J Small Anim Pract. 2021 Nov;62(11):948-958. doi: 10.1111/jsap.13398. Epub 2021 Jul 15.

Prevalence of subclinical bactibilia in apparently healthy shelter dogs.

The Journal of small animal practice

E Verwey, A Gal, F Kettner, W J Botha, P Pazzi

PMID: 34264529 DOI: 10.1111/jsap.13398

Abstract

OBJECTIVES: To determine the prevalence of subclinical bactibilia in apparently healthy shelter dogs and characterise serum liver enzymes activities, hepatobiliary histopathology and bile cytology in apparently healthy dogs with and without bactibilia.

MATERIALS AND METHODS: Healthy, abandoned dogs euthanased for non-medical reasons were prospectively recruited for this cross-sectional study. Whole blood, collected immediately before euthanasia, was submitted for serum liver enzyme activity (alkaline phosphatase, alanine aminotransferase and gamma-glutamyl transferase) analyses. Bile, gall bladder and liver samples were collected aseptically from dogs within 25 minutes of euthanasia. Bile was submitted for bacterial culture and cytology in all dogs. Gall bladder and liver samples were submitted for histopathological examination in bactibilic dogs and nine randomly selected non-bactibilic dogs.

RESULTS: Sixty-five healthy dogs were included in this study. Bactibilia was diagnosed in 10.8% (7/65) of dogs, with 9.2% (6/65) of dogs diagnosed on cytological examination and 4.6% (3/65) on culture. Elevated alanine aminotransferase activities were present in one bactibilic and five non-bactibilic dogs; and elevated gamma-glutamyl transferase activities in one bactibilic and two non-bactibilic dogs. No dogs had elevated alkaline phosphatase activities. Histopathological changes in bactibilic and non-bactibilic dogs included lymphoplasmocellular cholecystitis (7/7 and 9/9), gall bladder oedema (7/7 and 9/9), hepatic vacuolar degeneration (6/7 and 8/9), cholangitis (5/7 and 7/9), hepatic nodular hyperplasia (3/7 and 5/9) and hepatic cholestasis (2/7 and 4/9).

CLINICAL SIGNIFICANCE: This study confirms that subclinical bactibilia occurs in a small number of apparently healthy shelter dogs and that subclinical hepatobiliary histopathological abnormalities can occur in apparently healthy bactibilic and non-bactibilic dogs.

© 2021 British Small Animal Veterinary Association.

References

1. Besso, J. G., Wrigley, R. H., Gliatto, J. M., et al. (2000) Ultrasonographic appearance and clinical findings in 14 dogs with gallbladder mucocele. Veterinary Radiology and Ultrasound 41, 261-271 - PubMed
2. Center, S. A. (2009) Diseases of the gallbladder and biliary tree. Veterinary Clinics of North America: Small Animal Practice 39, 543-598 - PubMed
3. Center, S. A. (2012) Hepatobiliary infections. In: Infectious Diseases of the Dog and Cat. 3rd edn. Ed C. E. Greene. Saunders/Elsevier, St. Louis, Mosby. pp 981-1012 - PubMed
4. Chida, Y., Sudo, N., Sonoda, J., et al. (2004) Electric foot shock stress-induced exacerbation of alpha-galactosylceramide-triggered apoptosis in mouse liver. Hepatology (Baltimore, Md.) 39, 1131-1140 - PubMed
5. Cullen, J. M., Van den Ingh, T. S., Van Winkle, T., et al. (2006) Morphological classification of parenchymal disorders of the canine and feline liver: 1 Normal histology, reversible hepatocytic injury and hepatic amyloidosis. In: WSAVA Standards for Clinical and Histological Diagnosis of Canine and Feline Liver Disease. 1st edn. Eds J. Rothuizen, S. E. Bunch, J. A. Charles, J. M. Cullen, V. J. Desmet, V. Szatmari, D. C. Twedt, T. S. Van den Ingh, T. Van Winkle and R. J. Washabau. Elsevier Health Sciences, Amsterdam, Netherlands. pp 77-83 - PubMed
6. Funke, G., Von Graevenitz, A., Clarridge, J. E., et al. (1997) Clinical microbiology of Coryneform bacteria. Clinical Microbiology Reviews 10, 125-159 - PubMed
7. Gaskill, C. L., Miller, L. M., Mattoon, J. S., et al. (2005) Liver histopathology and liver and serum alanine aminotransferase and alkaline phosphatase activities in epileptic dogs receiving phenobarbital. Veterinary Pathology 42, 147-160 - PubMed
8. Howe, L. M., Boothe, D. M. & Boothe, H. W. (1999) Detection of portal and systemic bacteremia in dogs with severe induced hepatic disease and multiple portosystemic shunts. American Journal of Veterinary Research 60, 181-185 - PubMed
9. Hudspeth, M. K., Citron, D. M. & Goldstein, E. J. (1997) Evaluation of a novel specimen transport system (Venturi Transystem) for anaerobic bacteria. Clinical Infectious Diseases 25, S132-S133 - PubMed
10. Kook, P. H., Lutz, S., Reichler, I. M., et al. (2011) Comparative Bacteriologic and Molecular Examinations of Gallbladder Bile of Healthy Dogs. Oral Research Communications of the 21st ECVIM-CA Congress. September 8 to 10. Seville, Spain. p 1495 - PubMed
11. Kook, P. H., Schellenberg, S., Grest, P., et al. (2010) Microbiologic evaluation of gallbladder bile of healthy dogs and dogs with iatrogenic hypercortisolism: a pilot study. Journal of Veterinary Internal Medicine 24, 224-228 - PubMed
12. Laine, L., Lewin, D. N., Naritoku, W., et al. (1997) Prospective comparison of H&E, giemsa, and genta stains for the diagnosis of helicobacter pylori. Gastrointestinal Endoscopy 45, 463-467 - PubMed
13. Laurila, J. J., Ala-Kokko, T. I., Laurila, P. A., et al. (2005) Histopathology of acute acalculous cholecystitis in critically ill patients. Histopathology 47, 485-492 - PubMed
14. Lawrence, Y. A., Ruaux, C. G., Nemanic, S., et al. (2015) Characterization, treatment, and outcome of bacterial cholecystitis and bactibilia in dogs. Journal of the American Veterinary Medical Association 246, 982-989 - PubMed
15. Lidbury, J. A., Rodrigues Hoffmann, A., Ivanek, R., et al. (2017) Interobserver agreement using histological scoring of the canine liver. Journal of Veterinary Internal Medicine 31, 778-783 - PubMed
16. Lleo, M. M., Ghidini, V., Tafi, M. C., et al. (2014) Detecting the presence of bacterial DNA by PCR can be useful in diagnosing culture-negative cases of infection, especially in patients with suspected infection and antibiotic therapy. FEMS Microbiology Letters 354, 153-160 - PubMed
17. Molinero, N., Ruiz, L., Milani, C., et al. (2019) The human gallbladder microbiome is related to the physiological state and the biliary metabolic profile. Microbiome 7, 100 - PubMed
18. Namvar, A. E., Bastarahang, S., Abbasi, N., et al. (2014) Clinical characteristics of Staphylococcus epidermidis: a systematic review. GMS Hygiene and Infection Control 9, Doc23 - PubMed
19. Neel, J. A., Tarigo, J. & Grindem, C. B. (2006) Gallbladder aspirate from a dog. Veterinary Clinical Pathology 35, 467-470 - PubMed
20. Niza, M. M. R. E., Ferreira, A. J. A., Peleteiro, M. C., et al. (2004) Bacteriological study of the liver in dogs. Journal of Small Animal Practice 45, 401-404 - PubMed
21. Nuriel-Ohayon, M., Neuman, H. & Koren, O. (2016) Microbial changes during pregnancy, birth, and infancy. Frontiers in Microbiology 7, 1031 - PubMed
22. Ohta, T., Nagakawa, T., Tsukioka, Y., et al. (1992) Proliferative activity of bile duct epithelium after bacterial infection in dogs. Scandinavian Journal of Gastroenterology 27, 845-851 - PubMed
23. O'Neill, E. J., Day, M. J., Hall, E. J., et al. (2006) Bacterial cholangitis/cholangiohepatitis with or without concurrent cholecystitis in four dogs. Journal of Small Animal Practice 47, 325-335 - PubMed
24. Oswald, G. P., Twedt, D. C. & Steyn, P. (1994) Campylobacter-jejuni bacteremia and acute cholecystitis in 2 dogs. Journal of the American Animal Hospital Association 30, 165-169 - PubMed
25. Park, J. W., Lee, J. K., Lee, K. T., et al. (2014) How to interpret the bile culture results of patients with biliary tract infections. Clinics and Research in Hepatology and Gastroenterology 38, 300-309 - PubMed
26. Pashmakova, M. B., Piccione, J., Bishop, M. A., et al. (2017) Agreement between microscopic examination and bacterial culture of bile samples for detection of bactibilia in dogs and cats with hepatobiliary disease. Journal of the American Veterinary Medical Association 250, 1007-1013 - PubMed
27. Peters, L. M., Glanemann, B., Garden, O. A., et al. (2016) Cytological findings of 140 bile samples from dogs and cats and associated clinical pathological data. Journal of Veterinary Internal Medicine 30, 123-131 - PubMed
28. Pourhoseingholi, M. A., Vahedi, M. & Rahimzadeh, M. (2013) Sample size calculation in medical studies. Gastroenterology Hepatol Bed Bench 6, 14-17 - PubMed
29. Saito, K. & Nakanuma, Y. (1992) Lactoferrin and lysozyme in the intrahepatic bile duct of normal livers and hepatolithiasis. An immunohistochemical study. Journal of Hepatology 15, 147-153 - PubMed
30. Savary-Bataille, K. C. M., Bunch, S. E., Spaulding, K. A., et al. (2003) Percutaneous ultrasound-guided cholecystocentesis in healthy cats. Journal of Veterinary Internal Medicine 17, 298-303 - PubMed
31. Scott-Conner, C. E. & Grogan, J. B. (1994) The pathophysiology of biliary obstruction and its effect on phagocytic and immune function. Journal of Surgical Research 57, 316-336 - PubMed
32. Sjodahl, R., Tagesson, C. & Wetterfors, J. (1978) On the pathogenesis of acute cholecystitis. Surgery, Gynecology and Obstetrics 146, 199-202 - PubMed
33. Stevens, A., Lowe, J. S., Young, B., et al. (2002) Notes on commonly used staining methods. In: Wheater's Basic Histopathology: A Colour Atlas and Text. 4th edn. Eds A. Stevens, J. S. Lowe and B. Young. Elsevier Limited, Churchill Livingstone, London. pp 284-285 - PubMed
34. Sung, J. Y., Costerton, J. W. & Shaffer, E. A. (1992) Defense system in the biliary-tract against bacterial infection. Digestive Diseases and Sciences 37, 689-696 - PubMed
35. Sung, J. Y., Shaffer, E. A., Olson, M. E., et al. (1991) Bacterial invasion of the biliary system by way of the portal-venous system. Hepatology 14, 313-317 - PubMed
36. Tamborini, A., Jahns, H., Mcallister, H., et al. (2016) Bacterial cholangitis, cholecystitis, or both in dogs. Journal of Veterinary Internal Medicine 30, 1046-1055 - PubMed
37. Thoresen, S. I., Tverdal, A., Havre, G., et al. (1995) Effects of storage time and freezing temperature on clinical chemical parameters from canine serum and heparinized plasma. Veterinary Clinical Pathology 24, 129-133 - PubMed
38. Van den Ingh, T. S., Cullen, J. M., Twedt, D. C., et al. (2006a) Morphological classification of biliary disorders of the canine and feline liver. In: WSAVA Standards for Clinical and Histological Diagnosis of Canine and Feline Liver Disease. 1st edn. Eds J. Rothuizen, S. E. Bunch, J. A. Charles, J. M. Cullen, V. J. Desmet, V. Szatmari, D. C. Twedt, T. S. Van den Ingh, T. Van Winkle and R. J. Washabau. Elsevier Health Sciences, Amsterdam, Netherlands. pp 61-75 - PubMed
39. Van den Ingh, T. S., Van Winkle, T., Cullen, J. M., et al. (2006b) Morphological classification of parenchymal disorders of the canine and feline liver: 2 hepatocellular death, hepatitis and cirrhosis. In: WSAVA Standards for Clinical and Histological Diagnosis of Canine and Feline Liver Disease. 1st edn. Eds J. Rothuizen, S. E. Bunch, J. A. Charles, J. M. Cullen, V. J. Desmet, V. Szatmari, D. C. Twedt, T. S. Van den Ingh, T. Van Winkle and R. J. Washabau. Elsevier Health Sciences, Amsterdam, Netherlands. pp 85-100 - PubMed
40. Vancanneyt, M., Devriese, L. A., De Graef, E. M., et al. (2004) Streptococcus minor sp. nov., from faecal samples and tonsils of domestic animals. International Journal of Systematic and Evolutionary Microbiology 54, 449-452 - PubMed
41. Verdier, J., Luedde, T. & Sellge, G. (2015) Biliary mucosal barrier and microbiome. Viszeralmedizin 31, 156-161 - PubMed
42. Wagner, K. A., Hartmann, F. A. & Trepanier, L. A. (2007) Bacterial culture results from liver, gallbladder, or bile in 248 dogs and cats evaluated for hepatobiliary disease: 1998-2003. Journal of Veterinary Internal Medicine 21, 417-424 - PubMed
43. Woo, P. C. Y., Fung, A. A. Y., Lau, S. K. P., et al. (2002) Identification by 16S rRNA gene sequencing of lactobacillus salivarius bacteremic cholecystitis. Journal of Clinical Microbiology 40, 265-267 - PubMed

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