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Doğum Sonrası İlk On Günde Loşyada Bulunan Patojen Bakteriler Süt Sığırlarında Boş Gün Süresini Uzatır

Yıl 2021, Cilt 16, Sayı 1, 32 - 40, 26.04.2021

Öz

Bu çalışmanın amacı, postpartum erken dönemde loşyadan izole edilen bakterilerin (Escherichia coli, Trueperella pyogenes, Prevotella melaninogenica ve Fusobacterium necrophorum) antibiyotik direnç profili, virülans geni ve bunların ineklerde yeniden gebe kalma süresi üzerindeki etkilerini değerlendirmektir. Çalışma, birden fazla doğum yapmış 36 Simental inekten postpartum ilk 10 gündeki uterus akıntısından elde edilen izolatlar üzerinde gerçekleştirildi. Kültür ve biyokimyasal özellikleri belirlenen izolatların virülans genleri polimeraz zincir reaksiyonu ile incelendi. İzolatların antimikrobiyal duyarlılıkları disk difüzyon yöntemi ile saptandı. Çalışmadaki izole edilen T. pyogenes (n = 97) ve E. coli'nin (n = 47) virülans geni taşıdığı, ancak F. necrophorum (n = 16) ve P. melaninogenica (n = 15)’nın taşımadığı belirlendi. Tüm izolatlar beta − laktam antibiyotiklere ve tetrasikline karşı önemli derecede duyarlıydı. E. coli ve T. pyogenes, bu çalışmada aminoglikozid antibiyotiklere duyarlı iken F. necrophorum ve P. melaninogenica dirençliydi. E. coli ve F. necrophorum trimetoprim − sülfametoksazole duyarlı iken T. pyogenes ve P. melaninogenica dirençliydi. Ayrıca, E. coli, T. pyogenes, P. melaninogenica ve F. necrophorum’un yeniden gebe kalma süresi uzayan hayvanlarda öne çıkan bakteriler idi (P<0.05). Bu bulgular, uterus bakterilerinin yeniden gebe kalma süresinin uzamasına neden olduğunu ve uterus infeksiyonlarının tedavisinde ilk seçenek olarak beta − laktam türevi antibiyotiklerin kullanılabileceğini ortaya koymaktadır.

Kaynakça

  • 1. Sheldon IM., Lewis GS., LeBlanc S., Gilbert RO., 2006. Defining postpartum uterine disease in cattle. Theriogenology, 65, 1516-1530.
  • 2. McDougall S., Hussein H., Aberdein D., Buckle K., Roche J., Burke C., Mitchell M., Meier S., 2011. Relationships between cytology, bacteriology and vaginal discharge scores and reproductive performance in dairy cattle. Theriogenology, 76, 229−240.
  • 3. Pascottini OB., Van Schyndel SJ., Spricigo JW., Rousseau J., Weese JS., LeBlanc SJ., 2020. Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis. Sci Rep, 10, 12353.
  • 4. Pohl A., Lübke-Becker A., Heuwieser W., 2018. Minimum inhibitory concentrations of frequently used antibiotics against Escherichia coli and Trueperella pyogenes isolated from uteri of postpartum dairy cows. J Dairy Sci, 101, 1355-1364.
  • 5. LeBlanc SJ., 2008. Postpartum uterine disease and dairy herd reproductive performance: A review. Vet J, 176, 102-114.
  • 6. Sheldon IM., Price SB., Cronin J., Gilbert RO., Gadsby JE., 2009. Mechanisms of infertility associated with clinical and subclinical endometritis in high producing dairy cattle. Reprod Domest Anim, 44, 1−9.
  • 7. de Cassia Bicudo L., Oba E., Bicudo SD., da Silva Leite D., Siqueira AK., de Souza Monobe MM., Nogueira M., de Figueiredo Pantoja JC., Listoni FJ., Ribeiro MG., 2019. Virulence factors and phylogenetic group profile of uterine Escherichia coli in early postpartum of high-producing dairy cows. Anim Prod Sci, 59, 1898-1905.
  • 8. Moreno E., Planells I., Prats G., Planes, AM., Moreno G., Andreu A., 2005. Comparative study of Escherichia coli virulence determinants in strains causing urinary tract bacteremia versus strains causing pyelonephritis and other sources of bacteremia. Diagn Microbiol Infect Dis, 53, 93-99.
  • 9. Santos TM., Gilbert RO., Bicalho RC., 2011. Metagenomic analysis of the uterine bacterial microbiota in healthy and metritic postpartum dairy cows. J Dairy Sci, 94, 291-302.
  • 10. Williams EJ., Fischer DP., Pfeiffer DU., England GC., Noakes DE., Dobson H., Sheldon IM., 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology, 63, 102-117.
  • 11. Zhou H., Bennett G., Hickford JG., 2009. Variation in Fusobacterium necrophorum strains present on the hooves of footrot infected sheep, goats and cattle. Vet Microbiol, 135, 363-367.
  • 12. Yoshida A., Tachibana M., Ansai T., Takehara T., 2005. Multiplex polymerase chain reaction assay for simultaneous detection of black−pigmented Prevotella species in oral specimens. Oral Microbiol Immun, 20, 43-46.
  • 13. Gilbert RO., Shin ST., Guard CL., Erb HN., Frajblat M., 2005. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology, 64, 1879−1888.
  • 14. Winn WC., Allen S., Hall GS., Janda W., 2006. Koneman's Color Atlas and Textbook of Diagnostic Microbiology. Lippincott Williams & Wilkins, Baltimore.
  • 15. Ertaş HB., Kılıç A., Özbey G., Muz A., 2005. Isolation of Arcanobacterium (Actinomyces) pyogenes from abscessed cattle kidney and identification by PCR. Turk J Vet Anim Sci, 29, 455-459.
  • 16. Clinical & Laboratory Standards Institute 2006. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria; proposed guideline. M45−P. CLSI, 6-7.
  • 17. Clinical & Laboratory Standards Institute 2015. Performance standards for antimicrobial susceptibility testing; twenty−fifth informational supplement. M100−S25. CLSI, 35.
  • 18. Adiguzel MC., Diren Sigirci B., Celik B., Kahraman BB., Metiner K., Ikiz S., Bagcigil AF., Ak S., Ozgur NY., 2018. Phenotypic and genotypic examination of antimicrobial resistance in thermophilic Campylobacter species isolated from poultry in Turkey. J Vet Res, 62, 463-468.
  • 19. Dohmen MJ., Joop K., Sturk A., Bols, PEJ., Lohuis JACM., 2000. Relationship between intra−uterine bacterial contamination, endotoxin levels and the development of endometritis in postpartum cows with dystocia or retained placenta. Theriogenology, 54, 1019−1032.
  • 20. Sharma A., Singh M., Kumar P., Sharma A., Kashyap A., Neelam IB., Sharma A., Chaudhary N., Sharma P., 2017. Bacterial isolation, culture sensitivity test, endometrial cytology of postpartum cows and assessment of their reproductive performance. Int J Curr Microbiol Appl Sci, 6, 519-527.
  • 21. Takamtha A., Phanaratkitti V., Adirekkiet O., Panyapornwitaya V., Boonyayatra S., Kraeusukol K., 2013. Prevalence of isolated bacteria from clinical endometritis uterine and antimicrobial susceptibility in postpartum dairy cows. Chiang Mai V J, 11, 237-245.
  • 22. Chen H., Fu K., Pang B., Wang J., Li H., Jiang Z., Feng Y., Tian W., Cao R., 2020. Determination of uterine bacterial community in postpartum dairy cows with metritis based on 16S rDNA sequencing. Vet Anim Sci, 20, 100102.
  • 23. Bicalho ML., Lima FS., Machado VS., Bicalho MLS., Lima FS., Machado VS., Meira JREB., Ganda EK., Foditsch C., Bicalho RC., Gilbert R O., 2016. Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology, 85, 267-274.
  • 24. Brick TA., Schuenemann GM., Bas S., Daniels JB., Pinto CR., Rings DM., Rajala-Schultz PJ., 2012. Effect of intrauterine dextrose or antibiotic therapy on reproductive performance of lactating dairy cows diagnosed with clinical endometritis. J Dairy Sci, 95, 1894-1905.
  • 25. Appiah MO., Wang J., Lu W., 2020. Microflora in the reproductive tract of cattle: A review (Running Title: The Microflora and Bovine Reproductive Tract). Agriculture, 10, 232.
  • 26. Lima FS., 2020. Recent advances and future directions for uterine diseases diagnosis, pathogenesis, and management in dairy cows. Anim Reprod, 17, e20200063.
  • 27. Papich MG., 2002. Saunders Handbook of Veterinary Drugs. Elsevier, North Carolina.
  • 28. Piersanti RL., Zimpel R., Molinari PC., Dickson MJ., Ma Z., Jeong KC., Santos JE., Sheldon IM., Bromfield JJ., 2019. A model of clinical endometritis in Holstein heifers using pathogenic Escherichia coli and Trueperella pyogenes. J Dairy Sci, 102, 2686-2697.
  • 29. Galvao KN., Bicalho RC., Jeon SJ., 2019. Symposium review: The uterine microbiome associated with the development of uterine disease in dairy cows. J Dairy Sci, 102, 11786-11797.
  • 30. Galvao KN., Greco LF., Vilela JM., Filho MFS., Santos JEP., 2009. Effect of intrauterine infusion of ceftiofur on uterine health and fertility in dairy cows. J Dairy Sci, 92, 1532-1542.
  • 31. Sens A., Heuwieser W., 2013. Presence of Escherichia coli, Trueperella pyogenes, α−hemolytic streptococci, and coagulase−negative staphylococci and prevalence of subclinical endometritis. J Dairy Sci, 96, 6347-6354.
  • 32. Sheldon IM., Noakes DE., Rycroft AN., Pfeiffer DU., Dobson H., 2002. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction, 123, 837-845.
  • 33. Azawi OI., 2008. Postpartum uterine infection in cattle. Anim Reprod Sci, 105, 187-208.
  • 34. Staton GJ., Crosby−Durrani H., Roberts G., Gilbert RO., Gadsby JE., 2020. Novel ulcerative leg lesions in yearling lambs: Clinical features, microbiology and histopathology. Vet Microbiol, 247, 108790.
  • 35. Brodzki P., Bochniarz M., Brodzki A., Wrona Z., Wawron W., 2014. Trueperella pyogenes and Escherichia coli as an etiological factor of endometritis in cows and the susceptibility of these bacteria to selected antibiotics. Pol J Vet Sci, 17, 657-664.
  • 36. Gautam G., Nakao T., Koike K., Long ST., Yusuf M., Ranasinghe RMSBK., Hayashi A., 2010. Spontaneous recovery or persistence of postpartum endometritis and risk factors for its persistence in Holstein cows. Theriogenology, 73, 168-179.
  • 37. Green MP., Ledgard AM., Beaumont SE., Berg MC., McNatty KP., Peterson AJ., Back PJ., 2011. Long−term alteration of follicular steroid concentrations in relation to subclinical endometritis in postpartum dairy cows. Anim Sci J, 89, 3551-3560.
  • 38. Jeon SJ., Cunha F., Vieira−Neto A., Bicalho RC., Lima S., Bicalho ML., Galvao KN., 2017. Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome, 5, 109.

Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows

Yıl 2021, Cilt 16, Sayı 1, 32 - 40, 26.04.2021

Öz

The aims of this study were to evaluate the antibiotic resistance profiles and virulence genes of bacteria (Escherichia coli, Trueperella pyogenes, Prevotella melaninogenica, and Fusobacterium necrophorum) isolated from lochia during early postpartum and their effects on days open. The study was conducted on isolates, which were obtained from uterine discharges in the first 10 days of postpartum period, from 36 multiparous Simmental cows. The virulence genes of the isolates were investigated by polymerase chain reaction. The antimicrobial susceptibilities of the isolates were examined by the disc diffusion method. T. pyogenes (n = 97) and E. coli (n = 47) were revealed to carry the virulence gene (name of the gene), but not F. necrophorum (n = 16) and P. melaninogenica (n = 15). All isolates tested in this study were significantly sensitive to beta−lactam and tetracycline. E. coli and T. pyogenes were susceptible to aminoglycoside antibiotics, while F. necrophorum and P. melaninogenica were resistant to them. E. coli and F. necrophorum were susceptible to trimethoprim−sulfamethoxazole while T. pyogenes and P. melaninogenica were resistant. Those bacteria were predominant in cows with a prolonged days open (P<0.05). The uterine bacteria are responsible for prolonged days open and beta−lactam−derived antibiotics could be used as the first choice in the treatment of fresh cow uterine infections.

Kaynakça

  • 1. Sheldon IM., Lewis GS., LeBlanc S., Gilbert RO., 2006. Defining postpartum uterine disease in cattle. Theriogenology, 65, 1516-1530.
  • 2. McDougall S., Hussein H., Aberdein D., Buckle K., Roche J., Burke C., Mitchell M., Meier S., 2011. Relationships between cytology, bacteriology and vaginal discharge scores and reproductive performance in dairy cattle. Theriogenology, 76, 229−240.
  • 3. Pascottini OB., Van Schyndel SJ., Spricigo JW., Rousseau J., Weese JS., LeBlanc SJ., 2020. Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis. Sci Rep, 10, 12353.
  • 4. Pohl A., Lübke-Becker A., Heuwieser W., 2018. Minimum inhibitory concentrations of frequently used antibiotics against Escherichia coli and Trueperella pyogenes isolated from uteri of postpartum dairy cows. J Dairy Sci, 101, 1355-1364.
  • 5. LeBlanc SJ., 2008. Postpartum uterine disease and dairy herd reproductive performance: A review. Vet J, 176, 102-114.
  • 6. Sheldon IM., Price SB., Cronin J., Gilbert RO., Gadsby JE., 2009. Mechanisms of infertility associated with clinical and subclinical endometritis in high producing dairy cattle. Reprod Domest Anim, 44, 1−9.
  • 7. de Cassia Bicudo L., Oba E., Bicudo SD., da Silva Leite D., Siqueira AK., de Souza Monobe MM., Nogueira M., de Figueiredo Pantoja JC., Listoni FJ., Ribeiro MG., 2019. Virulence factors and phylogenetic group profile of uterine Escherichia coli in early postpartum of high-producing dairy cows. Anim Prod Sci, 59, 1898-1905.
  • 8. Moreno E., Planells I., Prats G., Planes, AM., Moreno G., Andreu A., 2005. Comparative study of Escherichia coli virulence determinants in strains causing urinary tract bacteremia versus strains causing pyelonephritis and other sources of bacteremia. Diagn Microbiol Infect Dis, 53, 93-99.
  • 9. Santos TM., Gilbert RO., Bicalho RC., 2011. Metagenomic analysis of the uterine bacterial microbiota in healthy and metritic postpartum dairy cows. J Dairy Sci, 94, 291-302.
  • 10. Williams EJ., Fischer DP., Pfeiffer DU., England GC., Noakes DE., Dobson H., Sheldon IM., 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology, 63, 102-117.
  • 11. Zhou H., Bennett G., Hickford JG., 2009. Variation in Fusobacterium necrophorum strains present on the hooves of footrot infected sheep, goats and cattle. Vet Microbiol, 135, 363-367.
  • 12. Yoshida A., Tachibana M., Ansai T., Takehara T., 2005. Multiplex polymerase chain reaction assay for simultaneous detection of black−pigmented Prevotella species in oral specimens. Oral Microbiol Immun, 20, 43-46.
  • 13. Gilbert RO., Shin ST., Guard CL., Erb HN., Frajblat M., 2005. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology, 64, 1879−1888.
  • 14. Winn WC., Allen S., Hall GS., Janda W., 2006. Koneman's Color Atlas and Textbook of Diagnostic Microbiology. Lippincott Williams & Wilkins, Baltimore.
  • 15. Ertaş HB., Kılıç A., Özbey G., Muz A., 2005. Isolation of Arcanobacterium (Actinomyces) pyogenes from abscessed cattle kidney and identification by PCR. Turk J Vet Anim Sci, 29, 455-459.
  • 16. Clinical & Laboratory Standards Institute 2006. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria; proposed guideline. M45−P. CLSI, 6-7.
  • 17. Clinical & Laboratory Standards Institute 2015. Performance standards for antimicrobial susceptibility testing; twenty−fifth informational supplement. M100−S25. CLSI, 35.
  • 18. Adiguzel MC., Diren Sigirci B., Celik B., Kahraman BB., Metiner K., Ikiz S., Bagcigil AF., Ak S., Ozgur NY., 2018. Phenotypic and genotypic examination of antimicrobial resistance in thermophilic Campylobacter species isolated from poultry in Turkey. J Vet Res, 62, 463-468.
  • 19. Dohmen MJ., Joop K., Sturk A., Bols, PEJ., Lohuis JACM., 2000. Relationship between intra−uterine bacterial contamination, endotoxin levels and the development of endometritis in postpartum cows with dystocia or retained placenta. Theriogenology, 54, 1019−1032.
  • 20. Sharma A., Singh M., Kumar P., Sharma A., Kashyap A., Neelam IB., Sharma A., Chaudhary N., Sharma P., 2017. Bacterial isolation, culture sensitivity test, endometrial cytology of postpartum cows and assessment of their reproductive performance. Int J Curr Microbiol Appl Sci, 6, 519-527.
  • 21. Takamtha A., Phanaratkitti V., Adirekkiet O., Panyapornwitaya V., Boonyayatra S., Kraeusukol K., 2013. Prevalence of isolated bacteria from clinical endometritis uterine and antimicrobial susceptibility in postpartum dairy cows. Chiang Mai V J, 11, 237-245.
  • 22. Chen H., Fu K., Pang B., Wang J., Li H., Jiang Z., Feng Y., Tian W., Cao R., 2020. Determination of uterine bacterial community in postpartum dairy cows with metritis based on 16S rDNA sequencing. Vet Anim Sci, 20, 100102.
  • 23. Bicalho ML., Lima FS., Machado VS., Bicalho MLS., Lima FS., Machado VS., Meira JREB., Ganda EK., Foditsch C., Bicalho RC., Gilbert R O., 2016. Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology, 85, 267-274.
  • 24. Brick TA., Schuenemann GM., Bas S., Daniels JB., Pinto CR., Rings DM., Rajala-Schultz PJ., 2012. Effect of intrauterine dextrose or antibiotic therapy on reproductive performance of lactating dairy cows diagnosed with clinical endometritis. J Dairy Sci, 95, 1894-1905.
  • 25. Appiah MO., Wang J., Lu W., 2020. Microflora in the reproductive tract of cattle: A review (Running Title: The Microflora and Bovine Reproductive Tract). Agriculture, 10, 232.
  • 26. Lima FS., 2020. Recent advances and future directions for uterine diseases diagnosis, pathogenesis, and management in dairy cows. Anim Reprod, 17, e20200063.
  • 27. Papich MG., 2002. Saunders Handbook of Veterinary Drugs. Elsevier, North Carolina.
  • 28. Piersanti RL., Zimpel R., Molinari PC., Dickson MJ., Ma Z., Jeong KC., Santos JE., Sheldon IM., Bromfield JJ., 2019. A model of clinical endometritis in Holstein heifers using pathogenic Escherichia coli and Trueperella pyogenes. J Dairy Sci, 102, 2686-2697.
  • 29. Galvao KN., Bicalho RC., Jeon SJ., 2019. Symposium review: The uterine microbiome associated with the development of uterine disease in dairy cows. J Dairy Sci, 102, 11786-11797.
  • 30. Galvao KN., Greco LF., Vilela JM., Filho MFS., Santos JEP., 2009. Effect of intrauterine infusion of ceftiofur on uterine health and fertility in dairy cows. J Dairy Sci, 92, 1532-1542.
  • 31. Sens A., Heuwieser W., 2013. Presence of Escherichia coli, Trueperella pyogenes, α−hemolytic streptococci, and coagulase−negative staphylococci and prevalence of subclinical endometritis. J Dairy Sci, 96, 6347-6354.
  • 32. Sheldon IM., Noakes DE., Rycroft AN., Pfeiffer DU., Dobson H., 2002. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction, 123, 837-845.
  • 33. Azawi OI., 2008. Postpartum uterine infection in cattle. Anim Reprod Sci, 105, 187-208.
  • 34. Staton GJ., Crosby−Durrani H., Roberts G., Gilbert RO., Gadsby JE., 2020. Novel ulcerative leg lesions in yearling lambs: Clinical features, microbiology and histopathology. Vet Microbiol, 247, 108790.
  • 35. Brodzki P., Bochniarz M., Brodzki A., Wrona Z., Wawron W., 2014. Trueperella pyogenes and Escherichia coli as an etiological factor of endometritis in cows and the susceptibility of these bacteria to selected antibiotics. Pol J Vet Sci, 17, 657-664.
  • 36. Gautam G., Nakao T., Koike K., Long ST., Yusuf M., Ranasinghe RMSBK., Hayashi A., 2010. Spontaneous recovery or persistence of postpartum endometritis and risk factors for its persistence in Holstein cows. Theriogenology, 73, 168-179.
  • 37. Green MP., Ledgard AM., Beaumont SE., Berg MC., McNatty KP., Peterson AJ., Back PJ., 2011. Long−term alteration of follicular steroid concentrations in relation to subclinical endometritis in postpartum dairy cows. Anim Sci J, 89, 3551-3560.
  • 38. Jeon SJ., Cunha F., Vieira−Neto A., Bicalho RC., Lima S., Bicalho ML., Galvao KN., 2017. Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome, 5, 109.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Bilimleri ve Hizmetleri
Bölüm Araştırma Makaleleri
Yazarlar

Mehmet Cemal ADIGUZEL>
ATATURK UNIVERSITY, FACULTY OF VETERINARY, DEPARTMENT OF PRE-CLINICAL SCIENCES, DEPARTMENT OF MICROBIOLOGY
0000-0002-2385-9649
Türkiye


Seyda CENGİZ> (Sorumlu Yazar)
ATATURK UNIVERSITY, FACULTY OF VETERINARY, DEPARTMENT OF PRE-CLINICAL SCIENCES, DEPARTMENT OF MICROBIOLOGY
Türkiye


Mehmet CENGİZ>
ATATURK UNIVERSITY, FACULTY OF VETERINARY, DEPARTMENT OF CLINICAL SCIENCES, DEPARTMENT OF OBSTETRICS AND GYNECOLOGY
Türkiye


Armağan HAYIRLI>
ATATURK UNIVERSITY, FACULTY OF VETERINARY, DEPARTMENT OF ZOOTECHNICS AND ANIMAL FEEDING, DEPARTMENT OF ANIMAL NUTRITION AND ANIMAL FEEDING DISEASES
Türkiye

Destekleyen Kurum Scientific Research Projects Coordination Unit of Atatürk University
Proje Numarası THD−2017−6207
Yayımlanma Tarihi 26 Nisan 2021
Yayınlandığı Sayı Yıl 2021, Cilt 16, Sayı 1

Kaynak Göster

Bibtex @araştırma makalesi { ataunivbd845646, journal = {Atatürk Üniversitesi Veteriner Bilimleri Dergisi}, issn = {1306-6137}, eissn = {2147-9615}, address = {}, publisher = {Atatürk Üniversitesi}, year = {2021}, volume = {16}, number = {1}, pages = {32 - 40}, title = {Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows}, key = {cite}, author = {Adıguzel, Mehmet Cemal and Cengiz, Seyda and Cengiz, Mehmet and Hayırlı, Armağan} }
APA Adıguzel, M. C. , Cengiz, S. , Cengiz, M. & Hayırlı, A. (2021). Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows . Atatürk Üniversitesi Veteriner Bilimleri Dergisi , 16 (1) , 32-40 . Retrieved from https://dergipark.org.tr/tr/pub/ataunivbd/issue/62017/845646
MLA Adıguzel, M. C. , Cengiz, S. , Cengiz, M. , Hayırlı, A. "Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows" . Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16 (2021 ): 32-40 <https://dergipark.org.tr/tr/pub/ataunivbd/issue/62017/845646>
Chicago Adıguzel, M. C. , Cengiz, S. , Cengiz, M. , Hayırlı, A. "Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows". Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16 (2021 ): 32-40
RIS TY - JOUR T1 - Doğum Sonrası İlk On Günde Loşyada Bulunan Patojen Bakteriler Süt Sığırlarında Boş Gün Süresini Uzatır AU - Mehmet CemalAdıguzel, SeydaCengiz, MehmetCengiz, ArmağanHayırlı Y1 - 2021 PY - 2021 N1 - DO - T2 - Atatürk Üniversitesi Veteriner Bilimleri Dergisi JF - Journal JO - JOR SP - 32 EP - 40 VL - 16 IS - 1 SN - 1306-6137-2147-9615 M3 - UR - Y2 - 2021 ER -
EndNote %0 Atatürk Üniversitesi Veteriner Bilimleri Dergisi Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows %A Mehmet Cemal Adıguzel , Seyda Cengiz , Mehmet Cengiz , Armağan Hayırlı %T Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows %D 2021 %J Atatürk Üniversitesi Veteriner Bilimleri Dergisi %P 1306-6137-2147-9615 %V 16 %N 1 %R %U
ISNAD Adıguzel, Mehmet Cemal , Cengiz, Seyda , Cengiz, Mehmet , Hayırlı, Armağan . "Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows". Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16 / 1 (Nisan 2021): 32-40 .
AMA Adıguzel M. C. , Cengiz S. , Cengiz M. , Hayırlı A. Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021; 16(1): 32-40.
Vancouver Adıguzel M. C. , Cengiz S. , Cengiz M. , Hayırlı A. Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021; 16(1): 32-40.
IEEE M. C. Adıguzel , S. Cengiz , M. Cengiz ve A. Hayırlı , "Pathogenic Bacteria Present in the Lochia First 10−Day Postpartum Prolongs Days Open in Dairy Cows", Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 16, sayı. 1, ss. 32-40, Nis. 2021