Combining real-time polymerase chain reaction using SYBR green i detection and sequencing to identify vertebrate bloodmeals in fleas

Journal of Medical Entomology

Volumn 49, Issue 6, 2012, Pages 1442-1452

  Graham, Christine B ^a   Black, William C ^b   Boegler, Karen A ^a   Montenieri, John A ^a   Holmes, Jennifer L ^a   Gage, Kenneth L ^a   Eisen, Rebecca J ^a  

^a NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

bloodmeal identification; cutoff; flea; real time PCR; threshold cycle

Indexed keywords

DNA; FLUORESCENT DYE; ORGANIC COMPOUND; SYBR GREEN I;

ANIMAL; ARTICLE; CAT; CHEMISTRY; CTENOCEPHALIDES; DISEASE TRANSMISSION; HOST RANGE; HUMAN; PARASITOLOGY; PHYSIOLOGY; PLAGUE; RAT; REAL TIME POLYMERASE CHAIN REACTION; YERSINIA PESTIS;

ANIMALS; CATS; CTENOCEPHALIDES; DNA; FLUORESCENT DYES; HOST SPECIFICITY; HUMANS; ORGANIC CHEMICALS; PLAGUE; RATS; REAL-TIME POLYMERASE CHAIN REACTION; YERSINIA PESTIS;

CAPRA HIRCUS; CTENOCEPHALIDES FELIS; RATTUS; SIPHONAPTERA (FLEAS); VERTEBRATA; YERSINIA PESTIS;

EID: 84869860006     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12071     Document Type: Article

References (64)

1. Ali Oshaghi, M., A. R. Chavshin, H. Vatandoost, F. Yaaghoobi, F. Mohtarami, and N. Noorjah. 2006. Effects of postingestion and physical conditions onPCRamplication of host blood meal DNA in mosquitoes. Exp. Parasitol. 112: 232-236.
2. Allan, B. F., L. S. Goessling, G. A. Storch, and R. E. Thach. 2010. Blood meal analysis to identify reservoir hosts for Amblyomma americanum ticks. Emerg. Infect. Dis. 16: 433-440.
3. Amatre, G., N. Babi, R. E. Enscore, A. Ogen-Odoi, L. A. Atiku, A. Akol, K. L. Gage, and R. J. Eisen. 2009. Flea diversity and infestation prevalence on rodents in a plague-endemic region of Uganda.Am.J. Trop. Med. Hyg. 81: 718-724.
4. Bartsch, S., B. Bauer, A. Wiemann, P.-H. Clausen, and S. Steuber. 2009. Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitol. Res. 105: 373-380.
5. Bio-Rad Laboratories. 2006. Real-time PCR applications guide. Bio-Rad Laboratories, Hercules, CA.
6. Borchert, J. N., J. J. Mach, T. J. Linder, A. Ogen-Odoi, and S. Angualia. 2007. Invasive rats and bubonic plague in Northwest Uganda, pp. 283-293. In G. W. Witmer, W. C. Pitt, and A. Fagerstone (eds.), Managing Vertebrate Invasive Species: Proceedings of an International Symposium. U.S. Dep. Agric./APHIS Wildlife Services, National Wildlife Research Center, Fort Collins, CO.
7. Bustin, S. A., V. Benes, J. A. Garson, J. Hellemans, J. Huggett, M. Kubista, R. Mueller, T. Nolan, M. W. Pfaffl, G. L. Shipley, J. Vandesompele, and C. T. Wittwer. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55: 611-622.
8. Caraguel, C.G.B., H. Stryhn, N. Gagne, I. R. Dohoo, and K. L. Hammell. 2011. Selection of a cutoff value for real-time polymerase chain reaction results to t a diagnostic purpose: analytical and epidemiologic approaches. J. Vet. Diagn. Invest. 23: 2-15.
9. Chow-Shaffer, E., B. Sina, W. A. Hawley, J. De Benedictis, and T. W. Scott. 2000. Laboratory and eld evaluation of polymerase chain reaction-based forensic DNA proling for use in identication of human blood meal sources of Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 37: 492-502.
10. Coulson, R.M.R., C. F. Curtis, P. D. Ready, N. Hill, and D. F. Smith. 1990. Amplication and analysis of human DNA present in mosquito bloodmeals. Med. Vet. Entomol. 4: 357-366.
11. Davey, J. S., C. S. Casey, I. F. Burgess, and J. Cable. 2007. DNA detection rates of host mtDNA in bloodmeals of human body lice (Pediculus humanus L., 1758). Med. Vet. Entomol. 21: 293-296. (Pubitemid 47493874)
12. Deguilloux, M. F., S. Ricaud, R. Leahy, and M. H. Pemonge. 2011. Analysis of ancient human DNA and primer contamination: one step backward one step forward. Forensic Sci. Int. 210: 102-109.
13. Dryden, M. W. 1989. Host association, on-host longevity and egg production of Ctenocephalides felis felis. Vet. Parasitol. 34: 117-122. (Pubitemid 19278206)
14. Dryden, M. W., and S. M. Gaafar. 1991. Blood consumption by the cat ßea, Ctenocephalides felis (Siphonaptera: Pulicidae). J. Med. Entomol. 28: 394-400.
15. Eisen, R. J., A. P. Wilder, S.W.Bearden, J. A. Montenieri, and K. L. Gage. 2007. Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efcient as transmission by blocked ßeas. J. Med. Entomol. 44: 678-682. (Pubitemid 47083503)
16. Eisen, R. J., S. W. Bearden, A. P. Wilder, J. A. Montenieri, M. F. Antolin, and K. L. Gage. 2006. Early-phase transmission of Yersinia pestis by unblocked ßeas as a mechanism explaining rapidly spreading plague epizootics. Proc. Natl. Acad. Sci. U.S.A. 103: 15380-15385. (Pubitemid 44625600)
17. Eisen, R. J., J. L. Holmes, A. M. Schotthoefer, S. M. Vetter, J. A. Montenieri, and K. L. Gage. 2008a. Demonstration of early-phase transmission of Yersinia pestis by the mouse ßea, Aetheca wagneri (Siphonaptera: Ceratophylidae), and implications for the role of deer mice as enzootic reservoirs. J. Med. Entomol. 45: 1160-1164.
18. Eisen, R. J., S. M. Vetter, J. L. Holmes, S. W. Bearden, J. A. Montenieri, and K. L. Gage. 2008b. Source of host blood affects prevalence of infection and bacterial loads of Yersinia pestis in ßeas. J. Med. Entomol. 45: 933-938.
19. Eisen, R. J., J. N. Borchert, J. L. Holmes, G. Amatre, K. Van Wyk, R. E. Enscore, N. Babi, L. A. Atiku, A. P. Wilder, S. M. Vetter, S. W. Bearden, J. A. Montenieri, and K. L. Gage. 2008c. Early-phase transmission of Yersinia pestis by cat ßeas (Ctenocephalides felis) and their potential role as vectors in a plague-endemic region of Uganda. Am. J. Trop. Med. Hyg. 78: 949-956. (Pubitemid 351967814)
20. Fagbemi, B. O. 1982. Effect of Ctenocephalides felis strongylus infestation on the performance of West African dwarf sheep and goats. Vet. Quart. 4: 92-95.
21. Franklin, H. A., P. Stapp, and A. Cohen. 2010. Polymerase chain reaction (PCR) identication of rodent blood meals conrms host sharing by ßea vectors of plague. J. Vector Ecol. 35: 363-371.
22. Gratz, N. G. 1999. Rodent reservoirs and ßea vectors of natural foci of plague, pp. 63-96. In D. T. Dennis, K. L. Gage, N. Gratz, J. D. Poland, and E. Tikhomirov (eds.), Plague Manual: Epidemiology, Distribution, Surveillance and Control. World Health Organization, Geneva, Switzerland.
23. Gunson, R. N., S. Bennett, A. Maclean, and W. F. Carman. 2008. Using multiplex real time PCR in order to streamline a routine diagnostic service. J. Clin. Virol. 43: 372-375.
24. Haouas, N., B. Pesson, R. Boudabous, J. P. Dedet, H. Babba, and C. Ravel. 2007. Development of a molecular tool for the identication of leishmania reservoir hosts by blood meal analysis in the insect vectors. Am. J. Trop. Med. Hyg. 77: 1054-1059. (Pubitemid 351837792)
25. Hinkle, N. C., P. G. Koehler, W. H. Kern, and R. S. Patterson. 1991. Hematophagous strategies of the cat ßea (Siphonaptera: Pulicidae). Fla. Entomol. 74: 377-385.
26. Humair, P. F., V. Douet, F. Moran Cadenas, L. M. Schouls, I. Van De Pol, and L. Gern. 2007. Molecular identication of bloodmeal source in Ixodes ricinus ticks using 12S rDNA as a genetic marker. J. Med. Entomol. 44: 869-880. (Pubitemid 47442068)
27. Ivanova, N. V., T. S. Zemlak, R. H. Hanner, and P.D.N. Hebert. 2007. Universal primer cocktails for sh DNA barcoding. Mol. Ecol. Notes 7: 544-548. (Pubitemid 47035520)
28. Jones, K. E., N. G. Patel, M. A. Levy, A. Storeygard, D. Balk, J. L. Gittleman, and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature 451: U990-U994.
29. Kaal, J. F., K. Baker, and P. R. Torgerson. 2006. Epidemiology of ßea infestation of ruminants in Libya. Vet. Parasitol. 141: 313-318.
30. Kemp, B. M., and D. G. Smith. 2005. Use of bleach to eliminate contaminating DNA from the surface of bones and teeth. Forensic Sci. Int. 154: 53-61. (Pubitemid 41338725)
31. Kent, R., L. Juliusson, M. Weissmann, S. Evans, and N. Komar. 2009. Seasonal blood-feeding behavior of Culex tarsalis (Diptera: Culicidae) in Weld County, Colorado, 2007. J. Med. Entomol. 46: 380-390.
32. Kent, R. J. 2009. Molecular methods for arthropod bloodmeal identication and applications to ecological and vector-borne disease studies. Mol. Ecol. Resour. 9: 4-18.
33. Kent, R. J., and D. E. Norris. 2005. Identication of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome b. Am. J. Trop. Med. Hyg. 73: 336-342. (Pubitemid 41278709)
34. Kilpatrick, A. M., L. D. Kramer, S. R. Campbell, E. O. Alleyne, A. P. Dobson, and P. Daszak. 2005. West Nile virus risk assessment and the bridge vector paradigm. Emerg. Infect. Dis. 11: 42-429.
35. King, W. V., and C. G. Bull. 1923. The blood feeding habits of malaria-carrying mosquitoes. Am. J. Hyg. 3: 497-513.
36. Kirstein, F., and J. S. Gray. 1996. Amolecular marker for the identication of the zoonotic reservoirs of Lyme borreliosis by analysis of the blood meal in its European vector Ixodes ricinus. Appl. Environ. Microb. 62: 4060-4065. (Pubitemid 26371506)
37. Kirstein, F., and J. S. Gray. 1999. Blood meal identication in ticks: a promising tool in ecological research on tickborne diseases. Zentralbl. Bakteriol. 289: 760-764. (Pubitemid 30047290)
38. Krasnov, B. R., C. Korine, N. V. Burdelova, I. S. Khokhlova, and B. Pinshow. 2007. Between-host phylogenetic distance and feeding efciency in hematophagous ectoparasites: rodent ßeas and a bat host. Parasitol. Res. 101: 36-371.
39. Krasnov, B. R., M. Sarfati, M. S. Arakelyan, I. S. Khokhlova, N. V. Burdelova, and A. A. Degen. 2003. Host specicity and foraging efciency in blood-sucking parasite: feeding patterns of the ßea Parapulex chephrenis on two species of desert rodents. Parasitol. Res. 90: 393-399. (Pubitemid 36995197)
40. Lanciotti, R. S., A. J. Kerst, R. S. Nasci, M. S. Godsey, C. J. Mitchell, H. M. Savage, N. Komar, N. A. Panella, B. C. Allen, K. E. Volpe, B. S. Davis, and J. T. Roehrig. 2000. Rapid detection of West Nile virus from human clinical specimens, eld-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J. Clin. Microbiol. 38: 4066-4071. (Pubitemid 32233206)
41. Lee, J. H., H. Hassan, G. Hill, E. W. Cupp, T. B. Higazi, C. J. Mitchell, M. S. Godsey, and T. R. Unnasch. 2002. Identication of mosquito avian-derived blood meals by polymerase chain reaction-heteroduplex analysis.Am.J. Trop. Med. Hyg. 66: 599-604.
42. Linville, J. G., and J. D. Wells. 2002. Surface sterilization of a maggot using bleach does not interfere with mitochondrial DNA analysis of crop contents. J. Forensic Sci. 47: 105-1059.
43. Linville, J. G., J. Hayes, and J. D. Wells. 2004. Mitochondrial DNAand STR analyses of maggot crop contents: effect of specimen preservation technique. J. Forensic Sci. 49: 341- 344. (Pubitemid 38298462)
44. Lorange, E. A., B. L. Race, F. Sebbane, and B. J. Hinnebusch. 2005. Poor vector competence of ßeas and the evolution of hypervirulence in Yersinia pestis. J. Infect. Dis. 191: 1907-1912. (Pubitemid 40705399)
45. Mota, J., J. C. Chacon, A. E. Gutiterrez-Cabrera, V. Sanchez- Cordero, R. A. Wirtz, R. Ordoez, F. Panzera, and J. M. Ramsey. 2007. Identication of blood meal source and infection with Trypanosoma cruzi of Chagas disease vectors using a multiplex cytochrome b polymerase chain reaction assay. Vector-Borne Zoon. Dis. 7: 617-627.
46. Mukabana, W. R., W. Takken, and B.G.J. Knols. 2002a. Analysis of arthropod bloodmeals using molecular genetic markers. Trends Parasitol. 18: 50-509.
47. Mukabana, W. R., W. Takken, P. Seda, G. F. Killeen, W. A. Hawley, and B.G.J. Knols. 2002b. Extent of digestion affects the success of amplifying human DNA from blood meals of Anopheles gambiae (Diptera: Culicidae). Bull. Entomol. Res. 92: 233-239. (Pubitemid 34623050)
48. Ngo, K. A., and L. D. Kramer. 2003. Identication of mosquito bloodmeals using polymerase chain reaction (PCR) with order-specic primers. J. Med. Entomol. 40: 21-222.
49. Pant, C. P., V. Houba, and H. D. Engers. 1987. Bloodmeal identication in vectors. Parasitol. Today 3: 324-326.
50. Pichon, B., D. Egan, M. Rogers, and J. Gray. 2003. Detection and identication of pathogens and host DNA in unfed host-seeking Ixodes ricinus L. (Acari: Ixodidae). J. Med. Entomol. 40: 723-731. (Pubitemid 37399548)
51. Pizarro, J. C., and L. Stevens. 2008. A new method for forensic DNA analysis of the blood meal in Chagas disease vectors demonstrated using Triatoma infestans from Chuquisaca, Bolivia. PLoS One 3: 1-8.
52. Pollitzer, R. 1954. Plague, World Health Organization Monograph Series. World Health Organization, Geneva, Switzerland.
53. Ririe, K. M., R. P. Rasmussen, and C. T. Wittwer. 1997. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal. Biochem. 245: 154-160. (Pubitemid 27082244)
54. Rurangirwa, F. R., S. H. Minja, A. J. Musoke, V. M. Nantulya, J. Grootenhuis, and S. K. Moloo. 1986. Production and evaluation of specic antisera against sera of various vertebrate species for identication of bloodmeals of Glossina morsitans centralis. Acta Tropica. 43: 379-389. (Pubitemid 17221427)
55. Silverman, J., and A. G. Appel. 1994. Adult cat ßea (Siphonaptera: Pulicidae) excretion of host blood proteins in relation to larval nutrition. J. Med. Entomol. 31: 26-271.
56. Steuber, S., A. Abdel-Rady, and P. H. Clausen. 2005. PCRRFLP analysis: a promising technique for host species identication of blood meals from tsetse ßies (Diptera: Glossinidae). Parasitol. Res. 97: 247-254. (Pubitemid 41542549)
57. Tempelis, C. H. 1975. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J. Med. Entomol. 11: 63-653.
58. Tollenaere, C., L. Rahalison, M. Ranjalahy, J. M. Duplantier, S. Rahelinirina, S. Telfer, and C. Brouat. 2010. Susceptibility to Yersinia pestis experimental infection in wild Rattus rattus, reservoir of plague in Madagascar. Ecohealth 7: 242-247.
59. Urban, C., F. Gruber, M. Kundi, F. G. Falkner, F. Dorner, and T. Hammerle. 2000. A systematic and quantitative analysis of PCR template contamination. J. Forensic Sci. 45: 1307-1311.
60. Van den Hurk, A. F., I. L. Smith, and G. A. Smith. 2007. Development and evaluation of real-time polymerase chain reaction assays to identify mosquito (Diptera: Culicidae) bloodmeals originating from native Australian mammals. J. Med. Entomol. 44: 8-92.
61. von Wurmb-Schwark, N., A. Heinrich, M. Freudenberg, M. Gebuhr, and T. Schwark. 2008. The impact ofDNAcontamination of bone samples in forensic case analysis and anthropological research. Legal Med. (Tokyo, Japan) 10: 12-130.
62. Washino, R. K., and C. H. Tempelis. 1983. Mosquito host bloodmeal identication: methodology and data analysis. Annu. Rev. Entomol. 28: 179-201.
63. Wilder, A. P., R. J. Eisen, S. W. Bearden, J. A. Montenieri, K. L. Gage, and M. F. Antolin. 2008. Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis. Vector-Borne Zoon. Dis. 8: 359-367. (Pubitemid 351860458)
64. Woods, M. E., J. A. Montenieri, R. J. Eisen, N. S. Zeidner, J. N. Borchert, A. Laudisoit, N. Babi, L. A. Atiku, R. E. Enscore, and K. L. Gage. 2009. Identication of ßea blood meals using multiplexed real-time polymerase chain reaction targeting mitochondrial gene fragments. Am. J. Trop. Med. Hyg. 80: 998-1003.