Not “out of Nantucket”: Babesia microti in southern New England comprises at least two major populations

Particle and Fibre Toxicology

Sam R Telford¹  Heidi K Goethert¹ 

[1]Department of Infectious Disease and Global Health, Cummings School of Veterinary Medicine, Tufts University, 200 Westboro Rd, North Grafton, 01536, MA, USA

关键词: Emergence;    VNTR;    Epidemiology;    New England;    Babesia microti;   

Others  :  1148677
DOI  :  10.1186/s13071-014-0546-y

 received in 2014-10-17, accepted in 2014-11-18,  发布年份 2014

【 摘 要 】

Background

Deer tick-transmitted human babesiosis due to Babesia microti appears to be expanding its distribution and prevalence in the northeastern United States. One hypothesis for this emergence is the introduction of parasites into new sites from areas of long-standing transmission, such as Nantucket Island, Massachusetts.

Methods

We developed a typing system based on variable number tandem repeat loci that distinguished individual B. microti genotypes. We thereby analyzed the population structure of parasites from 11 sites, representing long-standing and newly emerging transmission in southern New England (northeastern United States), and compared their haplotypes and allele frequencies to determine the most probable number of B. microti populations represented by our enzootic collections. We expected to find evidence for a point source introduction across southern New England, with all parasites clearly derived from Nantucket, the site with the most intense longstanding transmission.

Results

B. microti in southern New England comprises at least two major populations, arguing against a single source. The Nantucket group comprises Martha's Vineyard, Nantucket and nearby Cape Cod. The Connecticut/Rhode Island (CT/RI) group consists of all the samples from those states along with samples from emerging sites in Massachusetts.

Conclusions

The expansion of B. microti in the southern New England mainland is not due to parasites from the nearby terminal moraine islands (Nantucket group), but rather from the CT/RI group. The development of new B. microti foci is likely due to a mix of local intensification of transmission within relict foci across southern New England as well as long distance introduction events.

【 授权许可】

   
2014 Goethert and Telford; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Piesman J, Spielman A: Host-associations and seasonal abundance of immature Ixodes dammini in southeastern Massachusetts. Ann Entomol Soc Am 1979, 72:829-832.
• [2]Spielman A, Etkind P, Piesman J, Ruebush TK 2nd, Juranek DD, Jacobs MS: Reservoir hosts of human babesiosis on Nantucket Island. Am J Trop Med Hyg 1981, 30:560-565.
• [3]Telford SR 3rd, Mather TN, Adler GH, Spielman A: Short-tailed shrews as reservoirs of the agents of Lyme disease and human babesiosis. J Parasitol 1990, 76:681-683.
• [4]Telford SR III, Gorenflot A, Brasseur P, Spielman A: Babesial infections of humans and wildlife. In Parasitic Protozoa. Volume 5. 2nd edition. Academic Press, New York; 1993:1-47.
• [5]Vannier E, Krause PJ: Human babesiosis. N Engl J Med 2012, 366:2397-2407.
• [6]Stramer SL, Hollinger FB, Katz LM, Kleinman S, Metzel PS, Gregory KR, Dodd RY: Emerging infectious disease agents and their potential threat to transfusion safety. Transfusion (Paris) 2009, 49:1S-29S.
• [7]Acosta MEP, Ender PT, Smith EM, Jahre JA: Babesia microti infection, Eastern Pennsylvania, USA. Emerg Infect Dis 2013, 19:1105-1107.
• [8]Herwaldt BL, McGovern PC, Gerwel MP, Easton RM, MacGregor RR: Endemic babesiosis in another eastern state: New Jersey. Emerg Infect Dis 2003, 9:184.
• [9]Stafford KC, Williams SC, Magnarelli LA, Bharadwaj A, Ertel S-H, Nelson RS: Expansion of zoonotic babesiosis and reported human cases, Connecticut, 2001–2010. J Med Entomol 2014, 51:245-252.
• [10]Pfeiffer CD, Kazmierczak JJ, Davis JP: Epidemiologic features of human babesiosis in Wisconsin, 1996–2005. WMJ Off Publ State Med Soc Wis 2007, 106:191-195.
• [11]Tonnetti L, Thorp AM, Deisting B, Bachowski G, Johnson ST, Wey AR, Hodges JS, Leiby DA, Mair D: Babesia microti seroprevalence in Minnesota blood donors. Transfusion (Paris) 2013, 53:1698-1705.
• [12]Joseph JT, Roy SS, Shams N, Visintainer P, Nadelman RB, Hosur S, Nelson J, Wormser GP: Babesiosis in lower Hudson Valley, New York, USA. Emerg Infect Dis 2011, 17:843-847.
• [13]Cornillot E, Hadj-Kaddour K, Dassouli A, Noel B, Ranwez V, Vacherie B, Augagneur Y, Brès V, Duclos A, Randazzo S, Carcy B, Debierre-Grockiego F, Delbecq S, Moubri-Ménage K, Shams-Eldin H, Usmani-Brown S, Bringaud F, Wincker P, Vivarès CP, Schwarz RT, Schetters TP, Krause PJ, Gorenflot A, Berry V, Barbe V, Mamoun CB: Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Res 2012, 40:9102-9114.
• [14]Matyas BT, Nieder HS, Telford SR: Pneumonic tularemia on Martha’s Vineyard. Ann N Y Acad Sci 2007, 1105:351-377.
• [15]Spielman A, Wilson ML, Levine JF, Piesman J: Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annu Rev Entomol 1985, 30:439-460.
• [16]Dammin GJ, Spielman A, Benach JL, Piesman J: The rising incidence of clinical Babesia microti infection. Hum Pathol 1981, 12:398-400.
• [17]Anderson JF, Magnarelli LA, Kurz J: Intraerythrocytic parasites in rodent populations of Connecticut: Babesia and Grahamella Species. J Parasitol 1979, 65:599-604.
• [18]Piesman J, Mather TN, Donahue J, Levine J, Campbell JD, Karakashian SJ, Spielman A: Comparative prevalence of Babesia microti and Borrelia burgdorferi in four populations of Ixodes dammini in eastern Massachusetts. Acta Trop 1986, 43:263-270.
• [19]Piesman J: Ixodes dammini: Its role in transmitting Babesia microti to man. Doctoral thesis, Harvard School of Public Health, Boston, MA; 1980.
• [20]Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML: Preparation of PCR quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT). Biotechniques 2000, 29:52-54.
• [21]Ohmori S, Kawai A, Takada N, Saito-Ito A: Development of real-time PCR assay for differential detection and quantification for multiple Babesia microti-genotypes. Parasitol Int 2011, 60:403-409.
• [22]Rozen S, Skaletsky H: Primer3. ; 1998.
• [23]Toonen RJ, Hughes S: Increased throughput for fragment analysis on an ABI PRISM 377 automated sequencer using a membrane comb and STRand software. BioTechniques 2001, 31:1320-1324.
• [24]Rudzinska MA, Spielman A, Lewengrub S, Trager W, Piesman J: Sexuality in piroplasms as revealed by electron microscopy in Babesia microti. Proc Natl Acad Sci 1983, 80:2966-2970.
• [25]Tibayrenc M, Ayala FJ: The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 2002, 18:405-410.
• [26]Ross A, Koepfli C, Li X, Schoepflin S, Siba P, Mueller I, Felger I, Smith T: Estimating the numbers of malaria infections in blood samples using high-resolution genotyping data. PLoS One 2012, 7:e42496.
• [27]Van den Eede P, Van der Auwera G, Delgado C, Huyse T, Soto-Calle VE, Gamboa D, Grande T, Rodriguez H, Llanos A, Anne J, Erhart A, D’Alessandro U: Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malar J 2010, 9:151. BioMed Central Full Text
• [28]Piesman J, Karakashian SJ, Lewengrub S, Rudzinska MA, Spielman A: Development of Babesia microti sporozoites in adult Ixodes dammini. Int J Parasitol 1986, 16:381-385.
• [29]Hammer Ø, Harper DAT, Ryan PD: PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 2001, 4:1-9.
• [30]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [31]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005, 14:2611-2620.
• [32]Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carriço JA: PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 2012, 13:87. BioMed Central Full Text
• [33]Goethert HK, Telford SR: What is Babesia microti? Parasitology 2003, 127:301-309.
• [34]Simuunza M, Bilgic H, Karagenc T, Syakalima M, Shiels B, Tait A, Weir W: Population genetic analysis and sub-structuring in Babesia bovis. Mol Biochem Parasitol 2011, 177:106-115.
• [35]Muleya W, Namangala B, Simuunza M, Nakao R, Inoue N, Kimura T, Ito K, Sugimoto C, Sawa H: Population genetic analysis and sub-structuring of Theileria parva in the northern and eastern parts of Zambia. Parasit Vectors 2012, 5:1-11. BioMed Central Full Text
• [36]Anderson TJC, Haubold B, Williams JT, Estrada-Franco§ JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 2000, 17:1467-1482.
• [37]Gunawardena S, Karunaweera ND, Ferreira MU, Phone-Kyaw M, Pollack RJ, Alifrangis M, Rajakaruna RS, Konradsen F, Amerasinghe PH, Schousboe ML, Galappaththy GNL, Abeyasinghe RR, Hartl DL, Wirth DF: Geographic structure of Plasmodium vivax: microsatellite analysis of parasite populations from Sri Lanka, Myanmar, and Ethiopia. Am J Trop Med Hyg 2010, 82:235-242.
• [38]Herwaldt BL, Montgomery S, Woodhall D, Bosserman E: Babesiosis surveillance — 18 states, 2011. Morb Mortal Wkly Rep 2012, 61:505-509.
• [39]Massachusetts Department of Public Health: www.mass.gov/eohhs/docs/dph/cdc/babesiosis-surveillance-2013.pdf, accessed November 1, 2014
• [40]Telford SR III, Spielman A: Enzootic transmission of Babesia microti. In Tick Borne Pathog Host-Vector Interface. University of Minnesota College of Agriculture, St. Paul, MN; 1992:259-264.
• [41]Foster D, Motzkin G: Historical Influences on the Landscape of Martha’s Vineyard: Perspecitves on the Management of the Manuel F. Correllus State Forest. Harvard University: [Harvard Forest Paper, vol. #23], Petersham, Massachusetts; 1999.
• [42]Johnson C: A list of the insect fauna of Nantucket, MA. Proc Maria Mitchell Assoc Nantucket 1930, III.
• [43]Bishopp FC, Smith CN: A new species of Ixodes from Massachusetts. Proceeding Entomol Soc Wash 1937, 39:133-138.
• [44]Hertig M, Smiley D: The problem of controlling wood ticks on Martha’s Vineyard. The Vineyard Gazette 1937, 92(36):1-10.
• [45]Telford SR, Dawson JE, Katavolos P, Warner CK, Kolbert CP, Persing DH: Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proc Natl Acad Sci 1996, 93:6209-6214.
• [46]Tyzzer EE: Cytoecetes microti, n. g., n. sp., a parasite developing in granulocytes and infective for small rodents. Parasitology 1938, 30:242-257.
• [47]Spielman A, Clifford CM, Piesman J, Corwin MD: Human babesiosis on Nantucket Island, USA: description of the vector, Ixodes (Ixodes) dammini, n. sp. (Acarina: Ixodidae). J Med Entomol 1979, 15:218-234.
• [48]Goethert HK, Shani I, Telford SR: Genotypic diversity of Francisella tularensis infecting Dermacentor variabilis ticks on Martha’s Vineyard, Massachusetts. J Clin Microbiol 2004, 42:4968-4973.
• [49]Sakamoto JM, Goddard J, Rasgon JL: Population and demographic structure of Ixodes scapularis Say in the eastern United States. PLoS One 2014, 9:e101389.
• [50]Rich SM, Caporale DA, Telford SR, Kocher TD, Hartl DL, Spielman A: Distribution of Ixodes ricinus-like ticks in eastern North America. Proc Natl Acad Sci U S A 1995, 92:6284-6288.
• [51]Rosenthal BM, Spielman A: Reduced variation among northern deer tick populations at an autosomal microsatellite locus. J Vector Ecology 2004, 29:227-235.
• [52]Telford S III: The name Ixodes dammini epidemiologically justified. Emerg Infect Dis 1998, 4:132-134.
• [53]Telford SR III: Deer tick transmitted zoonoses in the eastern United States. In Conserv Med Ecol Health Pract. Oxford University Press, New York; 2002:310-324.
• [54]Cronon W: Changes in the Land. Hill and Wang, New York; 1983.
• [55]Larrousse F, King AG, Wolbach SB: The overwintering in Massachusetts of Ixodiphagus caucurtei. Science 1928, 67:351-353.
• [56]Spielman A: Lyme disease and human babesiosis: evidence incriminating vector and reservoir hosts. Pp 147–165. In Biology of Parasitism: A Molecular and Immunological Approach. Edited by Englund PT, Sher A, Alan R. Liss Inc, NY; 1988.
• [57]Severinghaus CW, Brown CP: History of the white-tailed deer in New York. N Y Fish Game J 1956, 3:129.
• [58]Hoen AG, Margos G, Bent SJ, Diuk-Wasser MA, Barbour A, Kurtenbach K, Fish D: Phylogeography of Borrelia burgdorferi in the eastern United States reflects multiple independent Lyme disease emergence events. Proc Natl Acad Sci 2009, 106:15013-15018.
• [59]Redfield A: Ontogeny of a salt marsh estuary. Science 1965, 147:50-55.
• [60]Carson RL: Parker river: a national wildlife refuge. Conservation in Action 1947, 2:1-15.
• [61]Lastavica CC, Wilson ML, Berardi VP, Spielman A, Deblinger RD: Rapid emergence of a focal epidemic of Lyme disease in coastal Massachusetts. N Engl J Med 1989, 320:133-137.
• [62]Piesman J, Spielman A, Etkind P, Ruebush TK, Juranek D: Role of deer in the epizootiology of Babesia microti in Massachusetts, USA. J Med Entomol 1979, 15:537-540.
• [63]Goethert HK, Telford SR: Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. Am J Trop Med Hyg 2003, 69:455-460.
• [64]Telford SR, Spielman A: Enzootic transmission of the agent of Lyme disease in rabbits. Am J Trop Med Hyg 1989, 41:482-490.
• [65]Peirce MA: Nuttallia França, 1909 (Babesiidae) preoccupied by Nuttallia Dall, 1898 (Psammobiidae): a re-appraisal of the taxonomic position of the avian piroplasms. Int J Parasitol 1975, 5:285-287.