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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Norovirus infections in young children in Lusaka Province, Zambia: clinical characteristics and molecular epidemiology

Authors: Leigh M. Howard, Innocent Mwape, Mpanji Siwingwa, Michelo Simuyandi, M. Brad Guffey, Jeffrey S. A. Stringer, Benjamin H. Chi, Kathryn M. Edwards, Roma Chilengi

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

The burden, clinical features, and molecular epidemiology of norovirus infection in young children in southern Africa are not well defined.

Methods

Using data from a health facility-based surveillance study of children <5 years in Lusaka Province, Zambia presenting with diarrhea, we assessed the burden of norovirus infection. A convenience sample of 454 stool specimens was tested for norovirus using reverse-transcriptase polymerase chain reaction (RT-PCR). RT-PCR positive samples underwent additional nucleotide sequencing for genogroup and genotype identification. Clinical features and severity of diarrheal illnesses were compared between norovirus-positive and -negative subjects using Chi-squared and t-tests.

Results

Norovirus was detected in 52/454 (11.5%) specimens tested. Abdominal pain, fever, and vomiting were the most common presenting features in norovirus-associated illnesses. However, there were no significant differences in the clinical features of norovirus-positive compared to norovirus-negative illnesses. Of 43 isolates that were available for sequencing, 31 (72.1%) were genogroup II (GII) and 12 (27.9%) were genogroup I (GI). The distribution of genotypes was diverse.

Conclusions

Noroviruses were detected in approximately 10% of young children with diarrhea in the Lusaka Province of Zambia, with GII representing the majority of infections. These findings support the role of norovirus in symptomatic diarrhea disease in Africa. Further studies are needed to confirm these observations and to evaluate prevention strategies.
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Literature
1.
go back to reference Koo HL, Ajami N, Atmar RL, DuPont HL. Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med. 2010;10(50):61–70.PubMedPubMedCentral Koo HL, Ajami N, Atmar RL, DuPont HL. Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med. 2010;10(50):61–70.PubMedPubMedCentral
2.
3.
go back to reference Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725–30.CrossRefPubMed Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725–30.CrossRefPubMed
4.
go back to reference Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, et al. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med. 2013;368(12):1121–30.CrossRefPubMedPubMedCentral Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, et al. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med. 2013;368(12):1121–30.CrossRefPubMedPubMedCentral
5.
go back to reference Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A, DuPont HL, Atmar RL. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J Pediatr Infect Dis Soc. 2013;2(1):57–60.CrossRef Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A, DuPont HL, Atmar RL. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J Pediatr Infect Dis Soc. 2013;2(1):57–60.CrossRef
6.
go back to reference Chilengi R, Rudd C, Bolton C, Guffey B, Masumbu PK, Stringer J. Successes, challenges, and lessons learned in accelerating introduction of rotavirus immunisation in Zambia. World J Vaccines. 2015;5:43–53.CrossRef Chilengi R, Rudd C, Bolton C, Guffey B, Masumbu PK, Stringer J. Successes, challenges, and lessons learned in accelerating introduction of rotavirus immunisation in Zambia. World J Vaccines. 2015;5:43–53.CrossRef
7.
go back to reference Beres LK, Tate JE, Njobvu L, Chibwe B, Rudd C, Guffey MB, Stringer JS, Parashar UD, Chilengi R. A preliminary assessment of rotavirus vaccine effectiveness in Zambia. Clin Infect Dis. 2016;62 Suppl 2:S175–82.CrossRefPubMed Beres LK, Tate JE, Njobvu L, Chibwe B, Rudd C, Guffey MB, Stringer JS, Parashar UD, Chilengi R. A preliminary assessment of rotavirus vaccine effectiveness in Zambia. Clin Infect Dis. 2016;62 Suppl 2:S175–82.CrossRefPubMed
8.
go back to reference Beres LK, Tate JE, Njobvu L, Chilbwe B, Rudd C, Guffey M. Brad, Stringer, JAS, Parashar UD, Chilengi R. A preliminary assessment of rotavirus vaccine effectiveness in Zambia. Clin Infect Dis. 2016;62 Suppl 2:S175-82. Beres LK, Tate JE, Njobvu L, Chilbwe B, Rudd C, Guffey M. Brad, Stringer, JAS, Parashar UD, Chilengi R. A preliminary assessment of rotavirus vaccine effectiveness in Zambia. Clin Infect Dis. 2016;62 Suppl 2:S175-82.
9.
go back to reference Vinje J, Koopmans MP. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis. 1996;174(3):610–5.CrossRefPubMed Vinje J, Koopmans MP. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis. 1996;174(3):610–5.CrossRefPubMed
10.
go back to reference Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25.PubMed Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25.PubMed
11.
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(10):2731–9.CrossRefPubMedPubMedCentral 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(10):2731–9.CrossRefPubMedPubMedCentral
12.
go back to reference Zharkikh A, Li WH. Estimation of confidence in phylogeny: the complete-and-partial bootstrap technique. Mol Phylogenet Evol. 1995;4(1):44–63.CrossRefPubMed Zharkikh A, Li WH. Estimation of confidence in phylogeny: the complete-and-partial bootstrap technique. Mol Phylogenet Evol. 1995;4(1):44–63.CrossRefPubMed
13.
go back to reference Huhti L, Szakal ED, Puustinen L, Salminen M, Huhtala H, Valve O, Blazevic V, Vesikari T. Norovirus GII-4 causes a more severe gastroenteritis than other noroviruses in young children. J Infect Dis. 2011;203(10):1442–4.CrossRefPubMedPubMedCentral Huhti L, Szakal ED, Puustinen L, Salminen M, Huhtala H, Valve O, Blazevic V, Vesikari T. Norovirus GII-4 causes a more severe gastroenteritis than other noroviruses in young children. J Infect Dis. 2011;203(10):1442–4.CrossRefPubMedPubMedCentral
14.
go back to reference Ruuska T, Vesikari T. Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis. 1990;22(3):259–67.CrossRefPubMed Ruuska T, Vesikari T. Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand J Infect Dis. 1990;22(3):259–67.CrossRefPubMed
15.
go back to reference Wikswo ME, Desai R, Edwards KM, Staat MA, Szilagyi PG, Weinberg GA, Curns AT, Lopman B, Vinje J, Parashar UD, et al. Clinical profile of children with norovirus disease in rotavirus vaccine era. Emerg Infect Dis. 2013;19(10):1691–3.CrossRefPubMedPubMedCentral Wikswo ME, Desai R, Edwards KM, Staat MA, Szilagyi PG, Weinberg GA, Curns AT, Lopman B, Vinje J, Parashar UD, et al. Clinical profile of children with norovirus disease in rotavirus vaccine era. Emerg Infect Dis. 2013;19(10):1691–3.CrossRefPubMedPubMedCentral
16.
go back to reference Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case–control study. Lancet. 2013;382(9888):209–22.CrossRefPubMed Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case–control study. Lancet. 2013;382(9888):209–22.CrossRefPubMed
17.
go back to reference Platts-Mills JA, Babji S, Bodhidatta L, Gratz J, Haque R, Havt A, McCormick BJ, McGrath M, Olortegui MP, Samie A, et al. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob Health. 2015;3(9):e564–75.CrossRefPubMed Platts-Mills JA, Babji S, Bodhidatta L, Gratz J, Haque R, Havt A, McCormick BJ, McGrath M, Olortegui MP, Samie A, et al. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob Health. 2015;3(9):e564–75.CrossRefPubMed
18.
go back to reference Rouhani S, Penataro Yori P, Paredes Olortegui M, Siguas Salas M, Rengifo Trigoso D, Mondal D, Bodhidatta L, Platts-Mills J, Samie A, Kabir F, et al. Norovirus infection and acquired immunity in 8 countries: results from the MAL-ED study. Clin Infect Dis. 2016;62(10):1210–7.CrossRefPubMedPubMedCentral Rouhani S, Penataro Yori P, Paredes Olortegui M, Siguas Salas M, Rengifo Trigoso D, Mondal D, Bodhidatta L, Platts-Mills J, Samie A, Kabir F, et al. Norovirus infection and acquired immunity in 8 countries: results from the MAL-ED study. Clin Infect Dis. 2016;62(10):1210–7.CrossRefPubMedPubMedCentral
19.
go back to reference Breurec S, Vanel N, Bata P, Chartier L, Farra A, Favennec L, Franck T, Giles-Vernick T, Gody JC, Luong Nguyen LB, et al. Etiology and epidemiology of diarrhea in hospitalized children from low income country: a matched case–control study in Central African Republic. PLoS Negl Trop Dis. 2016;10(1):e0004283.CrossRefPubMedPubMedCentral Breurec S, Vanel N, Bata P, Chartier L, Farra A, Favennec L, Franck T, Giles-Vernick T, Gody JC, Luong Nguyen LB, et al. Etiology and epidemiology of diarrhea in hospitalized children from low income country: a matched case–control study in Central African Republic. PLoS Negl Trop Dis. 2016;10(1):e0004283.CrossRefPubMedPubMedCentral
20.
go back to reference Krumkamp R, Sarpong N, Schwarz NG, Adlkofer J, Loag W, Eibach D, Hagen RM, Adu-Sarkodie Y, Tannich E, May J. Gastrointestinal infections and diarrheal disease in Ghanaian infants and children: an outpatient case–control study. PLoS Negl Trop Dis. 2015;9(3):e0003568.CrossRefPubMedPubMedCentral Krumkamp R, Sarpong N, Schwarz NG, Adlkofer J, Loag W, Eibach D, Hagen RM, Adu-Sarkodie Y, Tannich E, May J. Gastrointestinal infections and diarrheal disease in Ghanaian infants and children: an outpatient case–control study. PLoS Negl Trop Dis. 2015;9(3):e0003568.CrossRefPubMedPubMedCentral
21.
go back to reference Kabayiza JC, Andersson ME, Nilsson S, Bergstrom T, Muhirwa G, Lindh M. Real-time PCR identification of agents causing diarrhea in Rwandan children less than 5 years of age. Pediatr Infect Dis J. 2014;33(10):1037–42.CrossRefPubMed Kabayiza JC, Andersson ME, Nilsson S, Bergstrom T, Muhirwa G, Lindh M. Real-time PCR identification of agents causing diarrhea in Rwandan children less than 5 years of age. Pediatr Infect Dis J. 2014;33(10):1037–42.CrossRefPubMed
22.
go back to reference Elfving K, Andersson M, Msellem MI, Welinder-Olsson C, Petzold M, Bjorkman A, Trollfors B, Martensson A, Lindh M. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J Clin Microbiol. 2014;52(3):916–23.CrossRefPubMedPubMedCentral Elfving K, Andersson M, Msellem MI, Welinder-Olsson C, Petzold M, Bjorkman A, Trollfors B, Martensson A, Lindh M. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J Clin Microbiol. 2014;52(3):916–23.CrossRefPubMedPubMedCentral
23.
go back to reference Trainor E, Lopman B, Iturriza-Gomara M, Dove W, Ngwira B, Nakagomi O, Nakagomi T, Parashar U, Cunliffe N. Detection and molecular characterisation of noroviruses in hospitalised children in Malawi, 1997–2007. J Med Virol. 2013;85(7):1299–306.CrossRefPubMed Trainor E, Lopman B, Iturriza-Gomara M, Dove W, Ngwira B, Nakagomi O, Nakagomi T, Parashar U, Cunliffe N. Detection and molecular characterisation of noroviruses in hospitalised children in Malawi, 1997–2007. J Med Virol. 2013;85(7):1299–306.CrossRefPubMed
24.
go back to reference Oluwatoyin Japhet M, Adeyemi Adesina O, Famurewa O, Svensson L, Nordgren J. Molecular epidemiology of rotavirus and norovirus in Ile-Ife, Nigeria: high prevalence of G12P[8] rotavirus strains and detection of a rare norovirus genotype. J Med Virol. 2012;84(9):1489–96.CrossRefPubMed Oluwatoyin Japhet M, Adeyemi Adesina O, Famurewa O, Svensson L, Nordgren J. Molecular epidemiology of rotavirus and norovirus in Ile-Ife, Nigeria: high prevalence of G12P[8] rotavirus strains and detection of a rare norovirus genotype. J Med Virol. 2012;84(9):1489–96.CrossRefPubMed
25.
go back to reference Mans J, de Villiers JC, du Plessis NM, Avenant T, Taylor MB. Emerging norovirus GII.4 2008 variant detected in hospitalised paediatric patients in South Africa. J Clin Virol. 2010;49(4):258–64.CrossRefPubMed Mans J, de Villiers JC, du Plessis NM, Avenant T, Taylor MB. Emerging norovirus GII.4 2008 variant detected in hospitalised paediatric patients in South Africa. J Clin Virol. 2010;49(4):258–64.CrossRefPubMed
26.
go back to reference Mattison K, Sebunya TK, Shukla A, Noliwe LN, Bidawid S. Molecular detection and characterization of noroviruses from children in Botswana. J Med Virol. 2010;82(2):321–4.CrossRefPubMed Mattison K, Sebunya TK, Shukla A, Noliwe LN, Bidawid S. Molecular detection and characterization of noroviruses from children in Botswana. J Med Virol. 2010;82(2):321–4.CrossRefPubMed
27.
go back to reference Huynen P, Mauroy A, Martin C, Savadogo LG, Boreux R, Thiry E, Melin P, De Mol P. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from Bobo Dioulasso, Burkina Faso. J Clin Virol. 2013;58(3):515–21.CrossRefPubMed Huynen P, Mauroy A, Martin C, Savadogo LG, Boreux R, Thiry E, Melin P, De Mol P. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from Bobo Dioulasso, Burkina Faso. J Clin Virol. 2013;58(3):515–21.CrossRefPubMed
28.
go back to reference Mans J, Murray TY, Nadan S, Netshikweta R, Page NA, Taylor MB. Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiol Infect. 2016;144(5):907–16.CrossRefPubMed Mans J, Murray TY, Nadan S, Netshikweta R, Page NA, Taylor MB. Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiol Infect. 2016;144(5):907–16.CrossRefPubMed
Metadata
Title
Norovirus infections in young children in Lusaka Province, Zambia: clinical characteristics and molecular epidemiology
Authors
Leigh M. Howard
Innocent Mwape
Mpanji Siwingwa
Michelo Simuyandi
M. Brad Guffey
Jeffrey S. A. Stringer
Benjamin H. Chi
Kathryn M. Edwards
Roma Chilengi
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2206-2

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