Update on rotavirus vaccine underperformance in low- to middle-income countries and next-generation vaccines

References

• Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF, Ahmed T, Armah G, Bines JE, Brewer TG, Colombara DV, et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr. 2018;172:958–65. doi:10.1001/jamapediatrics.2018.1960.
   PubMed Web of Science ®Google Scholar
• Liu J, Platts-Mills JA, Juma J, Kabir F, Nkeze J, Okoi C, Operario DJ, Uddin J, Ahmed S, Alonso PL, et al. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. Lancet. 2016;388(10051):1291–301. doi:10.1016/S0140-6736(16)31529-X.
   PubMed Web of Science ®Google Scholar
• Platts-Mills JA, Liu J, Rogawski ET, Kabir F, Lertsethtakarn P, Siguas M, Khan SS, Praharaj I, Murei A, Nshama R, et al. Use of quantitative molecular diagnostic methods to assess the aetiology, burden, and clinical characteristics of diarrhoea in children in low-resource settings: a reanalysis of the MAL-ED cohort study. Lancet Glob Health. 2018;6(12):e1309–e18. doi:10.1016/S2214-109X(18)30349-8.
   PubMed Web of Science ®Google Scholar
• Clark A, Black R, Tate J, Roose A, Kotloff K, Lam D, Blackwelder W, Parashar U, Lanata C, Kang G, et al. Estimating global, regional and national rotavirus deaths in children aged <5 years: current approaches, new analyses and proposed improvements. PLoS One. 2017;12:e0183392.
   PubMed Web of Science ®Google Scholar
• Tate JE, Burton AH, Boschi-Pinto C, Parashar UD. World health organization-coordinated global rotavirus surveillance N. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000-2013. Clin Infect Dis. 2016;62:S96–S105.
   PubMed Web of Science ®Google Scholar
• Steele AD, Victor JC, Carey ME, Tate JE, Atherly DE, Pecenka C, Diaz Z, Parashar UD, Kirkwood CD. Experiences with rotavirus vaccines: can we improve rotavirus vaccine impact in developing countries? Hum Vaccin Immunother. 2019;15(6):1215–27. doi:10.1080/21645515.2018.1553593.
   PubMed Web of Science ®Google Scholar
• Estes MK. Principles of Mucosal Immunology. In: Smith PD, MacDonald TT, Blumberg RS, editors. Viral Infections: rotavirus infection. New York, NY: Garland Science; 2013. p. 377–80.
   Google Scholar
• Greenberg HB, Estes MK. Rotaviruses: from pathogenesis to vaccination. Gastroenterology. 2009;136(6):1939–51. doi:10.1053/j.gastro.2009.02.076.
   PubMed Web of Science ®Google Scholar
• Dennehy PH. Rotavirus vaccines: an overview. Clin Microbiol Rev. 2008;21(1):198–208. doi:10.1128/CMR.00029-07.
   PubMed Web of Science ®Google Scholar
• Crawford SE, Ramani S, Tate JE, Parashar UD, Svensson L, Hagbom M, Franco MA, Greenberg HB, O’Ryan M, Kang G, et al. Rotavirus infection. Nat Rev Dis Primers. 2017;3:17083.
   PubMed Web of Science ®Google Scholar
• Hagbom M, Istrate C, Engblom D, Karlsson T, Rodriguez-Diaz J, Buesa J, Taylor JA, Loitto VM, Magnusson KE, Ahlman H, et al. Rotavirus stimulates release of serotonin (5-HT) from human enterochromaffin cells and activates brain structures involved in nausea and vomiting. PLoS Pathog. 2011;7:e1002115. doi:10.1371/journal.ppat.1002115.
   PubMed Web of Science ®Google Scholar
• Angel J, Franco MA, Greenberg HB. Rotavirus vaccines: recent developments and future considerations. Nat Rev Microbiol. 2007;5:529–39.
   PubMed Web of Science ®Google Scholar
• Dennehy PH. Transmission of rotavirus and other enteric pathogens in the home. Pediatr Infect Dis J. 2000;19(Supplement):S103–5. doi:10.1097/00006454-200010001-00003.
   PubMedGoogle Scholar
• Velazquez FR, Matson DO, Calva JJ, Guerrero L, Morrow AL, Carter-Campbell S, Glass RI, Estes MK, Pickering LK, Ruiz-Palacios GM. Rotavirus infection in infants as protection against subsequent infections. N Engl J Med. 1996;335(14):1022–28. doi:10.1056/NEJM199610033351404.
   PubMed Web of Science ®Google Scholar
• Gladstone BP, Ramani S, Mukhopadhya I, Muliyil J, Sarkar R, Rehman AM, Jaffar S, Gomara MI, Gray JJ, Brown DW, et al. Protective effect of natural rotavirus infection in an Indian birth cohort. N Engl J Med. 2011;365(4):337–46. doi:10.1056/NEJMoa1006261.
   PubMed Web of Science ®Google Scholar
• Ramig RF. Pathogenesis of intestinal and systemic rotavirus infection. J Virol. 2004;78(19):10213–20. doi:10.1128/JVI.78.19.10213-10220.2004.
   PubMed Web of Science ®Google Scholar
• Payne DC, Parashar U. Chapter 13: rotavirus. Roush SW, Baldy LB, Kirkconnell Hall MA, editors. Manual for the surveillance of vaccine-preventable diseases: centers for disease control and prevention, Last reviewed. May18 2018.
   Google Scholar
• WHO Prequalified Vaccines. 2020 September 9 [accessed 2020 September 10]. https://extranet.who.int/pqvdata/.
   Google Scholar
• Ruiz-Palacios GM, Perez-Schael I, Velazquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, et al. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med. 2006;354(1):11–22. doi:10.1056/NEJMoa052434.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, Dallas MJ, Heyse JF, Goveia MG, Black SB, et al. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006;354:23–33. doi:10.1056/NEJMoa052664.
   PubMed Web of Science ®Google Scholar
• Armah GE, Sow SO, Breiman RF, Dallas MJ, Tapia MD, Feikin DR, Binka FN, Steele AD, Laserson KF, Ansah NA, et al. Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, double-blind, placebo-controlled trial. Lancet. 2010;376(9741):606–14. doi:10.1016/S0140-6736(10)60889-6.
   PubMed Web of Science ®Google Scholar
• Colgate ER, Haque R, Dickson DM, Carmolli MP, Mychaleckyj JC, Nayak U, Qadri F, Alam M, Walsh MC, Diehl SA, et al. Delayed dosing of oral rotavirus vaccine demonstrates decreased risk of rotavirus gastroenteritis associated with serum zinc: a randomized controlled trial. Clin Infect Dis. 2016;63(5):634–41. doi:10.1093/cid/ciw346.
   PubMed Web of Science ®Google Scholar
• Madhi SA, Cunliffe NA, Steele D, Witte D, Kirsten M, Louw C, Ngwira B, Victor JC, Gillard PH, Cheuvart BB, et al. Effect of human rotavirus vaccine on severe diarrhea in African infants. N Engl J Med. 2010;362(4):289–98. doi:10.1056/NEJMoa0904797.
   PubMed Web of Science ®Google Scholar
• Zaman K, Dang DA, Victor JC, Shin S, Yunus M, Dallas MJ, Podder G, Vu DT, Le TP, Luby SP, et al. Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial. Lancet. 2010;376:615–23. doi:10.1016/S0140-6736(10)60755-6.
   PubMed Web of Science ®Google Scholar
• WHO.Rotavirus vaccines:an update. Wkly Epidemiol Rec. 2009; 84: 533–40.
   PubMedGoogle Scholar
• Jonesteller CL, Burnett E, Yen C, Tate JE, Parashar UD. Effectiveness of rotavirus vaccination: a systematic review of the first decade of global postlicensure data, 2006-2016. Clin Infect Dis. 2017;65:840–50. doi:10.1093/cid/cix369.
   PubMed Web of Science ®Google Scholar
• Zaman K, Sack DA, Neuzil KM, Yunus M, Moulton LH, Sugimoto JD, Fleming JA, Hossain I, Arifeen SE, Azim T, et al. Effectiveness of a live oral human rotavirus vaccine after programmatic introduction in Bangladesh: A cluster-randomized trial. PLoS Med. 2017;14(4):e1002282. doi:10.1371/journal.pmed.1002282.
   PubMed Web of Science ®Google Scholar
• Bonkoungou IJO, Aliabadi N, Leshem E, Kam M, Nezien D, Drabo MK, Nikiema M, Ouedraogo B, Medah I, Konate S, et al. Impact and effectiveness of pentavalent rotavirus vaccine in children <5years of age in Burkina Faso. Vaccine. 2018;36:7170–78.
   PubMed Web of Science ®Google Scholar
• Ali Z, Harastani H, Hammadi M, Reslan L, Ghanem S, Hajar F, Sabra A, Haidar A, Inati A, Rajab M, et al. Rotavirus genotypes and vaccine effectiveness from a sentinel, hospital-based, surveillance study for three consecutive rotavirus seasons in Lebanon. PLoS One. 2016;11(8):e0161345. doi:10.1371/journal.pone.0161345.
   PubMed Web of Science ®Google Scholar
• Bennett A, Pollock L, Jere KC, Pitzer VE, Parashar U, Tate JE, Heyderman RS, Mwansambo C, French N, Nakagomi O, et al. Direct and possible indirect effects of vaccination on rotavirus hospitalisations among children in Malawi four years after programmatic introduction. Vaccine. 2018;36(47):7142–48. doi:10.1016/j.vaccine.2018.04.030.
   PubMedGoogle Scholar
• Lopez AL, Daag JV, Esparagoza J, Bonifacio J, Fox K, Nyambat B, Parashar UD, Ducusin MJ, Tate JE. Effectiveness of monovalent rotavirus vaccine in the Philippines. Sci Rep. 2018;8(1):14291. doi:10.1038/s41598-018-32595-9.
   PubMed Web of Science ®Google Scholar
• Jani B, Hokororo A, McHomvu J, Cortese MM, Kamugisha C, Mujuni D, Kallovya D, Parashar UD, Mwenda JM, Lyimo D, et al. Detection of rotavirus before and after monovalent rotavirus vaccine introduction and vaccine effectiveness among children in mainland Tanzania. Vaccine. 2018;36(47):7149–56. doi:10.1016/j.vaccine.2018.01.071.
   PubMedGoogle Scholar
• Platts-Mills JA, Amour C, Gratz J, Nshama R, Walongo T, Mujaga B, Maro A, McMurry TL, Liu J, Mduma E, et al. Impact of rotavirus vaccine introduction and postintroduction etiology of diarrhea requiring hospital admission in Haydom, Tanzania, a rural African setting. Clin Infect Dis. 2017;65(7):1144–51. doi:10.1093/cid/cix494.
   PubMed Web of Science ®Google Scholar
• Tharmaphornpilas P, Jiamsiri S, Boonchaiya S, Rochanathimoke O, Thinyounyong W, Tuntiwitayapun S, Guntapong R, Riewpaiboon A, Rasdjarmrearnsook AO, Glass RI. Evaluating the first introduction of rotavirus vaccine in Thailand: moving from evidence to policy. Vaccine. 2017;35:796–801. doi:10.1016/j.vaccine.2016.12.043.
   PubMed Web of Science ®Google Scholar
• Mujuru HA, Burnett E, Nathoo KJ, Ticklay I, Gonah NA, Mukaratirwa A, Berejena C, Manangazira P, Rupfutse M, Weldegebriel GG, et al. Monovalent rotavirus vaccine effectiveness against rotavirus hospitalizations among children in Zimbabwe. Clin Infect Dis. 2019;69(8):1339–44. doi:10.1093/cid/ciy1096.
   PubMed Web of Science ®Google Scholar
• Burnett E, Parashar UD, Tate JE. Global impact of rotavirus vaccination on diarrhea hospitalizations and deaths among children <5 years old: 2006-2019. J Infect Dis. 2020. doi:10.1093/infdis/jiaa081.
   Web of Science ®Google Scholar
• Aliabadi N, Antoni S, Mwenda JM, Weldegebriel G, Biey JNM, Cheikh D, Fahmy K, Teleb N, Ashmony HA, Ahmed H, et al. Global impact of rotavirus vaccine introduction on rotavirus hospitalisations among children under 5 years of age, 2008-16: findings from the global rotavirus surveillance Network. Lancet Glob Health. 2019;7:e893–e903. doi:10.1016/S2214-109X(19)30207-4.
   PubMed Web of Science ®Google Scholar
• Shioda K, de Oliveira LH, Sanwogou J, Rey-Benito G, Nunez Azzad D, Castillo RE, Gamarra Ramirez ML, Von Horoch MR, Weinberger DM, Pitzer VE. Identifying signatures of the impact of rotavirus vaccines on hospitalizations using sentinel surveillance data from Latin American countries. Vaccine. 2020;38(2):323–29. doi:10.1016/j.vaccine.2019.10.010.
   PubMed Web of Science ®Google Scholar
• Weldegebriel G, Mwenda JM, Chakauya J, Daniel F, Masresha B, Parashar UD, Tate JE. Impact of rotavirus vaccine on rotavirus diarrhoea in countries of East and Southern Africa. Vaccine. 2018;36(47):7124–30. doi:10.1016/j.vaccine.2017.10.050.
   PubMedGoogle Scholar
• Bar-Zeev N, King C, Phiri T, Beard J, Mvula H, Crampin AC, Heinsbroek E, Lewycka S, Tate JE, Parashar UD, et al. Impact of monovalent rotavirus vaccine on diarrhoea-associated post-neonatal infant mortality in rural communities in Malawi: a population-based birth cohort study. Lancet Glob Health. 2018;6(9):e1036–e44. doi:10.1016/S2214-109X(18)30314-0.
   PubMed Web of Science ®Google Scholar
• Inchauste L, Patzi M, Halvorsen K, Solano S, Montesano R, Iniguez V. Impact of rotavirus vaccination on child mortality, morbidity, and rotavirus-related hospitalizations in Bolivia. Int J Infect Dis. 2017;61:79–88. doi:10.1016/j.ijid.2017.06.006.
   PubMed Web of Science ®Google Scholar
• Shah MP, Tate JE, Mwenda JM, Steele AD, Parashar UD. Estimated reductions in hospitalizations and deaths from childhood diarrhea following implementation of rotavirus vaccination in Africa. Expert Rev Vaccines. 2017;16(10):987–95. doi:10.1080/14760584.2017.1371595.
   PubMed Web of Science ®Google Scholar
• Burnett E, Tate JE, Kirkwood CD, Nelson EAS, Santosham M, Steele AD, Parashar UD. Estimated impact of rotavirus vaccine on hospitalizations and deaths from rotavirus diarrhea among children <5 in Asia. Expert Rev Vaccines. 2018;17:453–60.
   PubMed Web of Science ®Google Scholar
• Rosettie KL, Vos T, Mokdad AH, Flaxman AD, Khalil I, Troeger C, Weaver MR. Indirect rotavirus vaccine effectiveness for the prevention of rotavirus hospitalization: a systematic review and meta-analysis. Am J Trop Med Hyg. 2018;98(4):1197–201. doi:10.4269/ajtmh.17-0705.
   PubMed Web of Science ®Google Scholar
• Saha S, Santosham M, Hussain M, Black RE, Saha SK. Rotavirus vaccine will improve child survival by more than just preventing diarrhea: evidence from Bangladesh. Am J Trop Med Hyg. 2018;98(2):360–63. doi:10.4269/ajtmh.17-0586.
   PubMed Web of Science ®Google Scholar
• Bhandari N, Rongsen-Chandola T, Bavdekar A, John J, Antony K, Taneja S, Goyal N, Kawade A, Kang G, Rathore SS, et al. Efficacy of a monovalent human-bovine (116E) rotavirus vaccine in Indian infants: a randomised, double-blind, placebo-controlled trial. Lancet. 2014;383(9935):2136–43. doi:10.1016/S0140-6736(13)62630-6.
   PubMed Web of Science ®Google Scholar
• Bhandari N, Rongsen-Chandola T, Bavdekar A, John J, Antony K, Taneja S, Goyal N, Kawade A, Kang G, Rathore SS, et al. Efficacy of a monovalent human-bovine (116E) rotavirus vaccine in Indian children in the second year of life. Vaccine. 2014;32(Suppl 1):A110–6. doi:10.1016/j.vaccine.2014.04.079.
   PubMed Web of Science ®Google Scholar
• Naik SP, Zade JK, Sabale RN, Pisal SS, Menon R, Bankar SG, Gairola S, Dhere RM. Stability of heat stable, live attenuated Rotavirus vaccine (ROTASIIL®). Vaccine. 2017;35(22):2962–69. doi:10.1016/j.vaccine.2017.04.025.
   PubMed Web of Science ®Google Scholar
• Isanaka S, Guindo O, Langendorf C, Matar Seck A, Plikaytis BD, Sayinzoga-Makombe N, McNeal MM, Meyer N, Adehossi E, Djibo A, et al. Efficacy of a low-cost, heat-stable oral rotavirus vaccine in Niger. N Engl J Med. 2017;376(12):1121–30. doi:10.1056/NEJMoa1609462.
   PubMed Web of Science ®Google Scholar
• Kulkarni PS, Desai S, Tewari T, Kawade A, Goyal N, Garg BS, Kumar D, Kanungo S, Kamat V, Kang G, et al. A randomized Phase III clinical trial to assess the efficacy of a bovine-human reassortant pentavalent rotavirus vaccine in Indian infants. Vaccine. 2017;35(45):6228–37. doi:10.1016/j.vaccine.2017.09.014.
   PubMed Web of Science ®Google Scholar
• Rathi N, Desai S, Kawade A, Venkatramanan P, Kundu R, Lalwani SK, Dubey AP, Venkateswara Rao J, Narayanappa D, Ghildiyal R, et al. A Phase III open-label, randomized, active controlled clinical study to assess safety, immunogenicity and lot-to-lot consistency of a bovine-human reassortant pentavalent rotavirus vaccine in Indian infants. Vaccine. 2018;36(52):7943–49. doi:10.1016/j.vaccine.2018.11.006.
   PubMed Web of Science ®Google Scholar
• Kawade A, Babji S, Kamath V, Raut A, Kumar CM, Kundu R, Venkatramanan P, Lalwani SK, Bavdekar A, Juvekar S, et al. Immunogenicity and lot-to-lot consistency of a ready to use liquid bovine-human reassortant pentavalent rotavirus vaccine (ROTASIIL - Liquid) in Indian infants. Vaccine. 2019;37(19):2554–60. doi:10.1016/j.vaccine.2019.03.067.
   PubMed Web of Science ®Google Scholar
• Malik A, Haldar P, Ray A, Shet A, Kapuria B, Bhadana S, Santosham M, Ghosh RS, Steinglass R, Kumar R. Introducing rotavirus vaccine in the universal immunization programme in India: from evidence to policy to implementation. Vaccine. 2019;37(39):5817–24. doi:10.1016/j.vaccine.2019.07.104.
   PubMed Web of Science ®Google Scholar
• Debellut F, Jaber S, Bouzya Y, Sabbah J, Barham M, Abu-Awwad F, Hjaija D, Ramlawi A, Pecenka C, Clark A, et al. Introduction of rotavirus vaccination in Palestine: an evaluation of the costs, impact, and cost-effectiveness of ROTARIX and ROTAVAC. PLoS One. 2020;15(2):e0228506. doi:10.1371/journal.pone.0228506.
   PubMed Web of Science ®Google Scholar
• Kirkwood CD, Steele AD. Rotavirus vaccines in China: improvement still required. JAMA Netw Open. 2018;1(4):e181579. doi:10.1001/jamanetworkopen.2018.1579.
   PubMed Web of Science ®Google Scholar
• Fu C, Wang M, Liang J, He T, Wang D, Xu J. Effectiveness of Lanzhou lamb rotavirus vaccine against rotavirus gastroenteritis requiring hospitalization: a matched case-control study. Vaccine. 2007;25(52):8756–61. doi:10.1016/j.vaccine.2007.10.036.
   PubMed Web of Science ®Google Scholar
• Li J, Zhang Y, Yang Y, Liang Z, Tian Y, Liu B, Gao Z, Jia L, Chen L, Wang Q. Effectiveness of Lanzhou lamb rotavirus vaccine in preventing gastroenteritis among children younger than 5 years of age. Vaccine. 2019;37:3611–16. doi:10.1016/j.vaccine.2019.03.069.
   PubMed Web of Science ®Google Scholar
• Fu C, He Q, Xu J, Xie H, Ding P, Hu W, Dong Z, Liu X, Wang M. Effectiveness of the Lanzhou lamb rotavirus vaccine against gastroenteritis among children. Vaccine. 2012;31(1):154–58. doi:10.1016/j.vaccine.2012.10.078.
   PubMed Web of Science ®Google Scholar
• Fu C, Tate JE, Jiang B. Effectiveness of Lanzhou lamb rotavirus vaccine against hospitalized gastroenteritis: further analysis and update. Hum Vaccin. 2010;6:953. doi:10.4161/hv.6.11.12847.
   PubMed Web of Science ®Google Scholar
• Zhen SS, Li Y, Wang SM, Zhang XJ, Hao ZY, Chen Y, Wang D, Zhang YH, Zhang ZY, Ma JC, et al. Effectiveness of the live attenuated rotavirus vaccine produced by a domestic manufacturer in China studied using a population-based case-control design. Emerg Microbes Infect. 2015;4:e64. doi:10.1038/emi.2015.64.
   PubMed Web of Science ®Google Scholar
• Dang DA, Nguyen VT, Vu DT, Nguyen TH, Nguyen DM, Yuhuan W, Baoming J, Nguyen DH, Le TL, Rotavin MVTG. A dose-escalation safety and immunogenicity study of a new live attenuated human rotavirus vaccine (Rotavin-M1) in Vietnamese children. Vaccine. 2012;30(Suppl 1):A114–21. doi:10.1016/j.vaccine.2011.07.118.
   PubMed Web of Science ®Google Scholar
• Xia S, Du J, Su J, Liu Y, Huang L, Yu Q, Xie Z, Gao J, Xu B, Gao X, et al. Efficacy, immunogenicity and safety of a trivalent live human-lamb reassortant rotavirus vaccine (LLR3) in healthy Chinese infants: A randomized, double-blind, placebo-controlled trial. Vaccine. 2020;38(46):7393–400. doi:10.1016/j.vaccine.2020.04.038.
   PubMed Web of Science ®Google Scholar
• Li RC, Huang T, Li Y, Luo D, Tao J, Fu B, Si G, Nong Y, Mo Z, Liao X, et al. Human rotavirus vaccine (RIX4414) efficacy in the first two years of life: a randomized, placebo-controlled trial in China. Hum Vaccin Immunother. 2014;10:11–18. doi:10.4161/hv.26319.
   PubMed Web of Science ®Google Scholar
• Mo Z, Mo Y, Li M, Tao J, Yang X, Kong J, Wei D, Fu B, Liao X, Chu J, et al. Efficacy and safety of a pentavalent live human-bovine reassortant rotavirus vaccine (RV5) in healthy Chinese infants: A randomized, double-blind, placebo-controlled trial. Vaccine. 2017;35(43):5897–904. doi:10.1016/j.vaccine.2017.08.081.
   PubMed Web of Science ®Google Scholar
• Parker EP, Ramani S, Lopman BA, Church JA, Iturriza-Gomara M, Prendergast AJ, Grassly NC. Causes of impaired oral vaccine efficacy in developing countries. Future Microbiol. 2018;13:97–118. doi:10.2217/fmb-2017-0128.
   PubMed Web of Science ®Google Scholar
• Desselberger U. Differences of rotavirus vaccine effectiveness by country: likely causes and contributing factors. Pathogens. 2017;6(4):65. doi:10.3390/pathogens6040065.
   PubMed Web of Science ®Google Scholar
• Angel J, Steele AD, Franco MA. Correlates of protection for rotavirus vaccines: possible alternative trial endpoints, opportunities, and challenges. Hum Vaccin Immunother. 2014;10(12):3659–71. doi:10.4161/hv.34361.
   PubMed Web of Science ®Google Scholar
• Cheuvart B, Neuzil KM, Steele AD, Cunliffe N, Madhi SA, Karkada N, Han HH, Vinals C. Association of serum anti-rotavirus immunoglobulin A antibody seropositivity and protection against severe rotavirus gastroenteritis: analysis of clinical trials of human rotavirus vaccine. Hum Vaccin Immunother. 2014;10(2):505–11. doi:10.4161/hv.27097.
   PubMed Web of Science ®Google Scholar
• Lee B, Carmolli M, Dickson DM, Colgate ER, Diehl SA, Uddin MI, Islam S, Hossain M, Rafique TA, Bhuiyan TR, et al. Rotavirus-specific immunoglobulin a responses are impaired and serve as a suboptimal correlate of protection among infants in Bangladesh. Clin Infect Dis. 2018;67(2):186–92. doi:10.1093/cid/ciy076.
   PubMed Web of Science ®Google Scholar
• Liu GF, Hille D, Kaplan SS, Goveia MG. Postdose 3 G1 serum neutralizing antibody as correlate of protection for pentavalent rotavirus vaccine. Hum Vaccin Immunother. 2017;13(10):2357–63. doi:10.1080/21645515.2017.1356522.
   PubMed Web of Science ®Google Scholar
• Angel J, Franco MA, Greenberg HB. Rotavirus immune responses and correlates of protection. Curr Opin Virol. 2012;2(4):419–25. doi:10.1016/j.coviro.2012.05.003.
   PubMed Web of Science ®Google Scholar
• Church JA, Parker EP, Kirkpatrick BD, Grassly NC, Prendergast AJ. Interventions to improve oral vaccine performance: a systematic review and meta-analysis. Lancet Infect Dis. 2019;19(2):203–14. doi:10.1016/S1473-3099(18)30602-9.
   PubMed Web of Science ®Google Scholar
• Gruber JF, Gruber LM, Weber RP, Becker-Dreps S, Jonsson Funk M. Rotavirus vaccine schedules and vaccine response among infants in low- and middle-income countries: a systematic review. Open Forum Infect Dis. 2017;4(2):ofx066. doi:10.1093/ofid/ofx066.
   PubMed Web of Science ®Google Scholar
• Kirkpatrick BD, Colgate ER, Mychaleckyj JC, Haque R, Dickson DM, Carmolli MP, Nayak U, Taniuchi M, Naylor C, Qadri F, et al. The “performance of rotavirus and oral polio vaccines in developing countries” (PROVIDE) study: description of methods of an interventional study designed to explore complex biologic problems. Am J Trop Med Hyg. 2015;92:744–51.
   PubMed Web of Science ®Google Scholar
• Gruber JF, Becker-Dreps S, Hudgens MG, Brookhart MA, Thomas JC, Jonsson Funk M. Timing of rotavirus vaccine doses and severe rotavirus gastroenteritis among vaccinated infants in low- and middle-income countries. Epidemiology. 2018;29(6):867–75. doi:10.1097/EDE.0000000000000909.
   PubMed Web of Science ®Google Scholar
• Armah G, Lewis KD, Cortese MM, Parashar UD, Ansah A, Gazley L, Victor JC, McNeal MM, Binka F, Steele AD, et al. Controlled trial of the impact of alternative dosing schedules on the immune response to human rotavirus vaccine in rural Ghanaian infants. J Infect Dis. 2016;213:1678–85. doi:10.1093/infdis/jiw023.
   PubMed Web of Science ®Google Scholar
• Ali SA, Kazi AM, Cortese MM, Fleming JA, Parashar UD, Jiang B, McNeal MM, Steele D, Bhutta Z, Zaidi A. Impact of different dosing schedules on the immunogenicity of the human rotavirus vaccine in infants in Pakistan: a randomized trial. J Infect Dis. 2014;210(11):1772–79. doi:10.1093/infdis/jiu335.
   PubMed Web of Science ®Google Scholar
• Kompithra RZ, Paul A, Manoharan D, Babji S, Sarkar R, Mathew LG, Kang G. Immunogenicity of a three dose and five dose oral human rotavirus vaccine (RIX4414) schedule in south Indian infants. Vaccine. 2014;32(Suppl 1):A129–33. doi:10.1016/j.vaccine.2014.03.002.
   PubMed Web of Science ®Google Scholar
• Cunliffe NA, Witte D, Ngwira BM, Todd S, Bostock NJ, Turner AM, Chimpeni P, Victor JC, Steele AD, Bouckenooghe A, et al. Efficacy of human rotavirus vaccine against severe gastroenteritis in Malawian children in the first two years of life: a randomized, double-blind, placebo controlled trial. Vaccine. 2012;30(Suppl 1):A36–43. doi:10.1016/j.vaccine.2011.09.120.
   PubMed Web of Science ®Google Scholar
• Madhi SA, Kirsten M, Louw C, Bos P, Aspinall S, Bouckenooghe A, Neuzil KM, Steele AD. Efficacy and immunogenicity of two or three dose rotavirus-vaccine regimen in South African children over two consecutive rotavirus-seasons: a randomized, double-blind, placebo-controlled trial. Vaccine. 2012;30(Suppl 1):A44–51. doi:10.1016/j.vaccine.2011.08.080.
   PubMed Web of Science ®Google Scholar
• WHO.Rotavirus vaccines. WHO position paper - January 2013. Wkly Epidemiol Rec. 2013; 88: 49–64.
   PubMedGoogle Scholar
• Patel M, Glass RI, Jiang B, Santosham M, Lopman B, Parashar U. A systematic review of anti-rotavirus serum IgA antibody titer as a potential correlate of rotavirus vaccine efficacy. J Infect Dis. 2013;208(2):284–94. doi:10.1093/infdis/jit166.
   PubMed Web of Science ®Google Scholar
• Clark A, van Zandvoort K, Flasche S, Sanderson C, Bines J, Tate J, Parashar U, Jit M. Efficacy of live oral rotavirus vaccines by duration of follow-up: a meta-regression of randomised controlled trials. Lancet Infect Dis. 2019;19(7):717–27. doi:10.1016/S1473-3099(19)30126-4.
   PubMed Web of Science ®Google Scholar
• Zaman K, Fleming JA, Victor JC, Yunus M, Bari TI, Azim T, Rahman M, Mowla SM, Bellini WJ, McNeal M, et al. Noninterference of rotavirus vaccine with measles-rubella vaccine at 9 months of age and improvements in antirotavirus immunity: a randomized trial. J Infect Dis. 2016;213(11):1686–93. doi:10.1093/infdis/jiw024.
   PubMed Web of Science ®Google Scholar
• Burnett E, Lopman BA, Parashar UD. Potential for a booster dose of rotavirus vaccine to further reduce diarrhea mortality. Vaccine. 2017;35(51):7198–203. doi:10.1016/j.vaccine.2017.10.027.
   PubMed Web of Science ®Google Scholar
• Dennehy PH, Brady RC, Halperin SA, Ward RL, Alvey JC, Fischer FH Jr., Innis BL, Rathfon H, Schuind A, De Vos B, et al. Comparative evaluation of safety and immunogenicity of two dosages of an oral live attenuated human rotavirus vaccine. Pediatr Infect Dis J. 2005;24(6):481–88. doi:10.1097/01.inf.0000164763.55558.71.
   PubMed Web of Science ®Google Scholar
• Phua KB, Quak SH, Lee BW, Emmanuel SC, Goh P, Han HH, De Vos B, Bock HL. Evaluation of RIX4414, a live, attenuated rotavirus vaccine, in a randomized, double-blind, placebo-controlled phase 2 trial involving 2464 Singaporean infants. J Infect Dis. 2005;192(Suppl 1):S6–S16. doi:10.1086/431511.
   PubMedGoogle Scholar
• Salinas B, Perez Schael I, Linhares AC, Ruiz Palacios GM, Guerrero ML, Yarzabal JP, Cervantes Y, Costa Clemens S, Damaso S, Hardt K, et al. Evaluation of safety, immunogenicity and efficacy of an attenuated rotavirus vaccine, RIX4414: A randomized, placebo-controlled trial in Latin American infants. Pediatr Infect Dis J. 2005;24:807–16. doi:10.1097/01.inf.0000178294.13954.a1.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Karvonen A, Korhonen T, Espo M, Lebacq E, Forster J, Zepp F, Delem A, De Vos B. Safety and immunogenicity of RIX4414 live attenuated human rotavirus vaccine in adults, toddlers and previously uninfected infants. Vaccine. 2004;22(21–22):2836–42. doi:10.1016/j.vaccine.2004.01.044.
   PubMed Web of Science ®Google Scholar
• Vesikari T, Clark HF, Offit PA, Dallas MJ, DiStefano DJ, Goveia MG, Ward RL, Schodel F, Karvonen A, Drummond JE, et al. Effects of the potency and composition of the multivalent human-bovine (WC3) reassortant rotavirus vaccine on efficacy, safety and immunogenicity in healthy infants. Vaccine. 2006;24(22):4821–29. doi:10.1016/j.vaccine.2006.03.025.
   PubMed Web of Science ®Google Scholar
• Dhingra MS, Kundu R, Gupta M, Kanungo S, Ganguly N, Singh MP, Bhattacharya MK, Ghosh R, Kumar R, Sur D, et al. Evaluation of safety and immunogenicity of a live attenuated tetravalent (G1-G4) Bovine-Human Reassortant Rotavirus vaccine (BRV-TV) in healthy Indian adults and infants. Vaccine. 2014;32(Suppl 1):A117–23. doi:10.1016/j.vaccine.2014.03.069.
   PubMed Web of Science ®Google Scholar
• Zade JK, Kulkarni PS, Desai SA, Sabale RN, Naik SP, Dhere RM. Bovine rotavirus pentavalent vaccine development in India. Vaccine. 2014;32(Suppl 1):A124–8. doi:10.1016/j.vaccine.2014.03.003.
   PubMed Web of Science ®Google Scholar
• Lee B, Dickson DM, Alam M, Afreen S, Kader A, Afrin F, Ferdousi T, Damon CF, Gullickson SK, McNeal MM, et al. The effect of increased inoculum on oral rotavirus vaccine take among infants in Dhaka, Bangladesh: A double-blind, parallel group, randomized, controlled trial. Vaccine. 2020;38(1):90–99. doi:10.1016/j.vaccine.2019.09.088.
   PubMed Web of Science ®Google Scholar
• Appaiahgari MB, Glass R, Singh S, Taneja S, Rongsen-Chandola T, Bhandari N, Mishra S, Vrati S. Transplacental rotavirus IgG interferes with immune response to live oral rotavirus vaccine ORV-116E in Indian infants. Vaccine. 2014;32(6):651–56. doi:10.1016/j.vaccine.2013.12.017.
   PubMed Web of Science ®Google Scholar
• Becker-Dreps S, Vilchez S, Velasquez D, Moon SS, Hudgens MG, Zambrana LE, Jiang B. Rotavirus-specific IgG antibodies from mothers’ serum may inhibit infant immune responses to the pentavalent rotavirus vaccine. Pediatr Infect Dis J. 2015;34:115–16. doi:10.1097/INF.0000000000000481.
   PubMed Web of Science ®Google Scholar
• Moon SS, Groome MJ, Velasquez DE, Parashar UD, Jones S, Koen A, van Niekerk N, Jiang B, Madhi SA. Prevaccination rotavirus serum IgG and IgA are associated with lower immunogenicity of live, oral human rotavirus vaccine in South African infants. Clin Infect Dis. 2016;62:157–65. doi:10.1093/cid/civ828.
   PubMed Web of Science ®Google Scholar
• Steele AD, Madhi SA, Cunliffe NA, Vesikari T, Phua KB, Lim FS, Nelson EA, Lau YL, Huang LM, Karkada N, et al. Incidence of rotavirus gastroenteritis by age in African, Asian and European children: relevance for timing of rotavirus vaccination. Hum Vaccin Immunother. 2016;12:2406–12. doi:10.1080/21645515.2016.1179412.
   PubMed Web of Science ®Google Scholar
• Hasso-Agopsowicz M, Ladva CN, Lopman B, Sanderson C, Cohen AL, Tate JE, Riveros X, Henao-Restrepo AM, Clark A; Global Rotavirus Surveillance N, et al. Global review of the age distribution of rotavirus disease in children aged <5 years before the introduction of rotavirus vaccination. Clin Infect Dis. 2019;69:1071–78.
   PubMed Web of Science ®Google Scholar
• Moon SS, Tate JE, Ray P, Dennehy PH, Archary D, Coutsoudis A, Bland R, Newell ML, Glass RI, Parashar U, et al. Differential profiles and inhibitory effect on rotavirus vaccines of nonantibody components in breast milk from mothers in developing and developed countries. Pediatr Infect Dis J. 2013;32:863–70.
   PubMed Web of Science ®Google Scholar
• Moon SS, Wang Y, Shane AL, Nguyen T, Ray P, Dennehy P, Baek LJ, Parashar U, Glass RI, Jiang B. Inhibitory effect of breast milk on infectivity of live oral rotavirus vaccines. Pediatr Infect Dis J. 2010;29:919–23. doi:10.1097/INF.0b013e3181e232ea.
   PubMed Web of Science ®Google Scholar
• Laucirica DR, Triantis V, Schoemaker R, Estes MK, Ramani S. Milk oligosaccharides inhibit human rotavirus infectivity in MA104 cells. J Nutr. 2017;147:1709–14.
   PubMed Web of Science ®Google Scholar
• Bautista-Marquez A, Velasquez DE, Esparza-Aguilar M, Luna-Cruz M, Ruiz-Moran T, Sugata K, Jiang B, Parashar U, Patel M, Richardson V. Breastfeeding linked to the reduction of both rotavirus shedding and IgA levels after Rotarix(R) immunization in Mexican infants. Vaccine. 2016;34:5284–89. doi:10.1016/j.vaccine.2016.09.006.
   PubMed Web of Science ®Google Scholar
• Groome MJ, Moon SS, Velasquez D, Jones S, Koen A, van Niekerk N, Jiang B, Parashar UD, Madhi SA. Effect of breastfeeding on immunogenicity of oral live-attenuated human rotavirus vaccine: a randomized trial in HIV-uninfected infants in Soweto, South Africa. Bull World Health Organ. 2014;92:238–45. doi:10.2471/BLT.13.128066.
   PubMed Web of Science ®Google Scholar
• Rongsen-Chandola T, Strand TA, Goyal N, Flem E, Rathore SS, Arya A, Winje BA, Lazarus R, Shanmugasundaram E, Babji S, et al. Effect of withholding breastfeeding on the immune response to a live oral rotavirus vaccine in North Indian infants. Vaccine. 2014;32(Suppl 1):A134–9. doi:10.1016/j.vaccine.2014.04.078.
   PubMed Web of Science ®Google Scholar
• Ali A, Kazi AM, Cortese MM, Fleming JA, Moon S, Parashar UD, Jiang B, McNeal MM, Steele D, Bhutta Z, et al. Impact of withholding breastfeeding at the time of vaccination on the immunogenicity of oral rotavirus vaccine–a randomized trial. PLoS One. 2015;10:e0127622. doi:10.1371/journal.pone.0127622.
   PubMed Web of Science ®Google Scholar
• Kambhampati A, Payne DC, Costantini V, Lopman BA. Host genetic susceptibility to enteric viruses: a systematic review and metaanalysis. Clin Infect Dis. 2016;62(1):11–18. doi:10.1093/cid/civ873.
   PubMed Web of Science ®Google Scholar
• Lee B, Dickson DM, deCamp AC, Ross Colgate E, Diehl SA, Uddin MI, Sharmin S, Islam S, Bhuiyan TR, Alam M, et al. Histo-blood group antigen phenotype determines susceptibility to genotype-specific rotavirus infections and impacts measures of rotavirus vaccine efficacy. J Infect Dis. 2018;217:1399–407. doi:10.1093/infdis/jiy054.
   PubMed Web of Science ®Google Scholar
• Sun X, Guo N, Li J, Yan X, He Z, Li D, Jin M, Xie G, Pang L, Zhang Q, et al. Rotavirus infection and histo-blood group antigens in the children hospitalized with diarrhoea in China. Clin Microbiol Infect. 2016;22(8):740 e1–3. doi:10.1016/j.cmi.2016.06.007.
   PubMed Web of Science ®Google Scholar
• Ayouni S, Sdiri-Loulizi K, de Rougemont A, Estienney M, Ambert-Balay K, Aho S, Hamami S, Aouni M, Neji-Guediche M, Pothier P, et al. Rotavirus P[8] Infections in persons with secretor and nonsecretor phenotypes, Tunisia. Emerg Infect Dis. 2015;21(11):2055–58. doi:10.3201/eid2111.141901.
   PubMed Web of Science ®Google Scholar
• Nordgren J, Sharma S, Bucardo F, Nasir W, Gunaydin G, Ouermi D, Nitiema LW, Becker-Dreps S, Simpore J, Hammarstrom L, et al. Both Lewis and secretor status mediate susceptibility to rotavirus infections in a rotavirus genotype-dependent manner. Clin Infect Dis. 2014;59:1567–73. doi:10.1093/cid/ciu633.
   PubMed Web of Science ®Google Scholar
• Armah GE, Cortese MM, Dennis FE, Yu Y, Morrow AL, McNeal MM, Lewis KDC, Awuni DA, Armachie J, Parashar UD. Rotavirus vaccine take in infants is associated with secretor status. J Infect Dis. 2019;219(5):746–49. doi:10.1093/infdis/jiy573.
   PubMed Web of Science ®Google Scholar
• Kazi AM, Cortese MM, Yu Y, Lopman B, Morrow AL, Fleming JA, McNeal MM, Steele AD, Parashar UD, Zaidi AKM, et al. Secretor and salivary ABO blood group antigen status predict rotavirus vaccine take in infants. J Infect Dis. 2017;215(5):786–89. doi:10.1093/infdis/jix028.
   PubMed Web of Science ®Google Scholar
• Pollock L, Bennett A, Jere KC, Dube Q, Mandolo J, Bar-Zeev N, Heyderman RS, Cunliffe NA, Iturriza-Gomara M. Nonsecretor histo-blood group antigen phenotype is associated with reduced risk of clinical rotavirus vaccine failure in Malawian infants. Clin Infect Dis. 2019;69:1313–19. doi:10.1093/cid/ciy1067.
   PubMed Web of Science ®Google Scholar
• Williams FB, Kader A, Colgate ER, Dickson DM, Carmolli M, Uddin MI, Sharmin S, Islam S, Bhuiyan TR, Alam M, et al. Maternal secretor status affects oral rotavirus vaccine response in breastfed infants in Bangladesh. J Infect Dis. 2020. doi:10.1093/infdis/jiaa101.
   Web of Science ®Google Scholar
• Parker EPK, Praharaj I, Zekavati A, Lazarus RP, Giri S, Operario DJ, Liu J, Houpt E, Iturriza-Gomara M, Kampmann B, et al. Influence of the intestinal microbiota on the immunogenicity of oral rotavirus vaccine given to infants in south India. Vaccine. 2018;36(2):264–72. doi:10.1016/j.vaccine.2017.11.031.
   PubMed Web of Science ®Google Scholar
• Baker JM, Tate JE, Leon J, Haber MJ, Lopman BA. Antirotavirus IgA seroconversion rates in children who receive concomitant oral poliovirus vaccine: A secondary, pooled analysis of Phase II and III trial data from 33 countries. PLoS Med. 2019;16:e1003005. doi:10.1371/journal.pmed.1003005.
   PubMed Web of Science ®Google Scholar
• Church JA, Rogawski McQuade ET, Mutasa K, Taniuchi M, Rukobo S, Govha M, Lee B, Carmolli MP, Chasekwa B, Ntozini R, et al. Enteropathogens and rotavirus vaccine immunogenicity in a cluster randomized trial of improved water, sanitation and hygiene in rural Zimbabwe. Pediatr Infect Dis J. 2019;38(12):1242–48. doi:10.1097/INF.0000000000002485.
   PubMed Web of Science ®Google Scholar
• Jorba J, Diop OM, Iber J, Henderson E, Zhao K, Quddus A, Sutter R, Vertefeuille JF, Wenger J, Wassilak SGF, et al. Update on vaccine-derived poliovirus outbreaks - worldwide, January 2018-June 2019. MMWR Morb Mortal Wkly Rep. 2019;68:1024–28. doi:10.15585/mmwr.mm6845a4.
   PubMed Web of Science ®Google Scholar
• Polio endgame strategy 2019-2023: eradication, integration, certification and containment. Geneva, Switzerland: World Health Organization; 2019. (WHO/Polio/19.04). Licence: CC BY-NC-SA 3.0 IGO
   Google Scholar
• Strategy for the response to type 2 circulating vaccine-derived poliovirus 2020-2021: an addendum to the polio endgame strategy 2019-2023. Geneva, Switzerland: World Health Organization; 2020. (WHO/Polio/20.02). License CC BY-NC-SA 3.0 IGO
   Google Scholar
• Clinical summary for novel oral polio vaccine type 2 (nOPV2). Global polio eradication initiative; 2020 May [ accessed 2020 June 01]. http://polioeradication.org/nopv2/.
   Google Scholar
• Taniuchi M, Platts-Mills JA, Begum S, Uddin MJ, Sobuz SU, Liu J, Kirkpatrick BD, Colgate ER, Carmolli MP, Dickson DM, et al. Impact of enterovirus and other enteric pathogens on oral polio and rotavirus vaccine performance in Bangladeshi infants. Vaccine. 2016;34(27):3068–75. doi:10.1016/j.vaccine.2016.04.080.
   PubMed Web of Science ®Google Scholar
• Harris V, Ali A, Fuentes S, Korpela K, Kazi M, Tate J, Parashar U, Wiersinga WJ, Giaquinto C, de Weerth C, et al. Rotavirus vaccine response correlates with the infant gut microbiota composition in Pakistan. Gut Microbes. 2018;9(2):93–101. doi:10.1080/19490976.2017.1376162.
   PubMed Web of Science ®Google Scholar
• Harris VC, Armah G, Fuentes S, Korpela KE, Parashar U, Victor JC, Tate J, de Weerth C, Giaquinto C, Wiersinga WJ, et al. Significant Correlation Between the Infant Gut Microbiome and Rotavirus Vaccine Response in Rural Ghana. J Infect Dis. 2017;215(1):34–41. doi:10.1093/infdis/jiw518.
   PubMed Web of Science ®Google Scholar
• Harris VC, Haak BW, Handley SA, Jiang B, Velasquez DE, Hykes BL Jr., Droit L, Berbers GAM, Kemper EM, van Leeuwen EMM, et al. Effect of antibiotic-mediated microbiome modulation on rotavirus vaccine immunogenicity: a human, randomized-control proof-of-concept trial. Cell Host Microbe. 2018;24(2):197–207e4. doi:10.1016/j.chom.2018.07.005.
   PubMed Web of Science ®Google Scholar
• Ramani S, Stewart CJ, Laucirica DR, Ajami NJ, Robertson B, Autran CA, Shinge D, Rani S, Anandan S, Hu L, et al. Human milk oligosaccharides, milk microbiome and infant gut microbiome modulate neonatal rotavirus infection. Nat Commun. 2018;9(1):5010. doi:10.1038/s41467-018-07476-4.
   PubMedGoogle Scholar
• Church JA, Rukobo S, Govha M, Lee B, Carmolli MP, Chasekwa B, Ntozini R, Mutasa K, McNeal MM, Majo FD, et al. The Impact of Improved Water, Sanitation, and Hygiene on Oral Rotavirus Vaccine Immunogenicity in Zimbabwean Infants: substudy of a Cluster-randomized Trial. Clin Infect Dis. 2019;69(12):2074–81. doi:10.1093/cid/ciz140.
   PubMed Web of Science ®Google Scholar
• Rogawski McQuade ET, Platts-Mills JA, Gratz J, Zhang J, Moulton LH, Mutasa K, Majo FD, Tavengwa N, Ntozini R, Prendergast AJ, et al. Impact of water quality, sanitation, handwashing, and nutritional interventions on enteric infections in rural Zimbabwe: the Sanitation Hygiene Infant Nutrition Efficacy (SHINE) trial. J Infect Dis. 2020;221(8):1379–86. doi:10.1093/infdis/jiz179.
   PubMed Web of Science ®Google Scholar
• Lazarus RP, John J, Shanmugasundaram E, Rajan AK, Thiagarajan S, Giri S, Babji S, Sarkar R, Kaliappan PS, Venugopal S, et al. The effect of probiotics and zinc supplementation on the immune response to oral rotavirus vaccine: A randomized, factorial design, placebo-controlled study among Indian infants. Vaccine. 2018;36:273–79.
   PubMed Web of Science ®Google Scholar
• Marie C, Ali A, Chandwe K, Petri WA Jr., Kelly P. Pathophysiology of environmental enteric dysfunction and its impact on oral vaccine efficacy. Mucosal Immunol. 2018;11(5):1290–98. doi:10.1038/s41385-018-0036-1.
   PubMed Web of Science ®Google Scholar
• Church JA, Parker EP, Kosek MN, Kang G, Grassly NC, Kelly P, Prendergast AJ. Exploring the relationship between environmental enteric dysfunction and oral vaccine responses. Future Microbiol. 2018;13:1055–70. doi:10.2217/fmb-2018-0016.
   PubMed Web of Science ®Google Scholar
• Liu TC, VanBuskirk K, Ali SA, Kelly MP, Holtz LR, Yilmaz OH, Sadiq K, Iqbal N, Amadi B, Syed S, et al. A novel histological index for evaluation of environmental enteric dysfunction identifies geographic-specific features of enteropathy among children with suboptimal growth. PLoS Negl Trop Dis. 2020;14:e0007975. doi:10.1371/journal.pntd.0007975.
   PubMed Web of Science ®Google Scholar
• Kosek MN, Investigators M-EN. Causal pathways from enteropathogens to environmental enteropathy: findings from the MAL-ED birth cohort study. EBioMedicine. 2017;18:109–17. doi:10.1016/j.ebiom.2017.02.024.
   PubMed Web of Science ®Google Scholar
• Naylor C, Lu M, Haque R, Mondal D, Buonomo E, Nayak U, Mychaleckyj JC, Kirkpatrick B, Colgate R, Carmolli M, et al. Environmental enteropathy, oral vaccine failure and growth faltering in infants in Bangladesh. EBioMedicine. 2015;2(11):1759–66. doi:10.1016/j.ebiom.2015.09.036.
   PubMed Web of Science ®Google Scholar
• Mahfuz M, Das S, Mazumder RN, Masudur Rahman M, Haque R, Bhuiyan MMR, Akhter H, Sarker MSA, Mondal D, Muaz SSA, et al. Bangladesh Environmental Enteric Dysfunction (BEED) study: protocol for a community-based intervention study to validate non-invasive biomarkers of environmental enteric dysfunction. BMJ Open. 2017;7(8):e017768. doi:10.1136/bmjopen-2017-017768.
   PubMed Web of Science ®Google Scholar
• Rogawski ET, Platts-Mills JA, Colgate ER, Haque R, Zaman K, Petri WA, Kirkpatrick BD. Quantifying the Impact of Natural Immunity on Rotavirus Vaccine Efficacy Estimates: A Clinical Trial in Dhaka, Bangladesh (PROVIDE) and a Simulation Study. J Infect Dis. 2018;217(6):861–68. doi:10.1093/infdis/jix668.
   PubMed Web of Science ®Google Scholar
• Taniuchi M, Sobuz SU, Begum S, Platts-Mills JA, Liu J, Yang Z, Wang XQ, Petri WA Jr., Haque R, Houpt ER. Etiology of diarrhea in Bangladeshi infants in the first year of life analyzed using molecular methods. J Infect Dis. 2013;208:1794–802. doi:10.1093/infdis/jit507.
   PubMed Web of Science ®Google Scholar
• Mokomane M, Tate JE, Steenhoff AP, Esona MD, Bowen MD, Lechiile K, Pernica JM, Kasvosve I, Parashar UD, Goldfarb DM. Evaluation of the Influence of gastrointestinal coinfections on rotavirus vaccine effectiveness in Botswana. Pediatr Infect Dis J. 2018;37(3):e58–e62. doi:10.1097/INF.0000000000001828.
   PubMed Web of Science ®Google Scholar
• Praharaj I, Platts-Mills JA, Taneja S, Antony K, Yuhas K, Flores J, Cho I, Bhandari N, Revathy R, Bavdekar A, et al. Diarrheal Etiology and Impact of Coinfections on rotavirus vaccine efficacy estimates in a clinical trial of a monovalent human-bovine (116E) oral rotavirus vaccine, Rotavac, India. Clin Infect Dis. 2019;69:243–50. doi:10.1093/cid/ciy896.
   PubMed Web of Science ®Google Scholar
• VIEW-hub.org. RV-Vaccine Access: #Children without Access. [ accessed 2020 Sep17]. https://view-hub.org/map/?set=children-without-access&group=vaccine-access&category=rv.
   Google Scholar
• Chen MY, Kirkwood CD, Bines J, Cowley D, Pavlic D, Lee KJ, Orsini F, Watts E, Barnes G, Danchin M. Rotavirus specific maternal antibodies and immune response to RV3-BB neonatal rotavirus vaccine in New Zealand. Hum Vaccin Immunother. 2017;13:1126–35. doi:10.1080/21645515.2016.1274474.
   PubMed Web of Science ®Google Scholar
• Bines JE, At Thobari J, Satria CD, Handley A, Watts E, Cowley D, Nirwati H, Ackland J, Standish J, Justice F, et al. Human neonatal rotavirus vaccine (RV3-BB) to target rotavirus from birth. N Engl J Med. 2018;378(8):719–30. doi:10.1056/NEJMoa1706804.
   PubMed Web of Science ®Google Scholar
• Boniface K, Byars SG, Cowley D, Kirkwood CD, Bines JE. Human neonatal rotavirus vaccine (RV3-BB) produces vaccine take irrespective of histo-blood group antigen status. J Infect Dis. 2020;221(7):1070–78. doi:10.1093/infdis/jiz333.
   PubMed Web of Science ®Google Scholar
• Cowley D, Sari RM, Handley A, Watts E, Bachtiar NS, At Thobari J, Satria CD, Bogdanovic-Sakran N, Nirwati H, Orsini F, et al. Immunogenicity of four doses of oral poliovirus vaccine when co-administered with the human neonatal rotavirus vaccine (RV3-BB). Vaccine. 2019;37(49):7233–39. doi:10.1016/j.vaccine.2019.09.071.
   PubMed Web of Science ®Google Scholar
• Fix A, Kirkwood CD, Steele D, Flores J.. Next-generation rotavirus vaccine developers meeting: Summary of a meeting sponsored by PATH and the Bill & Melinda Gates Foundation (19-20 June 2019, Geneva). Vaccine 2020. doi:10.1016/j.vaccine.2020.11.034.
   Google Scholar
• Wen X, Wen K, Cao D, Li G, Jones RW, Li J, Szu S, Hoshino Y, Yuan L. Inclusion of a universal tetanus toxoid CD4(+) T cell epitope P2 significantly enhanced the immunogenicity of recombinant rotavirus ΔVP8* subunit parenteral vaccines. Vaccine. 2014;32:4420–27. doi:10.1016/j.vaccine.2014.06.060.
   PubMed Web of Science ®Google Scholar
• Groome MJ, Koen A, Fix A, Page N, Jose L, Madhi SA, McNeal M, Dally L, Cho I, Power M, et al. Safety and immunogenicity of a parenteral P2-VP8-P[8] subunit rotavirus vaccine in toddlers and infants in South Africa: a randomised, double-blind, placebo-controlled trial. Lancet Infect Dis. 2017;17(8):843–53. doi:10.1016/S1473-3099(17)30242-6.
   PubMed Web of Science ®Google Scholar
• Groome MJ, Fairlie L, Morrison J, Fix A, Koen A, Masenya M, Jose L, Madhi SA, Page N, McNeal M, et al. Safety and immunogenicity of a parenteral trivalent P2-VP8 subunit rotavirus vaccine: a multisite, randomised, double-blind, placebo-controlled trial. Lancet Infect Dis. 2020;20(7):851–63. doi:10.1016/S1473-3099(20)30001-3.
   PubMed Web of Science ®Google Scholar
• Esona MD, Foytich K, Wang Y, Shin G, Wei G, Gentsch JR, Glass RI, Jiang B. Molecular characterization of human rotavirus vaccine strain CDC-9 during sequential passages in Vero cells. Hum Vaccin. 2010;6(3):247–53. doi:10.4161/hv.6.3.10409.
   Web of Science ®Google Scholar
• Jiang B, Wang Y, Glass RI. Does a monovalent inactivated human rotavirus vaccine induce heterotypic immunity? Evidence from animal studies. Hum Vaccin Immunother. 2013;9(8):1634–37. doi:10.4161/hv.24958.
   PubMed Web of Science ®Google Scholar
• Wang Y, Azevedo M, Saif LJ, Gentsch JR, Glass RI, Jiang B. Inactivated rotavirus vaccine induces protective immunity in gnotobiotic piglets. Vaccine. 2010;28(33):5432–36. doi:10.1016/j.vaccine.2010.06.006.
   PubMed Web of Science ®Google Scholar
• Resch TK, Wang Y, Moon SS, Joyce J, Li S, Prausnitz M, Jiang B. Inactivated rotavirus vaccine by parenteral administration induces mucosal immunity in mice. Sci Rep. 2018;8:561. doi:10.1038/s41598-017-18973-9.
   PubMed Web of Science ®Google Scholar
• Conner ME, Crawford SE, Barone C, O’Neal C, Zhou YJ, Fernandez F, Parwani A, Saif LJ, Cohen J, Estes MK. Rotavirus subunit vaccines. Arch Virol Suppl. 1996;12:199–206.
   PubMedGoogle Scholar
• Wang Y, Vlasova A, Velasquez DE, Saif LJ, Kandasamy S, Kochba E, Levin Y, Jiang B. Skin vaccination against rotavirus using microneedles: proof of concept in gnotobiotic piglets. PLoS One. 2016;11:e0166038. doi:10.1371/journal.pone.0166038.
   PubMed Web of Science ®Google Scholar
• Crawford SE, Labbe M, Cohen J, Burroughs MH, Zhou YJ, Estes MK. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J Virol. 1994;68:5945–52. doi:10.1128/JVI.68.9.5945-5952.1994.
   PubMed Web of Science ®Google Scholar
• Crawford SE, Estes MK, Ciarlet M, Barone C, O’Neal CM, Cohen J, Conner ME. Heterotypic protection and induction of a broad heterotypic neutralization response by rotavirus-like particles. J Virol. 1999;73(6):4813–22. doi:10.1128/JVI.73.6.4813-4822.1999.
   PubMed Web of Science ®Google Scholar
• Jiang B, Estes MK, Barone C, Barniak V, O’Neal CM, Ottaiano A, Madore HP, Conner ME. Heterotypic protection from rotavirus infection in mice vaccinated with virus-like particles. Vaccine. 1999;17(7–8):1005–13. doi:10.1016/S0264-410X(98)00317-X.
   PubMed Web of Science ®Google Scholar
• O’Neal CM, Crawford SE, Estes MK, Conner ME. Rotavirus virus-like particles administered mucosally induce protective immunity. J Virol. 1997;71:8707–17. doi:10.1128/JVI.71.11.8707-8717.1997.
   PubMed Web of Science ®Google Scholar
• Fernandez FM, Conner ME, Hodgins DC, Parwani AV, Nielsen PR, Crawford SE, Estes MK, Saif LJ. Passive immunity to bovine rotavirus in newborn calves fed colostrum supplements from cows immunized with recombinant SA11 rotavirus core-like particle (CLP) or virus-like particle (VLP) vaccines. Vaccine. 1998;16:507–16. doi:10.1016/S0264-410X(97)80004-7.
   PubMed Web of Science ®Google Scholar
• Blazevic V, Lappalainen S, Nurminen K, Huhti L, Vesikari T. Norovirus VLPs and rotavirus VP6 protein as combined vaccine for childhood gastroenteritis. Vaccine. 2011;29(45):8126–33. doi:10.1016/j.vaccine.2011.08.026.
   PubMed Web of Science ®Google Scholar
• Malm M, Heinimaki S, Vesikari T, Blazevic V. Rotavirus capsid VP6 tubular and spherical nanostructures act as local adjuvants when co-delivered with norovirus VLPs. Clin Exp Immunol. 2017;189(3):331–41. doi:10.1111/cei.12977.
   PubMed Web of Science ®Google Scholar
• Tan M, Huang P, Xia M, Fang PA, Zhong W, McNeal M, Wei C, Jiang W, Jiang X. Norovirus P particle, a novel platform for vaccine development and antibody production. J Virol. 2011;85:753–64. doi:10.1128/JVI.01835-10.
   PubMed Web of Science ®Google Scholar
• Xia M, Huang P, Jiang X, Tan M. Immune response and protective efficacy of the S particle presented rotavirus VP8* vaccine in mice. Vaccine. 2019;37(30):4103–10. doi:10.1016/j.vaccine.2019.05.075.
   PubMed Web of Science ®Google Scholar
• Liu MA. A comparison of plasmid DNA and mRNA as vaccine technologies. Vaccines (Basel). 2019;7:37. doi:10.3390/vaccines7020037.
   PubMed Web of Science ®Google Scholar
• Desselberger U. Potential of plasmid only based reverse genetics of rotavirus for the development of next-generation vaccines. Curr Opin Virol. 2020;44:1–6. doi:10.1016/j.coviro.2020.04.004.
   PubMed Web of Science ®Google Scholar
• Holmgren J, Parashar UD, Plotkin S, Louis J, Ng SP, Desauziers E, Picot V, Saadatian-Elahi M. Correlates of protection for enteric vaccines. Vaccine. 2017;35:3355–63. doi:10.1016/j.vaccine.2017.05.005.
   PubMed Web of Science ®Google Scholar