Rotavirus Vaccines for Infants in Developing Countries in Africa and Asia: Considerations from a World Health Organization Sponsored Consultation
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1 SUPPLEMENT ARTICLE Rotavirus Vaccines for Infants in Developing Countries in Africa and Asia: Considerations from a World Health Organization Sponsored Consultation A. Duncan Steele, 1,2 Manish Patel, 3 Umesh D. Parashar, 3 John C. Victor, 2 Teresa Aguado, 1 and Kathleen M. Neuzil 2 1 Initiative for Vaccine Research, World Health Organization, Geneva, Switzerland; 2 Rotavirus Vaccine Programme, PATH, Seattle, Washington; and 3 Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia The World Health Organization (WHO) and its international partners have prioritized the development of rotavirus vaccines for the past 3 decades. In November 2005, the WHO s Strategic Advisory Group of Experts first reviewed the clinical efficacy data from 2 new live attenuated oral rotavirus vaccines, which demonstrated excellent protective efficacy against severe rotavirus disease in regions where they were evaluated. Despite these successes, the WHO has urged the clinical evaluation of these vaccines in populations of Africa and Asia, where most of the deaths due to rotavirus occur, and has emphasized the need for ongoing postlicensure safety monitoring in countries introducing vaccines. Clinical studies in Africa and Asia will soon provide data on the efficacy of both new vaccines in these populations. A WHO international consultative meeting convened to evaluate how to use these imminent data for the future use of rotavirus vaccines in developing countries. In brief, it was agreed that (1) even vaccines with lesser efficacy in developing countries, compared with industrialized countries, would still lead to substantial public health benefits and would be cost-effective in saving lives in Africa and Asia; (2) criteria, such as the WHO mortality strata and local epidemiology of rotavirus infection, would be appropriate measures for extrapolating the clinical data to other regions and countries; and (3) research toward understanding the programmatic limitations of rotavirus vaccine use may help develop strategies to improve vaccine uptake and overall impact. Rotavirus is associated with an annual toll of more than half a million deaths among infants and young children worldwide, with 185% of these deaths occurring in developing countries [1]. General improvements in the Potential conflicts of interest: none reported. Financial support: Initiative for Vaccine Research, World Health Organization. Supplement sponsorship: This article was published as part of a supplement entitled Global Rotavirus Surveillance: Preparing for the Introduction of Rotavirus Vaccines, which was prepared as a project of the Rotavirus Vaccine Program, a partnership between PATH, the World Health Organization, and the US Centers for Disease Control and Prevention, and was funded in full or in part by the GAVI Alliance. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention (CDC). This article received clearance through the appropriate channels at the CDC prior to submission. Presented in part: 3rd Annual Global Immunization Meeting, Geneva, Switzerland, February 2008; and 8th Global Vaccine Research Forum, Paris, France, July Reprints or correspondence: Dr. Duncan Steele, Rotavirus Vaccine Programme, PATH, 1455 Leary Way NW, Seattle, WA (dsteele@path.org). The Journal of Infectious Diseases 2009; 200: by the Infectious Diseases Society of America. All rights reserved /2009/20009S1-0008$15.00 DOI: / overall management and outcome of diarrheal diseases as the result of global interventions, such as oral rehydration therapy, the World Health Organization (WHO) program on Integrated Management of Childhood Illnesses, and zinc treatment, have been observed over the past 2 decades. However, the effect of this improvement on the magnitude of rotavirus infection has not been significant, which indicates that these successful interventions against the bacterial and parasitic microbes causing diarrheal illness may have a less dramatic effect on rotavirus infection and disease. Furthermore, as estimates of the mortality associated with diarrheal diseases decrease globally [2], the proportion of hospitalizations due to severe rotavirus infection has been observed to increase [3]. Thus, to specifically reduce the burden of rotavirus disease, the WHO, the GAVI Alliance (formerly known as the Global Alliance for Vaccines and Immunization), and the international community have prioritized the development and in- Rotavirus Vaccines for Infants in Developing Countries JID 2009:200 (Suppl 1) S63
2 Figure 1. Global map showing the regions and GAVI Alliance eligible countries approved for rotavirus vaccine subsidy in impact 1 (blue) and impact 2 (green) countries. troduction of rotavirus vaccines for almost 30 years [4 6]. In 2006, tremendous strides forward in the fight against rotavirus disease occurred. Clinical studies of each of the 2 new rotavirus vaccines (Rotarix [GlaxoSmithKline Biologicals] and RotaTeq [Merck]) that involved 160,000 infants in Latin America, Europe, and the United States demonstrated excellent protective efficacy (185% and 195%, respectively) against severe rotavirus disease in these settings [7, 8]. In addition, the vaccines demonstrated comparable efficacy against severe rotavirus in equivalent settings when both were evaluated in Europe. The 2 vaccines were also reported to be safe with respect to intussusception and were soon licensed in the countries of manufacture (by the European Medicines Agency for Rotarix and by the US Food and Drug Administration for RotaTeq). The prompt introduction of the vaccines in many countries in the Americas and in some countries in Europe followed [9]. Nevertheless, despite these successes, several questions remained about the potential impact of these live attenuated oral rotavirus vaccines among children in developing countries of Africa and Asia, where the major burden of severe rotavirus disease is seen [10]. In fact, as early as 1997, the WHO recommended that clinical trials be required in these developing countries to understand the efficacy of oral vaccines among infants living in impoverished conditions [5, 6]. In November 2005, the WHO s Strategic Advisory Group of Experts (SAGE) first reviewed the clinical trial data of the 2 oral live attenuated rotavirus vaccines [11]. Noting that live oral vaccines may not be fully effective in protecting the poorest children in developing countries [11, p 8], SAGE considered that rotavirus vaccine introduction would be appropriate in regions where successful phase III trials have been conducted. The WHO strongly recommended the inclusion of rotavirus vaccination in the national immunization programs in countries and regions where vaccine efficacy data suggested a significant public health impact (ie, in Latin America and Europe) and where the appropriate infrastructure and financing mechanisms were available [11]. SAGE also urged the generation of efficacy data in Africa and Asia, and efficacy trials of the 2 vaccines are now underway among impoverished populations in these regions. After the SAGE recommendations were es- S64 JID 2009:200 (Suppl 1) Steele et al
3 Table 1. Characteristics of the Clinical Trial Sites Conducting Efficacy Studies in Africa and Asia Vaccine, country Setting(s) No. of participants Comments Time when results wereorwillbe available Rotarix (GSK Biologicals) South Africa Urban, squatter 3167 High background prevalence of HIV infection; strain surveillance ongoing Malawi Rural and urban 1773 High background prevalence of HIV infection; strain surveillance ongoing RotaTeq (Merck) Ghana Rural 1800 High background prevalence of malaria; strain surveillance ongoing 4th quarter th quarter nd quarter 2009 Kenya Rural 787 High prevalence of HIV infection and malaria 2nd quarter 2009 Mali Urban 1950 High background prevalence of malaria 2nd quarter 2009 Bangladesh Rural 896 High prevalence of malnutrition and diarrheal diseases; strain surveillance ongoing 2nd quarter 2009 Vietnam Urban 483 2nd quarter 2009 NOTE. Data are derived from HIV, human immunodeficiency virus. tablished in November 2006, the GAVI Alliance Board approved an investment case for public sector procurement of rotavirus vaccines for eligible countries in Latin America and Europe (Figure 1). The GAVI Alliance further stated that a recommendation for purchase of rotavirus vaccines for Africa and Asia would be made in a second phase after results of the ongoing clinical trials in these regions are available and after SAGE makes a recommendation for vaccine use globally. This process is thought to likely occur during 2009 and early KEY UNADDRESSED ISSUES REGARDING ROTAVIRUS VACCINES FOR AFRICA AND ASIA Several key questions regarding development, testing, and implementation of rotavirus vaccines for countries in Africa and Asia have not been fully addressed. First, the current SAGE recommendation for use of rotavirus vaccines has led to some confusion, leaving some eastern Mediterranean countries, for instance, unclear as to why they have not qualified for GAVI Alliance procurement, even though from a rotavirus epidemiological and population socioeconomic viewpoint, some Mediterranean countries may be more similar to GAVI Alliance countries in Latin America and eastern Europe than those in sub-saharan Africa and Southeast Asia. More broadly, this raises the issue of how data from these ongoing trials in some countries of Africa and Asia should be extrapolated to regions without clinical trial data. Second, although the efficacy of live attenuated oral rotavirus vaccines in developing countries is expected to be lower than that seen in industrialized and middle-income countries, the level of protective efficacy that would be required to garner a WHO SAGE global recommendation or a GAVI Alliance approval for vaccine subsidy in developing countries with high levels of rotavirus-associated mortality has not been established. Third, what specific research should be pursued to potentially improve the performance of rotavirus vaccines, in the event that efficacy data from ongoing trials are suboptimal? Fourth, what are the key programmatic considerations (eg, age of vaccine administration, vaccination schedule, and postlicensure safety monitoring) to consider for use of vaccines in these settings? Finally, for vaccines from emerging market producers that are still in early stages of development, what is the optimal strategy for testing and implementation? More specifically, should prelicensure trials of these vaccines be required to demonstrate safety with respect to intussusception in prelicensure trials, and what should be the most relevant clinical end points for efficacy? To address these issues, the WHO, the US Centers for Disease Control and Prevention, and the Rotavirus Vaccine Programme at PATH convened a meeting of global-, regional-, and countrylevel rotavirus experts and immunization opinion leaders in November The deliberations of this group are summarized in this article. INTERPRETATION OF RESULTS OF ONGOING CLINICAL TRIALS IN AFRICA AND ASIA AND EXTRAPOLATION OF DATA The rotavirus vaccine trials in impoverished populations in Africa and Asia were designed to evaluate the efficacy of currently licensed rotavirus vaccines against the outcome of severe rotavirus gastroenteritis, as recommended by the WHO (Table 1) [12]. In addition, these studies will address an important set of secondary outcomes, including strain-specific efficacy, efficacy against rotavirus disease of any severity, effectiveness against severe gastroenteritis due to any cause, vaccine immunogenicity, and efficacy of different dosing regimens ( Rotavirus Vaccines for Infants in Developing Countries JID 2009:200 (Suppl 1) S65
4 Figure 2. Ranking of the site countries for rotavirus vaccine trials against various parameters. Data are derived from [15]. GDP, gross domestic product; HIV, human immunodeficiency virus. As recommended by the WHO, the rotavirus vaccines in these trials are given concomitantly with Expanded Programme on Immunization vaccines, including oral polio vaccine [12]. Phase III randomized controlled clinical efficacy studies of the 2 rotavirus vaccines are ongoing in 5 countries in Africa and 2 countries in Asia (Table 1). Multicenter efficacy trials of both vaccines are ongoing in Africa for Rotarix in South Africa and Malawi and for RotaTeq in Ghana, Mali, and Kenya. In Asia, a multicenter efficacy trial for RotaTeq is also ongoing at sites in Vietnam and Bangladesh. Full results from these trials were or will be available for SAGE and other decision makers to review during Although these particular studies will answer important questions about the use of these vaccines in Africa and Asia, it was acknowledged that no single study can answer all of the questions about rotavirus vaccine use in diverse populations. Thus, results from these studies should be interpreted in the context of previous trials and ongoing effectiveness studies in early-introducer countries. Many factors may contribute to reduced efficacy of live attenuated oral rotavirus vaccines in populations in developing countries [13]. These include substantial differences in the epidemiology of rotavirus disease between the industrialized world and developing countries, competing infections with other enteric agents, maternal antibodies and antibodies in breast milk, concomitant administration of oral polio vaccine, or factors that impair the host immune response (eg, malnutrition, interfering microbes, and infection, such as human immunodeficiency virus [HIV] infection, malaria, and tuberculosis). Nevertheless, even a vaccine with suboptimal efficacy may substantially reduce rotavirus-associated mortality in resource-poor countries in Africa and Asia and could be considered to be a cost-effective intervention (Table 2). Because of the potential impact of these vaccines even at moderate levels of efficacy, an absolute point estimate of efficacy below which vaccine is deemed to have failed was not considered to be appropriate. The current clinical trial sites in Africa and Asia include countries with the highest mortality among children aged!5 years according to the WHO strata [15]; data from these countries will provide a framework for how the currently available rotavirus vaccines perform in some of the most impoverished regions of the world (Table 3 and Figure 2). The question of how to use the data from the current clinical trial sites for both rotavirus vaccines for extrapolation to regions (eg, the Middle Eastern region) or countries not included in these trials is important to consider. One such criterion for extrapolation might be the WHO mortality strata [15], which are potentially more reflective of the environmental and social conditions in which populations are living in resource-poor regions with endemic disease and, thus, are more predictive of how live attenuated oral vaccines might perform in a country than is the country s geographic location. It is also important that, in addition to the WHO mortality strata, gathering and comparing epidemiological data (eg, seasonality, strains, and age distribution) on rotavirus disease would provide additional criteria for extrapolation of efficacy data on rotavirus vaccines in Asia and Africa. However, not all of these data related to the reasons for a lower efficacy would likely be available before a global recommendation, and postlicensure effectiveness studies will be additional important sources of information on the public health benefit of rotavirus vaccines. S66 JID 2009:200 (Suppl 1) Steele et al
5 Table 2. Estimates of Cumulative Impact and Cost-Effectiveness for 51 GAVI Alliance Eligible Countries in Africa and Asia during Predicted vaccine efficacy, % Potential no. of lives saved Cost per DALY averted, US$ , million million million million 27 NOTE. life year. Generated using data from [1] and [14]. DALY, disability-adjusted RESEARCH CONSIDERATIONS AND POSTLICENSURE MONITORING OF VACCINE SAFETY AND EFFECTIVENESS Many of the research challenges to the good performance of live attenuated oral rotavirus vaccines in developing countries are described in this supplement by Shane et al [13]. Some of these questions have been examined in clinical trials initiated by the WHO and funded by the international public sector. Thus, the question of rotavirus vaccine interaction with oral polio vaccine has been examined with varying vaccine concentrations, numbers of doses, and schedules of administration in infants in Bangladesh and South Africa [16, 17]. In addition, a phase II safety and immunogenicity study involving HIVinfected infants has been conducted, and the results should be available in early 2009 [18]. Furthermore, the group acknowledged that some of the factors proposed would be difficult to pragmatically address for the programmatic use of rotavirus vaccines (eg, changes in breastfeeding practices), although understanding their impact may be important for evaluating how to enhance vaccine uptake in the event that efficacy is found to be suboptimal in the ongoing trials. The WHO Global Advisory Committee for Vaccine Safety is reviewing the safety data generated on both of these vaccines on an ongoing basis. Although the WHO Global Advisory Committee for Vaccine Safety has found the prelicensure safety data for these vaccines to be reassuring to date, it has emphasized the need for ongoing postlicensure safety monitoring [19]. Ongoing safety surveillance in the United States with the introduction of RotaTeq has also been reassuring [20]. In addition, several studies of postlicensure vaccine impact and safety of rotavirus vaccines are underway in Latin America, and data from these studies will likely become available in the next 1 2 years. Similarly, evaluations are ongoing to address the impact and effectiveness of vaccination in reducing the burden of severe rotavirus disease in early-introducing countries in the Americas and Europe. For instance, the introduction of RotaTeq in Nicaragua is being evaluated for vaccine impact, and similar studies are planned in El Salvador with Rotarix. These postlicensure evaluations will assess vaccine performance in less than the ideal conditions in clinical trials and will also provide key data on issues such as effectiveness of a partial series of vaccination and strain-specific effectiveness. Furthermore, these evaluations could demonstrate unanticipated benefits of vaccination, such as the substantial indirect benefit to unvaccinated persons of reduction of transmission of rotavirus because of vaccination of a proportion of the population (ie, herd benefits). Likewise, a cluster-randomized vaccine effectiveness study with Rotarix is underway in Bangladesh, and this trial could provide valuable information on potential herd benefits in a developing country. DEVELOPMENT OF OTHER CANDIDATE ROTAVIRUS VACCINES In addition to consideration of how the currently licensed rotavirus vaccines may be evaluated, the research agenda for the future and for the alternative vaccine candidates under development is important. Other current live attenuated oral rotavirus vaccine candidates include the bovine-human reassortant (UK strain) rotavirus vaccine, the neonatal rotavirus vaccine candidates 116E and RV3, and future nonliving rotavirus vaccine candidates (Table 4). The live attenuated rotavirus vaccine candidates (UK reassortant, 116E, and RV3) are currently under clinical development by vaccine manufacturers in Brazil, China, India, and Indonesia, with support from the international public health sector in most of these initiatives. Table 3. Clinical Trial Sites, by World Health Organization (WHO) Mortality Strata WHO mortality strata Mortality rate among children aged!5 years Mortality rate among men Vaccine trial sites in Africa Vaccine trial sites in Asia A Very low Very low B Low Low Vietnam C Low High D High High Ghana, Mali Bangladesh E High Very high South Africa, Malawi, Kenya NOTE. Data are derived from [15]. Rotavirus Vaccines for Infants in Developing Countries JID 2009:200 (Suppl 1) S67
6 Table 4. Alternative Nonliving Approaches to Rotavirus Vaccines Candidate Properties Preclinical evaluation Level of protection Developer VP6 Inactivated virus Virus-like particles Escherichia coli expressed recombinant protein Viral particles inactivated by physical or chemical methods Expressed recombinant viral proteins (various combinations of VP2, VP4, VP6, and VP7) Tested in mice Tested in mice, rabbits, and gnotobiotic piglets Tested in mice, rabbits, and gnotobiotic piglets Effective in reducing or preventing rotavirus shedding when given orally, intranasally, or intrarectally with adjuvant Effective in reducing or preventing rotavirus shedding with or without adjuvants Effective in reducing or preventing rotavirus shedding in mice and rabbits; adjuvants enhance protective effect; more effective after intranasal delivery than after oral delivery R. Ward; Children s Hospital Cincinnati B. Jiang; CDC, Atlanta M. Conner; Baylor College of Medicine, Houston NOTE. Adapted from [21]. CDC, Centers for Disease Control and Prevention. In most cases, the vaccines have undergone phase I and II clinical studies showing some level of proof of principle, and phase III clinical trials are planned. In addition, the UK bovinehuman reassortant vaccine is being developed by several vaccine manufacturers and biotechnology companies. Finally, the rhesus-human reassortant vaccine, which was licensed as Rota- Shield by Wyeth Vaccines, is being further developed by an international foundation. Similar to the WHO recommendations for the current clinical trials with the licensed rotavirus vaccines, trials of these new rotavirus vaccines should evaluate efficacy against severe rotavirus disease on the basis of a consistently applied standardized severity score that would be comparable across studies [12]. Postlicensure studies that measure reductions in mortality could also be considered, although these studies will be technically challenging to conduct and will require considerable investment of resources. Demonstration of serotype cross-protection against each of the epidemiologically important strains is unlikely in the clinical trials, because it is impossible to predict which strain will be more prevalent during the period of the trials. Finally, the new rotavirus vaccines in development should undergo a rigorous process of national and international regulatory review. Although monitoring for intussusception with these candidate oral rotavirus vaccines will be important, generation of these data would likely occur through postlicensure monitoring rather than through prelicensure clinical trials. Because intussusception is uncommon early in life, when rotavirus vaccines are administered (with an estimated rate of cases per 100,000 infants per year), very large and expensive clinical trials that are similar to the trials of the 2 licensed vaccines would be required to evaluate safety. Furthermore, by the time that these candidate rotavirus vaccines are introduced into routine immunization programs in Africa and Asia, considerable postmarketing safety data on the 2 current vaccines would be available from early-introducer countries in the Americas and Europe to inform deliberations about safety. Several nonliving approaches for parenteral rotavirus vaccine candidates are in development, and most have undergone animal testing, although none has yet been evaluated in humans [21]. The question of whether this approach to rotavirus vaccines is needed for developing countries will, to some extent, depend on the successful introduction of safe, efficacious, and affordable live attenuated rotavirus vaccines in the poorest countries and on the impact that these vaccines are able to make to reduce the global burden of disease. Because of the many potential challenges to the successful performance of live attenuated oral rotavirus vaccines in developing countries and the possibility that these vaccines may be associated with intussusception, it would be prudent to consider further development of these nonliving vaccines as an insurance policy if live oral vaccines are not successful. PROGRAMMATIC CONSIDERATIONS Enormous progress has been achieved in the development of safe and effective rotavirus vaccines, which are being introduced into childhood immunization schedules worldwide. The WHO Position Paper on Rotavirus Vaccines supports their introduction [22]. Nevertheless, the full promise of rotavirus vaccines to have an impact on the global mortality may not yet be within our reach not necessarily because of the effect of the vaccines but because of the systems that are required to deliver them. Barriers still exist to the full implementation and delivery of rotavirus vaccines, including the dynamics of the systems used to deliver vaccines in these infant populations. These include (1) the predicted impact on the cold chain of both current vaccine formulations; (2) the relatively low immunization coverage in many countries, particularly Africa; (3) the delay for the administration of the routine Expanded Programme on S68 JID 2009:200 (Suppl 1) Steele et al
7 Immunization vaccines, especially when coupled with the age restriction on the use of these vaccines [22]; and (4) the ability to reach infants in the hard-to-reach areas, who may have the lowest vaccination coverage and, potentially, the highest risk of death from acute dehydrating rotavirus diarrhea. The rotavirus vaccines that we have today and, potentially, those of tomorrow are likely to make a significant difference in the magnitude of rotavirus-associated disease and mortality in all regions of the world. However, no matter how good the vaccines might be in Africa and Asia, we will need to bolster the systems used to deliver these vaccines for their full impact to be realized. References 1. Parashar U, Burton A, Lanata C, et al. Global mortality associated with rotavirus disease among children in J Infect Dis 2009; 200(Suppl 1):S9 15 (in this supplement). 2. Kosek M, Bern C, Guerrant RL. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and Bull World Health Organ 2003; 81: Bresee JS, Hummelman E, Nelson EAS, Glass RI. Rotavirus in Asia: the importance of surveillance for informing decisions about rotavirus vaccines. J Infect Dis 2005; 192(Suppl 1):S de Zoysa I, Feachem RV. Interventions for the control of diarrhoeal diseases among young children: rotavirus and cholera immunization. Bull World Health Organ 1985; 63: World Health Organization report of the meeting on rotavirus vaccines for the immunization of children in developing countries. Geneva: World Health Organization, World Health Organization report of the meeting on the future directions for rotavirus research in developing countries. Geneva: World Health Organization, Ruiz-Palacios GM, Perez-Schael I, Velasquez R, et al. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl JMed2006; 354: Vesikari T, Matson DO, Dennehy P, et al. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 2006; 354: De Oliveira LH, Danovaro-Holliday MC, Ruiz Matus C, Andrus JK. Rotavirus vaccine introduction in the Americas: progress and lessons. Expert Rev Vaccines 2008; 7: Glass RI, Bresee JS, Turcois R, Fischer TK, Parashar U, Steele AD. Rotavirus vaccines: targeting the developing world. J Infect Dis 2005; 192(Suppl 1):S World Health Organization conclusions and recommendations from SAGE. Wkly Epidemiol Rec 2006; 81: World Health Organization guidelines to assure the quality, safety and efficacy of live attenuated rotavirus vaccines (oral). WHO technical report series no Geneva: World Health Organization, Patel M, Shane AL, Parashar UD, Jiang B, Gentsch JR, Glass RI. Oral rotavirus vaccines: how well will they work where they are needed most? J Infect Dis 2009; 200(Suppl 1):S39 48 (in this supplement). 14. Atherly D, Dreibelbis R, Parashar UD, Levin C, Wecker J, Rheingans RD. Rotavirus vaccination: cost-effectiveness and impact on child mortality in developing countries. J Infect Dis 2009; 200(Suppl 1):S28 38 (in this supplement). 15. World Health Organization (WHO). List of member states by WHO region and mortality stratum, Available at: whr/2003/en/member_states_ _en.pdf. Accessed 23 June Zaman K, Sack DA, Yunus M, et al. Successful co-administration of a human rotavirus and oral poliovirus vaccines in Bangladeshi infants in a 2-dose schedule at 12 and 16 weeks of age. Vaccine 2009; 27: Steele AD, De Vos BV, Tumbo JM, et al. Co-administration study in South African infants of a live-attenuated oral human rotavirus vaccine (RIX4414) and poliovirus vaccines. Vaccine 2008 (Epub ahead of print). 18. Steele AD, Cunliffe N, Tumbo J, Madhi SA, De Vos B, Bouckenooghe A. A review of rotavirus infection in and vaccination of human immunodeficiency virus infected children. J Infect Dis 2009; 200(Suppl 1):S57 62 (in this supplement). 19. Report of the Global Advisory Committee on Vaccine Safety. Wkly Epidemiol Rec 2006; 81: Centers for Disease Control and Prevention. Postmarketing monitoring of intussusception after RotaTeq vaccination United States, February 1, 2006 February 15, MMWR Morb Mortal Wkly Rep 2007; 56: Ward RD, McNeal MM, Steele AD. Does the world need another rotavirus vaccine? Ther Clin Risk Manag 2008; 4: World Health Organization position paper on rotavirus vaccines. Wkly Epidemiol Rec 2007; 82: Rotavirus Vaccines for Infants in Developing Countries JID 2009:200 (Suppl 1) S69
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