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Open Access 01-12-2020 | Research article

Rotavirus group A genotype circulation patterns across Kenya before and after nationwide vaccine introduction, 2010–2018

Authors: Mike J. Mwanga, Betty E. Owor, John B. Ochieng, Mwanajuma H. Ngama, Billy Ogwel, Clayton Onyango, Jane Juma, Regina Njeru, Elijah Gicheru, Grieven P. Otieno, Sammy Khagayi, Charles N. Agoti, Godfrey M. Bigogo, Richard Omore, O. Yaw Addo, Seheri Mapaseka, Jacqueline E. Tate, Umesh D. Parashar, Elizabeth Hunsperger, Jennifer R. Verani, Robert F. Breiman, D. James Nokes

Published in: BMC Infectious Diseases | Issue 1/2020

Abstract

Background

Kenya introduced the monovalent G1P [8] Rotarix® vaccine into the infant immunization schedule in July 2014. We examined trends in rotavirus group A (RVA) genotype distribution pre- (January 2010–June 2014) and post- (July 2014–December 2018) RVA vaccine introduction.

Methods

Stool samples were collected from children aged < 13 years from four surveillance sites across Kenya: Kilifi County Hospital, Tabitha Clinic Nairobi, Lwak Mission Hospital, and Siaya County Referral Hospital (children aged < 5 years only). Samples were screened for RVA using enzyme linked immunosorbent assay (ELISA) and VP7 and VP4 genes sequenced to infer genotypes.

Results

We genotyped 614 samples in pre-vaccine and 261 in post-vaccine introduction periods. During the pre-vaccine introduction period, the most frequent RVA genotypes were G1P [8] (45.8%), G8P [4] (15.8%), G9P [8] (13.2%), G2P [4] (7.0%) and G3P [6] (3.1%). In the post-vaccine introduction period, the most frequent genotypes were G1P [8] (52.1%), G2P [4] (20.7%) and G3P [8] (16.1%). Predominant genotypes varied by year and site in both pre and post-vaccine periods. Temporal genotype patterns showed an increase in prevalence of vaccine heterotypic genotypes, such as the commonly DS-1-like G2P [4] (7.0 to 20.7%, P < .001) and G3P [8] (1.3 to 16.1%, P < .001) genotypes in the post-vaccine introduction period. Additionally, we observed a decline in prevalence of genotypes G8P [4] (15.8 to 0.4%, P < .001) and G9P [8] (13.2 to 5.4%, P < .001) in the post-vaccine introduction period. Phylogenetic analysis of genotype G1P [8], revealed circulation of strains of lineages G1-I, G1-II and P [8]-1, P [8]-III and P [8]-IV. Considerable genetic diversity was observed between the pre and post-vaccine strains, evidenced by distinct clusters.

Conclusion

Genotype prevalence varied from before to after vaccine introduction. Such observations emphasize the need for long-term surveillance to monitor vaccine impact. These changes may represent natural secular variation or possible immuno-epidemiological changes arising from the introduction of the vaccine. Full genome sequencing could provide insights into post-vaccine evolutionary pressures and antigenic diversity.

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Troeger C, Forouzanfar M, Rao PC, Khalil I, Brown A, Reiner RC, et al. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the global burden of disease study 2015. Lancet Infect Dis [Internet]. 2017;17(9):909–48 Available from: https://www.thelancet.com/journals/laninf/article/PIIS1473-3099(17)30276-1/fulltext.

Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr. 2018;98121:1–8 Available from: http://archpedi.jamanetwork.com/article.aspx?doi=10.1001/jamapediatrics.2018.1960.

Tate JE, Burton AH, Boschi-Pinto C, Parashar UD, Agocs M, Serhan F, et al. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000-2013. Clin Infect Dis. 2016;62(Suppl 2):S96–105 Available from: https://academic.oup.com/cid/article/62/suppl_2/S96/2478843.PubMed

Desselberger U. Rotaviruses. Virus Res. 2014;190:75–96 Available from: https://www.sciencedirect.com/science/article/pii/S0168170214002640?via%3Dihub.PubMed

Metagenomics V. Virus classification [internet]. 2018. Available from: https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification.

Bányai K, László B, Duque J, Steele AD, Nelson EAS, Gentsch JR, et al. Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine. 2012;30(SUPPL. 1):A122–30 Available from: https://linkinghub.elsevier.com/retrieve/pii/S0264410X11015532.PubMed

Seheri LM, Magagula NB, Peenze I, Rakau K, Ndadza A, Mwenda JM, et al. Rotavirus strain diversity in Eastern and Southern African countries before and after vaccine introduction. Vaccine. 2017; Available from: https://doi.org/10.1016/j.vaccine.2017.11.068.

Mwenda JM, Ntoto KM, Abebe A, Enweronu-Laryea C, Amina I, Mchomvu J, et al. Burden and epidemiology of rotavirus diarrhea in selected African countries: preliminary results from the African Rotavirus Surveillance Network. J Infect Dis. 2010;202(Suppl 1):S5–11 Available from: https://academic.oup.com/jid/article/202/Supplement_1/S5/849136.PubMed

Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K, Rahman M, et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol. 2009;4(10):1303–16 Available from: https://academic.oup.com/jid/article/218/4/546/5001444.PubMed

10.

World Health Organization. Rotavirus vaccines WHO position paper - January 2013. Wkly Epidemiol Rec. 2013;88(5):49–64 Available from: http://www.who.int/wer/2013/wer8805.pdf.

11.

Mwenda JM, Parashar UD, Cohen AL, Tate JE. Impact of rotavirus vaccines in Sub-Saharan African countries. Vaccine. 2018; Available from: https://doi.org/10.1016/j.vaccine.2018.06.026.

12.

De Vos B, Han HH, Bouckenooghe A, Debrus S, Gillard P, Ward R, et al. Live attenuated human rotavirus vaccine, RIX4414, provides clinical protection in infants against rotavirus strains with and without shared G and P genotypes: integrated analysis of randomized controlled trials. Pediatr Infect Dis J. 2009;28(4):261–6 Available from: https://journals.lww.com/pidj/Abstract/2009/04000/Live_Attenuated_Human_Rotavirus_Vaccine,_RIX4414,.1.aspx.PubMed

13.

Wandera EA, Mohammad S, Bundi M, Nyangao J, Galata A, Kathiiko C, et al. Impact of rotavirus vaccination on rotavirus hospitalization rates among a resource-limited rural population in Mbita, Western Kenya. Trop Med Int Health. 2018;00(00):1–8 Available from: http://doi.wiley.com/10.1111/tmi.13040%0A. http://www.ncbi.nlm.nih.gov/pubmed/29432666.

14.

Khagayi S, Omore R, Otieno GP, Ogwel B, Ochieng JB, Juma J, et al. Effectiveness of Monovalent Rotavirus Vaccine Against Hospitalization With Acute Rotavirus Gastroenteritis in Kenyan Children. Clin Infect Dis. 2019; Available from: https://academic.oup.com/cid/advance-article/doi/10.1093/cid/ciz664/5536640.

15.

Otieno GP, Bottomley C, Khagayi S, Adetifa I, Ngama M, Omore R, et al. Impact of the introduction of rotavirus vaccine on hospital admissions for diarrhoea among children in Kenya: A controlled interrupted time series analysis. Clin Infect Dis [Internet]. 2019;(Cdc):1–8. Available from: https://academic.oup.com/cid/advance-article/doi/10.1093/cid/ciz912/5572563.

16.

Tate JE, Ngabo F, Donnen P, Gatera M, Uwimana J, Rugambwa C, et al. Effectiveness of Pentavalent rotavirus vaccine under conditions of routine use in Rwanda. Clin Infect Dis [Internet]. 2016;62(suppl 2):S208–12 Available from: https://academic.oup.com/cid/article-lookup/doi/10.1093/cid/civ1016.PubMed

17.

Bar-Zeev N, Kapanda L, Tate JE, Jere KC, Iturriza-Gomara M, Nakagomi O, et al. Effectiveness of a monovalent rotavirus vaccine in infants in Malawi after programmatic roll-out: an observational and case-control study. Lancet Infect Dis. 2015;15(4):422–8 Available from: https://www.thelancet.com/journals/laninf/article/PIIS1473-3099(14)71060-6/fulltext.PubMedPubMedCentral

18.

Armah G, Pringle K, Enweronu-Laryea CC, Ansong D, Mwenda JM, Diamenu SK, et al. Impact and effectiveness of monovalent rotavirus vaccine against severe rotavirus diarrhea in Ghana. Clin Infect Dis. 2016;62(April):S200–7 Available from: https://academic.oup.com/cid/article/62/suppl_2/S200/2478863.PubMed

19.

Scott JAG, Bauni E, Moisi JC, Ojal J, Gatakaa H, Nyundo C, et al. Profile: the Kilifi health and demographic surveillance system (KHDSS). Int J Epidemiol. 2012;41(3):650–7 Available from: https://academic.oup.com/ije/article/41/3/650/837001.PubMedPubMedCentral

20.

Nokes DJ, Abwao J, Pamba A, Peenze I, Dewar J, Maghenda JK, et al. Incidence and clinical characteristics of group a rotavirus infections among children admitted to hospital in Kilifi, Kenya. PLoS Med. 2008;5(7):1154–62 Available from: https://journals.plos.org/plosmedicine/article?id=10.1371/journal.pmed.0050153.

21.

Odhiambo FO, Laserson KF, Sewe M, Hamel MJ, Feikin DR, Adazu K, et al. Profile: the KEMRI/CDC health and demographic surveillance system-Western Kenya. Int J Epidemiol. 2012;41(4):977–87 Available from: https://academic.oup.com/ije/article/41/4/977/689203.PubMed

22.

Feikin DR, Olack B, Bigogo GM, Audi A, Cosmas L, Aura B, et al. The burden of common infectious disease syndromes at the clinic and household level from population-based surveillance in rural and urban Kenya. PLoS One. 2011;6(1):1–10 Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0016085.

23.

Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, et al. Identification of group a rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol. 1992;30(6):1365–73 Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC265294.PubMedPubMedCentral

24.

Gómara MI, Cubitt D, Desselberger U, Gray J. Amino acid substitution within the VP7 protein of G2 rotavirus strains associated with failure to serotype. J Clin Microbiol. 2001;39(10):3796–8 Available from: https://jcm.asm.org/content/39/10/3796.PubMedPubMedCentral

25.

Pickett BE, Greer DS, Zhang Y, Stewart L, Zhou L, Sun G, et al. Virus pathogen database and analysis resource (ViPR): a comprehensive bioinformatics database and analysis resource for the coronavirus research community. Viruses. 2012;4(11):3209–26 Available from: https://www.mdpi.com/1999-4915/4/11/3209.PubMedPubMedCentral

26.

John B O, Sammy K, Billy O, Reuben O, Evans A, Jane J, et al. Distribution of rotavirus genotypes among children with diarrhea prior to vaccine introduction in Western Kenya. J Infect Dis Epidemiol [Internet]. 2019 Mar 31;5(1). Available from: https://www.clinmedjournals.org/articles/jide/journal-of-infectious-diseases-and-epidemiology-jide-5-070.php?jid=jide.

27.

Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, et al. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol. 1990;28(2):276–82 Available from: https://jcm.asm.org/content/28/2/276.PubMedPubMedCentral

28.

Iturriza-Gómara M, Kang G, Gray J. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol. 2004;31(4):259–65 Available from: https://www.sciencedirect.com/science/article/abs/pii/S1386653204001520?via%3Dihub.PubMed

29.

Iturriza-gómara M, Green J, Brown DWG, Desselberger U, Gray JJ, Green JON, et al. Diversity within the VP4 gene of rotavirus P [8] strains : implications for reverse transcription-PCR genotyping. J Clin Microbiol. 2000;38(2):1–5 Available from: https://jcm.asm.org/content/38/2/898.

30.

Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2017;20(4):1–7 Available from: http://academic.oup.com/bib/article/doi/10.1093/bib/bbx108/4106928/MAFFT-online-service-multiple-sequence-alignment.

31.

Larsson A. AliView : a fast and lightweight alignment viewer and editor for large datasets. Oxford Univesity [Internet]. 2014;30(22):3276–8. Available from: https://academic.oup.com/bioinformatics/article/30/22/3276/2391211.

32.

Nguyen L, Schmidt HA, Haeseler A Von, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Oxford Univesity [Internet]. 2014;32(1):268–74. Available from: https://doi.org/10.1093/molbev/msu300.

33.

Cavanaugh JE. Model selection: Bayesian information criterion. Wiley StatsRef Stat Ref Online. 2016;2(20):1–3 Available from: http://doi.wiley.com/10.1002/9781118445112.stat00247.pub2.

34.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. Available from. https://doi.org/10.1093/molbev/msy096.PubMedPubMedCentralCrossRef

35.

Roczo-Farkas S, Kirkwood CD, Cowley D, Barnes GL, Bishop RF, Bogdanovic-Sakran N, et al. The impact of rotavirus vaccines on genotype diversity: a comprehensive analysis of 2 decades of Australian surveillance data. J Infect Dis. 2018;218(4):546–54 Available from: https://academic.oup.com/jid/article/218/4/546/5001444.PubMed

36.

Zeller M, Rahman M, Heylen E, De Coster S, De Vos S, Arijs I, et al. Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium. Vaccine. 2010;28(47):7507–13. Available from. https://doi.org/10.1016/j.vaccine.2010.09.004.PubMedCrossRef

37.

Gelaw A, Pietsch C, Liebert UG. Molecular epidemiology of rotaviruses in Northwest Ethiopia after national vaccine introduction. Infect Genet Evol. 2018;65(June):300–7. Available from. https://doi.org/10.1016/j.meegid.2018.08.016.PubMedCrossRef

38.

Rahajamanana VL, Raboba JL, Rakotozanany A, Razafindraibe NJ, Andriatahirintsoa EJPR, Razafindrakoto AC, et al. Impact of rotavirus vaccine on all-cause diarrhea and rotavirus hospitalizations in Madagascar. Vaccine. 2018;36(47):7198–204. Available from. https://doi.org/10.1016/j.vaccine.2017.08.091.PubMedCrossRef

39.

Utsumi T, Wahyuni RM, Doan YH, Dinana Z, Soegijanto S, Fujii Y, et al. Equine-like G3 rotavirus strains as predominant strains among children in Indonesia in 2015–2016. Infect Genet Evol. 2018;61(June):224–8. Available from. https://doi.org/10.1016/j.meegid.2018.03.027.PubMedCrossRef

40.

Steele AD, Victor JC, Carey ME, Tate JE, Atherly DE, Pecenka C, et al. Experiences with rotavirus vaccines: can we improve rotavirus vaccine impact in developing countries? Hum Vaccin Immunother. 2019;5515:1–13. Available from. https://doi.org/10.1080/21645515.2018.1553593.CrossRef

41.

Dóró R, Marton S, Bartókné AH, Lengyel G, Agócs Z, Jakab F, et al. Equine-like G3 rotavirus in Hungary, 2015 -is it a novel intergenogroup reassortant pandemic strain? Acta Microbiol Immunol Hung. 2016;63(2):243–55. Available from. https://doi.org/10.1556/030.63.2016.2.8.PubMedCrossRef

42.

Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol. 2008;82(7):3204–19 Available from: http://jvi.asm.org/cgi/doi/10.1128/JVI.02257-07.PubMedPubMedCentral

43.

Yen C, Figueroa JR, Uribe ES, del Carmen-Hernández L, Tate JE, Parashar UD, et al. Monovalent rotavirus vaccine provides protection against an emerging fully heterotypic G9P[4] rotavirus strain in Mexico. J Infect Dis. 2011;204(5):783–6 Available from: https://academic.oup.com/jid/article-lookup/doi/10.1093/infdis/jir390.PubMed

44.

Steele AD, Neuzil KM, Cunliffe NA, Madhi SA, Bos P, Ngwira B, et al. Human rotavirus vaccine Rotarix™ provides protection against diverse circulating rotavirus strains in African infants: a randomized controlled trial. BMC Infect Dis. 2012;12(1):213 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3462149&tool=pmcentrez&rendertype=abstract.PubMedPubMedCentral

45.

Matthijnssens J, Potgieter CA, Ciarlet M, Parreno V, Martella V, Banyai K, et al. Are human P [14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol. 2009;83(7):2917–29 Available from: http://jvi.asm.org/cgi/doi/10.1128/JVI.02246-08.PubMedPubMedCentral

46.

Carvalho-Costa FA, Araújo IT, Santos De Assis RM, Fialho AM, De Assis Martins CMM, Bóia MN, et al. Rotavirus genotype distribution after vaccine introduction, Rio de Janeiro, Brazil. Emerg Infect Dis. 2009;15(1):95–7 Available from: https://wwwnc.cdc.gov/eid/article/15/1/07-1136_article.PubMedPubMedCentral

47.

Mukaratirwa A, Berejena C, Nziramasanga P, Ticklay I, Gonah A, Nathoo K, et al. Distribution of rotavirus genotypes associated with acute diarrhoea in Zimbabwean children less than five years old before and after rotavirus vaccine introduction. Vaccine. 2018; Available from. https://doi.org/10.1016/j.vaccine.2018.03.069.

48.

Kaneko M, Takanashi S, Thongprachum A, Hanaoka N, Fujimoto T, Nagasawa K, et al. Identification of vaccine-derived rotavirus strains in children with acute gastroenteritis in Japan, 2012-2015. PLoS One. 2017;12(9):2012–5. Available from. https://doi.org/10.1371/journal.pone.0184067.CrossRef

49.

Payne DC, Edwards KM, Bowen MD, Keckley E, Peters J, Esona MD, et al. Sibling transmission of vaccine-derived rotavirus (RotaTeq) associated with rotavirus gastroenteritis. Pediatrics. 2010;125(2) Available from. https://doi.org/10.1542/peds.2009-1901.

50.

Bennett A, Pollock L, Jere KC, Pitzer VE, Lopman B, Parashar U, et al. Infrequent transmission of monovalent human rotavirus vaccine virus to household contacts of vaccinated infants in Malawi. J Infect Dis. 2019;219(11):1730–4. Available from. https://doi.org/10.1093/infdis/jiz002.PubMedPubMedCentralCrossRef

Title: Rotavirus group A genotype circulation patterns across Kenya before and after nationwide vaccine introduction, 2010–2018
Authors: Mike J. Mwanga
Betty E. Owor
John B. Ochieng
Mwanajuma H. Ngama
Billy Ogwel
Clayton Onyango
Jane Juma
Regina Njeru
Elijah Gicheru
Grieven P. Otieno
Sammy Khagayi
Charles N. Agoti
Godfrey M. Bigogo
Richard Omore
O. Yaw Addo
Seheri Mapaseka
Jacqueline E. Tate
Umesh D. Parashar
Elizabeth Hunsperger
Jennifer R. Verani
Robert F. Breiman
D. James Nokes
Publication date: 01-12-2020
Publisher: BioMed Central
Published in: BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-020-05230-0

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