1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 40, 03/Oct/2024
  4. Article
Research Open Access
Like 0
Download

Urban development

Abstract

Background

Brown rats () are synanthropic rodents with worldwide distribution, which are known to harbour many zoonotic pathogens and parasites. No systematic zoonotic surveys targeting multiple pathogens and parasites have previously been conducted in urban rats in Finland.

Aim

In Helsinki, Finland, we explored the presence and prevalence in brown rats of certain pathogens and parasites (including helminths, viruses and bacteria) across potentially zoonotic taxa.

Methods

We opportunistically received rat carcasses from pest management operators and citizens from 2018 to 2023. We searched for heart- or lungworms, performed rat diaphragm digestion to check for and morphologically identified intestinal helminths. We assessed virus exposure by immunofluorescence assay or PCR, and detected bacteria by PCR () or culture ().

Results

Among the rats investigated for helminths, no heart- or lungworms or species were detected and the most common finding was the cestode (in 9.7% of individuals sampled, 28/288). For some of the surveyed virus taxa, several rats were seropositive (orthopoxviruses, 5.2%, 11/211; arenaviruses, 2.8%, 6/211; hantaviruses 5.2%, 11/211) or tested positive by PCR (rat hepatitis E virus, 1.8%, 4/216). (6.6%, 17/259) and (1.2%, 2/163) bacteria were also present in the rat population examined.

Conclusions

Prevalences of potentially zoonotic pathogens and parasites in brown rats in Helsinki appeared low. This may explain low or non-existent diagnosis levels of rat-borne pathogen and parasite infections reported in people there. Nevertheless, further assessment of under-diagnosis, which cannot be excluded, would enhance understanding the risks of zoonoses.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.40.2400031
2024-10-03
2024-10-07
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.40.2400031
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/40/eurosurv-29-40-2.html?itemId=/content/10.2807/1560-7917.ES.2024.29.40.2400031&mimeType=html&fmt=ahah

References

  1. Hassell JM, Muloi DM, VanderWaal KL, Ward MJ, Bettridge J, Gitahi N, et al. Epidemiological connectivity between humans and animals across an urban landscape. Proc Natl Acad Sci USA. 2023;120(29):e2218860120.  https://doi.org/10.1073/pnas.2218860120  PMID: 37450494 
  2. Gibb R, Redding DW, Chin KQ, Donnelly CA, Blackburn TM, Newbold T, et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature. 2020; 584(7821):398-402.  https://doi.org/10.1038/s41586-020-2562-8  PMID: 32759999 
  3. Albery GF, Carlson CJ, Cohen LE, Eskew EA, Gibb R, Ryan SJ, et al. Urban-adapted mammal species have more known pathogens. Nat Ecol Evol. 2022;6(6):794-801.  https://doi.org/10.1038/s41559-022-01723-0  PMID: 35501480 
  4. Meerburg BG, Singleton GR, Kijlstra A. Rodent-borne diseases and their risks for public health. Crit Rev Microbiol. 2009;35(3):221-70.  https://doi.org/10.1080/10408410902989837  PMID: 19548807 
  5. Himsworth CG, Parsons KL, Jardine C, Patrick DM. 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. 2013;13(6):349-59.  https://doi.org/10.1089/vbz.2012.1195  PMID: 23590323 
  6. Rothenburger JL, Himsworth CH, Nemeth NM, Pearl DL, Jardine CM. Environmental Factors and Zoonotic Pathogen Ecology in Urban Exploiter Species. EcoHealth. 2017;14(3):630-41.  https://doi.org/10.1007/s10393-017-1258-5  PMID: 28631116 
  7. Shackleton CM, Ruwanza S, Sinasson Sanni GK, Bennett S, De Lacy P, Modipa R, et al. Unpacking Pandora’s Box: Understanding and Categorising Ecosystem Disservices for Environmental Management and Human Wellbeing. Ecosystems (N Y). 2016;19(4):587-600.  https://doi.org/10.1007/s10021-015-9952-z 
  8. Vanwambeke SO, Linard C, Gilbert M. Emerging challenges of infectious diseases as a feature of land systems. Curr Opin Environ Sustain. 2019;38:31-36.  https://doi.org/10.1016/j.cosust.2019.05.005 
  9. de Cock MP, de Vries A, Fonville M, Esser HJ, Mehl C, Ulrich RG, et al. Increased rat-borne zoonotic disease hazard in greener urban areas. Sci Total Environ. 2023;896:165069.  https://doi.org/10.1016/j.scitotenv.2023.165069  PMID: 37392874 
  10. Strand TM, Lundkvist Å. Rat-borne diseases at the horizon. A systematic review on infectious agents carried by rats in Europe 1995-2016. Infect Ecol Epidemiol. 2019;9(1):1553461.  https://doi.org/10.1080/20008686.2018.1553461  PMID: 30834071 
  11. Global Burden of Disease Collaborative Network. Global Burden of Disease Study 2019 (GBD 2019). Seattle, United States: Institute for Health Metrics and Evaluation; 2020.
  12. Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, de la Fuente J. Effects of environmental change on zoonotic disease risk: an ecological primer. Trends Parasitol. 2014;30(4):205-14.  https://doi.org/10.1016/j.pt.2014.02.003  PMID: 24636356 
  13. Syrjänen J, Mustonen J, Vapalahti O, Henttonen H, Vaheri A. Jyrsijöiden levittämät sairaudet Suomessa. [Rodent dissemination of diseases in Finland]. Duodecim. 2005;121(3):295-302. PMID: 15787287 
  14. Strand TM, Pineda S, Backhans A, Jakobsen F, Råsbäck T, Lõhmus M, et al. Detection of Leptospira in Urban Swedish Rats: Pest Control Interventions as a Promising Source of Rats Used for Surveillance. Vector Borne Zoonotic Dis. 2019;19(6):414-20.  https://doi.org/10.1089/vbz.2017.2262  PMID: 30785372 
  15. Robinson SJ, Finer R, Himsworth CG, Pearl DL, Rousseau J, Weese JS, et al. Evaluating the utility of pest control sourced rats for zoonotic pathogen surveillance. Zoonoses Public Health. 2022;69(5):468-74.  https://doi.org/10.1111/zph.12936  PMID: 35253370 
  16. European Commission. Commission implementing regulation (EU) 2015/1375 of 10 August 2015 laying down specific rules on official controls for Trichinella in meat. 2015. Available from: http://www.iss.it/crlp/index.php
  17. Gliga DS, Pisanu B, Walzer C, Desvars-Larrive A. Helminths of urban rats in developed countries: a systematic review to identify research gaps. Parasitol Res. 2020;119(8):2383-97.  https://doi.org/10.1007/s00436-020-06776-3  PMID: 32607706 
  18. Ribas A, de Bellocq JG, Ros A, Ndiaye PI, Miquel J. Morphometrical and genetic comparison of two nematode species: H. spumosa and H. dahomensis (Nematoda, Heterakidae). Acta Parasitol. 2013;58(3):389-98.  https://doi.org/10.2478/s11686-013-0156-4  PMID: 23990438 
  19. Durette-Desset MC. Le genre Nippostrongylus Lane, 1923, (Nématode-Héligmosomatidé). [The genus Nippostrongylus Lane, 1923 (Nematoda-Heligmosomatidae)]. Ann Parasitol Hum Comp. 1970;45(6):815-21.  https://doi.org/10.1051/parasite/1970456815  PMID: 5535153 
  20. Khalil LF, Jones A, Bray RA. Keys to the cestode parasites of vertebrates. Wallingford: CAB International; 1994.
  21. de Boer P, Rahaoui H, Leer RJ, Montijn RC, van der Vossen JMBM. Real-time PCR detection of Campylobacter spp.: A comparison to classic culturing and enrichment. Food Microbiol. 2015;51:96-100.  https://doi.org/10.1016/j.fm.2015.05.006  PMID: 26187833 
  22. Chaban B, Musil KM, Himsworth CG, Hill JE. Development of cpn60-based real-time quantitative PCR assays for the detection of 14 Campylobacter species and application to screening of canine fecal samples. Appl Environ Microbiol. 2009;75(10):3055-61.  https://doi.org/10.1128/AEM.00101-09  PMID: 19304828 
  23. Ahmed A, Engelberts MFM, Boer KR, Ahmed N, Hartskeerl RA. Development and validation of a real-time PCR for detection of pathogenic leptospira species in clinical materials. PLoS One. 2009;4(9):e7093.  https://doi.org/10.1371/journal.pone.0007093  PMID: 19763264 
  24. Johne R, Plenge-Bönig A, Hess M, Ulrich RG, Reetz J, Schielke A. Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol. 2010;91(Pt 3):750-8.  https://doi.org/10.1099/vir.0.016584-0  PMID: 19889929 
  25. Widén F, Ayral F, Artois M, Olofson AS, Lin J. PCR detection and analysis of potentially zoonotic Hepatitis E virus in French rats. Virol J. 2014;11(1):90.  https://doi.org/10.1186/1743-422X-11-90  PMID: 24886183 
  26. Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bönig A, Gregersen H, et al. Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect Genet Evol. 2012;12(5):947-56.  https://doi.org/10.1016/j.meegid.2012.02.021  PMID: 22554648 
  27. Kallio-Kokko H, Laakkonen J, Rizzoli A, Tagliapietra V, Cattadori I, Perkins SE, et al. Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy. Epidemiol Infect. 2006;134(4):830-6.  https://doi.org/10.1017/S0950268805005431  PMID: 16371172 
  28. Kinnunen PM, Henttonen H, Hoffmann B, Kallio ER, Korthase C, Laakkonen J, et al. Orthopox virus infections in Eurasian wild rodents. Vector Borne Zoonotic Dis. 2011;11(8):1133-40.  https://doi.org/10.1089/vbz.2010.0170  PMID: 21453121 
  29. Forbes KM, Voutilainen L, Jääskeläinen A, Sironen T, Kinnunen PM, Stuart P, et al. Serological survey of rodent-borne viruses in finnish field voles. Vector Borne Zoonotic Dis. 2014;14(4):278-83.  https://doi.org/10.1089/vbz.2013.1526  PMID: 24689532 
  30. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1).  https://doi.org/10.18637/jss.v067.i01 
  31. Pearson KX. On the criterion that a given system of deviations from the probable in the case of a correlated system of variables is such that it can be reasonably supposed to have arisen from random sampling. Lond Edinb Dublin Philos Mag J Sci. 1900;50(302):157-75.  https://doi.org/10.1080/14786440009463897 
  32. Dyk V, Tilc K, Hanuskova Z. Endoparasites of the rat (Rattus norvegicus, Berkenhout, 1769) in old and modern city districts and in the zoological garden. Acta Vet Brno. 1975;44:245-51.
  33. Galán-Puchades MT, Sanxis-Furió J, Pascual J, Bueno-Marí R, Franco S, Peracho V, et al. First survey on zoonotic helminthosis in urban brown rats (Rattus norvegicus) in Spain and associated public health considerations. Vet Parasitol. 2018;259(June):49-52.  https://doi.org/10.1016/j.vetpar.2018.06.023  PMID: 30056983 
  34. Desvars-Larrive A, Hammed A, Hodroge A, Berny P, Benoît E, Lattard V, et al. Population genetics and genotyping as tools for planning rat management programmes. J Pest Sci. 2019;92(2):691-705.  https://doi.org/10.1007/s10340-018-1043-4 
  35. Milazzo C, Ribas A, Casanova JC, Cagnin M, Geraci F, Di Bella C. Helminths of the brown rat (Rattus norvegicus) (Berkenhout, 1769) in the city of Palermo, Italy. Helminthologia. 2010;47(4):238-40.  https://doi.org/10.2478/s11687-010-0037-4 
  36. Kataranovski M, Mirkov I, Belij S, Popov A, Petrović Z, Gačić Z, et al. Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat. Parasite. 2011;18(2):189-96.  https://doi.org/10.1051/parasite/2011182189  PMID: 21678796 
  37. Franssen F, Swart A, van Knapen F, van der Giessen J. Helminth parasites in black rats (Rattus rattus) and brown rats (Rattus norvegicus) from different environments in the Netherlands. Infect Ecol Epidemiol. 2016;6(1):31413.  https://doi.org/10.3402/iee.v6.31413  PMID: 27193418 
  38. McGarry JW, Higgins A, White NG, Pounder KC, Hetzel U. Zoonotic helminths of urban brown rats (Rattus norvegicus) in the UK: neglected public health considerations? Zoonoses Public Health. 2015;62(1):44-52.  https://doi.org/10.1111/zph.12116  PMID: 24661776 
  39. Ryll R, Bernstein S, Heuser E, Schlegel M, Dremsek P, Zumpe M, et al. Detection of rat hepatitis E virus in wild Norway rats (Rattus norvegicus) and Black rats (Rattus rattus) from 11 European countries. Vet Microbiol. 2017;208:58-68.  https://doi.org/10.1016/j.vetmic.2017.07.001  PMID: 28888650 
  40. Heyman P, Baert K, Plyusnina A, Cochez C, Lundkvist A, Esbroeck MV, et al. Serological and genetic evidence for the presence of Seoul hantavirus in Rattus norvegicus in Flanders, Belgium. Scand J Infect Dis. 2009;41(1):51-6.  https://doi.org/10.1080/00365540802459994  PMID: 18821445 
  41. Boey K, Shiokawa K, Rajeev S. Leptospira infection in rats: A literature review of global prevalence and distribution. PLoS Negl Trop Dis. 2019;13(8):e0007499.  https://doi.org/10.1371/journal.pntd.0007499  PMID: 31398190 
  42. Zilber AL, Belli P, Artois M, Kodjo A, Djelouadji Z. First Observation of Leptospira interrogans in the Lungs of Rattus norvegicus. BioMed Res Int. 2016;2016:9656274.  https://doi.org/10.1155/2016/9656274  PMID: 27800495 
  43. Ayral F, Zilber AL, Bicout DJ, Kodjo A, Artois M, Djelouadji Z. Distribution of leptospira interrogans by multispacer sequence typing in urban Norway rats (Rattus norvegicus): A survey in France in 2011-2013. PLoS One. 2015;10(10):e0139604.  https://doi.org/10.1371/journal.pone.0139604  PMID: 26447693 
  44. Ayral F, Artois J, Zilber AL, Widén F, Pounder KC, Aubert D, et al. The relationship between socioeconomic indices and potentially zoonotic pathogens carried by wild Norway rats: a survey in Rhône, France (2010-2012). Epidemiol Infect. 2015;143(3):586-99.  https://doi.org/10.1017/S0950268814001137  PMID: 24838220 
  45. Jensen PM, Magnussen E. Is it too cold for Leptospira interrrogans transmission on the Faroese Islands? Infect Dis (Lond). 2016;48(2):156-60.  https://doi.org/10.3109/23744235.2015.1092579  PMID: 26442766 
  46. Ferreira AS, Costa P, Rocha T, Amaro A, Vieira ML, Ahmed A, et al. Direct detection and differentiation of pathogenic Leptospira species using a multi-gene targeted real time PCR approach. PLoS One. 2014;9(11):e112312.  https://doi.org/10.1371/journal.pone.0112312  PMID: 25398140 
  47. Heuser E, Fischer S, Ryll R, Mayer-Scholl A, Hoffmann D, Spahr C, et al. Survey for zoonotic pathogens in Norway rat populations from Europe. Pest Manag Sci. 2017;73(2):341-8.  https://doi.org/10.1002/ps.4339  PMID: 27299665 
  48. Collares-Pereira M, Mathias ML, Santos-Reis M, Ramalhinho MG, Duarte-Rodrigues P. Rodents and Leptospira transmission risk in Terceira island (Azores). Eur J Epidemiol. 2000;16(12):1151-7.  https://doi.org/10.1023/A:1010916132497  PMID: 11484805 
  49. Vitale M, Agnello S, Chetta M, Amato B, Vitale G, Bella CD, et al. Human leptospirosis cases in Palermo Italy. The role of rodents and climate. J Infect Public Health. 2018;11(2):209-14.  https://doi.org/10.1016/j.jiph.2017.07.024  PMID: 28802826 
  50. Broom JC, Gibson EA. Infection rates of Rattus norvegicus with Leptospira icterohaemorrhagiae in Great Britain. I. A rural area in Carmarthenshire, Wales. J Hyg (Lond). 1953;51(3):416-25.  https://doi.org/10.1017/S0022172400015837  PMID: 13096748 
  51. Krøjgaard LH, Villumsen S, Markussen MDK, Jensen JS, Leirs H, Heiberg AC. High prevalence of Leptospira spp. in sewer rats (Rattus norvegicus). Epidemiol Infect. 2009;137(11):1586-92.  https://doi.org/10.1017/S0950268809002647  PMID: 19393116 
  52. Collares-Pereira M, Korver H, Terpstra WJ, Santos-Reis M, Ramalhinho MG, Mathias ML, et al. First epidemiological data on pathogenic leptospires isolated on the Azorean islands. Eur J Epidemiol. 1997;13(4):435-41.  https://doi.org/10.1023/A:1007383405833  PMID: 9258550 
  53. Aviat F, Blanchard B, Michel V, Blanchet B, Branger C, Hars J, et al. Leptospira exposure in the human environment in France: A survey in feral rodents and in fresh water. Comp Immunol Microbiol Infect Dis. 2009;32(6):463-76.  https://doi.org/10.1016/j.cimid.2008.05.004  PMID: 18639932 
  54. Millán J, Cevidanes A, Chirife AD, Candela MG, León-Vizcaíno L. Risk factors of Leptospira infection in Mediterranean periurban micromammals. Zoonoses Public Health. 2018;65(1):e79-85.  https://doi.org/10.1111/zph.12411  PMID: 29058382 
  55. Rislakki V, Salminen A. Investigations of leptospirosis in rats in Finland. Acta Pathol Microbiol Scand. 1955;37(1):121-31.  https://doi.org/10.1111/j.1699-0463.1955.tb00927.x  PMID: 14398273 
  56. Raulo S, Kyyrö J, Gadd T, Hallanvuo S, Hietanen P, Oksanen A, et al. Suomen zoonoositilanne ja riskit yhteisen terveyden näkökulmasta: Yhteenveto zoonoosien suuntauksista ja lähteistä 2011-2021. [Finland's zoonotic situation and risks from the perspective of One Health: Summary of trends and sources of zoonoses 2011-2021]. Helsinki; 2023.
  57. Tiainen OA. Occurrence of Trichinella spiralis Ow. (Nematoda, Trichinelloidea) in rats at the Helsinki City Zoological Gardens. Ann Zool Fenn. 1966;3:4.
  58. Mikkonen T, Valkama J, Wihlman H, Sukura A. Spatial variation of Trichinella prevalence in rats in Finnish waste disposal sites. J Parasitol. 2005;91(1):210-3.  https://doi.org/10.1645/GE-3230RN  PMID: 15856908 
  59. Oksanen A, Interisano M, Isomursu M, Heikkinen P, Tonanzi D, Oivanen L, et al. Trichinella spiralis prevalence among wildlife of a boreal region rapidly reduced in the absence of spillover from the domestic cycle. Vet Parasitol. 2018;262:1-5.  https://doi.org/10.1016/j.vetpar.2018.09.002  PMID: 30389004 
  60. Malakauskas A, Kapel CMO, Webster P. Infectivity, persistence and serological response of nine Trichinella genotypes in rats. Parasite. 2001;8(2) Suppl;S216-22.  https://doi.org/10.1051/parasite/200108s2216  PMID: 11484361 
  61. Pozio E. Factors affecting the flow among domestic, synanthropic and sylvatic cycles of Trichinella. Vet Parasitol. 2000;93(3-4):241-62.  https://doi.org/10.1016/S0304-4017(00)00344-7  PMID: 11099840 
  62. Olkkola S, Rossi M, Jaakkonen A, Simola M, Tikkanen J, Hakkinen M, et al. Host-Dependent Clustering of Campylobacter Strains From Small Mammals in Finland. Front Microbiol. 2021;11:621490.  https://doi.org/10.3389/fmicb.2020.621490  PMID: 33584588 
  63. Le Moine V, Vannier P, Jestin A. Microbiological Studies of Wild Rodents in Farms as Carriers of Pig Infectious Agents. Prev Vet Med. 1987;4(5-6):399-408.  https://doi.org/10.1016/0167-5877(87)90026-2 
  64. Backhans A, Jacobson M, Hansson I, Lebbad M, Lambertz ST, Gammelgård E, et al. Occurrence of pathogens in wild rodents caught on Swedish pig and chicken farms. Epidemiol Infect. 2013;141(9):1885-91.  https://doi.org/10.1017/S0950268812002609  PMID: 23174339 
  65. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, et al. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio. 2014;5(5):e01933-14.  https://doi.org/10.1128/mBio.01933-14  PMID: 25316698 
  66. Kato Y, Nakai Y, Matsushita M, Takagi Y, Kohzaki KI, Kaneuchi C. Detection of Salmonella and Campylobacter from rats trapped at restaurants and a fish market. Nippon Juishikai Zasshi. 1999;52(3):194-7.  https://doi.org/10.12935/jvma1951.52.194 
  67. Seguin B, Boucaud-Maître Y, Quenin P, Lorgue G. Bilan épidémiologique d’un échantillon de 91 rats (Rattus norvegicus) capturés dans les égouts de Lyon. [Epidemiologic evaluation of a sample of 91 rats (Rattus norvegicus) captured in the sewers of Lyon]. Zentralbl Bakteriol Mikrobiol Hyg A. 1986;261(4):539-46.  https://doi.org/10.1016/S0176-6724(86)80088-8  PMID: 3532637 
  68. Galán-Puchades MT, Gómez-Samblás M, Osuna A, Sáez-Durán S, Bueno-Marí R, Fuentes MV. Autochthonous Angiostrongylus cantonensis lungworms in urban rats, Valencia, Spain, 2021. Emerg Infect Dis. 2022;28(12):2564-7.  https://doi.org/10.3201/eid2812.220418  PMID: 36418005 
  69. Barratt J, Chan D, Sandaradura I, Malik R, Spielman D, Lee R, et al. Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology. 2016;143(9):1087-118.  https://doi.org/10.1017/S0031182016000652  PMID: 27225800 
  70. Morgan ER, Modry D, Paredes-Esquivel C, Foronda P, Traversa D. Angiostrongylosis in Animals and Humans in Europe. Pathogens. 2021;10(10):1236.  https://doi.org/10.3390/pathogens10101236  PMID: 34684185 
  71. Angley LP, Combs M, Firth C, Frye MJ, Lipkin I, Richardson JL, et al. Spatial variation in the parasite communities and genomic structure of urban rats in New York City. Zoonoses Public Health. 2018;65(1):e113-23.  https://doi.org/10.1111/zph.12418  PMID: 29143489 
  72. Byers KA, Booker TR, Combs M, Himsworth CG, Munshi-South J, Patrick DM, et al. Using genetic relatedness to understand heterogeneous distributions of urban rat-associated pathogens. Evol Appl. 2020;14(1):198-209.  https://doi.org/10.1111/eva.13049  PMID: 33519965 
  73. Richardson JL, Silveira G, Soto Medrano I, Arietta AZ, Mariani C, Pertile AC, et al. Significant genetic impacts accompany an urban rat control campaign in Salvador, Brazil. Front Ecol Evol. 2019;7:115.  https://doi.org/10.3389/fevo.2019.00115 
  74. Davis DE. The characteristics of rat populations. Q Rev Biol. 1953;28(4):373-401.  https://doi.org/10.1086/399860  PMID: 13121239 
  75. Nygren NV, Tuomas JA. Rotta kuntalaisena – rottien esiintyminen ja hallinta. [Rat as a municipal citizen – rat occurrence and control]. Suom Eläinlääkl. 2022;128(6):331-7.
  76. Lee MJ, Byers KA, Donovan CM, Bidulka JJ, Stephen C, Patrick DM, et al. Effects of culling on Leptospira interrogans carriage by rats. Emerg Infect Dis. 2018;24(2):356-60.  https://doi.org/10.3201/eid2402.171371  PMID: 29350160 
  77. Bagan H, Yamagata Y. Land-cover change analysis in 50 global cities by using a combination of Landsat data and analysis of grid cells. Environ Res Lett. 2014;9(6):064015.  https://doi.org/10.1088/1748-9326/9/6/064015 
  78. Nygård H. Kompostoida vaiko polttaa? keskustelu jätteenkäsittelyn vaihtoehdoista 1950-luvulla. In: Näkökulmia Helsingin ympäristöhistoriaan [Compost or incinerate? discussion of alternatives to waste treatment in the 1950s. In: Perspectives on Helsinki's environmental history]. Helsinki: Edita/Helsingin kaupungin tietokeskus; 2001. p. 90-101.
  79. Sane J, Ollgren J, Makary P, Vapalahti O, Kuusi M, Lyytikäinen O. Regional differences in long-term cycles and seasonality of Puumala virus infections, Finland, 1995-2014. Epidemiol Infect. 2016;144(13):2883-8.  https://doi.org/10.1017/S0950268816000765  PMID: 27113030 
  80. Stryjek R, Kalinowski A, Parsons MH. Unbiased sampling for rodents and other small mammals: How to overcome neophobia through use of an electronic-triggered live trap-A preliminary test. Front Ecol Evol. 2019;7(FEB):11.  https://doi.org/10.3389/fevo.2019.00011 
  81. Robinson SJ, Pearl DL, Himsworth CG, Weese JS, Lindsay LR, Dibernardo A, et al. Environmental and sociodemographic factors associated with zoonotic pathogen occurrence in Norway rats (Rattus norvegicus) from Windsor, Ontario. Zoonoses Public Health. 2024;71(4):416-28.  https://doi.org/10.1111/zph.13120  PMID: 38419369 
Potentially zoonotic pathogens and parasites in opportunistically sourced urban brown rats (Rattus norvegicus) in and around Helsinki, Finland, 2018 to 2023
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Tuomas+Aivelo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Aivelo Tuomas</a>, <a href="/search?value1=Hussein+Alburkat&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Alburkat Hussein</a>, <a href="/search?value1=Nina+Suomalainen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Suomalainen Nina</a>, <a href="/search?value1=Rebekka+Kukowski&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kukowski Rebekka</a>, <a href="/search?value1=Petra+Heikkinen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Heikkinen Petra</a>, <a href="/search?value1=Antti+Oksanen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Oksanen Antti</a>, <a href="/search?value1=Otso+Huitu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Huitu Otso</a>, <a href="/search?value1=Rauni+Kivist%C3%B6&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kivistö Rauni</a>, <a href="/search?value1=Tarja+Sironen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sironen Tarja</a></span>. Potentially zoonotic pathogens and parasites in opportunistically sourced urban brown rats (Rattus norvegicus) in and around Helsinki, Finland, 2018 to 2023. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(40):pii=2400031. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.40.2400031" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.40.2400031</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 11 Jan 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 13 May 2024 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.40.2400031
/content/10.2807/1560-7917.ES.2024.29.40.2400031
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error