Skip to main content
Top
Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Viral aetiology influenza like illnesses in Santa Cruz, Bolivia (2010–2012)

Authors: Julie Delangue, Yelin Roca Sanchez, Géraldine Piorkowski, Maël Bessaud, Cécile Baronti, Laurence Thirion-Perrier, Roxana Loayza Mafayle, Cinthia Avila Ardaya, Gabriela Añez Aguilera, Jimmy Revollo Guzman, Javier Lora Riera, Xavier de Lamballerie

Published in: Virology Journal | Issue 1/2014

Login to get access

Abstract

Background

Acute respiratory infections represent a serious public health issue worldwide but virological aetiologies of Influenza Like Illnesses (ILIs) remain largely unknown in developing countries. This study represents the first attempt to characterise viral aetiologies of ILIs in Bolivia.

Methods

It was performed in Santa Cruz city from January 2010 to September 2012, based on 564 naso-pharyngeal swabs collected in a National Reference Laboratory and real-time PCR techniques, viral cultures and phylogenetic analyses.

Results

50.2% of samples were positive for at least one virus with influenza viruses (Flu A: ~15%; Flu B: ~9%), rhinoviruses (~8%), coronaviruses (~5%) and hRSV (~4%) being the most frequently identified. The pattern of viral infections varied according to age groups. The elucidation rate was the highest (>60%) amongst patients under 10 yo and the lowest (<40%) amongst patients ≥60 yo. Nearly 3% of samples showed dual viral infections. Epidemiological peaks were associated with a predominant virus but generally included 30-50% of infections by different viruses. Unexpectedly, the frequency of influenza in the 0–4 yo population was very low and a complete hRSV eclipse occurred in 2011. Genetic analyses indicated that distinct evolutionary lineages of Flu A(H1N1)pdm2009, Flu A/H3N2 and Flu B have co-circulated in Bolivia in the study period, originating from Central and North America, Europe, Asia and Australia.

Conclusion

Our results emphasise the requirement for a reinforced epidemiological and genetic follow-up of influenza and other ILIs in Bolivia to further inform the preparation of vaccines used in the region, guide vaccination campaigns and improve the medical management of patients.
Appendix
Available only for authorised users
Literature
1.
go back to reference Williams BG, Gouws E, Boschi-Pinto C, Bryce J, Dye C: Estimates of world-wide distribution of child deaths from acute respiratory infections. Lancet Infect Dis 2002, 2: 25-32. 10.1016/S1473-3099(01)00170-0PubMedCrossRef Williams BG, Gouws E, Boschi-Pinto C, Bryce J, Dye C: Estimates of world-wide distribution of child deaths from acute respiratory infections. Lancet Infect Dis 2002, 2: 25-32. 10.1016/S1473-3099(01)00170-0PubMedCrossRef
2.
go back to reference Bryce J, Boschi-Pinto C, Shibuya K, Black RE: WHO estimates of the causes of death in children. Lancet 2005, 365: 1147-1152. 10.1016/S0140-6736(05)71877-8PubMedCrossRef Bryce J, Boschi-Pinto C, Shibuya K, Black RE: WHO estimates of the causes of death in children. Lancet 2005, 365: 1147-1152. 10.1016/S0140-6736(05)71877-8PubMedCrossRef
3.
go back to reference Mulholland K: Global burden of acute respiratory infections in children: implications for interventions. Pediatr Pulmonol 2003, 36: 469-474. 10.1002/ppul.10344PubMedCrossRef Mulholland K: Global burden of acute respiratory infections in children: implications for interventions. Pediatr Pulmonol 2003, 36: 469-474. 10.1002/ppul.10344PubMedCrossRef
4.
go back to reference Ruuskanen O, Lahti E, Jennings LC, Murdoch DR: Viral pneumonia. Lancet 2011, 377: 1264-1275. 10.1016/S0140-6736(10)61459-6PubMedCrossRef Ruuskanen O, Lahti E, Jennings LC, Murdoch DR: Viral pneumonia. Lancet 2011, 377: 1264-1275. 10.1016/S0140-6736(10)61459-6PubMedCrossRef
5.
go back to reference Kieninger E, Regamey N: Rhinoviruses: markers of, or causative for, recurrent wheeze and asthma? Eur Respir J 2012, 39: 238-239. 10.1183/09031936.00181411PubMedCrossRef Kieninger E, Regamey N: Rhinoviruses: markers of, or causative for, recurrent wheeze and asthma? Eur Respir J 2012, 39: 238-239. 10.1183/09031936.00181411PubMedCrossRef
6.
go back to reference Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, Child Health Epidemiology Reference Group of WHO and UNICEF: Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012, 379: 2151-2161. 10.1016/S0140-6736(12)60560-1PubMedCrossRef Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, Child Health Epidemiology Reference Group of WHO and UNICEF: Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012, 379: 2151-2161. 10.1016/S0140-6736(12)60560-1PubMedCrossRef
7.
go back to reference Forshey BM, Laguna-Torres VA, Vilcarromero S, Bazan I, Rocha C, Morrison AC, Stoddard ST, Alegre Y, Gomez J, Scott TW, Kochel TJ: Epidemiology of influenza-like illness in the Amazon Basin of Peru, 2008–2009. Influenza Other Respi Viruses 2010, 4: 235-243. 10.1111/j.1750-2659.2010.00139.xCrossRef Forshey BM, Laguna-Torres VA, Vilcarromero S, Bazan I, Rocha C, Morrison AC, Stoddard ST, Alegre Y, Gomez J, Scott TW, Kochel TJ: Epidemiology of influenza-like illness in the Amazon Basin of Peru, 2008–2009. Influenza Other Respi Viruses 2010, 4: 235-243. 10.1111/j.1750-2659.2010.00139.xCrossRef
8.
go back to reference Douce RW, Aleman W, Chicaiza-Ayala W, Madrid C, Sovero M, Delgado F, Rodas M, Ampuero J, Chauca G, Perez J, Garcia J, Kochel T, Halsey ES, Laguna-Torres VA: Sentinel surveillance of influenza-like-illness in two cities of the tropical country of Ecuador: 2006–2010. PLoS One 2011, 6: e22206. 10.1371/journal.pone.0022206PubMedPubMedCentralCrossRef Douce RW, Aleman W, Chicaiza-Ayala W, Madrid C, Sovero M, Delgado F, Rodas M, Ampuero J, Chauca G, Perez J, Garcia J, Kochel T, Halsey ES, Laguna-Torres VA: Sentinel surveillance of influenza-like-illness in two cities of the tropical country of Ecuador: 2006–2010. PLoS One 2011, 6: e22206. 10.1371/journal.pone.0022206PubMedPubMedCentralCrossRef
10.
go back to reference Klimov AI, Garten R, Russell C, Barr IG, Besselaar TG, Daniels R, Engelhardt OG, Grohmann G, Itamura S, Kelso A, McCauley J, Odagiri T, Smith D, Tashiro M, Xu X, Webby R, Wang D, Ye Z, Yuelong S, Zhang W, Cox N, Writing Committee of the World Health Organization Consultation on Southern Hemisphere Influenza Vaccine Composition for 2012: WHO recommendations for the viruses to be used in the 2012 Southern Hemisphere Influenza Vaccine: Epidemiology, antigenic and genetic characteristics of influenza A(H1N1)pdm09, A(H3N2) and B influenza viruses collected from February to September 2011. Vaccine 2012, 30: 6461-6471. 10.1016/j.vaccine.2012.07.089PubMedCrossRef Klimov AI, Garten R, Russell C, Barr IG, Besselaar TG, Daniels R, Engelhardt OG, Grohmann G, Itamura S, Kelso A, McCauley J, Odagiri T, Smith D, Tashiro M, Xu X, Webby R, Wang D, Ye Z, Yuelong S, Zhang W, Cox N, Writing Committee of the World Health Organization Consultation on Southern Hemisphere Influenza Vaccine Composition for 2012: WHO recommendations for the viruses to be used in the 2012 Southern Hemisphere Influenza Vaccine: Epidemiology, antigenic and genetic characteristics of influenza A(H1N1)pdm09, A(H3N2) and B influenza viruses collected from February to September 2011. Vaccine 2012, 30: 6461-6471. 10.1016/j.vaccine.2012.07.089PubMedCrossRef
11.
go back to reference Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ: Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 2011, 119: 439-445.PubMedPubMedCentralCrossRef Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ: Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 2011, 119: 439-445.PubMedPubMedCentralCrossRef
12.
go back to reference Bellei N, Carraro E, Perosa A, Watanabe A, Arruda E, Granato C: Acute respiratory infection and influenza-like illness viral etiologies in Brazilian adults. J Med Virol 2008, 80: 1824-1827. 10.1002/jmv.21295PubMedCrossRef Bellei N, Carraro E, Perosa A, Watanabe A, Arruda E, Granato C: Acute respiratory infection and influenza-like illness viral etiologies in Brazilian adults. J Med Virol 2008, 80: 1824-1827. 10.1002/jmv.21295PubMedCrossRef
13.
go back to reference Freitas FT: Sentinel surveillance of influenza and other respiratory viruses, Brazil, 2000–2010. Braz J Infect Dis 2013, 17: 62-68. 10.1016/j.bjid.2012.09.001PubMedCrossRef Freitas FT: Sentinel surveillance of influenza and other respiratory viruses, Brazil, 2000–2010. Braz J Infect Dis 2013, 17: 62-68. 10.1016/j.bjid.2012.09.001PubMedCrossRef
14.
go back to reference Cabeca TK, Granato C, Bellei N: Epidemiological and clinical features of human coronavirus infections among different subsets of patients. Influenza Other Respi Viruses 2013, 7: 1040-1047. 10.1111/irv.12101CrossRef Cabeca TK, Granato C, Bellei N: Epidemiological and clinical features of human coronavirus infections among different subsets of patients. Influenza Other Respi Viruses 2013, 7: 1040-1047. 10.1111/irv.12101CrossRef
15.
go back to reference Albuquerque MC, Varella RB, Santos N: Acute respiratory viral infections in children in Rio de Janeiro and Teresopolis, Brazil. Rev Inst Med Trop Sao Paulo 2012, 54: 249-255. 10.1590/S0036-46652012000500003PubMedCrossRef Albuquerque MC, Varella RB, Santos N: Acute respiratory viral infections in children in Rio de Janeiro and Teresopolis, Brazil. Rev Inst Med Trop Sao Paulo 2012, 54: 249-255. 10.1590/S0036-46652012000500003PubMedCrossRef
16.
go back to reference Drexler JF, Grywna K, Lukashev A, Stocker A, Almeida PS, Wieseler J, Ribeiro TC, Petersen N, Ribeiro Hda C Jr, Belalov I, Kümmerer BM, Drosten C: Full genome sequence analysis of parechoviruses from Brazil reveals geographical patterns in the evolution of non-structural genes and intratypic recombination in the capsid region. J Gen Virol 2011, 92: 564-571. 10.1099/vir.0.022525-0PubMedCrossRef Drexler JF, Grywna K, Lukashev A, Stocker A, Almeida PS, Wieseler J, Ribeiro TC, Petersen N, Ribeiro Hda C Jr, Belalov I, Kümmerer BM, Drosten C: Full genome sequence analysis of parechoviruses from Brazil reveals geographical patterns in the evolution of non-structural genes and intratypic recombination in the capsid region. J Gen Virol 2011, 92: 564-571. 10.1099/vir.0.022525-0PubMedCrossRef
17.
go back to reference Ninove L, Nougairede A, Gazin C, Thirion L, Delogu I, Zandotti C, Charrel RN, De Lamballerie X: RNA and DNA bacteriophages as molecular diagnosis controls in clinical virology: a comprehensive study of more than 45,000 routine PCR tests. PLoS One 2011, 6: e16142. 10.1371/journal.pone.0016142PubMedPubMedCentralCrossRef Ninove L, Nougairede A, Gazin C, Thirion L, Delogu I, Zandotti C, Charrel RN, De Lamballerie X: RNA and DNA bacteriophages as molecular diagnosis controls in clinical virology: a comprehensive study of more than 45,000 routine PCR tests. PLoS One 2011, 6: e16142. 10.1371/journal.pone.0016142PubMedPubMedCentralCrossRef
18.
go back to reference van Elden LJ, Nijhuis M, Schipper P, Schuurman R, van Loon AM: Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J Clin Microbiol 2001, 39: 196-200. 10.1128/JCM.39.1.196-200.2001PubMedPubMedCentralCrossRef van Elden LJ, Nijhuis M, Schipper P, Schuurman R, van Loon AM: Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J Clin Microbiol 2001, 39: 196-200. 10.1128/JCM.39.1.196-200.2001PubMedPubMedCentralCrossRef
19.
go back to reference Ninove L, Gazin C, Gould EA, Nougairede A, Flahault A, Charrel RN, Zandotti C, de Lamballerie X: A simple method for molecular detection of Swine-origin and human-origin influenza a virus. Vector Borne Zoonotic Dis 2010, 10: 237-240. 10.1089/vbz.2009.0110PubMedCrossRef Ninove L, Gazin C, Gould EA, Nougairede A, Flahault A, Charrel RN, Zandotti C, de Lamballerie X: A simple method for molecular detection of Swine-origin and human-origin influenza a virus. Vector Borne Zoonotic Dis 2010, 10: 237-240. 10.1089/vbz.2009.0110PubMedCrossRef
20.
go back to reference Kuypers J, Wright N, Ferrenberg J, Huang ML, Cent A, Corey L, Morrow R: Comparison of real-time PCR assays with fluorescent-antibody assays for diagnosis of respiratory virus infections in children. J Clin Microbiol 2006, 44: 2382-2388. 10.1128/JCM.00216-06PubMedPubMedCentralCrossRef Kuypers J, Wright N, Ferrenberg J, Huang ML, Cent A, Corey L, Morrow R: Comparison of real-time PCR assays with fluorescent-antibody assays for diagnosis of respiratory virus infections in children. J Clin Microbiol 2006, 44: 2382-2388. 10.1128/JCM.00216-06PubMedPubMedCentralCrossRef
21.
go back to reference van Elden LJ, van Loon AM, van der Beek A, Hendriksen KA, Hoepelman AI, van Kraaij MG, Schipper P, Nijhuis M: Applicability of a real-time quantitative PCR assay for diagnosis of respiratory syncytial virus infection in immunocompromised adults. J Clin Microbiol 2003, 41: 4378-4381. 10.1128/JCM.41.9.4378-4381.2003PubMedPubMedCentralCrossRef van Elden LJ, van Loon AM, van der Beek A, Hendriksen KA, Hoepelman AI, van Kraaij MG, Schipper P, Nijhuis M: Applicability of a real-time quantitative PCR assay for diagnosis of respiratory syncytial virus infection in immunocompromised adults. J Clin Microbiol 2003, 41: 4378-4381. 10.1128/JCM.41.9.4378-4381.2003PubMedPubMedCentralCrossRef
22.
go back to reference van Elden LJ, van Loon AM, van Alphen F, Hendriksen KA, Hoepelman AI, van Kraaij MG, Oosterheert JJ, Schipper P, Schuurman R, Nijhuis M: Frequent detection of human coronaviruses in clinical specimens from patients with respiratory tract infection by use of a novel real-time reverse-transcriptase polymerase chain reaction. J Infect Dis 2004, 189: 652-657. 10.1086/381207PubMedCrossRef van Elden LJ, van Loon AM, van Alphen F, Hendriksen KA, Hoepelman AI, van Kraaij MG, Oosterheert JJ, Schipper P, Schuurman R, Nijhuis M: Frequent detection of human coronaviruses in clinical specimens from patients with respiratory tract infection by use of a novel real-time reverse-transcriptase polymerase chain reaction. J Infect Dis 2004, 189: 652-657. 10.1086/381207PubMedCrossRef
23.
go back to reference Garbino J, Gerbase MW, Wunderli W, Deffernez C, Thomas Y, Rochat T, Ninet B, Schrenzel J, Yerly S, Perrin L, Soccal PM, Nicod L, Kaiser L: Lower respiratory viral illnesses: improved diagnosis by molecular methods and clinical impact. Am J Respir Crit Care Med 2004, 170: 1197-1203. 10.1164/rccm.200406-781OCPubMedCrossRef Garbino J, Gerbase MW, Wunderli W, Deffernez C, Thomas Y, Rochat T, Ninet B, Schrenzel J, Yerly S, Perrin L, Soccal PM, Nicod L, Kaiser L: Lower respiratory viral illnesses: improved diagnosis by molecular methods and clinical impact. Am J Respir Crit Care Med 2004, 170: 1197-1203. 10.1164/rccm.200406-781OCPubMedCrossRef
24.
go back to reference Heim A, Ebnet C, Harste G, Pring-Akerblom P: Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol 2003, 70: 228-239. 10.1002/jmv.10382PubMedCrossRef Heim A, Ebnet C, Harste G, Pring-Akerblom P: Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol 2003, 70: 228-239. 10.1002/jmv.10382PubMedCrossRef
25.
go back to reference Bennett S, Harvala H, Witteveldt J, McWilliam Leitch EC, McLeish N, Templeton K, Gunson R, Carman WF, Simmonds P: Rapid simultaneous detection of enterovirus and parechovirus RNAs in clinical samples by one-step real-time reverse transcription-PCR assay. J Clin Microbiol 2011, 49: 2620-2624. 10.1128/JCM.02445-10PubMedPubMedCentralCrossRef Bennett S, Harvala H, Witteveldt J, McWilliam Leitch EC, McLeish N, Templeton K, Gunson R, Carman WF, Simmonds P: Rapid simultaneous detection of enterovirus and parechovirus RNAs in clinical samples by one-step real-time reverse transcription-PCR assay. J Clin Microbiol 2011, 49: 2620-2624. 10.1128/JCM.02445-10PubMedPubMedCentralCrossRef
26.
go back to reference Maertzdorf J, Wang CK, Brown JB, Quinto JD, Chu M, de Graaf M, van den Hoogen BG, Spaete R, Osterhaus AD, Fouchier RA: Real-time reverse transcriptase PCR assay for detection of human metapneumoviruses from all known genetic lineages. J Clin Microbiol 2004, 42: 981-986. 10.1128/JCM.42.3.981-986.2004PubMedPubMedCentralCrossRef Maertzdorf J, Wang CK, Brown JB, Quinto JD, Chu M, de Graaf M, van den Hoogen BG, Spaete R, Osterhaus AD, Fouchier RA: Real-time reverse transcriptase PCR assay for detection of human metapneumoviruses from all known genetic lineages. J Clin Microbiol 2004, 42: 981-986. 10.1128/JCM.42.3.981-986.2004PubMedPubMedCentralCrossRef
27.
go back to reference Lu X, Chittaganpitch M, Olsen SJ, Mackay IM, Sloots TP, Fry AM, Erdman DD: Real-time PCR assays for detection of bocavirus in human specimens. J Clin Microbiol 2006, 44: 3231-3235. 10.1128/JCM.00889-06PubMedPubMedCentralCrossRef Lu X, Chittaganpitch M, Olsen SJ, Mackay IM, Sloots TP, Fry AM, Erdman DD: Real-time PCR assays for detection of bocavirus in human specimens. J Clin Microbiol 2006, 44: 3231-3235. 10.1128/JCM.00889-06PubMedPubMedCentralCrossRef
28.
go back to reference Inoue E, Wang X, Osawa Y, Okazaki K: Full genomic amplification and subtyping of influenza A virus using a single set of universal primers. Microbiol Immunol 2010, 54: 129-134. 10.1111/j.1348-0421.2009.00193.xPubMedCrossRef Inoue E, Wang X, Osawa Y, Okazaki K: Full genomic amplification and subtyping of influenza A virus using a single set of universal primers. Microbiol Immunol 2010, 54: 129-134. 10.1111/j.1348-0421.2009.00193.xPubMedCrossRef
29.
go back to reference Li Q, Kun-yu W, Zi L, Ye Z, Jie D, Li-guo Z, Zhi-qing Z: Screening of the high yield influenza B virus on MDCK cell and cloning of its whole genome. Int Congr Ser 2004, 1263: 610-614.CrossRef Li Q, Kun-yu W, Zi L, Ye Z, Jie D, Li-guo Z, Zhi-qing Z: Screening of the high yield influenza B virus on MDCK cell and cloning of its whole genome. Int Congr Ser 2004, 1263: 610-614.CrossRef
30.
31.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28: 2731-2739. 10.1093/molbev/msr121PubMedPubMedCentralCrossRef Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28: 2731-2739. 10.1093/molbev/msr121PubMedPubMedCentralCrossRef
Metadata
Title
Viral aetiology influenza like illnesses in Santa Cruz, Bolivia (2010–2012)
Authors
Julie Delangue
Yelin Roca Sanchez
Géraldine Piorkowski
Maël Bessaud
Cécile Baronti
Laurence Thirion-Perrier
Roxana Loayza Mafayle
Cinthia Avila Ardaya
Gabriela Añez Aguilera
Jimmy Revollo Guzman
Javier Lora Riera
Xavier de Lamballerie
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-35

Other articles of this Issue 1/2014

Virology Journal 1/2014 Go to the issue