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Molecular prevalence of Bartonella, Babesia, and hemotropic Mycoplasma species in dogs with hemangiosarcoma from across the United States


Autoři: Erin Lashnits aff001;  Pradeep Neupane aff001;  Julie M. Bradley aff001;  Toni Richardson aff001;  Rachael Thomas aff002;  Keith E. Linder aff003;  Matthew Breen aff002;  Ricardo G. Maggi aff001;  Edward B. Breitschwerdt aff001
Působiště autorů: Intracellular Pathogens Research Laboratory, Comparative Medicine Institute, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America aff001;  Department of Molecular Biomedical Sciences, Comparative Genomics, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America aff002;  Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America aff003;  Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0227234

Souhrn

Hemangiosarcoma (HSA), a locally invasive and highly metastatic endothelial cell neoplasm, accounts for two-thirds of all cardiac and splenic neoplasms in dogs. Bartonella spp. infection has been reported in association with neoplastic and non-neoplastic vasoproliferative lesions in animals and humans. The objective of this study was to determine the prevalence of Bartonella spp. in conjunction with two other hemotropic pathogens, Babesia spp. and hemotropic Mycoplasma spp., in tissues and blood samples from 110 dogs with histopathologically diagnosed HSA from throughout the United States. This was a retrospective, observational study using clinical specimens from 110 dogs with HSA banked by the biospecimen repository of the Canine Comparative Oncology and Genomics Consortium. Samples provided for this study from each dog included: fresh frozen HSA tumor tissue (available from n = 100 of the 110 dogs), fresh frozen non-tumor tissue (n = 104), and whole blood and serum samples (n = 108 and 107 respectively). Blood and tissues were tested by qPCR for Bartonella, hemotropic Mycoplasma, and Babesia spp. DNA; serum was tested for Bartonella spp. antibodies. Bartonella spp. DNA was amplified and sequenced from 73% of dogs with HSA (80/110). In contrast, hemotropic Mycoplasma spp. DNA was amplified from a significantly smaller proportion (5%, p<0.0001) and Babesia spp. DNA was not amplified from any dog. Of the 100 HSA tumor samples submitted, 34% were Bartonella PCR positive (32% of splenic tumors, 57% of cardiac tumors, and 17% of other tumor locations). Of 104 non-tumor tissues, 63% were Bartonella PCR positive (56% of spleen samples, 93% of cardiac samples, and 63% of skin/subcutaneous samples). Of dogs with Bartonella positive HSA tumor, 76% were also positive in non-tumor tissue. Bartonella spp. DNA was not PCR amplified from whole blood. This study documented a high prevalence of Bartonella spp. DNA in dogs with HSA from geographically diverse regions of the United States. While 73% of all tissue samples from these dogs were PCR positive for Bartonella DNA, none of the blood samples were, indicating that whole blood samples do not reflect tissue presence of this pathogen. Future studies are needed to further investigate the role of Bartonella spp. in the development of HSA.

Klíčová slova:

Bartonella – Dogs – Spleen – Polymerase chain reaction – Animal anatomy – Veterinary diagnostics – Babesia – Mycoplasma


Zdroje

1. Knoll LJ, Hogan DA, Leong JM, Heitman J, Condit RC. Pearls collections: What we can learn about infectious disease and cancer. PLOS Pathog. 2018 Mar 29;14(3):e1006915. doi: 10.1371/journal.ppat.1006915 29596508

2. Plummer M, de Martel C, Vignat J, Ferlay J, Bray F, Franceschi S. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Heal. 2016 Sep 1;4(9):e609–16.

3. Group IA for R on CW. Biological Agents: A review of human carcinogens. Vol. 100B, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Geneva, Switzerland; 2012.

4. Riley DR, Sieber KB, Robinson KM, White JR, Ganesan A, Nourbakhsh S, et al. Bacteria-Human Somatic Cell Lateral Gene Transfer Is Enriched in Cancer Samples. PLoS Comput Biol. 2013;9(6).

5. Lax AJ, Thomas W, Kuper H, Parsonnet J, et al. How bacteria could cause cancer: one step at a time. Trends Microbiol. 2002 Jun;10(6):293–9. doi: 10.1016/s0966-842x(02)02360-0 12088666

6. Molnar B, Galamb O, Sipos F, Leiszter K, Tulassay Z. Molecular Pathogenesis of Helicobacter pylori Infection: The Role of Bacterial Virulence Factors. Dig Dis. 2010;28(4–5):604–8. doi: 10.1159/000320060 21088410

7. Pagano JS, Blaser M, Buendia M-A, Damania B, Khalili K, Raab-Traub N, et al. Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol. 2004 Dec;14(6):453–71. doi: 10.1016/j.semcancer.2004.06.009 15489139

8. Prymak C, McKee LJ, Goldschmidt MH, Glickman LT. Epidemiologic, clinical, pathologic, and prognostic characteristics of splenic hemangiosarcoma and splenic hematoma in dogs: 217 cases (1985). J Am Vet Med Assoc. 1988 Sep 15;193(6):706–12. 3192450

9. Mullin C, Clifford CA. Histiocytic Sarcoma and Hemangiosarcoma Update. Vet Clin North Am Small Anim Pract. 2019 Jun 8;

10. Spangler WL, Culbertson MR. Prevalence, type, and importance of splenic diseases in dogs: 1,480 cases (1985–1989). J Am Vet Med Assoc. 1992 Mar 15;200(6):829–34. 1568933

11. Schultheiss PC. A Retrospective Study of Visceral and Nonvisceral Hemangiosarcoma and Hemangiomas in Domestic Animals. J Vet Diagnostic Investig. 2004 Nov 25;16(6):522–6.

12. Grüntzig K, Graf R, Boo G, Guscetti F, Hässig M, Axhausen KW, et al. Swiss Canine Cancer Registry 1955–2008: Occurrence of the Most Common Tumour Diagnoses and Influence of Age, Breed, Body Size, Sex and Neutering Status on Tumour Development. J Comp Pathol. 2016 Aug;155(2–3):156–70. doi: 10.1016/j.jcpa.2016.05.011 27406312

13. Hart BL, Hart LA, Thigpen AP, Willits NH. Neutering of German Shepherd Dogs: associated joint disorders, cancers and urinary incontinence. Vet Med Sci. 2016 Aug;2(3):191–9. doi: 10.1002/vms3.34 29067194

14. Kent MS, Burton JH, Dank G, Bannasch DL, Rebhun RB. Association of cancer-related mortality, age and gonadectomy in golden retriever dogs at a veterinary academic center (1989–2016). Bauer JA, editor. PLoS One. 2018 Feb 6;13(2):e0192578. doi: 10.1371/journal.pone.0192578 29408871

15. Treggiari E, Pedro B, Dukes-McEwan J, Gelzer AR, Blackwood L. A descriptive review of cardiac tumours in dogs and cats. Vet Comp Oncol. 2017 Jun;15(2):273–88. doi: 10.1111/vco.12167 26420436

16. Dana M. ONLINE CASE REPORTS Pericardial Hemangiosarcoma in a 10-Year-Old Papillon.

17. Johnson KA, Powers BE, Withrow SJ, Sheetz MJ, Curtis CR, Wrigley RH. Splenomegaly in dogs. Predictors of neoplasia and survival after splenectomy. J Vet Intern Med. 3(3):160–6. doi: 10.1111/j.1939-1676.1989.tb03092.x 2778749

18. Schick AR, Hayes GM, Singh A, Mathews KG, Higginbotham ML, Sherwood JM. Development and validation of a hemangiosarcoma likelihood prediction model in dogs presenting with spontaneous hemoabdomen: The HeLP score. J Vet Emerg Crit Care. 2019 May 17;29(3):239–45.

19. Batschinski K, Nobre A, Vargas-Mendez E, Tedardi M V, Cirillo J, Cestari G, et al. Canine visceral hemangiosarcoma treated with surgery alone or surgery and doxorubicin: 37 cases (2005–2014). Can Vet J = La Rev Vet Can. 2018;59(9):967–72.

20. Moore AS, Rassnick KM, Frimberger AE. Evaluation of clinical and histologic factors associated with survival time in dogs with stage II splenic hemangiosarcoma treated by splenectomy and adjuvant chemotherapy: 30 cases (2011–2014). J Am Vet Med Assoc. 2017 Sep 1;251(5):559–65. doi: 10.2460/javma.251.5.559 28828962

21. Tamburini BA, Phang TL, Fosmire SP, Scott MC, Trapp SC, Duckett MM, et al. Gene expression profiling identifies inflammation and angiogenesis as distinguishing features of canine hemangiosarcoma. BMC Cancer. 2010 Dec 9;10(1):619.

22. Varanat M, Maggi RG, Linder KE, Breitschwerdt EB. Molecular Prevalence of Bartonella, Babesia, and Hemotropic Mycoplasma sp. in Dogs with Splenic Disease. J Vet Intern Med. 2011;25(6):1284–91. doi: 10.1111/j.1939-1676.2011.00811.x 22092618

23. Beerlage C, Varanat M, Linder K, Maggi RG, Cooley J, Kempf VAJ, et al. Bartonella vinsonii subsp. berkhoffii and Bartonella henselae as potential causes of proliferative vascular diseases in animals. Med Microbiol Immunol. 2012 Aug 27;201(3):319–26. doi: 10.1007/s00430-012-0234-5 22450733

24. Kempf VAJ, Volkmann B, Schaller M, Sander CA, Alitalo K, Rieß T, et al. Evidence of a leading role for VEGF in Bartonella henselae -induced endothelial cell proliferations. Cell Microbiol. 2001 Sep;3(9):623–32. doi: 10.1046/j.1462-5822.2001.00144.x 11553014

25. Devraj G, Beerlage C, Brüne B, Kempf VAJ. Hypoxia and HIF-1 activation in bacterial infections. Microbes Infect. 2017 Mar;19(3):144–56. doi: 10.1016/j.micinf.2016.11.003 27903434

26. Berkowitz ST, Gannon KM, Carberry CA, Cortes Y. Resolution of spontaneous hemoabdomen secondary to peliosis hepatis following surgery and azithromycin treatment in a Bartonella species infected dog. J Vet Emerg Crit Care. 2016;00(0):1–7.

27. Yager JA, Best SJ, Maggi RG, Varanat M, Znajda N, Breitschwerdt EB. Bacillary angiomatosis in an immunosuppressed dog. Vet Dermatol. 2010 Mar;21(4):420–8. doi: 10.1111/j.1365-3164.2010.00879.x 20374571

28. Kostianovsky M. Angiogenic process in bacillary angiomatosis. Ultrastruct Pathol. 1994;18(3):349. doi: 10.3109/01913129409023203 7520641

29. Perkocha LA, Geaghan SM, Yen TS, Nishimura SL, Chan SP, Garcia-Kennedy R, et al. Clinical and pathological features of bacillary peliosis hepatis in association with human immunodeficiency virus infection. Vol. 323, The New England journal of medicine. 1990. p. 1581–6.

30. Anstead GM. The centenary of the discovery of trench fever, an emerging infectious disease of World War 1. Lancet Infect Dis. 2016;16(8):e164–72. doi: 10.1016/S1473-3099(16)30003-2 27375211

31. Berrich M, Kieda C, Grillon C, Monteil M, Lamerant N, Gavard J, et al. Differential effects of bartonella henselae on human and feline macro- and micro-vascular endothelial cells. PLoS One. 2011;6(5).

32. Lashnits E, Correa M, Hegarty BC, Birkenheuer A, Breitschwerdt EB. Bartonella Seroepidemiology in Dogs from North America, 2008–2014. J Vet Intern Med. 2018 Jan;32(1):222–31. doi: 10.1111/jvim.14890 29197186

33. Yancey CB, Hegarty BC, Qurollo BA, Levy MG, Birkenheuer AJ, Weber DJ, et al. Regional seroreactivity and vector-borne disease co-exposures in dogs in the United States from 2004–2010: utility of canine surveillance. Vector Borne Zoonotic Dis. 2014;14(10):724–32. doi: 10.1089/vbz.2014.1592 25325316

34. Mazcko C, Thomas R. The Establishment of the Pfizer-Canine Comparative Oncology and Genomics Consortium Biospecimen Repository. Vet Sci. 2015 Jul 7;2(3):127–30. doi: 10.3390/vetsci2030127 29061936

35. Breitschwerdt EB, Maggi RG, Duncan AW, Nicholson WL, Hegarty BC, Woods CW. Bartonella Species in Blood of Immunocompetent Persons with Animal and Arthropod Contact. Emerg Infect Dis. 2007 Jun;13(6):938–41. doi: 10.3201/eid1306.061337 17553243

36. Varanat M, Maggi RG, Linder KE, Horton S, Breitschwerdt EB. Cross-contamination in the Molecular Detection of Bartonella from Paraffin-embedded Tissues. Vet Pathol. 2009 Sep 9;46(5):940–4. doi: 10.1354/vp.08-VP-0259-B-BC 19429988

37. Maggi RG, Birkenheuer AJ, Hegarty BC, Bradley JM, Levy MG, Breitschwerdt EB. Comparison of serological and molecular panels for diagnosis of vector-borne diseases in dogs. Parasit Vectors. 2014;7(1):127.

38. Maggi RG, Mascarelli PE, Pultorak EL, Hegarty BC, Bradley JM, Mozayeni BR, et al. Bartonella spp. bacteremia in high-risk immunocompetent patients. Diagn Microbiol Infect Dis. 2011;71(4):430–7. doi: 10.1016/j.diagmicrobio.2011.09.001 21996096

39. McHugh ML. Interrater reliability: the kappa statistic. Biochem medica. 2012;22(3):276–82.

40. Balakrishnan N, Cherry Na, Linder KE, Pierce E, Sontakke N, Hegarty BC, et al. Experimental infection of dogs with Bartonella henselae and Bartonella vinsonii subsp. berkhoffii. Vet Immunol Immunopathol. 2013;156(1–2):153–8. doi: 10.1016/j.vetimm.2013.09.007 24120155

41. Southern BL, Neupane P, Ericson ME, Dencklau JC, Linder KE, Bradley JM, et al. Bartonella henselae in a dog with ear tip vasculitis. Vet Dermatol. 2018 Dec;29(6):537–e180. doi: 10.1111/vde.12695 30318847

42. Neupane P, Hegarty BC, Marr HS, Maggi RG, Birkenheuer AJ, Breitschwerdt EB. Evaluation of cell culture-grown Bartonella antigens in immunofluorescent antibody assays for the serological diagnosis of bartonellosis in dogs. J Vet Intern Med. 2018 Nov 1;32(6):1958–64. doi: 10.1111/jvim.15301 30307643

43. Pérez Vera C, Diniz PPVP, Pultorak EL, Maggi RG, Breitschwerdt EB. An unmatched case controlled study of clinicopathologic abnormalities in dogs with Bartonella infection. Comp Immunol Microbiol Infect Dis. 2013;36(5):481–7. doi: 10.1016/j.cimid.2013.04.001 23683861

44. Chomel BB, Kasten RW, Williams C, Wey AC, Henn JB, Maggi R, et al. Bartonella endocarditis: a pathology shared by animal reservoirs and patients. Ann N Y Acad Sci. 2009;1166:120–6. doi: 10.1111/j.1749-6632.2009.04523.x 19538271

45. MacDonald KA, Chomel BB, Kittleson MD, Kasten RW, Thomas WP, Pesavento P. A Prospective Study of Canine Infective Endocarditis in Northern California (1999–2001): Emergence of Bartonella as a Prevalent Etiologic Agent. J Vet Intern Med. 2004 Jan;18(1):56–64. doi: 10.1892/0891-6640(2004)18<56:apsoci>2.0.co;2 14765733

46. Roura X, Santamarina G, Tabar M-D, Francino O, Altet L. Polymerase chain reaction detection of Bartonella spp. in dogs from Spain with blood culture-negative infectious endocarditis. J Vet Cardiol. 2018 Aug 25;20(4):267–75. doi: 10.1016/j.jvc.2018.04.006 29807750

47. Fenimore A, Varanat M, Maggi R, Schultheiss P, Breitschwerdt E, Lappin MR. Bartonella spp. DNA in cardiac tissues from dogs in colorado and wyoming. J Vet Intern Med. 2011 May;25(3):613–6. doi: 10.1111/j.1939-1676.2011.0722.x 21539606

48. Clifford CA, Hughes D, Beal MW, Mackin AJ, Henry CJ, Shofer FS, et al. Plasma Vascular Endothelial Growth Factor Concentrations in Healthy Dogs and Dogs with Hemangiosarcoma. J Vet Intern Med. 2001;15(2):131. doi: 10.1892/0891-6640(2001)015<0131:pvegfc>2.3.co;2 11300596

49. Yonemaru K, Sakai H, Murakami M, Yanai T, Masegi T. Expression of vascular endothelial growth factor, basic fibroblast growth factor, and their receptors (flt-1, flk-1, and flg-1) in canine vascular tumors. Vet Pathol. 2006;43(6):971–80. doi: 10.1354/vp.43-6-971 17099154

50. Kodama A, Sakai H, Matsuura S, Murakami M, Murai A, Mori T, et al. Establishment of canine hemangiosarcoma xenograft models expressing endothelial growth factors, their receptors, and angiogenesis-associated homeobox genes. BMC Cancer. 2009 Oct 14;9:363. doi: 10.1186/1471-2407-9-363 19825192

51. Abou Asa S, Mori T, Maruo K, Khater A, El-sawak A, Abd el-Aziz E, et al. Analysis of genomic mutation and immunohistochemistry of platelet-derived growth factor receptors in canine vascular tumours. Vet Comp Oncol. 2015 Sep 1;13(3):237–45. doi: 10.1111/vco.12035 23611531

52. Göritz M, Müller K, Krastel D, Staudacher G, Schmidt P, Kühn M, et al. Canine splenic haemangiosarcoma: Influence of metastases, chemotherapy and growth pattern on post-splenectomy survival and expression of angiogenic factors. J Comp Pathol. 2013 Jul;149(1):30–9. doi: 10.1016/j.jcpa.2012.11.234 23276383

53. Pons MJ, Gomes C, Aguilar R, Barrios D, Aguilar-Luis MA, Ruiz J, et al. Immunosuppressive and angiogenic cytokine profile associated with Bartonella bacilliformis infection in post-outbreak and endemic areas of Carrion’s disease in Peru. Caimano MJ, editor. PLoS Negl Trop Dis. 2017 Jun 19;11(6):e0005684. doi: 10.1371/journal.pntd.0005684 28628613

54. Scheidegger F, Quebatte M, Mistl C, Dehio C. The Bartonella henselae VirB/Bep system interferes with vascular endothelial growth factor (VEGF) signalling in human vascular endothelial cells. Cell Microbiol. 2011 Mar 1;13(3):419–31. doi: 10.1111/j.1462-5822.2010.01545.x 21044238

55. Cerimele F, Brown LF, Bravo F, Ihler GM, Kouadio P, Arbiser JL. Infectious Angiogenesis: Bartonella bacilliformis Infection Results in Endothelial Production of Angiopoetin-2 and Epidermal Production of Vascular Endothelial Growth Factor. Am J Pathol. 2003 Oct 1;163(4):1321–7. doi: 10.1016/S0002-9440(10)63491-8 14507641

56. Kitchell BE, Fan TM, Kordick D, Breitschwerdt EB, Wollenberg G, Lichtensteiger CA. Peliosis hepatis in a dog infected with Bartonella henselae. J Am Vet Med Assoc. 2000 Feb;216(4):519–23. doi: 10.2460/javma.2000.216.519 10687006

57. Breitschwerdt EB, Maggi RG, Varanat M, Linder KE, Weinberg G. Isolation of Bartonella vinsonii subsp. berkhoffii genotype II from a boy with epithelioid hemangioendothelioma and a dog with hemangiopericytoma. J Clin Microbiol. 2009 Jun;47(6):1957–60. doi: 10.1128/JCM.00069-09 19369441

58. Mascarelli PE, Iredell JR, Maggi RG, Weinberg G, Breitschwerdt EB. Bartonella species bacteremia in two patients with epithelioid hemangioendothelioma. J Clin Microbiol. 2011 Nov 1;49(11):4006–12. doi: 10.1128/JCM.05527-11 21918021

59. Sykes JE, Westropp JL, Kasten RW, Chomel BB. Association between Bartonella species infection and disease in pet cats as determined using serology and culture. J Feline Med Surg. 2010;

60. Brenner EC, Chomel BB, Singhasivanon O-U, Namekata DY, Kasten RW, Kass PH, et al. Bartonella infection in urban and rural dogs from the tropics: Brazil, Colombia, Sri Lanka and Vietnam. Epidemiol Infect. 2012;141(1):1–8.

61. Cherry N, Diniz P, Maggi R, Hummel J, Hardie E, Behrend E, et al. Isolation or Molecular Detection of Bartonella henselae and Bartonella vinsonii subsp. berkhoffii from Dogs with Idiopathic Cavitary Effusions. J Vet Intern Med. 2009;23(1):186–9. doi: 10.1111/j.1939-1676.2008.0246.x 19175739

62. Perez C, Maggi RG, Diniz PPVP, Breitschwerdt EB. Molecular and serological diagnosis of Bartonella infection in 61 dogs from the United States. J Vet Intern Med. 2011;25(4):805–10. doi: 10.1111/j.1939-1676.2011.0736.x 21615498


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