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Vol. 50, No. 5, 2007
Issue release date: October 2007
Intervirology 2007;50:347–352
(DOI:10.1159/000107272)

Evidence of Vertical Transmission of Dengue Virus in Two Endemic Localities in the State of Oaxaca, Mexico

Günther J.a · Martínez-Muñoz J.P.b · Pérez-Ishiwara D.G.a · Salas-Benito J.a
aPrograma Institucional de Biomedicina Molecular, Escuela Nacional de Medicina y Homeopatía, Instituto Politécnico Nacional, Mexico City, and bLaboratorio Estatal de Salud Pública del Estado de Oaxaca, Oaxaca City, Oaxaca, Mexico
email Corresponding Author

Abstract

Background: Dengue virus is spread in tropical areas of the world and is the causative agent of dengue fever and dengue hemorrhagic fever. It is horizontally transmitted to humans by infected Aedes mosquitoes, but it is also able to be vertically or transovarially transmitted to insect progeny. Objective: In this work, we analyzed the vertical transmission of dengue virus in Aedes aegypti mosquitoes collected in two endemic localities in the state of Oaxaca, Mexico. Methods: The collected larvae were grown in the laboratory and transovarial transmission of dengue virus, either in larvae or newly emerged mosquitoes, was investigated using a semi-nested reverse transcription-polymerase chain reaction method. Results: Although the presence of dengue virus in larvae could not be demonstrated, the viral genome was amplified in 4 out of 43 pools of in-cage born mosquitoes: DEN 2, 3 and 4 serotypes were detected in 2 pools from Tuxtepec and two from Juchitán. Conclusion: The results presented here strongly suggest that dengue virus can be vertically transmitted in mosquitoes from Oaxaca, but more studies will be necessary to analyze the epidemiological impact of this mechanism of transmission.


 goto top of outline Key Words

  • Transovarial transmission
  • Dengue
  • Aedes aegypti
  • Reverse transcription-polymerase chain reaction
  • Dengue virus

 goto top of outline Abstract

Background: Dengue virus is spread in tropical areas of the world and is the causative agent of dengue fever and dengue hemorrhagic fever. It is horizontally transmitted to humans by infected Aedes mosquitoes, but it is also able to be vertically or transovarially transmitted to insect progeny. Objective: In this work, we analyzed the vertical transmission of dengue virus in Aedes aegypti mosquitoes collected in two endemic localities in the state of Oaxaca, Mexico. Methods: The collected larvae were grown in the laboratory and transovarial transmission of dengue virus, either in larvae or newly emerged mosquitoes, was investigated using a semi-nested reverse transcription-polymerase chain reaction method. Results: Although the presence of dengue virus in larvae could not be demonstrated, the viral genome was amplified in 4 out of 43 pools of in-cage born mosquitoes: DEN 2, 3 and 4 serotypes were detected in 2 pools from Tuxtepec and two from Juchitán. Conclusion: The results presented here strongly suggest that dengue virus can be vertically transmitted in mosquitoes from Oaxaca, but more studies will be necessary to analyze the epidemiological impact of this mechanism of transmission.

Copyright © 2007 S. Karger AG, Basel


 goto top of outline References
  1. Malavige GN, Fernando S, Fernando DJ, Seneviratne SL: Dengue viral infections. Postgrad Med J 2004;80:588–601.
  2. Domingo-Carrasco C, Gascón-Bustrenga J: Dengue y otras fiebres hemorrágicas virales. Enferm Infecc Microbiol Clín 2005;23:615–626.
  3. Guha-Sapir D, Schimmer B: Dengue fever: new paradigms for a changing epidemiology. Emerg Themes Epidemiol 2005;2:1–10.

    External Resources

  4. Kouri G: El dengue, un problema creciente de salud en las Américas. Rev Panam Salud Publica 2006;19:143–145.

    External Resources

  5. Reinert JF, Harbach RE: Generic and subgeneric status of aedine mosquito species (Diptera: Culicidae: Aedini) occurring in the Australasian region. Zootaxa 2005;887:1–10.
  6. Chevillon C, Failloux AB: Questions on viral population biology to complete dengue puzzle. Trends Microbiol 2003;11:425–421.

    External Resources

  7. Sumanochitrapon W, Strickman D, Sithiprasasna R, Kittayapong P, Innis BL: Effect of size and geographic origin of Aedes aegypti on oral infection with dengue-2 virus. Am J Trop Med Hyg 1998;58:283–286.
  8. Rosen L, Shroyer DA, Tesh RB, Freier JE, Lien JC: Transovarial transmission of dengue virus by mosquitoes: Aedes albopictus and Aedes aegypti. Am J Trop Med Hyg 1983;32:1108–1119.
  9. Rosen L: Sexual transmission of dengue viruses by Aedes albopictus. Am J Trop Med Hyg 1987;37:398–402.
  10. Khin MM, Than KA: Transovarial transmission of dengue 2 virus by Aedes aegypti in nature. Am J Trop Med Hyg1983;32:590–594.
  11. Hull B, Tikasingh E, de Souza M, Martinez R: Natural transovarial transmission of dengue 4 virus in Aedes aegypti in Trinidad. Am J Trop Med Hyg 1984;33:1248–1250.
  12. Thenmozhi V, Tewari SC, Manavalan R, Balasubramanian A, Gajanana A: Natural vertical transmission of dengue viruses in Aedes aegypti in southern India. Trans R Soc Trop Med Hyg 2000;94:507.
  13. Fouque F, Garinci R, Gaborit P: Epidemiological and entomological surveillance of the co-circulation of DEN-1, DEN-2 and DEN-4 viruses in French Guiana. Trop Med Int Health 2004;9:41–46.
  14. Joshi V, Sharma RC, Sharma Y, Adha S, Sharma K, Singh H, Purohit A, Singhi M: Importance of socioeconomic status and tree holes in distribution of Aedes mosquitoes (Diptera: Culicidae) in Jodhpur, Rajasthan, India. J Med Entomol 2006;43:330–336.
  15. Joshi V, Mourya DT, Sharma RC: Persistence of dengue-3 virus through transovarial transmission passage in successive generations of Aedes aegypti mosquitoes. Am J Trop Med Hyg 2002;67:158–161.
  16. Gonçalves de Castro M, Ribeiro Noriega RM, Gonçalves Schatzmayr H, Pereira Miagostovich M, Lourenço-de-Oliveira R: Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 2004;99:809–814.
  17. Mourya DT, Gokhale MD, Basu A, Barde PV, Sapkal GN, Padbidri VS, Gore MM: Horizontal and vertical transmission of dengue virus type two in highly and lowly susceptible strains of Aedes aegypti mosquitoes. Acta Virol 2001;45:67–71.
  18. Secretaria de Salud: Panorama epidemiológico del dengue y dengue hemorrágico en entidades federativas. México (available in www.cenave.gob.mx) 2006, pp 1–27.
  19. Seah CLK, Chow VTK, Tan HC, Chan YC: Rapid, single-step RT-PCR typing of dengue viruses using five NS3 gene primers. J Virol Methods 1995;51:193–200.
  20. Chow VTK, Chan YC, Yong R, Lee KM, Lim LK, Chung YK, Lam-Phua SG, Tan BT: Monitoring of dengue viruses in field-caught Aedes aegypti and Aedes albopictus mosquitoes by a type-specific polymerase chain reaction and cycle sequencing. Am J Trop Med Hyg 1998;58:578–586.
  21. Gould EA, Clegg JCS: Growth, titration and purification of alphaviruses and flaviviruses; in Mahy BWJ (ed): Virology: A Practical Approach. Oxford, IRL Press, 1991, pp 43–78.
  22. Kuno G, Oliver A: Maintaining mosquito cell lines at high temperatures: effects on the replication of flaviviruses. In Vitro Cell Dev Biol 1989;25:193–196.
  23. Helt AM, Harris E: S-phase-dependent enhancement of dengue virus replication in mosquito cells, but not in human cells. J Virol 2005;79:13218–13230.
  24. Yocupicio-Monroy M, Padmanabhan R, Medina F, del Angel RM: Mosquito La protein binds to the 3′ untranslated region of the positive and negative polarity dengue virus RNAs and relocates to the cytoplasm of infected cells. Virology 2007;357:29–40.
  25. Walter SD, Hildreth SW, Beaty BJ: Estimation of infection rates in populations of organisms using pools of variable size. Am J Epidemiol 1980;112:124–128.
  26. Nasci RS, Mitchell CJ: Arbovirus titer variation in field-collected mosquitoes. J Am Mosq Control Assoc 1996;12:167–171.
  27. Katholi CR, Unnasch TR: Important experimental parameters for determining infection rates in arthropod vectors using pool screening approaches. Am J Trop Med Hyg 2006;74:779–785.
  28. Kuno G, Chang GJ: Biological transmission of arboviruses: re-examination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends. Clin Microbiol Rev 2005;18:608–637.
  29. Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, Weaver SC: Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 2000;74:3227–3234.
  30. Vasilakis N, Shell EJ, Fokam EB, Mason PW, Hanley KA, Estes DM, Weaver SC: Potential of ancestral sylvatic dengue-2 viruses to re-emerge. Virology 2007;358:402–412.
  31. Salvan M, Mouchet J: Aedes albopictus et Aedes aegypti a I’Ile de La Reunion. Ann Soc Belge Med Trop 1994;74:323–326.

 goto top of outline Author Contacts

Dr. Juan Salas-Benito, Escuela Nacional de Medicina y Homeopatía del IPN
Guillermo Massieu Helguera 239 Frac
La Escalera Ticomán, México D.F. 07320 (Mexico)
Tel. +52 55 5729 6000, ext. 55536, Fax +52 55 5729 6000, ext. 55500
E-Mail jsalasb@yahoo.com


 goto top of outline Article Information

Received: March 6, 2007
Accepted after revision: June 5, 2007
Published online: August 15, 2007
Number of Print Pages : 6
Number of Figures : 1, Number of Tables : 3, Number of References : 31


 goto top of outline Publication Details

Intervirology (International Journal of Basic and Medical Virology)

Vol. 50, No. 5, Year 2007 (Cover Date: October 2007)

Journal Editor: Liebert, U.G. (Leipzig)
ISSN: 0300–5526 (print), 1423–0100 (Online)

For additional information: http://www.karger.com/INT


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Background: Dengue virus is spread in tropical areas of the world and is the causative agent of dengue fever and dengue hemorrhagic fever. It is horizontally transmitted to humans by infected Aedes mosquitoes, but it is also able to be vertically or transovarially transmitted to insect progeny. Objective: In this work, we analyzed the vertical transmission of dengue virus in Aedes aegypti mosquitoes collected in two endemic localities in the state of Oaxaca, Mexico. Methods: The collected larvae were grown in the laboratory and transovarial transmission of dengue virus, either in larvae or newly emerged mosquitoes, was investigated using a semi-nested reverse transcription-polymerase chain reaction method. Results: Although the presence of dengue virus in larvae could not be demonstrated, the viral genome was amplified in 4 out of 43 pools of in-cage born mosquitoes: DEN 2, 3 and 4 serotypes were detected in 2 pools from Tuxtepec and two from Juchitán. Conclusion: The results presented here strongly suggest that dengue virus can be vertically transmitted in mosquitoes from Oaxaca, but more studies will be necessary to analyze the epidemiological impact of this mechanism of transmission.



 goto top of outline Author Contacts

Dr. Juan Salas-Benito, Escuela Nacional de Medicina y Homeopatía del IPN
Guillermo Massieu Helguera 239 Frac
La Escalera Ticomán, México D.F. 07320 (Mexico)
Tel. +52 55 5729 6000, ext. 55536, Fax +52 55 5729 6000, ext. 55500
E-Mail jsalasb@yahoo.com


 goto top of outline Article Information

Received: March 6, 2007
Accepted after revision: June 5, 2007
Published online: August 15, 2007
Number of Print Pages : 6
Number of Figures : 1, Number of Tables : 3, Number of References : 31


 goto top of outline Publication Details

Intervirology (International Journal of Basic and Medical Virology)

Vol. 50, No. 5, Year 2007 (Cover Date: October 2007)

Journal Editor: Liebert, U.G. (Leipzig)
ISSN: 0300–5526 (print), 1423–0100 (Online)

For additional information: http://www.karger.com/INT


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Malavige GN, Fernando S, Fernando DJ, Seneviratne SL: Dengue viral infections. Postgrad Med J 2004;80:588–601.
  2. Domingo-Carrasco C, Gascón-Bustrenga J: Dengue y otras fiebres hemorrágicas virales. Enferm Infecc Microbiol Clín 2005;23:615–626.
  3. Guha-Sapir D, Schimmer B: Dengue fever: new paradigms for a changing epidemiology. Emerg Themes Epidemiol 2005;2:1–10.

    External Resources

  4. Kouri G: El dengue, un problema creciente de salud en las Américas. Rev Panam Salud Publica 2006;19:143–145.

    External Resources

  5. Reinert JF, Harbach RE: Generic and subgeneric status of aedine mosquito species (Diptera: Culicidae: Aedini) occurring in the Australasian region. Zootaxa 2005;887:1–10.
  6. Chevillon C, Failloux AB: Questions on viral population biology to complete dengue puzzle. Trends Microbiol 2003;11:425–421.

    External Resources

  7. Sumanochitrapon W, Strickman D, Sithiprasasna R, Kittayapong P, Innis BL: Effect of size and geographic origin of Aedes aegypti on oral infection with dengue-2 virus. Am J Trop Med Hyg 1998;58:283–286.
  8. Rosen L, Shroyer DA, Tesh RB, Freier JE, Lien JC: Transovarial transmission of dengue virus by mosquitoes: Aedes albopictus and Aedes aegypti. Am J Trop Med Hyg 1983;32:1108–1119.
  9. Rosen L: Sexual transmission of dengue viruses by Aedes albopictus. Am J Trop Med Hyg 1987;37:398–402.
  10. Khin MM, Than KA: Transovarial transmission of dengue 2 virus by Aedes aegypti in nature. Am J Trop Med Hyg1983;32:590–594.
  11. Hull B, Tikasingh E, de Souza M, Martinez R: Natural transovarial transmission of dengue 4 virus in Aedes aegypti in Trinidad. Am J Trop Med Hyg 1984;33:1248–1250.
  12. Thenmozhi V, Tewari SC, Manavalan R, Balasubramanian A, Gajanana A: Natural vertical transmission of dengue viruses in Aedes aegypti in southern India. Trans R Soc Trop Med Hyg 2000;94:507.
  13. Fouque F, Garinci R, Gaborit P: Epidemiological and entomological surveillance of the co-circulation of DEN-1, DEN-2 and DEN-4 viruses in French Guiana. Trop Med Int Health 2004;9:41–46.
  14. Joshi V, Sharma RC, Sharma Y, Adha S, Sharma K, Singh H, Purohit A, Singhi M: Importance of socioeconomic status and tree holes in distribution of Aedes mosquitoes (Diptera: Culicidae) in Jodhpur, Rajasthan, India. J Med Entomol 2006;43:330–336.
  15. Joshi V, Mourya DT, Sharma RC: Persistence of dengue-3 virus through transovarial transmission passage in successive generations of Aedes aegypti mosquitoes. Am J Trop Med Hyg 2002;67:158–161.
  16. Gonçalves de Castro M, Ribeiro Noriega RM, Gonçalves Schatzmayr H, Pereira Miagostovich M, Lourenço-de-Oliveira R: Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 2004;99:809–814.
  17. Mourya DT, Gokhale MD, Basu A, Barde PV, Sapkal GN, Padbidri VS, Gore MM: Horizontal and vertical transmission of dengue virus type two in highly and lowly susceptible strains of Aedes aegypti mosquitoes. Acta Virol 2001;45:67–71.
  18. Secretaria de Salud: Panorama epidemiológico del dengue y dengue hemorrágico en entidades federativas. México (available in www.cenave.gob.mx) 2006, pp 1–27.
  19. Seah CLK, Chow VTK, Tan HC, Chan YC: Rapid, single-step RT-PCR typing of dengue viruses using five NS3 gene primers. J Virol Methods 1995;51:193–200.
  20. Chow VTK, Chan YC, Yong R, Lee KM, Lim LK, Chung YK, Lam-Phua SG, Tan BT: Monitoring of dengue viruses in field-caught Aedes aegypti and Aedes albopictus mosquitoes by a type-specific polymerase chain reaction and cycle sequencing. Am J Trop Med Hyg 1998;58:578–586.
  21. Gould EA, Clegg JCS: Growth, titration and purification of alphaviruses and flaviviruses; in Mahy BWJ (ed): Virology: A Practical Approach. Oxford, IRL Press, 1991, pp 43–78.
  22. Kuno G, Oliver A: Maintaining mosquito cell lines at high temperatures: effects on the replication of flaviviruses. In Vitro Cell Dev Biol 1989;25:193–196.
  23. Helt AM, Harris E: S-phase-dependent enhancement of dengue virus replication in mosquito cells, but not in human cells. J Virol 2005;79:13218–13230.
  24. Yocupicio-Monroy M, Padmanabhan R, Medina F, del Angel RM: Mosquito La protein binds to the 3′ untranslated region of the positive and negative polarity dengue virus RNAs and relocates to the cytoplasm of infected cells. Virology 2007;357:29–40.
  25. Walter SD, Hildreth SW, Beaty BJ: Estimation of infection rates in populations of organisms using pools of variable size. Am J Epidemiol 1980;112:124–128.
  26. Nasci RS, Mitchell CJ: Arbovirus titer variation in field-collected mosquitoes. J Am Mosq Control Assoc 1996;12:167–171.
  27. Katholi CR, Unnasch TR: Important experimental parameters for determining infection rates in arthropod vectors using pool screening approaches. Am J Trop Med Hyg 2006;74:779–785.
  28. Kuno G, Chang GJ: Biological transmission of arboviruses: re-examination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends. Clin Microbiol Rev 2005;18:608–637.
  29. Wang E, Ni H, Xu R, Barrett AD, Watowich SJ, Gubler DJ, Weaver SC: Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 2000;74:3227–3234.
  30. Vasilakis N, Shell EJ, Fokam EB, Mason PW, Hanley KA, Estes DM, Weaver SC: Potential of ancestral sylvatic dengue-2 viruses to re-emerge. Virology 2007;358:402–412.
  31. Salvan M, Mouchet J: Aedes albopictus et Aedes aegypti a I’Ile de La Reunion. Ann Soc Belge Med Trop 1994;74:323–326.