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Implementation of Rotavirus Surveillance and Vaccine Introduction--World Health Organization African Region, 2007-2016.

Rotavirus is a leading cause of severe pediatric diarrhea globally, estimated to have caused 120,000 deaths among children aged <5 years in sub-Saharan Africa in 2013 (1). In 2009, the World Health Organization (WHO) recommended rotavirus vaccination for all infants worldwide (2). Two rotavirus vaccines are currently licensed globally: the monovalent Rotarix vaccine (RV1, GlaxoSmithKline; 2-dose series) and the pentavalent RotaTeq vaccine (RV5, Merck; 3-dose series). This report describes progress of rotavirus vaccine introduction (3), coverage (using estimates from WHO and the United Nations Children's Fund [UNICEF]) (4), and impact on pediatric diarrhea hospitalizations in the WHO African Region. By December 2016, 31 (66%) of 47 countries in the WHO African Region had introduced rotavirus vaccine, including 26 that introduced RV1 and five that introduced RV5. Among these countries, rotavirus vaccination coverage (completed series) was 77%, according to WHO/UNICEF population-weighted estimates. In 12 countries with surveillance data available before and after vaccine introduction, the proportion of pediatric diarrhea hospitalizations that were rotavirus-positive declined 33%, from 39% preintroduction to 26% following rotavirus vaccine introduction. These results support introduction of rotavirus vaccine in the remaining countries in the region and continuation of rotavirus surveillance to monitor impact.

The status of rotavirus vaccine introduction and 2016 WHO/UNICEF estimates of national vaccination coverage were obtained from the WHO repository (3,4). Among African Region countries that have introduced rotavirus vaccine into their national Expanded Programs on Immunization, most recommend that rotavirus doses coincide with administration of the infant doses of diphtheria and tetanus toxoids and pertussis (DTP) vaccine (at ages 6 and 10 weeks for RV1 and at ages 6,10, and 14 weeks for RV5); most countries are using RV1 (5). Because the WHO/UNICEF estimates do not include a coverage estimate for the first dose of rotavirus vaccine or the second dose of DTP vaccine, rotavirus vaccination coverage (completed series of either 2 RV1 or 3 RV5 doses) was compared with first-dose and third-dose coverage for DTP. Countries that have introduced rotavirus vaccine were grouped by year of vaccine introduction for analysis.

Rotavirus surveillance data were collected through sentinel hospitals participating in the African Rotavirus Surveillance Network (ARSN), which was established in four countries in 2006 and had expanded to 29 countries by 2016 (Figure) (6). Surveillance staff members at sentinel sites in ARSN enroll children aged <5 years who are hospitalized for acute diarrhea ([greater than or equal to] 3 looser than normal stools in a 24-hour period before hospitalization, with duration of illness [less than or equal to] 7 days before hospitalization) and collect a stool specimen, which is tested for rotavirus using an enzyme immunoassay. Countries were included in this analysis if their sites collected and tested at least 80 specimens over at least 11 months in a given year. The percentage of tested specimens that were positive for rotavirus was calculated in the vaccine preintroduction and postintroduction periods, by country. The year of rotavirus vaccine introduction was considered a transition period and was excluded from calculations.

Overall, 31 (66%) countries in the region had introduced rotavirus vaccine into their national immunization schedules by December 2016, with 26 introducing RV1 and five introducing RV5 (Table 1). Among all countries, completed series rotavirus vaccination coverage was 77% (population-weighted average); national coverage ranged from 24% (Sao Tome and Principe, 2016 introduction) to 98% (Rwanda, 2012 introduction). When grouping by year of vaccine introduction, the highest overall population-weighted coverage (82%) was in countries that introduced the vaccine before 2014. These same countries also had the smallest average percentage-point difference between completed rotavirus vaccination coverage and DTP1 coverage (overall, 11 percentage points less than DTP1).

Surveillance data were available for 12 and 18 countries during the vaccine preintroduction and postintroduction periods, respectively (Table 2). The average percentage of tested stool specimens that were positive for rotavirus during the vaccine preintroduction period was 41%, ranging from 20% (Ethiopia) to 51% (Togo). During the vaccine postintroduction period, the average percentage of rotavirus-positive specimens was 24%, ranging from 12% (Madagascar) to 41% (Mauritius). In the 12 countries with both vaccine preintroduction and postintroduction data, rotavirus positivity declined by 33% overall (range = 2%-62%), from 39% in the preintroduction period to 26% in the postintroduction period (p<0.001); in these countries, the overall population-weighted 2016 completed rotavirus vaccination series coverage was 82%. In 2016, the overall percentage of positive rotavirus stool specimens was 26% in countries that had introduced the vaccine in 2015 or earlier, and 43% in countries that had not yet introduced the vaccine (p<0.001).

Discussion

Countries in the WHO African Region have made significant progress in the introduction of rotavirus vaccines, with 31 (66%) of 47 member countries having introduced rotavirus vaccine into their national schedules by December 2016. In 2016, the overall completed series rotavirus vaccination coverage in these countries was 77%, which was lower than coverage for DTP1 and DTP3. Some of this difference might be attributable to challenges that are common to new vaccine introduction (e.g., it can take time for all vaccination clinics to have reliable cold chain space and a steady stock of a new vaccine). In addition, challenges specific to the recording and reporting of coverage for new vaccines include mid-year introductions, unavailability of updated data tools, and inadequate orientation of health workers on use of vaccine tally sheets. Another factor specific to rotavirus is the issue of age restrictions. Because of concerns about a potential increased risk for intussusception in older infants who receive the vaccine, WHO initially recommended that rotavirus vaccination be administered only to children aged <32 weeks (2). In 2013, WHO recommended lifting these restrictions based on new data and a risk-benefit analysis (7); however, some countries, or some health workers, might still be administering rotavirus vaccine with age restrictions. Additional research is needed to better understand the impact of lifting age restrictions on coverage, and the difference between rotavirus and DTP vaccination coverage.

Surveillance data from ARSN indicate that, among countries with data available both preceding and following rotavirus vaccine introduction, the proportion of rotavirus-positive hospitalizations for diarrhea among children aged <5 years declined 33% following rotavirus vaccine introduction; overall declines were especially notable in countries that had introduced rotavirus vaccine before 2015. These results are particularly encouraging given rotavirus vaccines' lower efficacy in low-income settings (50%-64% efficacy) than in high-income and middle-income settings (85%-100% efficacy) (8), which had raised concerns about the public health impact of their introduction. However, consistent with recent global analyses demonstrating substantial rotavirus vaccine impact across country income strata (9), the present analysis suggests that rotavirus vaccination has had a meaningful impact on rotavirus disease in Africa.

Sixteen countries in the WHO African Region had not yet introduced rotavirus vaccine as of December 2016; 10 are eligible for Gavi financial support, four of which have received approval. Apart from funding, other factors can affect rotavirus vaccine introduction and subsequent coverage. Coverage with routinely recommended vaccines, as a marker of immunization system function, highlights several countries in the region where the immunization infrastructure needs strengthening. Armed conflict and natural disasters, experienced by several countries in the region, can further stress immunization services. Even under routine circumstances, cold chain management, vaccine transportation, and human resource constraints can negatively affect vaccination coverage; these challenges might be experienced most acutely in countries with large rural populations.

The findings in this report are subject to at least five limitations. First, UNICEF/WHO coverage estimates are based on the best estimates of a combination of administrative data and survey data, each of which might be subject to overreporting or underreporting. Other factors potentially causing a discrepancy between rotavirus coverage and DTP coverage include the inability to compare the final dose of RV1 to the second dose of DTP, and the lack of data on coverage with the first dose of rotavirus vaccines. Second, although protocols for rotavirus surveillance are standardized across the entire network, there are a limited number of surveillance sites in each country; these might not be representative of pediatric diarrheal illness across the country and might provide an incomplete picture of impact. Third, immunization and surveillance data quality vary among countries. Fourth, not all sites have been able to conduct continuous rotavirus disease surveillance, and data were not included in these results if analysis criteria were not met. Finally, rotavirus surveillance data are not available for all countries before introduction, limiting the ability to assess vaccine impact in countries without vaccine preintroduction data or those that are not part of the ARSN.

Overall, substantial progress has been made in the introduction of rotavirus vaccine and surveillance for rotavirus disease in countries in the WHO African Region. In countries where rotavirus vaccine has been introduced, a substantial decline in the percentage of rotavirus-associated pediatric diarrhea hospitalizations was observed. As rotavirus vaccination coverage increases, an even greater decline might be expected; however, continuous surveillance is a critical component of measuring vaccine impact. Financial support from Gavi, the Vaccine Alliance, has played a key role in rotavirus vaccine introduction and rotavirus surveillance in the region (10). Nonetheless, Gavi support will not continue indefinitely; as their economies improve, countries will graduate from Gavi support and begin to finance the total cost of the vaccine. Maintaining surveillance for rotavirus disease will provide important data necessary to promoting continued investment in rotavirus vaccination. Rotavirus vaccination is a critical element in reducing child deaths from diarrhea and contributing to the improvement of child health globally.

Summary

What is already known about this topic?

Rotavirus is a leading cause of severe pediatric diarrhea worldwide, and a disproportionate number of deaths occur in countries in the World Health Organization (WHO) African Region. WHO recommends rotavirus vaccination for all infants worldwide.

What is added by this report?

As of December 2016, 31 of 47 (66%) countries in the WHO African Region had introduced rotavirus vaccination into their national schedules. Among these countries, the overall coverage for the completed series of rotavirus vaccination was 77% in 2016. In 12 countries with available sentinel hospital surveillance data before and after rotavirus vaccine introduction, the proportion of pediatric diarrhea hospitalizations that were rotavirus-positive declined 33%, from 39% to 26%.

What are the implications for public health practice?

Continued commitment to improving rotavirus vaccination coverage in the WHO African Region should contribute to reducing the morbidity and mortality associated with this disease. Maintaining and enhancing the existing surveillance network will be critical to the ability to measure vaccine impact.

Acknowledgment

Gavi, the Vaccine Alliance.

Conflict of interest

No conflicts of interest were reported.

References

(1.) Tate JE, Burton AH, Boschi-Pinto C, Parashar UD; World Health Organization-Coordinated Global Rotavirus Surveillance Network. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000-2013. Clin Infect Dis 2016;62(Suppl 2):S96-105. https://doi.org/10.1093/cid/civ1013

(2.) World Health Organization. Rotavirus vaccines: an update. Wkly Epidemiol Rec 2009;84:533-40.

(3.) World Health Organization. Immunization vaccines and biologicals database, September 2016. Geneva, Switzerland: World Health Organization; 2016. http://www.who.int/immunization/monitoring_ surveillance/data/en/

(4.) World Health Organization (WHO). WHO/UNICEF estimates of national immunization coverage. Geneva, Switzerland: World Health Organization/United Nations Children's Fund; 2016. http://www who.int/immunization/monitoring_surveillance/routine/coverage/en/ index4.html

(5.) World Health Organization (WHO). WHO vaccine-preventable diseases: monitoring system. 2017 global summary. Geneva, Switzerland: World Health Organization; 2017. http://apps.who.int/immunization_ monitoring/globalsummary/schedules

(6.) Mwenda JM, Tate JE, Parashar UD, et al. African rotavirus surveillance network: a brief overview. Pediatr Infect Dis J 2014;33(Suppl 1):S6-8. https://doi.org/10.1097/INF.0000000000000174

(7.) World Health Organization. Rotavirus vaccines. WHO position paper-- January 2013. Wkly Epidemiol Rec 2013;88:49-64.

(8.) Soares-Weiser K, Maclehose H, Bergman H, et al. Vaccines for preventing rotavirus diarrhoea: vaccines in use. Cochrane Database Syst Rev 2012;11:CD008521.

(9.) Burnett E, Jonesteller CL, Tate JE, Yen C, Parashar UD. Global impact of rotavirus vaccination on childhood hospitalizations and mortality from diarrhea. J Infect Dis 2017;215:1666-72. https://doi.org/10.1093/ infdis/jix186

(10.) Gavi, the Vaccine Alliance. Countries approved for support. Geneva, Switzerland, Gavi; 2017. http://www.gavi.org/results/countries-approved-for-support/

Jason M. Mwenda, PhD [1]; Rachel M. Burke, PhD [2,3]; Keith Shaba, MPH [1]; Richard Mihigo, MD [1]; Mable Carole Tevi- Benissan, MD [1]; Mutale Mumba, MBChB [1]; Joseph Nsiari-Muzeyi Biey, MD [1]; Dah Cheikh, MD [1]; Alain Poy, MSc [1]; Felicitas R. Zawaira, MD [1]; Negar Aliabadi, MD [2]; Jacqueline E. Tate, PhD [2]; Terri Hyde, MD [5]; Adam L. Cohen, MD [4]; Umesh D. Parashar, MBBS [2]

[1] World Health Organization Regional Office for Africa, Brazzaville, Republic of the Congo; [2] Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, CDC; [3] Epidemic Intelligence Service, CDC; [4] Department of Immunization, Vaccines, and Biologicals, World Health Organization, Geneva, Switzerland; 5Global Immunization Division, Center for Global Health, CDC.

Corresponding author: Jason M. Mwenda, jmwenda@who.int, +47-241-39669.

Caption: FIGURE. Rotavirus vaccine introduction status--World Health Organization (WHO) African Region, 2016
TABLE 1. Percentage coverage with first and third DTP vaccine doses
and completed rotavirus (RV) vaccination series--World Health
Organization African Region, 2016

                           Year RV vaccine   RV vaccine
Country                      introduced         type

Countries introducing RV         --              --
  vaccine 2009-2013 *
South Africa                    2009            RV1
Botswana                        2012            RV1
Ghana                           2012            RV1
Malawi                          2012            RV1
Rwanda ([dagger])               2012            RV5
Tanzania                        2012            RV1
Burkina Faso                    2013            RV5
Burundi                         2013            RV1
Ethiopia                        2013            RV1
Gambia ([dagger])               2013            RV5
Zambia                          2013            RV1
Countries introducing RV         --              --
  vaccine 2014 *
Angola                          2014            RV1
Cameroon                        2014            RV1
Republic of the Congo           2014            RV1
Eritrea                         2014            RV1
Kenya                           2014            RV1
Madagascar                      2014            RV1
Mali                            2014            RV5
Mauritania                      2014            RV1
Namibia                         2014            RV1
Niger                           2014            RV1
Senegal                         2014            RV1
Sierra Leone                    2014            RV1
Togo                            2014            RV1
Zimbabwe                        2014            RV1
Countries introducing RV         --              --
  vaccine 2015-2016 *
Guinea-Bissau                   2015            RV1
Mauritius                       2015            RV1
Mozambique                      2015            RV1
Swaziland                       2015            RV1
Liberia                         2016            RV1
Sao Tome and Principe           2016            RV5

                                 Coverage (%)
                           DTP1   DTP3   RV (completed
Country                                     series)

Countries introducing RV    93     88         82
  vaccine 2009-2013 *
South Africa                78     66         73
Botswana                    98     95         95
Ghana                       94     93         94
Malawi                      89     84         81
Rwanda ([dagger])           99     98         98
Tanzania                    99     97         96
Burkina Faso                95     91         91
Burundi                     97     94         96
Ethiopia                    86     77         63
Gambia ([dagger])           99     95         95
Zambia                      99     91         90
Countries introducing RV    89     79         73
  vaccine 2014 *
Angola                      79     64         53
Cameroon                    92     85         80
Republic of the Congo       85     80         80
Eritrea                     97     95         96
Kenya                       96     89         74
Madagascar                  84     77         78
Mali                        86     68         60
Mauritania                  87     73         73
Namibia                     98     92         86
Niger                       87     67         61
Senegal                     96     93         93
Sierra Leone                97     84         95
Togo                        93     89         90
Zimbabwe                    94     90         91
Countries introducing RV    92     81         73
  vaccine 2015-2016 *
Guinea-Bissau               95     87         61
Mauritius                   97     96         92
Mozambique                  90     80         76
Swaziland                   96     90         95
Liberia                     99     79         48
Sao Tome and Principe       97     96         24

                           Percentage-point difference
                                   in coverage
                           DTP1 versus    DTP3 versus
Country                    completed RV   completed RV

Countries introducing RV        11             6
  vaccine 2009-2013 *
South Africa                    5              -7
Botswana                        3              0
Ghana                           0              -1
Malawi                          8              3
Rwanda ([dagger])               1              0
Tanzania                        3              1
Burkina Faso                    4              0
Burundi                         1              -2
Ethiopia                        23             14
Gambia ([dagger])               4              0
Zambia                          9              1
Countries introducing RV        16             6
  vaccine 2014 *
Angola                          26             11
Cameroon                        12             5
Republic of the Congo           5              0
Eritrea                         1              -1
Kenya                           22             15
Madagascar                      6              -1
Mali                            26             8
Mauritania                      14             0
Namibia                         12             6
Niger                           26             6
Senegal                         3              0
Sierra Leone                    2             -11
Togo                            3              -1
Zimbabwe                        3              -1
Countries introducing RV        19             8
  vaccine 2015-2016 *
Guinea-Bissau                   34             26
Mauritius                       5              4
Mozambique                      14             4
Swaziland                       1              -5
Liberia                         51             31
Sao Tome and Principe           73             72

Abbreviations: DTP = diphtheria and tetanus toxoids and pertussis;
DTP1 = first dose of DTP vaccine; DTP3 = third dose of DTP vaccine;
RV1 = monovalent RV vaccine (Rotarix); RV5 = pentavalent RV vaccine
(RotaTeq).

* Summary data for introduction period are population-weighted
averages.

([dagger]) Country initially introduced RV5, but switched to RV1 in
2017.

TABLE 2. Rotavirus (RV) stool specimen surveillance results, by
country and vaccine introduction status--World Health Organization
African Region, 2008-2015

                 Year RV          Vaccine preintroduction period
                 vaccine          Years           RV         No (%)
                introduced      included       specimens    positive
Country                                         tested

Countries           --             --            9,916     3,685 (37)
introducing
2012-2013
Ghana              2012      2008, 2010-2011     2,374     1,161 (49)
Rwanda             2012           2011            240       121 (50)
Tanzania           2012         2009-2010         852       308 (36)
Zambia             2012         2007-2011        4,519     1,700 (38)
Burkina Faso       2013            NS             NS           NS
Ethiopia           2013         2008-2012        1,931      395 (20)
Gambia             2013            NS             NS           NS
Countries           --             --           14,062     5,628 (40)
  introducing
  2014
Angola             2014            NS             NS           NS
Cameroon           2014         2008-2013        3,449     1,398 (41)
Kenya              2014         2007-2013        4,406     1546 (35)
Madagascar         2014            NS             NS           NS
Niger              2014            NS             NS           NS
Senegal            2014         2011-2013         374       159 (43)
Togo               2014      2008, 2010-2013     1,028      526 (51)
Zimbabwe           2014        2008-2009,        4,805     1,999 (42)
                                2011-2013
Countries           --             --            1,319      626 (47)
  Introducing
  2015
Mauritius          2015         2010-2014        1,203      578 (48)
Mozambique         2015            NS             NS           NS
Swaziland          2015           2013            116       48 (41)

                 Year RV        Vaccine postintroduction period
                 vaccine       Years        RV         No (%)
                introduced   included    specimens    positive
Country                                   tested

Countries           --          --        20,389     5,544 (27)
introducing
2012-2013
Ghana              2012      2013-2016     1,494      405 (27)
Rwanda             2012      2013-2015     2,237      447 (20)
Tanzania           2012      2013-2016     8,615     2,186 (25)
Zambia             2012      2013-2016     5,227     1,700 (33)
Burkina Faso       2013      2014-2016     1,889      615 (33)
Ethiopia           2013      2014-2016      822       165 (20)
Gambia             2013        2014         105       26 (25)
Countries           --          --         6,704     1,552 (23)
  introducing
  2014
Angola             2014        2015         229       41 (18)
Cameroon           2014      2015-2016      973       197 (20)
Kenya              2014      2015-2016      688       158 (23)
Madagascar         2014      2015-2016      451       56 (12)
Niger              2014        2016         168       22 (13)
Senegal            2014      2015-2016      235       38 (16)
Togo               2014      2015-2016      319       119 (37)
Zimbabwe           2014      2015-2016     3,641      921 (25)

Countries           --          --         1,081      330 (31)
  Introducing
  2015
Mauritius          2015        2016         570       235 (41)
Mozambique         2015        2016         420       68 (16)
Swaziland          2015        2016         91        27 (30)

                 Year RV     % decline in
                 vaccine          RV
                introduced   positivity *
Country

Countries           --           27%
introducing
2012-2013
Ghana              2012          45%
Rwanda             2012          60%
Tanzania           2012          30%
Zambia             2012          14%
Burkina Faso       2013           NS
Ethiopia           2013           2%
Gambia             2013           NS
Countries           --           42%
  introducing
  2014
Angola             2014           NS
Cameroon           2014          50%
Kenya              2014          35%
Madagascar         2014           NS
Niger              2014           NS
Senegal            2014          62%
Togo               2014          27%
Zimbabwe           2014          39%

Countries           --           36%
  Introducing
  2015
Mauritius          2015          14%
Mozambique         2015           NS
Swaziland          2015          28%

Abbreviations: NS = No surveillance data available (surveillance not
started or data do not meet analysis criteria); RV = rotavirus
vaccine.

* Calculated only for countries with data on rotavirus vaccine
preintroduction and postintroduction. Percentage declines might not
correspond to preintroduction and postintroduction percentages because
of rounding.
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Author:Mwenda, Jason M.; Burke, Rachel M.; Shaba, Keith; Mihigo, Richard; Tevi-Benissan, Mable Carole; Mumb
Publication:Morbidity and Mortality Weekly Report
Date:Nov 3, 2017
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