It is becoming increasingly likely that rodents will drive future disease epidemics with the continued expansion of cities worldwide. Though transmission risk is a growing concern, relatively little is known about pathogens carried by urban rats. Here, we assess whether the diversity and prevalence of Bartonella bacteria differ according to the (co)occurrence of rat hosts across New Orleans, LA (NO), where both Norway (Rattus norvegicus) and roof rats (Rattus rattus) are found, relative to New York City (NYC) which only harbors Norway rats. We detected human pathogenic Bartonella species in both NYC and New Orleans rodents. We found that Norway rats in New Orleans harbored a more diverse assemblage of Bartonella than Norway rats in NYC and that Norway rats harbored a more diverse and distinct assemblage of Bartonella compared to roof rats in New Orleans. Additionally, Norway rats were more likely to be infected with Bartonella than roof rats in New Orleans. Flea infestation appears to be an important predictor of Bartonella infection in Norway rats across both cities. These findings illustrate that pathogen infections can be heterogeneous in urban rodents and indicate that further study of host species interactions could clarify variation in spillover risk across cities.
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Anderson BE, Neuman MA (1997) Bartonella spp. as emerging human pathogens. Clin Microbiol Rev 10:203–219.
Bai Y, Kosoy MY, Lerdthusnee K, Peruski LF, Richardson JH (2009) Prevalence and genetic heterogeneity of Bartonella strains cultured from rodents from 17 provinces in Thailand. Am J Trop Med Hyg 81:811–816. https://doi.org/10.4269/ajtmh.2009.09-0294
Bai Y, Malania L, Castillo DA, Moran D, Boonmar S, Chanlun A, Suksawat F, Maruyama S, Knobel D, Kosoy M (2013) Global distribution of Bartonella infections in domestic bovine and characterization of Bartonella bovis strains using multi-locus sequence typing. PLoS One 8:1–8. https://doi.org/10.1371/journal.pone.0080894
Billeter SA, Gundi VAKB, 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. https://doi.org/10.1128/AEM.06012-11
Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694. https://doi.org/10.1098/rsbl.2007.0393
Bordes F, Herbreteau V, Chaval Y, Tran A, Morand S (2013) The diversity of microparasites of rodents: a comparative analysis that helps in identifying rodent-borne rich habitats in Southeast Asia. CoAction 1:1–10.
Bouhsira E, Ferrandez Y, Liu MF, Franc M, Boulouis HJ, Biville F (2013) Ctenocephalides felis an in vitro potential vector for five Bartonella species. Comp Immunol Microbiol Infect Dis 36:105–111. https://doi.org/10.1016/j.cimid.2012.10.004
Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102. https://doi.org/10.1016/j.tree.2006.11.001
Buffet J-P, 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. https://doi.org/10.2217/FMB.13.77
Campbell BG, Little MD (1988) The finding of Angiostrongylus cantonensis in rats in New Orleans. Am J Trop Med Hyg 38:568–573.
Cayuela L, Gotelli NJ, Colwell RK (2015) Ecological and biogeographic null hypotheses for comparing rarefaction curves. Ecol Monogr 85:437–455. https://doi.org/10.1890/14-1261.1
Childs JE, McLafferty SL, Sadek R, Miller GL, Khan a S, DuPree ER, Advani R, Mills JN, Glass GE (1998) Epidemiology of rodent bites and prediction of rat infestation in New York City. Am J Epidemiol 148:78–87. https://doi.org/10.1093/oxfordjournals.aje.a009563
Comer JA, Diaz T, Vlahov D, Monterroso E, Childs JE (2001) Evidence of rodent-associated Bartonella and Rickettsia infections among intravenous drug users from Central and East Harlem, New York City. Am J Trop Med Hyg 65:855–860.
Cross RW, Waffa B, Freeman A, Riegel C, Moses LM, Bennett A, Safronetz D, Fischer ER, Feldmann H, Voss TG, Bausch DG (2014) Old world hantaviruses in rodents in New Orleans, Louisiana. Am J Trop Med Hyg 90:897–901. https://doi.org/10.4269/ajtmh.13-0683
Daly JS, Worthington MG, Brenner DONJ, Moss CW, Hollis DG, Weyant RS, Steigerwalt AG, Weaver RE, Daneshvar MI, Connor SPO (1993) Rochalimaea elizabethae sp. nov. isolates from a patient with endocarditis. J Clin Microbiol 31:872–881.
Despommier D, Ellis BR, Wilcox B a. (2007) The role of ecotones in emerging infectious diseases. Ecohealth 3:281–289. https://doi.org/10.1007/s10393-006-0063-3
Diniz PPVDP, Maggi RG, Schwartz DS, Cadenas MB, Bradley JM, Hegarty B, Breutschwerdt EB (2007) Canine bartonellosis: Serological and molecular prevalence in Brazil and evidence of co-infection with Bartonella henselae and Bartonella vinsonii subsp. berkhoffii. Vet Res 38:697–710. https://doi.org/10.1051/vetres:2007023
Dyer LA, Walla TR, Greeney HF, Stireman JO, Hazen RF (2010) Diversity of interactions: A metric for studies of biodiversity. Biotropica 42:281–289. https://doi.org/10.1111/j.1744-7429.2009.00624.x
Easterbrook JD, Ka JB, Vanasco NB, Reeves WK, Pu RH, Kosoy MY, Glass GE, Watson J, Klein SL (2007) A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. J Epidemiol Infect 135:1192–1199. https://doi.org/10.1017/S0950268806007746
Ellis BA, Regnery RL, Beati L, Bacellar F, Rood M, Glass GG, Marston E, Ksiazek TG, Jones D, Childs JE (1999) Rats of the genus Rattus are reservoir hosts for pathogenic Bartonella species: an Old World origin for a New World disease? J Infect Dis 180:220–224. https://doi.org/10.1086/314824
Eremeeva ME, Gerns HL, Lydy SL, Goo JS, Ryan ET, Mathew SS, Ferraro GA, Holden JM, Nicholson WL, Dasch GA, Koehler JE (2007) Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. N Engl J Med 356:2381–2387. https://doi.org/10.1056/NEJMoa065987
Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, Conte JM, Ng J, Garcia J, Bhuva NP, Lee B, Che X, Quan PL, Ian Lipkin W (2014) Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York city. MBio 5:1–16. https://doi.org/10.1128/mBio.01933-14
Frye MJ, Firth C, Bhat M, Firth MA, Che X, Lee D, Williams SH, Lipkin WI (2015) Preliminary survey of ectoparasites and associated pathogens from Norway rats in New York City. J Med Entomol 52:253–259. https://doi.org/10.1093/jme/tjv014
Furman DP and Catts EP (1970) Manual of Medical Entomology. Mayfield Publishing Company, 138-154.
Gulachenski A, Ghersi BM, Lesen AE, Blum MJ (2016) Abandonment, ecological assembly and public health risks in counter-urbanizing cities. Sustainability 8:1–26. https://doi.org/10.3390/su8050491
Gundi VAKB, Billeter SA, Rood MP, Kosoy MY (2012) Bartonella spp. in rats and Zoonoses, Los Angeles, California, USA. Emerg Infect Dis 18:631–633. https://doi.org/10.3201/eid1804.110816
Gutiérrez R, Krasnov B, Morick D, Gottlieb Y, Khokhlova IS, Harrus S (2015) Bartonella infection in rodents and their flea ectoparasites: an overview. Vector-Borne Zoonotic Dis 15:27–39. https://doi.org/10.1089/vbz.2014.1606
Han BA, Schmidt JP, Bowden SE, Drake JM (2015) Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci USA 112:7039–44. https://doi.org/10.1073/pnas.1501598112
Harms A, Dehio C (2012) Intruders below the Radar: Molecular pathogenesis of Bartonella spp. Clin Microbiol Rev 25:42–78. https://doi.org/10.1128/CMR.05009-11
Hawlena H, Bashary D, Abramsky Z, Krasnov BR (2007) Benefits, costs and constraints of anti-parasitic grooming in adult and juvenile rodents. Ethology 113:394–402. https://doi.org/10.1111/j.1439-0310.2007.01332.x
Himsworth CG, Bai Y, Kosoy MY, Wood H, DiBernardo A, Lindsay R, Bidulka J, Tang P, Jardine C, Patrick D (2015) An investigation of Bartonella spp., Rickettsia typhi, and Seoul hantavirus in rats (Rattus spp.) from an inner-city neighborhood of Vancouver, Canada: is pathogen presence a reflection of global and local rat population structure? Vector Borne Zoonotic Dis 15:21–6. https://doi.org/10.1089/vbz.2014.1657
Himsworth CG, Bidulka J, Parsons KL, Feng AYT, Tang P, Jardine CM, Kerr T, Mak S, Robinson J, Patrick DM (2013a) Ecology of Leptospira interrogans in Norway rats (Rattus norvegicus) in an inner-city neighborhood of Vancouver, Canada. PLoS Negl Trop Dis 7:e2270. https://doi.org/10.1371/journal.pntd.0002270
Himsworth CG, Parsons KL, Jardine C, Patrick DM (2013b) Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis 13:349–59. https://doi.org/10.1089/vbz.2012.1195
Jiyipong T, Jittapalapong S, Morand S, Raoult D, Rolain JM (2012) Prevalence and genetic diversity of Bartonella spp. in small mammals from Southeastern Asia. Appl Environ Microbiol 78:8463–8466. https://doi.org/10.1128/AEM.02008-12
Jones KE, Patel NG, Levy M a, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536
Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–52. https://doi.org/10.1038/nature09575
Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–98. https://doi.org/10.1111/j.1461-0248.2006.00885.x
King CM, Innes JG, Gleeson D, Fitzgerald N, Winstanley T, O’Brien B, Bridgman L, Cox N (2011) Reinvasion by ship rats (Rattus rattus) of forest fragments after eradication. Biol Invasions 13:2391–2408. https://doi.org/10.1007/s10530-011-0051-6
Kosoy M, Hayman DTS, Chan KS (2012) Bartonella bacteria in nature: Where does population variability end and a species start? Infect Genet Evol 12:894–904. https://doi.org/10.1016/j.meegid.2012.03.005
Kosoy M, Khlyap L, Cosson J-F, Morand S (2015) Aboriginal and invasive rats of genus Rattus as hosts of infectious agents. Vector Borne Zoonotic Dis 15:3–12. https://doi.org/10.1089/vbz.2014.1629
Kosoy MY, Regnery RL, Tzianabos T, Marston EL, Jones DC, Green D, Maupin G, Olson JG, Childs JE (1997) Distribution, diversity and host specificity of Bartonella in rodents from the Southeastern United States.
Krasnov BR, Shenbrot GI, Khokhlova IS, Poulin R (2007) Geographical variation in the “bottom-up” control of diversity: Fleas and their small mammalian hosts. Glob Ecol Biogeogr 16:179–186. https://doi.org/10.1111/j.1466-8238.2006.00273.x
Krasnov BR, Shenbrot GI, Medvedev SG, Vatschenok VS, Khokhlova IS (1997) Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114:159–173. https://doi.org/10.1017/S0031182096008347
Lewis JA, Zipperer WC, Ernstson H, Bernik BM, Hazen RF, Elmqvist T, Blum MJ. (2017) Socioecological disparities in New Orleans following Hurricane Katrina. Ecosphere 8:e01922. https://doi.org/10.1002/ecs2.1922
Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, Hudson PJ, Grenfell BT. (2009) Epidemic dynamics at the human-animal interface. Science 326:1362–1367. https://doi.org/10.1126/science.1177345
Mcguire B, Pizzuto T, Bemis WE, Getz LL (2006) General ecology of a rural population of Norway rats (Rattus norvegicus) based on intensive live trapping. Am Midl Nat 155:221–236.
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, LA, pp 1-8. https://doi.org/10.1109/GCE.2010.5676129
Morick D, Baneth G, Avidor B, Kosoy MY, Mumcuoglu KY, Mintz D, Eyal O, Goethe R, Mietze A, Shpigel N, Harrus S (2009) Detection of Bartonella spp. in wild rodents in Israel using HRM real-time PCR. Vet Microbiol 139:293–297. https://doi.org/10.1016/j.vetmic.2009.06.019
Morick D, Krasnov BR, Khokhlova IS, Gottlieb Y, Harrus S (2011) Investigation of Bartonella acquisition and transmission in Xenopsylla ramesis fleas (Siphonaptera: Pulicidae). Mol Ecol 20:2864–2870. https://doi.org/10.1111/j.1365-294X.2011.05033.x
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.
Rael RC, Peterson AC, Ghersi BM, Childs J, Blum MJ (2016) Disturbance, reassembly, and disease risk in socioecological systems. Ecohealth 13:450–455. https://doi.org/10.1007/s10393-016-1157-1
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rothschild M (1975) Recent advances in our knowledge of the order Siphonaptera. Ann Rev Entomol 20:241–259. https://doi.org/10.1146/annurev.en.20.010175.001325
Tsai YL, Chuang S Te, Chang CC, Kass PH, Chomel BB (2010) Bartonella species in small mammals and their ectoparasites in Taiwan. Am J Trop Med Hyg 83:917–923. https://doi.org/10.4269/ajtmh.2010.10-0083
We would like to thank T. Madere, F. Bauder, P. Smith, E. Guidry, A. Gulachenski, H. Rahn, A. Powell, J. Haydel, S. Triplett, S. Piper, and H. Patel for providing assistance with fieldwork and laboratory work. This study was supported by the National Science Foundation (BCS-1313703), the Louisiana Board of Regents LINK program and the National Institute of Environmental Health Sciences (5P30 ES009089) A. Peterson also was supported by a Louisiana Board of Regents graduate fellowship. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
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Peterson, A.C., Ghersi, B.M., Alda, F. et al. Rodent-Borne Bartonella Infection Varies According to Host Species Within and Among Cities. EcoHealth 14, 771–782 (2017). https://doi.org/10.1007/s10393-017-1291-4
- Rattus norvegicus
- Rattus rattus
- Rodent-borne pathogens