bulls frozen semen. Al-Anbar J. Vet Sci.. 5(1): 54-62.
Navya, M. (2012). Bacterial load in the neat, extended and frozen bull semen and its antibiogram. Msc. Bangalore, Karnataka Veterinary, Animal and Fisheries Sciences University, Bidar.
Patel, H.V., Patel, R.K. and Chauhan, J.B. (2011). Biochemical properties of microbial load in frozen semen of cattle. Wayamba J. Anim Sci.ISSN :2012-578X; P118 - P121
Peter, I.D., Bature, M., Mohammed, M.M., Stephen, J., Mustapha, A., Iliyasu, D., Naaya, I.U. and Wafar, E.S. (2023). Preputial Bacterial Flora and antibacterial Susceptibility in Camels in Maiduguri, North-eastern, Nigeria. J Sustain. Vet. Allied Sci, 4(2), 146-150. https://doi.org/10.54328/covm.josvas.2023.112
Poole, K. (2005). Aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 49(2): 479-487. Doi: 10.1128/AAC.49.2.479-487.2005 PMCID: PMC547279 PMID: 15673721
Romano, J.E., Zanoni, R.G., Mislei, B., Bucci, D., Mion, D. and Mari, G. (2022). Comparison between chlorhexidine and povidone-iodine solutions for flushing the preputial cavity on penile mucosa and semen bacterial counts in beef bulls. Theriogenol, 193:114-119. https://doi.org/10.1016/j.theriogenology.2022.09.012
Rota, A., Calicchio, E., Nardoni, S., Fratini, F., Ebani, V.V., Sgorbini, M., Panzani, D., Camillo F.and Mancianti F. (2011). Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions. Theriogenol 76 464–470. https://doi.org/10.1016/j.theriogenology.2011.02.023
Udoh, R.K. (1981). Geographical regions of Nigeria. Heinemann Education Books Ltd. Ibadan, 1-24.
Wickware, C.L., Johnson T.A. and Koziol, J.H. (2020). Composition and diversity of the Preputial microbiota in healthy Bulls. Theriogenol, 145, 231-237. doi: 10.1016/j.theriogenology.2019.11.002. Epub 2019 Nov 5. PMID: 31732161.
Yaniz, J.L., Marco-Aguado, M.A., Mateos, J.A. and Santolaria, P. (2010). Bacterial contamination of ram semen, antibiotic sensitivities, and effects on sperm quality during storage at 15°C. Anim. Reprod. Sci.1:142-149. doi: 10.1016/j.anireprosci.2010.08.006. Epub 2010 Aug 13. PMID: 20832206.
Zaid, N.W. and Al-Zubaidy, I.A. (2009). The effect of natural mating on the bacterial population of the endogenous Ram. Al-Anbar J. Vet Sci.. Vol. 2(1):31-35.