Infection by Rickettsia felis in Ctenocephalides felis felis Fleas from North of Colombia
-
Verónica Contreras
,
Andrés F. Londoño
,
Jorge Miranda
,
Salim Mattar
,
Leidy Y. Acevedo-Gutiérrez
,
Francisco J. Diaz
,
Juan D. Rodas
Abstract
Background: Rickettsia felis is an emergent Rickettsial agent whose main vector is Ctenocephalides felis, but ticks, mites and lice are also infected. We aimed to search for molecular evidence of Rickettsia spp. in fleas collected from dogs and wild rodents (Heteromys anomalous) from three villages of Córdoba and Antioquia provinces (Northern of Colombia), where outbreaks of rickettsioses have occurred, and discuss the possible role of fleas on endemic/enzootic regions for rickettsia.
Methods: During 2010 and 2012, 649 Ctenocephalides felis felis and 24 Pulex irritans fleas were removed from dogs and wild rodents (Heteromys anomalous), respectively, in 3 locations from Córdoba and Antioquia provinces (Colombia). These fleas were tested into pools for Rickettsial infection by PCR, targeting gltA, ompB, and ompA Rickettsial genes.
Results: Almost 20% (30/153) of C. felis felis pools contained Rickettsial DNA. The fragments of ompB gene showed high identity values between sequences from Necocli and Los Cordobas with R. felis strain from Senegal (100% and 99.7% respectively) and all were highly related by phylogenetic analyses. Rickettsial DNA in pools of P. irritans was not detected.
Conclusion: Our findings highlighted the endemicity of the infection by R. felis in fleas from northern of Colombia and showed the likely importance of dogs as hosts of C. felis felis fleas and their potential role as reservoirs of R. felis.
1. Mansueto P, Vitale G, Cascio A, Seidita A, Pepe I, Carroccio A, di Rosa S, Rinni GB, Cillari, Walker DH (2012) New Insight into Immunity and Im-munopathology of Rickettsial Diseases. Clin Dev Immunol. 2012: 967852.
2. Labruna MB, Mattar S, Nava S, Bermudez S, Venzal JM, Dolz G, Abarca K, Romero L, de Sousa R, Oteo J, Zavala-Castro J (2011) Rickettsioses in Latin America, Caribbean, Spain and Portugal. Revista MVZ Córdoba. 16(2): 2435–2457.
3. Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM (1997) Flea-borne rickettsioses: ecologic considera-tions. Emerg Infect Dis. 3: 319–327.
4. Wedincamp J Jr, Foil LD (2002) Vertical transmission of Rickettsia felis in the cat flea (Ctenocephalides felis Bouche). J Vector Ecol. 27: 96–101.
5. Henry KM, Jiang J, Rozmajzl PJ, Azad AF, Macaluso KR, Richards AL (2007) Development of quantitative real-time PCR assays to detect Rickettsia typhi and Rickettsia felis, the causative agents of murine typhus and flea-borne spot-ted fever. Mol Cell Probes. 21: 17–23.
6. Boostrom A, Beier M, Macaluso JA, Macaluso KR, Sprenger D, Hayes J, Rad-ulovic S, Azad AF (2002) Geographic association of Rickettsia felis-infected opossums with human murine typhus, Texas. Emerg Infect Dis. 8: 549–554.
7. Schriefer M, Sacci Jr, Taylor JP, HigginsJA, Azad AF (1994) Murine typhus: updated roles of multiple urban com-ponents and asecond typhus-like Rick-ettsia. J Med Entomol. 31: 681–685.
8. Williams SG, Sacci JB, Schriefer ME, Andersen EM, Fujioka KK, Sorvillo FJ, Barr AR, Azad AF (1992) Typhus and typhus-like rickettsiae associated with opossums and their fleas in Los Angeles County, California. J. Clin. Microbiol. 30: 1758–1762.
9. Case JB, Chomel B, Nicholson W, Foley J (2006) Serological survey of vector-borne zoonotic pathogens in pet cats and cats from animal shelters and feral colonies. J Feline Med Surg. 8: 111–117.
10. Psaroulaki A, Antoniou M, Papaeustathi-ou A, Toumazos P, Loukaides F, Tse-lentis Y (2006) First detection of Rick-ettsia felis in Ctenocephalides felis fleas parasitizing rats in Cyprus. Am J Trop Med Hyg. 74: 120–122.
11. Pérez-Osorio CE, Zavala-Velázquez JE, León JJ, Zavala-Castro JE (2008) Rick-ettsia felis as emergent global threat for humans. Emerging Infect Dis. 14(7): 1019–1023.
12. Hidalgo M, Montoya V, Martínez A, Mercado M, De la Ossa A, Vélez C, Estrada G, Pérez JE, Faccini-Martínez AA, Labruna MB (2013) Flea-borne ri-ckettsioses in the North of Caldas pro-vince, Colombia. Vector Borne Zoono-tic Dis. 13: 289–294
13. Ramírez-Hernández A, Montoya V, Mar-tínez A, Pérez JE, Mercado M, de la Ossa A, Vélez C, Estrada G, Correa MI, Duque L (2013) Molecular detec-tion of Rickettsia felis in different flea species from Caldas, Colombia. Am J Trop Med Hyg. 89: 453–459.
14. Hidalgo M, Miranda J, Heredia D, Zam-brano P, Vesga JF, Lizarazo D, Mattar S, Valbuena G (2011) Outbreak of Rocky Mountain spotted fever in Córdoba, Co-lombia. Mem Inst Oswaldo Cruz. 106(1):
117–118.
15. Pacheco O, Giraldo R, Martínez M, Hi-dalgo M, Galeano A, Echeverri I, Ech-evarría L, Parra E, Rey G (2008) Estu-dio De Brote Febril Hemorrágico En El Village De Alto De Mulatos-Distrito Especial Portuario De Turbo, Antio-quia. Inf Quinc Epidemiol Nac Vol. 13: 145–160,
16. Furman DP, Catts EP (1982). Manual of medical entomology. Cambridge Uni-versity. (Ed. 4).
17. Wenzel R, Vernon. T (1966) Ectopara-sites of Panama, Field Museum of Nat-ural History.
18. Linardi PM, Guimarães LR (2000) Si-fonápteros do Brasil. Mus Zool da Univ São Paulo. São Paulo. pp. 48–53.
19. Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Am-blyomma cooperi ticks from an area in the State of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 42: 90–98.
20. Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of Rick-ettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 173: 1576–1589.
21. Roux V, Raoult D (2000) Phylogenetic analysis of members of the genus Rick-ettsia using the gene encoding the outer membrane protein rOmpB (ompB). Int J Syst Evol Microbiol. 50: 1449–1455.
22. Tamura K, Stecher G, Peterson D, Filip-ski A, Kumar S (2013) MEGA6: Mo-lecular evolutionary genetics analysis Version 6.0. Mol Biol Evol. 30(12): 2725–2729
23. Fredrik Ronquist, Maxim Teslenko, Paul van der Mark, Daniel L. Ayres, Aaron Darling, Sebastian Höhna, Bret Larget, Liang Liu, Marc A. Suchard, John P.Huelsenbeck (2012) MrBayes 3.2: Ef-ficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61(3): 539–542
24. Gehrke FS, Gazeta GS, Souza ER, Ribei-ro A, Marrelli MT, Schumaker TT (2009) Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 in-fecting Rhipicephalus sanguineus and Ctenocephalides felis collected from dogs in a Brazilian potted fever focus in the State of Rio De Janeiro/Brazil. Clin Microbiol Infect. 15(Suppl 2): 267–268.
25. Abramowicz KF, Wekesa JW, Nwadike CN, Zambrano ML, Karpathy SE, Cec-il D, Burns J, Hu R, Eremeeva ME (2012) Rickettsia felis in cat fleas, Cten-ocephalides felis parasitizing opossums, San Bernardino County, California. Med Vet Entomol. 26: 458–462.
26. Tsai KH, Lu HY, Huang JH, Wang PJ, Wang HC, Huang CG, Wu WJ, Shu PY (2009) Rickettsia felis in cat fleas in Taiwan. Vector Borne Zoonotic Dis. 9: 561–563
27. Demeke T, Jenkins GR (2010) Influence of DNA extraction methods, PCR in-hibitors and quantification methods on realtime PCR assay of biotechnology derived traits. Anal Bioanal Chem. 396: 1977–1990.
28. Horta MC, Ogrzewalska M, Azevedo MC, Costa FB, Ferreira F, Labruna MB (2014) Rickettsia felis in Ctenocephalides felis felis from Five Geographic Regions of Brazil. Am J Trop Med Hyg. 91(1): 96–100.
29. Zavala-Velazquez J, Zavala-Castro J, Vado-Solis I, Ruiz-Sosa J, Moron C, Bouyer D, Walker D (2002) Identification of Ctenocephalides felis fleas as a host of Rickettsia felis, the agent of a spotted fever rickettsiosis in Yucatan, Mexico. Vector Borne Zoonotic Dis. 2: 69–75.
30. Troyo A, Álvarez D, Taylor L, Abdalla G,
Calderón-Arguedas Ó, Zambrano ML, Dasch GA, Lindblade K, Hun L, Ere-meeva ME (2012) Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg. 86: 1054–1056.
31. Venzal JM, Pérez‐Martínez L, Felix ML, Portillo A, Blanco JR, Oteo JA (2006) Prevalence of Rickettsia felis in Cten-ocephalides felis and Ctenocephalides canis from Uruguay. Ann N. Y Acad Sci. 1078: 305–308.
32. Hii SF, Kopp SR, Abdad MY, Thompson MF, O’Leary CA, Rees RL, Traub RJ (2011) Molecular Evidence Supports the Role of Dogs as Potential Reser-voirs for Rickettsia felis. Vector-Borne Zoonotic Dis. 8: 1007–1012.
33. Oteo JA, Portillo A, Santibáñez S, Blan-co JR, Pérez-Martínez L, Ibarra V (2006) Cluster of cases of human Rick-ettsia felis infection from Southern Eu-rope (Spain) diagnosed by PCR. J Clin Microbiol. 44(7): 2669–2671.
34. Sackal C, Laudisoit A, Kosoy M, Mas-sung R, Eremeeva ME, Karpathy SE, Van Wyk K, Gabitzsch E, Zeidner NS (2008) Bartonella spp. and Rickettsia felis in fleas, Democratic Republic of Congo. Emerg Infect Dis. 14: 1972–1974.
35. Faccini-Martínez AA, Forero-Becerra E, Cortés-Vecino J, Polo-Teran L, Jácome J, Vargas J, Valbuena G, Hidalgo M (2013) Caso probable de fiebre man-chada (Rickettsia felis) transmitida por pulgas. Biomédica. 33(1): 9–13.
36. Labruna MB, Walker D (2014) Rickett-sia felis and Changing Paradigms about Pathogenic Rickettsiae. EID. 20(10): 1768–1769.
2. Labruna MB, Mattar S, Nava S, Bermudez S, Venzal JM, Dolz G, Abarca K, Romero L, de Sousa R, Oteo J, Zavala-Castro J (2011) Rickettsioses in Latin America, Caribbean, Spain and Portugal. Revista MVZ Córdoba. 16(2): 2435–2457.
3. Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM (1997) Flea-borne rickettsioses: ecologic considera-tions. Emerg Infect Dis. 3: 319–327.
4. Wedincamp J Jr, Foil LD (2002) Vertical transmission of Rickettsia felis in the cat flea (Ctenocephalides felis Bouche). J Vector Ecol. 27: 96–101.
5. Henry KM, Jiang J, Rozmajzl PJ, Azad AF, Macaluso KR, Richards AL (2007) Development of quantitative real-time PCR assays to detect Rickettsia typhi and Rickettsia felis, the causative agents of murine typhus and flea-borne spot-ted fever. Mol Cell Probes. 21: 17–23.
6. Boostrom A, Beier M, Macaluso JA, Macaluso KR, Sprenger D, Hayes J, Rad-ulovic S, Azad AF (2002) Geographic association of Rickettsia felis-infected opossums with human murine typhus, Texas. Emerg Infect Dis. 8: 549–554.
7. Schriefer M, Sacci Jr, Taylor JP, HigginsJA, Azad AF (1994) Murine typhus: updated roles of multiple urban com-ponents and asecond typhus-like Rick-ettsia. J Med Entomol. 31: 681–685.
8. Williams SG, Sacci JB, Schriefer ME, Andersen EM, Fujioka KK, Sorvillo FJ, Barr AR, Azad AF (1992) Typhus and typhus-like rickettsiae associated with opossums and their fleas in Los Angeles County, California. J. Clin. Microbiol. 30: 1758–1762.
9. Case JB, Chomel B, Nicholson W, Foley J (2006) Serological survey of vector-borne zoonotic pathogens in pet cats and cats from animal shelters and feral colonies. J Feline Med Surg. 8: 111–117.
10. Psaroulaki A, Antoniou M, Papaeustathi-ou A, Toumazos P, Loukaides F, Tse-lentis Y (2006) First detection of Rick-ettsia felis in Ctenocephalides felis fleas parasitizing rats in Cyprus. Am J Trop Med Hyg. 74: 120–122.
11. Pérez-Osorio CE, Zavala-Velázquez JE, León JJ, Zavala-Castro JE (2008) Rick-ettsia felis as emergent global threat for humans. Emerging Infect Dis. 14(7): 1019–1023.
12. Hidalgo M, Montoya V, Martínez A, Mercado M, De la Ossa A, Vélez C, Estrada G, Pérez JE, Faccini-Martínez AA, Labruna MB (2013) Flea-borne ri-ckettsioses in the North of Caldas pro-vince, Colombia. Vector Borne Zoono-tic Dis. 13: 289–294
13. Ramírez-Hernández A, Montoya V, Mar-tínez A, Pérez JE, Mercado M, de la Ossa A, Vélez C, Estrada G, Correa MI, Duque L (2013) Molecular detec-tion of Rickettsia felis in different flea species from Caldas, Colombia. Am J Trop Med Hyg. 89: 453–459.
14. Hidalgo M, Miranda J, Heredia D, Zam-brano P, Vesga JF, Lizarazo D, Mattar S, Valbuena G (2011) Outbreak of Rocky Mountain spotted fever in Córdoba, Co-lombia. Mem Inst Oswaldo Cruz. 106(1):
117–118.
15. Pacheco O, Giraldo R, Martínez M, Hi-dalgo M, Galeano A, Echeverri I, Ech-evarría L, Parra E, Rey G (2008) Estu-dio De Brote Febril Hemorrágico En El Village De Alto De Mulatos-Distrito Especial Portuario De Turbo, Antio-quia. Inf Quinc Epidemiol Nac Vol. 13: 145–160,
16. Furman DP, Catts EP (1982). Manual of medical entomology. Cambridge Uni-versity. (Ed. 4).
17. Wenzel R, Vernon. T (1966) Ectopara-sites of Panama, Field Museum of Nat-ural History.
18. Linardi PM, Guimarães LR (2000) Si-fonápteros do Brasil. Mus Zool da Univ São Paulo. São Paulo. pp. 48–53.
19. Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Am-blyomma cooperi ticks from an area in the State of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 42: 90–98.
20. Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of Rick-ettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 173: 1576–1589.
21. Roux V, Raoult D (2000) Phylogenetic analysis of members of the genus Rick-ettsia using the gene encoding the outer membrane protein rOmpB (ompB). Int J Syst Evol Microbiol. 50: 1449–1455.
22. Tamura K, Stecher G, Peterson D, Filip-ski A, Kumar S (2013) MEGA6: Mo-lecular evolutionary genetics analysis Version 6.0. Mol Biol Evol. 30(12): 2725–2729
23. Fredrik Ronquist, Maxim Teslenko, Paul van der Mark, Daniel L. Ayres, Aaron Darling, Sebastian Höhna, Bret Larget, Liang Liu, Marc A. Suchard, John P.Huelsenbeck (2012) MrBayes 3.2: Ef-ficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61(3): 539–542
24. Gehrke FS, Gazeta GS, Souza ER, Ribei-ro A, Marrelli MT, Schumaker TT (2009) Rickettsia rickettsii, Rickettsia felis and Rickettsia sp. TwKM03 in-fecting Rhipicephalus sanguineus and Ctenocephalides felis collected from dogs in a Brazilian potted fever focus in the State of Rio De Janeiro/Brazil. Clin Microbiol Infect. 15(Suppl 2): 267–268.
25. Abramowicz KF, Wekesa JW, Nwadike CN, Zambrano ML, Karpathy SE, Cec-il D, Burns J, Hu R, Eremeeva ME (2012) Rickettsia felis in cat fleas, Cten-ocephalides felis parasitizing opossums, San Bernardino County, California. Med Vet Entomol. 26: 458–462.
26. Tsai KH, Lu HY, Huang JH, Wang PJ, Wang HC, Huang CG, Wu WJ, Shu PY (2009) Rickettsia felis in cat fleas in Taiwan. Vector Borne Zoonotic Dis. 9: 561–563
27. Demeke T, Jenkins GR (2010) Influence of DNA extraction methods, PCR in-hibitors and quantification methods on realtime PCR assay of biotechnology derived traits. Anal Bioanal Chem. 396: 1977–1990.
28. Horta MC, Ogrzewalska M, Azevedo MC, Costa FB, Ferreira F, Labruna MB (2014) Rickettsia felis in Ctenocephalides felis felis from Five Geographic Regions of Brazil. Am J Trop Med Hyg. 91(1): 96–100.
29. Zavala-Velazquez J, Zavala-Castro J, Vado-Solis I, Ruiz-Sosa J, Moron C, Bouyer D, Walker D (2002) Identification of Ctenocephalides felis fleas as a host of Rickettsia felis, the agent of a spotted fever rickettsiosis in Yucatan, Mexico. Vector Borne Zoonotic Dis. 2: 69–75.
30. Troyo A, Álvarez D, Taylor L, Abdalla G,
Calderón-Arguedas Ó, Zambrano ML, Dasch GA, Lindblade K, Hun L, Ere-meeva ME (2012) Rickettsia felis in Ctenocephalides felis from Guatemala and Costa Rica. Am J Trop Med Hyg. 86: 1054–1056.
31. Venzal JM, Pérez‐Martínez L, Felix ML, Portillo A, Blanco JR, Oteo JA (2006) Prevalence of Rickettsia felis in Cten-ocephalides felis and Ctenocephalides canis from Uruguay. Ann N. Y Acad Sci. 1078: 305–308.
32. Hii SF, Kopp SR, Abdad MY, Thompson MF, O’Leary CA, Rees RL, Traub RJ (2011) Molecular Evidence Supports the Role of Dogs as Potential Reser-voirs for Rickettsia felis. Vector-Borne Zoonotic Dis. 8: 1007–1012.
33. Oteo JA, Portillo A, Santibáñez S, Blan-co JR, Pérez-Martínez L, Ibarra V (2006) Cluster of cases of human Rick-ettsia felis infection from Southern Eu-rope (Spain) diagnosed by PCR. J Clin Microbiol. 44(7): 2669–2671.
34. Sackal C, Laudisoit A, Kosoy M, Mas-sung R, Eremeeva ME, Karpathy SE, Van Wyk K, Gabitzsch E, Zeidner NS (2008) Bartonella spp. and Rickettsia felis in fleas, Democratic Republic of Congo. Emerg Infect Dis. 14: 1972–1974.
35. Faccini-Martínez AA, Forero-Becerra E, Cortés-Vecino J, Polo-Teran L, Jácome J, Vargas J, Valbuena G, Hidalgo M (2013) Caso probable de fiebre man-chada (Rickettsia felis) transmitida por pulgas. Biomédica. 33(1): 9–13.
36. Labruna MB, Walker D (2014) Rickett-sia felis and Changing Paradigms about Pathogenic Rickettsiae. EID. 20(10): 1768–1769.
| Files | ||
| Issue | Vol 13 No 1 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i1.927 | |
| Keywords | ||
| Rickettsia felis Fleas Dogs Rodents Ctenocephalides felis | ||
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How to Cite
1.
Contreras V, Londoño AF, Miranda J, Mattar S, Acevedo-Gutiérrez LY, Diaz FJ, Rodas JD. Infection by Rickettsia felis in Ctenocephalides felis felis Fleas from North of Colombia. J Arthropod Borne Dis. 2019;13(1):1.
