Determination of Helicobacter heilmannii in cats by real time polymerase chain reaction and histopathology

Nevin Tuzcu; Zeynep Çelik; Gökhan Akçakavak; Ayşegül Bulut; Rabia Salik; Muhammed Öner; Vedat Kaya; Mehmet Tuzcu

doi:10.24880/maeuvfd.1218001

Research Article

Year 2023, Volume: 8 Issue: 2, 69 - 73, 31.08.2023

Nevin Tuzcu Zeynep Çelik Gökhan Akçakavak Ayşegül Bulut Rabia Salik Muhammed Öner Vedat Kaya Mehmet Tuzcu

https://doi.org/10.24880/maeuvfd.1218001

Cited By: 1

Abstract

References

1. Akcakavak, G., Tuzcu, M., Tuzcu, N., Celik, Z., Tural, A., & Dagar, O. (2023). Investigation with Real- Time PCR and Histopathology on the presence of H. felis, H. heilmannii and H. pylori in dogs. Revista Científica de la Facultad de Ciencias Veterinarias, 33(1), e33214, 1-7. https://doi.org/ 10.52973/rcfcv-e33214
2. Akhtardanesh, B., Jamshidi, S., Sasani, F., Mohammadi, M., Bokaee, S., & Zahraie Salehi, T. (2006). Helicobacter spp. infection and gastric lesions in domestic and stray cats. Veterinarski arhiv, 76(6), 479-488.
3. Bahadori, A., De Witte, C., Agin, M., De Bruyckere, S., Smet, A., Tümgör, G., Gökmen, T. G., Haesebrouck, F., & Köksal, F. (2018). Presence of gastric Helicobacter species in children suffering from gastric disorders in Southern Turkey. Helicobacter, 23(5), e12511. https://doi.org/ 10.1111/hel.12511
4. Blois, S. (2020). Helicobacter infection in small animals. MSD Manual Veterinary Manual.
5. Bruyette, D. (2020). Clinical Small Animal Internal Medicine. John Wiley & Sons.
6. Diker, K. S., Haziroğlu, R., Akan, M., Çelik, S., & Kabakçı, N. (2002). The prevalence, colonization sites and pathological effects of gastric helicobacters in dogs. Turkish journal of veterinary & animal sciences, 26(2), 345-351.
7. Eaton, K., Dewhirst, F., Radin, M. J., Fox, J., Paster, B., Krakowka, S., & Morgan, D. (1993). Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis. International journal of systematic and evolutionary microbiology, 43(1), 99-106. https://doi.org/10.1099/00207713-43-1-99.
8. Eaton, K., Dewhirst, F., Paster, B., Tzellas, N., Coleman, B., Paola, J., & Sherding, R. (1996). Prevalence and varieties of Helicobacter species in dogs from random sources and pet dogs: animal and public health implications. Journal of Clinical Microbiology, 34(12), 3165-3170. https://doi.org/10.1128/jcm.34.12.3165-3170.1996
9. Erginsoy, S., Sözmen, M., & Özcan, K. (2006). Gastric Helicobacter-like organisms in stray cats. Acta Veterinaria Brno, 75(1), 91-98. https://doi.org/10.2754/avb200675010091
10. Geyer, C., Colbatzky, F., Lechner, J., & Hermanns W (1993). Occurrence of spiral-shaped bacteria in gastric biopsies of dogs and cats. Veterinary Record, 133(1), 18-19
11. Gökalp, G., & Gökalp, A. B. (2021). Kedilerin Önemli Bakteriyel Zoonozu; Helicobacter Heilmannii. Journal of Anatolian Environmental and Animal Sciences, 6(3), 333-340. https://doi.org/10.35229/jaes.891405
12. Haesebrouck, F., Pasmans, F., Flahou, B., Chiers, K., Baele, M., Meyns, T., Decostere, A., & Ducatelle, R. (2009). Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clinical microbiology reviews, 22(2), 202-223. https://doi.org/10.1128/CMR.00041-08.
13. Happonen, I., Saari, S., Castren, L., Tyni, O., Hänninen, M. L., & Westermarck, E. (1996). Occurrence and topographical mapping of gastric Helicobacter‐like organisms and their association with histological changes in apparently healthy dogs and cats. Journal of Veterinary Medicine Series A, 43(1‐10), 305-315. https://doi.org/10.1111/j.1439-0442.1996.tb00457.x.
14. Happonen, I., Linden, J., Saari, S., Karjalainen, M., Hänninen, M.-L., Jalava, K., & Westermarck, E. (1998). Detection and effects of helicobacters in healthy dogs and dogs with signs of gastritis. Journal of the American Veterinary Medical Association, 213(12), 1767-1774.
15. Hermanns, W., Kregel, K., Breuer, W., & Lechner, J. (1995). Helicobacter-like organisms: histopathological examination of gastric biopsies from dogs and cats. Journal of comparative pathology, 112(3), 307-318. https://doi.org/10.1016/s0021-9975(05)80083-0.
16. Hong, S., Chung, Y., Kang, W.-G., & Kim, O. (2016). Detection of Helicobacter felis in a cat with gastric disease in laboratory animal facility. Laboratory Animal Research, 32(2), 122-127. https://doi.org/10.5625/lar.2016.32.2.122
17. Husnik, R., Klimes, J., Kovarikova, S., & Kolorz, M. (2022). Helicobacter Species and Their Association with Gastric Pathology in a Cohort of Dogs with Chronic Gastrointestinal Signs. Animals, 12(10), 1254. https://doi.org/10.3390/ani12101254
18. Jalava, K., Kaartinen, M., Utriainen, M., Happonen, I., & Hänninen, M.-L. (1997). Helicobacter salomonis sp. nov., a canine gastric Helicobacter sp. related to Helicobacter felis and Helicobacter bizzozeronii. International journal of systematic and evolutionary microbiology, 47(4), 975-982. https://doi.org/10.1099/00207713-47-4-975
19. Jalava, K., On, S. L., Vandamme, P. A., Happonen, I., Sukura, A., & Hänninen, M.-L. (1998). Isolation and identification of Helicobacter spp. from canine and feline gastric mucosa. Applied and Environmental Microbiology, 64(10), 3998-4006.
20. Kubota-Aizawa, S., Ohno, K., Kanemoto, H., Nakashima, K., Fukushima, K., Uchida, K., Chambers, J. K., Goto-Koshino, Y., Mimuro, H., & Watanabe, T. (2017). Epidemiological study on feline gastric Helicobacter spp. in Japan. Journal of veterinary medical science, 16-0567. https://doi.org/10.1292/jvms.16-0567.
21. Luna, L. G. (1968). Manual of histologic staining methods of the Armed Forces Institute of Pathology, McGraw-Hill.
22. Matos, R., De Witte, C., Smet, A., Berlamont, H., De Bruyckere, S., Amorim, I., Gärtner, F., & Haesebrouck, F. (2020). Antimicrobial susceptibility pattern of Helicobacter heilmannii and Helicobacter ailurogastricus isolates. Microorganisms, 8(6), 957.
23. Murray, P. R., Baron, E. J., Pfaller, M. A., Tenover, F. C., & Olken, R. H. (1995). Manual of Clinical Microbiology (6th Ed.). ASM Press, Washington, USA, 1247-1256.
24. Nakamura, M., Øverby, A., Michimae, H., Matsui, H., Takahashi, S., Mabe, K., Shimoyama, T., Sasaki, M., Terao, S., & Kamada, T. (2020). PCR analysis and specific immunohistochemistry revealing a high prevalence of non‐Helicobacter pylori Helicobacters in Helicobacter pylori‐negative gastric disease patients in Japan: High susceptibility to an Hp eradication regimen. Helicobacter, 25(5), e12700. https://doi.org/10.1111/hel.12700
25. Neiger, R., Dieterich, C., Burnens, A., Waldvogel, A., Corthésy-Theulaz, I., Halter, F., Lauterburg, B., & Schmassmann, A. (1998). Detection and prevalence of Helicobacter infection in pet cats. Journal of Clinical Microbiology, 36(3), 634-637.
26. Neiger, R., Tschudi, M. E., Burnens, A., Goke, B., & Schmassmann, A. (1999). Diagnosis and identification of gastric Helicobacter species by polymerase chain reaction in dogs. Microbial Ecology in Health and Disease, 11(4), 234-240. https://doi.org/10.1080/089106099435682
27. Neiger, R., & Simpson, K. W. (2000). Helicobacter infection in dogs and cats: facts and fiction. Journal of Veterinary Internal Medicine, 14(2), 125-133. https://doi.org/10.1892/0891-6640(2000)014<0125:iidacf>2.3.co;2.
28. Norris, C., Marks, S. L., Eaton, K., Torabian, S., Munn, R., & Solnick, J. V. (1999). Healthy cats are commonly colonized with "Helicobacter heilmannii" that is associated with minimal gastritis. Journal of Clinical Microbiology, 37(1), 189-194.
29. Otto, G., Hazell, S., Fox, J., Howlett, C., Murphy, J., O'Rourke, J., & Lee, A. (1994). Animal and public health implications of gastric colonization of cats by Helicobacter-like organisms. Journal of Clinical Microbiology, 32(4), 1043-1049. https://doi.org/10.1128/jcm.32.4.1043-1049.1994
30. Sağnak, N. S. (2007). İstanbul Yöresinde Sağlıklı ve Klinik Belirti Gösteren Köpeklerde Helicobacter pylori Varlığının Kültür, Polimerase Chain Reaction (PCR) ve Restriction Fragment Length Polymorphism (RFLP) ile Saptanması, Doktora Tezi, İ.Ü., Sağlık Bilimleri Enstitüsü.
31. Stolte, M., Wellens, E., Bethke, B., Ritter, M., & Eidt, H. (1994). Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scandinavian Journal of Gastroenterology, 29(12), 1061-1064. https://doi.org/10.3109/00365529409094888.
32. Tabrizi, A. S., Derakhshandeh, A., Esfandiari, A., & Atashi, Z. A. (2015). Identification of Helicobacter spp. in gastrointestinal tract, pancreas and hepatobiliary system of stray cats. Iranian Journal of Veterinary Research, 16(4), 374.

Determination of Helicobacter heilmannii in cats by real time polymerase chain reaction and histopathology

Year 2023, Volume: 8 Issue: 2, 69 - 73, 31.08.2023

Nevin Tuzcu Zeynep Çelik Gökhan Akçakavak Ayşegül Bulut Rabia Salik Muhammed Öner Vedat Kaya Mehmet Tuzcu

https://doi.org/10.24880/maeuvfd.1218001

Cited By: 1

Abstract

Helicobacter species such as Helicobacter heilmannii, Helicobacter pylori, Helicobacter felis, Helicobacter bizzozeronii, Helicobacter salomonis have been identified in cats and dogs, and research suggesting that these species may be zoonotic agents have increased in recent years. The aim of this study is to reveal the presence of H. heilmannii in stomach and liver tissues taken during necropsies of domestic, stray and shelter cats by real-time PCR and histopathology and to compare histopathological findings and real-time PCR results. The material of the study consisted of stomach and liver tissues taken from 41 cats who died from different causes and were necropsied. DNA of H. heilmannii was determined in the stomach tissues of 36 cats and the liver tissues of 24 cats in the study conducted with real-time PCR using specific primers of H. heilmannii. Epithelial degeneration in the stomach, fibrosis and oedema in the lamina propria and lymphoplasmacytic cell infiltration were detected histopathologically in the cats diagnosed with gastritis. Eight cats were positive in Hematoxylin-Eosin staining and nineteen cats were positive in the staining with Warthin Starry of the sections, in terms of Helicobacter-like microorganisms. Microscopically, dissociation of the remark cords and hydropic degeneration in hepatocytes and mononuclear cell infiltrations in some sections were determined in the livers. In conclusion, with this study, it was understood that real-time PCR analyses are very useful in determining H. heilmannii in cats. However, histopathological examinations are necessary to associate the presence of bacteria with the development of the disease.

Keywords

Cat, histopathology, real-time PCR, H. heilmannii

References

1. Akcakavak, G., Tuzcu, M., Tuzcu, N., Celik, Z., Tural, A., & Dagar, O. (2023). Investigation with Real- Time PCR and Histopathology on the presence of H. felis, H. heilmannii and H. pylori in dogs. Revista Científica de la Facultad de Ciencias Veterinarias, 33(1), e33214, 1-7. https://doi.org/ 10.52973/rcfcv-e33214
2. Akhtardanesh, B., Jamshidi, S., Sasani, F., Mohammadi, M., Bokaee, S., & Zahraie Salehi, T. (2006). Helicobacter spp. infection and gastric lesions in domestic and stray cats. Veterinarski arhiv, 76(6), 479-488.
3. Bahadori, A., De Witte, C., Agin, M., De Bruyckere, S., Smet, A., Tümgör, G., Gökmen, T. G., Haesebrouck, F., & Köksal, F. (2018). Presence of gastric Helicobacter species in children suffering from gastric disorders in Southern Turkey. Helicobacter, 23(5), e12511. https://doi.org/ 10.1111/hel.12511
4. Blois, S. (2020). Helicobacter infection in small animals. MSD Manual Veterinary Manual.
5. Bruyette, D. (2020). Clinical Small Animal Internal Medicine. John Wiley & Sons.
6. Diker, K. S., Haziroğlu, R., Akan, M., Çelik, S., & Kabakçı, N. (2002). The prevalence, colonization sites and pathological effects of gastric helicobacters in dogs. Turkish journal of veterinary & animal sciences, 26(2), 345-351.
7. Eaton, K., Dewhirst, F., Radin, M. J., Fox, J., Paster, B., Krakowka, S., & Morgan, D. (1993). Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis. International journal of systematic and evolutionary microbiology, 43(1), 99-106. https://doi.org/10.1099/00207713-43-1-99.
8. Eaton, K., Dewhirst, F., Paster, B., Tzellas, N., Coleman, B., Paola, J., & Sherding, R. (1996). Prevalence and varieties of Helicobacter species in dogs from random sources and pet dogs: animal and public health implications. Journal of Clinical Microbiology, 34(12), 3165-3170. https://doi.org/10.1128/jcm.34.12.3165-3170.1996
9. Erginsoy, S., Sözmen, M., & Özcan, K. (2006). Gastric Helicobacter-like organisms in stray cats. Acta Veterinaria Brno, 75(1), 91-98. https://doi.org/10.2754/avb200675010091
10. Geyer, C., Colbatzky, F., Lechner, J., & Hermanns W (1993). Occurrence of spiral-shaped bacteria in gastric biopsies of dogs and cats. Veterinary Record, 133(1), 18-19
11. Gökalp, G., & Gökalp, A. B. (2021). Kedilerin Önemli Bakteriyel Zoonozu; Helicobacter Heilmannii. Journal of Anatolian Environmental and Animal Sciences, 6(3), 333-340. https://doi.org/10.35229/jaes.891405
12. Haesebrouck, F., Pasmans, F., Flahou, B., Chiers, K., Baele, M., Meyns, T., Decostere, A., & Ducatelle, R. (2009). Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clinical microbiology reviews, 22(2), 202-223. https://doi.org/10.1128/CMR.00041-08.
13. Happonen, I., Saari, S., Castren, L., Tyni, O., Hänninen, M. L., & Westermarck, E. (1996). Occurrence and topographical mapping of gastric Helicobacter‐like organisms and their association with histological changes in apparently healthy dogs and cats. Journal of Veterinary Medicine Series A, 43(1‐10), 305-315. https://doi.org/10.1111/j.1439-0442.1996.tb00457.x.
14. Happonen, I., Linden, J., Saari, S., Karjalainen, M., Hänninen, M.-L., Jalava, K., & Westermarck, E. (1998). Detection and effects of helicobacters in healthy dogs and dogs with signs of gastritis. Journal of the American Veterinary Medical Association, 213(12), 1767-1774.
15. Hermanns, W., Kregel, K., Breuer, W., & Lechner, J. (1995). Helicobacter-like organisms: histopathological examination of gastric biopsies from dogs and cats. Journal of comparative pathology, 112(3), 307-318. https://doi.org/10.1016/s0021-9975(05)80083-0.
16. Hong, S., Chung, Y., Kang, W.-G., & Kim, O. (2016). Detection of Helicobacter felis in a cat with gastric disease in laboratory animal facility. Laboratory Animal Research, 32(2), 122-127. https://doi.org/10.5625/lar.2016.32.2.122
17. Husnik, R., Klimes, J., Kovarikova, S., & Kolorz, M. (2022). Helicobacter Species and Their Association with Gastric Pathology in a Cohort of Dogs with Chronic Gastrointestinal Signs. Animals, 12(10), 1254. https://doi.org/10.3390/ani12101254
18. Jalava, K., Kaartinen, M., Utriainen, M., Happonen, I., & Hänninen, M.-L. (1997). Helicobacter salomonis sp. nov., a canine gastric Helicobacter sp. related to Helicobacter felis and Helicobacter bizzozeronii. International journal of systematic and evolutionary microbiology, 47(4), 975-982. https://doi.org/10.1099/00207713-47-4-975
19. Jalava, K., On, S. L., Vandamme, P. A., Happonen, I., Sukura, A., & Hänninen, M.-L. (1998). Isolation and identification of Helicobacter spp. from canine and feline gastric mucosa. Applied and Environmental Microbiology, 64(10), 3998-4006.
20. Kubota-Aizawa, S., Ohno, K., Kanemoto, H., Nakashima, K., Fukushima, K., Uchida, K., Chambers, J. K., Goto-Koshino, Y., Mimuro, H., & Watanabe, T. (2017). Epidemiological study on feline gastric Helicobacter spp. in Japan. Journal of veterinary medical science, 16-0567. https://doi.org/10.1292/jvms.16-0567.
21. Luna, L. G. (1968). Manual of histologic staining methods of the Armed Forces Institute of Pathology, McGraw-Hill.
22. Matos, R., De Witte, C., Smet, A., Berlamont, H., De Bruyckere, S., Amorim, I., Gärtner, F., & Haesebrouck, F. (2020). Antimicrobial susceptibility pattern of Helicobacter heilmannii and Helicobacter ailurogastricus isolates. Microorganisms, 8(6), 957.
23. Murray, P. R., Baron, E. J., Pfaller, M. A., Tenover, F. C., & Olken, R. H. (1995). Manual of Clinical Microbiology (6th Ed.). ASM Press, Washington, USA, 1247-1256.
24. Nakamura, M., Øverby, A., Michimae, H., Matsui, H., Takahashi, S., Mabe, K., Shimoyama, T., Sasaki, M., Terao, S., & Kamada, T. (2020). PCR analysis and specific immunohistochemistry revealing a high prevalence of non‐Helicobacter pylori Helicobacters in Helicobacter pylori‐negative gastric disease patients in Japan: High susceptibility to an Hp eradication regimen. Helicobacter, 25(5), e12700. https://doi.org/10.1111/hel.12700
25. Neiger, R., Dieterich, C., Burnens, A., Waldvogel, A., Corthésy-Theulaz, I., Halter, F., Lauterburg, B., & Schmassmann, A. (1998). Detection and prevalence of Helicobacter infection in pet cats. Journal of Clinical Microbiology, 36(3), 634-637.
26. Neiger, R., Tschudi, M. E., Burnens, A., Goke, B., & Schmassmann, A. (1999). Diagnosis and identification of gastric Helicobacter species by polymerase chain reaction in dogs. Microbial Ecology in Health and Disease, 11(4), 234-240. https://doi.org/10.1080/089106099435682
27. Neiger, R., & Simpson, K. W. (2000). Helicobacter infection in dogs and cats: facts and fiction. Journal of Veterinary Internal Medicine, 14(2), 125-133. https://doi.org/10.1892/0891-6640(2000)014<0125:iidacf>2.3.co;2.
28. Norris, C., Marks, S. L., Eaton, K., Torabian, S., Munn, R., & Solnick, J. V. (1999). Healthy cats are commonly colonized with "Helicobacter heilmannii" that is associated with minimal gastritis. Journal of Clinical Microbiology, 37(1), 189-194.
29. Otto, G., Hazell, S., Fox, J., Howlett, C., Murphy, J., O'Rourke, J., & Lee, A. (1994). Animal and public health implications of gastric colonization of cats by Helicobacter-like organisms. Journal of Clinical Microbiology, 32(4), 1043-1049. https://doi.org/10.1128/jcm.32.4.1043-1049.1994
30. Sağnak, N. S. (2007). İstanbul Yöresinde Sağlıklı ve Klinik Belirti Gösteren Köpeklerde Helicobacter pylori Varlığının Kültür, Polimerase Chain Reaction (PCR) ve Restriction Fragment Length Polymorphism (RFLP) ile Saptanması, Doktora Tezi, İ.Ü., Sağlık Bilimleri Enstitüsü.
31. Stolte, M., Wellens, E., Bethke, B., Ritter, M., & Eidt, H. (1994). Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scandinavian Journal of Gastroenterology, 29(12), 1061-1064. https://doi.org/10.3109/00365529409094888.
32. Tabrizi, A. S., Derakhshandeh, A., Esfandiari, A., & Atashi, Z. A. (2015). Identification of Helicobacter spp. in gastrointestinal tract, pancreas and hepatobiliary system of stray cats. Iranian Journal of Veterinary Research, 16(4), 374.

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Details

Primary Language	English
Subjects	Health Care Administration
Journal Section	Research Articles
Authors	Nevin Tuzcu 0000-0001-5899-3955 Zeynep Çelik 0000-0002-9667-5728 Gökhan Akçakavak 0000-0001-5949-4752 Ayşegül Bulut 0000-0002-0085-3586 Rabia Salik 0000-0002-0364-697X Muhammed Öner 0000-0001-5905-1062 Vedat Kaya 0000-0002-5333-9898 Mehmet Tuzcu 0000-0003-3118-1054
Publication Date	August 31, 2023
Submission Date	December 12, 2022
Published in Issue	Year 2023 Volume: 8 Issue: 2

Cite

APA	Tuzcu, N., Çelik, Z., Akçakavak, G., Bulut, A., et al. (2023). Determination of Helicobacter heilmannii in cats by real time polymerase chain reaction and histopathology. Veterinary Journal of Mehmet Akif Ersoy University, 8(2), 69-73. https://doi.org/10.24880/maeuvfd.1218001

Cited By

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Etlik Veteriner Mikrobiyoloji Dergisi

https://doi.org/10.35864/evmd.1354193

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