#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Molecular detection and genetic characterization of Bartonella species from rodents and their associated ectoparasites from northern Tanzania


Autoři: Ndyetabura O. Theonest aff001;  Ryan W. Carter aff003;  Nelson Amani aff002;  Siân L. Doherty aff003;  Ephrasia Hugho aff002;  Julius D. Keyyu aff004;  Barbara K. Mable aff003;  Gabriel M. Shirima aff001;  Rigobert Tarimo aff001;  Kate M. Thomas aff002;  Daniel T. Haydon aff003;  Joram J. Buza aff001;  Kathryn J. Allan aff003;  Jo E. B. Halliday aff003
Působiště autorů: School of Life Sciences and Bioengineering, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania aff001;  Kilimanjaro Clinical Research Institute, Moshi, Tanzania aff002;  The Boyd Orr Centre for Population and Ecosystem Health, Institute of Biodiversity Animal Health and Comparative Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom aff003;  Tanzania Wildlife Research Institute, Arusha, Tanzania aff004;  Centre for International Health, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223667

Souhrn

Background

Bartonellae are intracellular bacteria, which can cause persistent bacteraemia in humans and a variety of animals. Several rodent-associated Bartonella species are human pathogens but data on their global distribution and epidemiology are limited. The aims of the study were to: 1) determine the prevalence of Bartonella infection in rodents and fleas; 2) identify risk factors for Bartonella infection in rodents; and 3) characterize the Bartonella genotypes present in these rodent and flea populations.

Methods and results

Spleen samples collected from 381 rodents representing six different species were tested for the presence of Bartonella DNA, which was detected in 57 individuals (15.0%; 95% CI 11.3–18.5), of three rodent species (Rattus rattus n = 54, Mastomys natalensis n = 2 and Paraxerus flavovottis n = 1) using a qPCR targeting the ssrA gene. Considering R. rattus individuals only, risk factor analysis indicated that Bartonella infection was more likely in reproductively mature as compared to immature individuals (OR = 3.42, p <0.001). Bartonella DNA was also detected in 53 of 193 Xenopsylla cheopis fleas (27.5%: 95% CI 21.3–34.3) collected from R.rattus individuals. Analysis of ssrA and gltA sequences from rodent spleens and ssrA sequences from fleas identified multiple genotypes closely related (≥ 97% similar) to several known or suspected zoonotic Bartonella species, including B. tribocorum, B. rochalimae, B. elizabethae and B. quintana.

Conclusions

The ssrA and gltA sequences obtained from rodent spleens and ssrA sequences obtained from fleas reveal the presence of a diverse set of Bartonella genotypes and increase our understanding of the bartonellae present in Tanzanian. Further studies are needed to fully characterise the prevalence, genotypes and diversity of Bartonella in different host populations and their potential impacts on human health.

Klíčová slova:

Bartonella – DNA extraction – Polymerase chain reaction – Rodents – Sequence analysis – Spleen – Tanzania – Fleas


Zdroje

1. Dehio C (2004) Molecular and cellular basis of Bartonella pathogenesis. Annu Rev Microbiol 58: 365–390. doi: 10.1146/annurev.micro.58.030603.123700 15487942

2. Castle KT, Kosoy M, Lerdthusnee K, Phelan L, Bai Y, Gage KL, et al. (2004) Prevalence and diversity of Bartonella in rodents of northern Thailand: a comparison with Bartonella in rodents from southern China. Am J Trop Med Hyg 70: 429–433. 15100459

3. Angelakis E, Khamphoukeo K, Grice D, Newton PN, Roux V, Aplin K, et al. (2009) Molecular detection of Bartonella species in rodents from the Lao PDR. Clin Microbiol Infect 15 Suppl 2: 95–97. doi: 10.1111/j.1469-0691.2008.02177.x 19374642

4. Okaro U, Addisu A, Casanas B, Anderson B (2017) Bartonella Species, an Emerging Cause of Blood-Culture-Negative Endocarditis. Clin Microbiol Rev 30: 709–746. doi: 10.1128/CMR.00013-17 28490579

5. Saisongkorh W, Rolain JM, Suputtamongkol Y, Raoult D (2009) Emerging Bartonella in humans and animals in Asia and Australia. J Med Assoc Thai 92: 707–731. 19459536

6. Kosoy M, Bai Y, Sheff K, Morway C, Baggett H, Maloney SA, et al. (2010) Identification of Bartonella infections in febrile human patients from Thailand and their potential animal reservoirs. Am J Trop Med Hyg 82: 1140–1145. doi: 10.4269/ajtmh.2010.09-0778 20519614

7. Anderson BE, Neuman MA (1997) Bartonella spp. as emerging human pathogens. Clin Microbiol Rev 10: 203–219. 9105751

8. Iralu J, Bai Y, Crook L, Tempest B, Simpson G, McKenzie T, et al. (2006) Rodent-associated Bartonella febrile illness, Southwestern United States. Emerg Infect Dis 12: 1081–1086. doi: 10.3201/eid1207.040397 16836824

9. Bonilla DL, Cole-Porse C, Kjemtrup A, Osikowicz L, Kosoy M (2014) Risk factors for human lice and bartonellosis among the homeless, San Francisco, California, USA. Emerg Infect Dis 20: 1645–1651. doi: 10.3201/eid2010.131655 25280380

10. Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR (2010) Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care (San Antonio) 20: 8–30. doi: 10.1111/j.1476-4431.2009.00496.x 20230432

11. Regier Y, O’Rourke F, Kempf VAJ (2016) Bartonella spp.—a chance to establish One Health concepts in veterinary and human medicine. Parasite Vector 9. ARTN 330.

12. Kosoy M, Murray M, Gilmore RD, Bai Y, Gage KL (2003) Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol 41: 645–650. doi: 10.1128/JCM.41.2.645-650.2003 12574261

13. Welch DF, Carroll KC, Hofmeister EK, Persing DH, Robison DA, Steigerwalt AG, et al. (1999) Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. J Clin Microbiol 37: 2598–2601. 10405408

14. Knap N, Duh D, Birtles R, Trilar T, Petrovec M, Avsic-Zupanc T (2007) Molecular detection of Bartonella species infecting rodents in Slovenia. Fems Immunol Med Mic 50: 45–50. doi: 10.1111/j.1574-695X.2007.00226.x 17374132

15. Probert W, Louie JK, Tucker JR, Longoria R, Hogue R, Moler S, et al. (2009) Meningitis Due to a "Bartonella washoensis"-Like Human Pathogen. J Clin Microbiol 47: 2332–2335. doi: 10.1128/JCM.00511-09 19439538

16. Crump JA, Morrissey AB, Nicholson WL, Massung RF, Stoddard RA, Galloway RL, et al. (2013) Etiology of Severe Non-malaria Febrile Illness in Northern Tanzania: A Prospective Cohort Study. PLoS Negl Trop Dis 7: e2324. doi: 10.1371/journal.pntd.0002324 23875053

17. Chinga-Alayo E, Huarcaya E, Nasarre C, del Aguila R, Llanos-Cuentas A (2004) The influence of climate on the epidemiology of bartonellosis in Ancash, Peru. Trans R Soc Trop Med Hyg 98: 116–124. doi: 10.1016/s0035-9203(03)00017-8 14964812

18. Breitschwerdt EB (2014) Bartonellosis: One Health Perspectives for an Emerging Infectious Disease. Ilar J 55: 46–58. doi: 10.1093/ilar/ilu015 24936029

19. Gutierrez R, Vayssier-Taussat M, Buffet JP, Harrus S (2017) Guidelines for the Isolation, Molecular Detection, and Characterization of Bartonella Species. Vector-Borne Zoonot 17: 42–50. doi: 10.1089/vbz.2016.1956 28055575

20. Diaz MH, Bai Y, Malania L, Winchell JM, Kosoy MY (2012) Development of a Novel Genus-Specific Real-Time PCR Assay for Detection and Differentiation of Bartonella Species and Genotypes. J Clin Microbiol 50: 1645–1649. doi: 10.1128/JCM.06621-11 22378904

21. Meheretu Y, Leirs H, Welegerima K, Breno M, Tomas Z, Kidane D, G et al. (2013) Bartonella prevalence and genetic diversity in small mammals from Ethiopia. Vector Borne Zoonotic Diseases 13: 164–175. doi: 10.1089/vbz.2012.1004 23421888

22. Halliday JE, Knobel DL, Agwanda B, Bai Y, Breiman RF, Cleaveland S, et al. (2015) Prevalence and diversity of small mammal-associated Bartonella species in rural and urban Kenya. PLoS Negl Trop Dis 9: e0003608. doi: 10.1371/journal.pntd.0003608 25781015

23. Pretorius AM, Beati L, Birtles RJ (2004) Diversity of bartonellae associated with small mammals inhabiting Free State province, South Africa. Int J Syst Evol Microbiol 54: 1959–1967. doi: 10.1099/ijs.0.03033-0 15545418

24. Laudisoit A, Falay D, Amundala N, Akaibe D, de Bellocq JG, Van Houtte N, et al. (2014) High prevalence of Rickettsia typhi and Bartonella species in rats and fleas, Kisangani, Democratic Republic of the Congo. Am J Trop Med Hyg 90: 463–468. doi: 10.4269/ajtmh.13-0216 24445202

25. Gundi VA, Kosoy MY, Makundi RH, Laudisoit A (2012) Identification of diverse Bartonella genotypes among small mammals from Democratic Republic of Congo and Tanzania. Am J Trop Med Hyg 87: 319–326. doi: 10.4269/ajtmh.2012.11-0555 22855765

26. Billeter SA, Borchert JN, Atiku LA, Mpanga JT, Gage KL, Kosoy MY (2014) Bartonella species in invasive rats and indigenous rodents from Uganda. Vector Borne Zoonotic Diseases 14: 182–188. doi: 10.1089/vbz.2013.1375 24575846

27. Home Office (2014) Guidance on the Operation of the Animals (Scientific Procedures) Act 1986.

28. Leary S, Underwood W, Anthony R, Cartner S, Corey D, Grandin T, et al. (2014) The AVMA Guidelines for the Euthanasia of Animals. Shaumburg, IL.: American Veterinary Medical Association.

29. Allan KJ, Halliday JEB, Moseley M, Carter RW, Ahmed A, Goris MGA, et al. (2018) Assessment of animal hosts of pathogenic Leptospira in northern Tanzania. PLoS Negl Trop Dis 12. ARTN e0006444. doi: 10.1371/journal.pntd.0006444 29879104

30. Cunningham D, Moors P. (1996) A guide to the identification and collection of New Zealand Rodents. Wellington: New Zealand: Wildlife Service Department.

31. Pratt HD, Wiseman JS (1962) Fleas of public health importance and their control. Communicable Disease Center, Atlanta, Georgia.

32. Billeter SA, Gundi VA, Rood MP, Kosoy MY (2011) Molecular detection and identification of Bartonella species in Xenopsylla cheopis fleas (Siphonaptera: Pulicidae) collected from Rattus norvegicus rats in Los Angeles, California. Appl Environ Microbiol 77: 7850–7852. doi: 10.1128/AEM.06012-11 21908631

33. Sanger F, Nicklen S, Coulson AR (1977) DNA Sequencing with Chain-Terminating Inhibitors. P Natl Acad Sci USA 74: 5463–5467. doi: 10.1073/pnas.74.12.5463 271968

34. Norman AF, Regnery R, Jameson P, Greene C, Krause DC (1995) Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol 33: 1797–1803. 7545181

35. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33: 187904.

36. Frank HK, Boyd SD, Hadly EA (2018) Global fingerprint of humans on the distribution of Bartonella bacteria in mammals. PLoS Negl Trop Dis 12: e0006865. doi: 10.1371/journal.pntd.0006865 30439961

37. Bai Y, Hayman DTS, Mckee CD, Kosoy MY (2015) Classification of Bartonella Strains Associated with Straw-Colored Fruit Bats (Eidolon helvum) across Africa Using a Multi-locus Sequence Typing Platform. PLoS Negl Trop Dis 9. ARTN e0003478. doi: 10.1371/journal.pntd.0003478 25635826

38. R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria.

39. Dorai-Raj S (2009) binom: Binomial Confidence Intervals For Several Parameterizations. R package version 1.0–5.

40. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67: 1–48. doi: 10.18637/jss.v067.i01

41. Tamura K (1992) Estimation of the Number of Nucleotide Substitutions When There Are Strong Transition-Transversion and G+C-Content Biases. Mol Biol Evol 9: 678–687. doi: 10.1093/oxfordjournals.molbev.a040752 1630306

42. Buffet JP, Kosoy M, Vayssier-Taussat M (2013) Natural history of Bartonella-infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiol 8: 1117–1128. doi: 10.2217/fmb.13.77 24020740

43. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, et al. (2014) Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio 5: e01933–01914. doi: 10.1128/mBio.01933-14 25316698

44. Peterson AC, Ghersi BM, Alda F, Firth C, Frye MJ, Bai Y, et al. (2017) Rodent-Borne Bartonella Infection Varies According to Host Species Within and Among Cities. Ecohealth 14: 771–782. doi: 10.1007/s10393-017-1291-4 29164472

45. Gundi VA, Kosoy MY, Myint KS, Shrestha SK, Shrestha MP, Pavlin JA, et al. (2010) Prevalence and genetic diversity of Bartonella species detected in different tissues of small mammals in Nepal. Appl Environ Microbiol 76: 8247–8254. doi: 10.1128/AEM.01180-10 21037303

46. Lipatova I, Paulauskas A, Puraite I, Radzijevskaja J, Balciauskas L, Gedminas V (2015) Bartonella infection in small mammals and their ectoparasites in Lithuania. Microbes Infect 17: 884–888. doi: 10.1016/j.micinf.2015.08.013 26344603

47. Kamani J, Morick D, Mumcuoglu KY, Harrus S (2013) Prevalence and diversity of Bartonella species in commensal rodents and ectoparasites from Nigeria, West Africa. PLoS Negl Trop Dis 7: e2246. doi: 10.1371/journal.pntd.0002246 23738028

48. Klangthong K, Promsthaporn S, Leepitakrat S, Schuster AL, McCardle PW, Kosoy M, et al. (2015) The Distribution and Diversity of Bartonella Species in Rodents and their ectoparasites across Thailand. Plos One 10. ARTN e0140856.

49. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421: 628–630. doi: 10.1038/nature01346 12571595

50. Li X-Y, Chen J-D, Li C-R (2018) Genotype characteristics of Bartonella and the infection in rodents in Guangdong Province, China. Zhongguo Ren Shou Gong Huan Bing Za Zhi 34: 482–486.

51. Tay ST, Mokhtar AS, Zain SNM, Low KC (2014) Short Report: Isolation and Molecular Identification of Bartonellae from Wild Rats (Rattus Species) in Malaysia. Am J Trop Med Hyg 90: 1039–1042.

52. Chipwaza B, Mhamphi GG, Ngatunga SD, Selemani M, Amuri M, Mugasa JP, et al. (2015) Prevalence of bacterial febrile illnesses in children in Kilosa district, Tanzania. PLoS Negl Trop Dis 9: e0003750. doi: 10.1371/journal.pntd.0003750 25955522


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#