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Expert Review of Anti-infective Therapy Volume 10, 2012 - Issue 5
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Review

Impact of rotavirus vaccines on rotavirus disease

Philippe Lepage Université Libre de Bruxelles and Infectious Diseases Unit, Hôpital Universitaire des Enfants Reine Fabiola, Brussels, Belgium. [email protected]
&
Anne Vergison Université Libre de Bruxelles and Infectious Diseases Unit, Hôpital Universitaire des Enfants Reine Fabiola, Brussels, Belgium
Pages 547-561 | Published online: 10 Jan 2014

References

  • Black RE, Cousens S, Johnson HL et al.; Child Health Epidemiology Reference Group of WHO and UNICEF. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375(9730), 1969–1987 (2010).
  • Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J, Parashar UD; the WHO-coordinated Global Rotavirus Surveillance Network. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 12, 136–141 (2011).
  • Soriano-Gabarró M, Mrukowicz J, Vesikari T, Verstraeten T. Burden of rotavirus disease in European Union countries. Pediatr. Infect. Dis. J. 25(1 Suppl.), S7–S11 (2006).
  • Payne DC, Staat MA, Edwards KM et al. Active, population-based surveillance for severe rotavirus gastroenteritis in children in the United States. Pediatrics 122(6), 1235–1243 (2008).
  • Forster J, Guarino A, Parez N et al.; Rotavirus Study Group. Hospital-based surveillance to estimate the burden of rotavirus gastroenteritis among European children younger than 5 years of age. Pediatrics 123(3), e393–e400 (2009).
  • Ciarlet M, Estes MK. Rotaviruses: basic biology, epidemiology and methodologies. In: Encyclopedia of Environmental Microbiology. Britton G (Ed.). John Wiley & Sons, NY, USA, 2573–2773 (2002).
  • Estes MK, Kapikian A. Rotaviruses. In: Fields Virology. Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin M, Roizman B, Straus SE (Eds). Kluwer Health/Lippincott, Williams and Wilkins, PA, USA, 1917–1974 (2007).
  • Matthijnssens J, Ciarlet M, Heiman E 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. 82(7), 3204–3219 (2008).
  • Matthijnssens J, Ciarlet M, Rahman M et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 153(8), 1621–1629 (2008).
  • Todd S, Page NA, Steele DA, Peenze I, Cunliffe NA. Rotavirus strain types circulating in Africa: review of studies published during 1997–2006. J. Infect. Dis. 202, S34–S42 (2010).
  • Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev. Med. Virol. 15(1), 29–56 (2005).
  • Meeting of the immunization Strategic Advisory Group of Experts, April 2009 – conclusions and recommendations. Wkly Epidemiol. Rec. 84(23), 220–236 (2009).
  • Meeting of the Strategic Advisory Group of Experts on immunization, October 2009 – conclusions and recommendations. Wkly Epidemiol. Rec. 84(50), 517–532 (2009).
  • Bernstein DI, Sack DA, Rothstein E et al. Efficacy of live, attenuated, human rotavirus vaccine 89-12 in infants: a randomised placebo-controlled trial. Lancet 354(9175), 287–290 (1999).
  • Heaton PM, Goveia MG, Miller JM, Offit P, Clark HF. Development of a pentavalent rotavirus vaccine against prevalent serotypes of rotavirus gastroenteritis. J. Infect. Dis. 192(Suppl. 1), S17–S21 (2005).
  • Matthijnssens J, Joelsson DB, Warakomski DJ et al. Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq. Virology 403(2), 111–127 (2010).
  • CDC. Recommended immunization schedules for persons aged 0 through 18 years – United States, 2012. MMWR 61(5), 1–4 (2012).
  • Vesikari T, Van Damme P, Giaquinto C et al.; Expert Working Group; European Society for Paediatric Infectious Diseases; European Society for Paediatric Gastroenterology, Hepatology, and Nutrition. European Society for Paediatric Infectious Diseases/European Society for Paediatric Gastroenterology, Hepatology, and Nutrition evidence-based recommendations for rotavirus vaccination in Europe: executive summary. J. Pediatr. Gastroenterol. Nutr. 46(5), 615–618 (2008).
  • Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR et al.; Human Rotavirus Vaccine Study Group. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N. Engl. J. Med. 354(1), 11–22 (2006).
  • Linhares AC, Velázquez FR, Pérez-Schael I et al.; Human Rotavirus Vaccine Study Group. Efficacy and safety of an oral live attenuated human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in LA infants: a randomised, double-blind, placebo-controlled Phase III study. Lancet 371(9619), 1181–1189 (2008).
  • Vesikari T, Karvonen A, Prymula R et al. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet 370(9601), 1757–1763 (2007).
  • Phua KB, Lim FS, Lau YL et al. Safety and efficacy of human rotavirus vaccine during the first 2 years of life in Asian infants: randomised, double-blind, controlled study. Vaccine 27(43), 5936–5941 (2009).
  • Madhi SA, Cunliffe NA, Steele D et al. Effect of human rotavirus vaccine on severe diarrhea in African infants. N. Engl. J. Med. 362(4), 289–298 (2010).
  • Vesikari T, Matson DO, Dennehy P et al.; Rotavirus Efficacy and Safety Trial (REST) Study Team. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N. Engl. J. Med. 354(1), 23–33 (2006).
  • Vesikari T, Itzler R, Karvonen A et al. RotaTeq, a pentavalent rotavirus vaccine: efficacy and safety among infants in Europe. Vaccine 28(2), 345–351 (2009).
  • Armah GE, Sow SO, Breiman RF 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 376(9741), 606–614 (2010).
  • Zaman K, Dang DA, Victor JC 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 376(9741), 615–623 (2010).
  • Ruuska T, Vesikari T. Rotavirus disease in Finnish children: use of numerical scores for clinical severity of diarrhoeal episodes. Scand. J. Infect. Dis. 22(3), 259–267 (1990).
  • Clark HF, Bernstein DI, Dennehy PH et al. Safety, efficacy, and immunogenicity of a live, quadrivalent human-bovine reassortant rotavirus vaccine in healthy infants. J. Pediatr. 144(2), 184–190 (2004).
  • Murphy TV, Gargiullo PM, Massoudi MS et al.; Rotavirus Intussusception Investigation Team. Intussusception among infants given an oral rotavirus vaccine. N. Engl. J. Med. 344(8), 564–572 (2001).
  • Glass RI, Parashar UD, Bresee JS et al. Rotavirus vaccines: current prospects and future challenges. Lancet 368(9532), 323–332 (2006).
  • Patel MM, Steele D, Gentsch JR, Wecker J, Glass RI, Parashar UD. Real-world impact of rotavirus vaccination. Pediatr. Infect. Dis. J. 30(Suppl 1), S1–S5 (2011).
  • Patel MM, Parashar UD. Assessing the effectiveness and public health impact of rotavirus vaccines after introduction in immunization programs. J. Infect. Dis. 200(Suppl 1), S291–S299 (2009).
  • John TJ, Samuel R. Herd immunity and herd effect: new insights and definitions. Eur. J. Epidemiol. 16(7), 601–606 (2000).
  • Hadler SC, Dietz V, Okwo-Bele JM, Cutts F. Immunization in developing countries. In: Vaccines (5th Edition). Plotkin SA, Orenstein WA, Offit P (Eds). Saunders-Elsevier, PA, USA, 1541–1571 (2008).
  • Richardson V, Hernandez-Pichardo J, Quintanar-Solares M et al. Effect of rotavirus vaccination on death from childhood diarrhea in Mexico. N. Engl. J. Med. 362(4), 299–305 (2010).
  • Richardson V, Parashar U, Patel M. Childhood diarrhea deaths after rotavirus vaccination in Mexico. N. Engl. J. Med. 365(8), 772–773 (2011).
  • Desai R, de Oliveira LH, Parashar UD, Lopman B, Tate JE, Patel MM. Reduction in morbidity and mortality from childhood diarrhoeal disease after species A rotavirus vaccine introduction in Latin America – a review. Mem. Inst. Oswaldo Cruz 106(8), 907–911 (2011).
  • do Carmo GM, Yen C, Cortes J et al. Decline in diarrhea mortality and admissions after routine childhood rotavirus immunization in Brazil: a time-series analysis. PLoS Med. 8(4), e1001024 (2011).
  • de Oliveira LH, Danovaro-Holliday MC, Sanwogou NJ, Ruiz-Matus C, Tambini G, Andrus JK. Progress in the introduction of the rotavirus vaccine in Latin America and the Caribbean: four years of accumulated experience. Pediatr. Infect. Dis. J. 30(1 Suppl.), S61–S66 (2011).
  • Quintanar-Solares M, Yen C, Richardson V, Esparza-Aguilar M, Parashar UD, Patel MM. Impact of rotavirus vaccination on diarrhea-related hospitalizations among children <5 years of age in Mexico. Pediatr. Infect. Dis. J. 30(1 Suppl.), S11–S15 (2011).
  • Patel M, Pedreira C, De Oliveira LH et al. Association between pentavalent rotavirus vaccine and severe rotavirus diarrhea among children in Nicaragua. JAMA 301(21), 2243–2251 (2009).
  • Mast TC, Khawaja S, Espinoza F et al. Case–control study of the effectiveness of vaccination with pentavalent rotavirus vaccine in Nicaragua. Pediatr. Infect. Dis. J. 30(11), e209–e215 (2011).
  • de Palma O, Cruz L, Ramos H et al. Effectiveness of rotavirus vaccination against childhood diarrhoea in El Salvador: case–control study. BMJ 340, c2825 (2010).
  • Yen C, Armero Guardado JA, Alberto P et al. Decline in rotavirus hospitalizations and health care visits for childhood diarrhea following rotavirus vaccination in El Salvador. Pediatr. Infect. Dis. J. 30(Suppl. 1), S6–S10 (2011).
  • Molto Y, Cortes JE, De Oliveira LH et al. Reduction of diarrhea-associated hospitalizations among children aged <5 years in Panama following the introduction of rotavirus vaccine. Pediatr. Infect. Dis. J. 30(Suppl. 1), S16–S20 (2011).
  • Gurgel RQ, Cuevas LE, Vieira SC et al. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerging Infect. Dis. 13(10), 1571–1573 (2007).
  • Correia JB, Patel MM, Nakagomi O et al. Effectiveness of monovalent rotavirus vaccine (Rotarix) against severe diarrhea caused by serotypically unrelated G2P[4] strains in Brazil. J. Infect. Dis. 201(3), 363–369 (2010).
  • Carvalho-Costa FA, Volotao Ede M, de Assis RM et al. Laboratory-based rotavirus surveillance during the introduction of a vaccination program, Brazil, 2005–2009. Pediatr. Infect. Dis. J. 30(Suppl. 1), S35–S41 (2011).
  • Fischer TK, Viboud C, Parashar U et al. Hospitalizations and deaths from diarrhea and rotavirus among children <5 years of age in the United States, 1993–2003. J. Infect. Dis. 195(8), 1117–1125 (2007).
  • Grimwood K, Lambert SB, Milne RJ. Rotavirus infections and vaccines: burden of illness and potential impact of vaccination. Paediatr. Drugs 12(4), 235–256 (2010).
  • Curns AT, Coffin F, Glasser JW, Glass RI, Parashar UD. Projected impact of the new rotavirus vaccination program on hospitalizations for gastroenteritis and rotavirus disease among US children <5 years of age during 2006–2015. J. Infect. Dis. 200(Suppl. 1), S49–S56 (2009).
  • Tate JE, Panozzo CA, Payne DC et al. Decline and change in seasonality of US rotavirus activity after the introduction of rotavirus vaccine. Pediatrics 124(2), 465–471 (2009).
  • Parashar UD, Glass RI. Rotavirus vaccines – early success, remaining questions. N. Engl. J. Med. 360(11), 1063–1065 (2009).
  • Staat MA, Payne DC, Donauer S et al.; New Vaccine Surveillance Network (NVSN). Effectiveness of pentavalent rotavirus vaccine against severe disease. Pediatrics 128(2), e267–e275 (2011).
  • Desai SN, Esposito DB, Shapiro ED, Dennehy PH, Vázquez M. Effectiveness of rotavirus vaccine in preventing hospitalization due to rotavirus gastroenteritis in young children in Connecticut, USA. Vaccine 28(47), 7501–7506 (2010).
  • Boom JA, Tate JE, Sahni LC et al. Effectiveness of pentavalent rotavirus vaccine in a large urban population in the United States. Pediatrics 125(2), e199–e207 (2010).
  • Cortes JE, Curns AT, Tate JE et al. Rotavirus vaccine and health care utilization for diarrhea in U.S. children. N. Engl. J. Med. 365(12), 1108–1117 (2011).
  • Curns AT, Steiner CA, Barrett M, Hunter K, Wilson E, Parashar UD. Reduction in acute gastroenteritis hospitalizations among US children after introduction of rotavirus vaccine: analysis of hospital discharge data from 18 US states. J. Infect. Dis. 201(11), 1617–1624 (2010).
  • Wang FT, Mast TC, Glass RJ, Loughlin J, Seeger JD. Effectiveness of the pentavalent rotavirus vaccine in preventing gastroenteritis in the United States. Pediatrics 125(2), e208–e213 (2010).
  • Chang HG, Smith PF, Tserenpuntsag B, Markey K, Parashar U, Morse DL. Reduction in hospitalizations for diarrhea and rotavirus infections in New York state following introduction of rotavirus vaccine. Vaccine 28(3), 754–758 (2010).
  • Clark HF, Lawley D, Mallette LA, DiNubile MJ, Hodinka RL. Decline in cases of rotavirus gastroenteritis presenting to The Children’s Hospital of Philadelphia after introduction of a pentavalent rotavirus vaccine. Clin. Vaccine Immunol. 16(3), 382–386 (2009).
  • Bégué RE, Perrin K. Reduction in gastroenteritis with the use of pentavalent rotavirus vaccine in a primary practice. Pediatrics 126(1), e40–e45 (2010).
  • Kirkwood CD, Boniface K, Bishop RF, Barnes GL. Australian Rotavirus Surveillance Program: annual report, 2009/2010. Commun. Dis. Intell. 34(4), 427–434 (2010).
  • Buttery JP, Lambert SB, Grimwood K et al. Reduction in rotavirus-associated acute gastroenteritis following introduction of rotavirus vaccine into Australia’s National Childhood vaccine schedule. Pediatr. Infect. Dis. J. 30(1 Suppl.), S25–S29 (2011).
  • Snelling TL, Schultz R, Graham J et al. Rotavirus and the indigenous children of the Australian outback: monovalent vaccine effective in a high-burden setting. Clin. Infect. Dis. 49(3), 428–431 (2009).
  • Snelling TL, Andrews RM, Kirkwood CD, Culvenor S, Carapetis JR. Case–control evaluation of the effectiveness of the G1P[8] human rotavirus vaccine during an outbreak of rotavirus G2P[4] infection in central Australia. Clin. Infect. Dis. 52(2), 191–199 (2011).
  • Field EJ, Vally H, Grimwood K, Lambert SB. Pentavalent rotavirus vaccine and prevention of gastroenteritis hospitalizations in Australia. Pediatrics 126(3), e506–e512 (2010).
  • Lambert SB, Faux CE, Hall L et al. Early evidence for direct and indirect effects of the infant rotavirus vaccine program in Queensland. Med. J. Aust. 191(3), 157–160 (2009).
  • Hanquet G, Ducoffre G, Vergison A et al. Impact of rotavirus vaccination on laboratory confirmed cases in Belgium. Vaccine 29(29–30), 4698–4703 (2011).
  • Jit M, Mangen MJ, Melliez H et al. An update to “The cost–effectiveness of rotavirus vaccination: comparative analyses for five European countries and transferability in Europe”. Vaccine 28(47), 7457–7459 (2010).
  • Gagneur A, Nowak E, Lemaitre T et al.; IVANHOE investigators. Impact of rotavirus vaccination on hospitalizations for rotavirus diarrhea: the IVANHOE study. Vaccine 29(21), 3753–3759 (2011).
  • Martinón-Torres F, Bouzón Alejandro M, Redondo Collazo L et al.; ROTACOST research team. Effectiveness of rotavirus vaccination in Spain. Hum. Vaccin. 7(7), 757–761 (2011).
  • Braeckman T, Van Herck K, Raes M, Vergison A, Sabbe M, Van Damme P. Rotavirus vaccines in Belgium: policy and impact. Pediatr. Infect. Dis. J. 30(1 Suppl.), S21–S24 (2011).
  • Raes M, Strens D, Vergison A, Verghote M, Standaert B. Reduction in pediatric rotavirus-related hospitalizations after universal rotavirus vaccination in Belgium. Pediatr. Infect. Dis. J. 30(7), e120–e125 (2011).
  • Zeller M, Rahman M, Heylen E et al. Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium. Vaccine 28(47), 7507–7513 (2010).
  • Paulke-Korinek M, Rendi-Wagner P, Kundi M, Kronik R, Kollaritsch H. Universal mass vaccination against rotavirus gastroenteritis: impact on hospitalization rates in austrian children. Pediatr. Infect. Dis. J. 29(4), 319–323 (2010).
  • Paulke-Korinek M, Kundi M, Rendi-Wagner P et al. Herd immunity after two years of the universal mass vaccination program against rotavirus gastroenteritis in Austria. Vaccine 29(15), 2791–2796 (2011).
  • Atkins KE, Shim E, Pitzer VE, Galvani AP. Impact of rotavirus vaccination on epidemiological dynamics in England and Wales. Vaccine 30(3), 552–564 (2012).
  • Yen C, Tate JE, Wenk JD, Harris JM 2nd, Parashar UD. Diarrhea-associated hospitalizations among US children over 2 rotavirus seasons after vaccine introduction. Pediatrics 127(1), e9–e15 (2010).
  • Tate JE, Mutuc JD, Panozzo CA et al. Sustained decline in rotavirus detections in the United States following the introduction of rotavirus vaccine in 2006. Pediatr. Infect. Dis. J. 30(1 Suppl.), S30–S34 (2011).
  • Kirkwood CD, Boniface K, Barnes GL, Bishop RF. Distribution of rotavirus genotypes after introduction of rotavirus vaccines, Rotarix® and RotaTeq®, into the National Immunization Program of Australia. Pediatr. Infect. Dis. J. 30(1 Suppl.), S48–S53 (2011).
  • Hull JJ, Teel EN, Kerin TK et al.; National Rotavirus Strain Surveillance System. United States rotavirus strain surveillance from 2005 to 2008: genotype prevalence before and after vaccine introduction. Pediatr. Infect. Dis. J. 30(1 Suppl.), S42–S47 (2011).
  • Payne DC, Staat MA, Edwards KM et al.; New Vaccine Surveillance Network (NVSN). Direct and indirect effects of rotavirus vaccination upon childhood hospitalizations in 3 US Counties, 2006-2009. Clin. Infect. Dis. 53(3), 245–253 (2011).
  • Lopman BA, Curns AT, Yen C, Parashar UD. Infant rotavirus vaccination may provide indirect protection to older children and adults in the United States. J. Infect. Dis. 204(7), 980–986 (2011).
  • Widdowson MA, Meltzer MI, Zhang X, Bresee JS, Parashar UD, Glass RI. Cost–effectiveness and potential impact of rotavirus vaccination in the United States. Pediatrics 119(4), 684–697 (2007).
  • Jit M, Bilcke J, Mangen MJ et al. The cost-effectiveness of rotavirus vaccination: Comparative analyses for five European countries and transferability in Europe. Vaccine 27(44), 6121–6128 (2009).
  • Glass RI. Unexpected benefits of rotavirus vaccination in the United States. J. Infect. Dis. 204(7), 975–977 (2011).
  • Patel MM, López-Collada VR, Bulhões MM et al. Intussusception risk and health benefits of rotavirus vaccination in Mexico and Brazil. N. Engl. J. Med. 364(24), 2283–2292 (2011).
  • Greenberg HB. Rotavirus vaccination and intussusception – act two. N. Engl. J. Med. 364(24), 2354–2355 (2011).
  • WHO. Rotavirus vaccine and intussusception: report from an expert consultation. Wkly Epidemiol. Rec. 86(30), 317–321 (2011).
  • Buttery JP, Danchin MH, Lee KJ et al.; PAEDS/APSU Study Group. Intussusception following rotavirus vaccine administration: post-marketing surveillance in the National Immunization Program in Australia. Vaccine 29(16), 3061–3066 (2011).
  • Shui IM, Baggs J, Patel M et al. Risk of intussusception following administration of a pentavalent rotavirus vaccine in US infants. JAMA 307(6), 598–604 (2012).
  • RotaTeq, Rotavirus vaccine, live, oral pentavalent, package insert. Merck, NJ, USA (2009).
  • Bakare N, Menschik D, Tiernan R, Hua W, Martin D. Severe combined immunodeficiency (SCID) and rotavirus vaccination: reports to the Vaccine Adverse Events Reporting System (VAERS). Vaccine 28(40), 6609–6612 (2010).
  • Rotarix™, Rotavirus vaccine, live, oral. Package insert. GlaxoSmithKline, Rixensart, Belgium (2010).
  • Steele AD, Madhi SA, Louw CE et al. Safety, Reactogenicity, and Immunogenicity of Human Rotavirus Vaccine RIX4414 in Human Immunodeficiency Virus-positive Infants in South Africa. Pediatr. Infect. Dis. J. 30(2), 125–130 (2011).
  • Donato CM, Ch’ng LS, Boniface KF et al. Identification of strains of rotavirus vaccine Rotateq® in infants with gastroenteritis following routine vaccination. J. Infect. Dis. doi:10.1093/infdis/jis361 (2012) Epub ahead of print.
  • Payne DC, Szilagyi PG, Staat MA et al. Secular variation in United States rotavirus disease rates and serotypes: implications for assessing the rotavirus vaccination program. Pediatr. Infect. Dis. J. 28(11), 948–953 (2009).
  • De Wals P, De Serres G. Comments on the paper “the effectiveness of serogroup C meningococcal vaccine estimated from routine surveillance data”. [Rivest P, Allard R. Vaccine 20, 2533–2536 (2002)]. Vaccine 21(19–20), 2260–2261 (2003).
  • Broome CV, Facklam RR, Fraser DW. Pneumococcal disease after pneumococcal vaccination: an alternative method to estimate the efficacy of pneumococcal vaccine. N. Engl. J. Med. 303(10), 549–552 (1980).

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