15-year experience with rotavirus vaccination in Mexico: a systematic literature review

Figures & data

Table 1. Inclusion and exclusion criteria

	Inclusion criteria	Exclusion criteria
Population	Any (not limited to risk groups or specific ages)	Populations with chronic diseases or underlying comorbidities that are not representative of the general population
Intervention	Registered/Licensed rotavirus vaccines in Mexico^± • Rotarix® (HRV) • RotaTeq® (BHRV)	All other vaccines
Comparator	All	None
Outcome	Vaccine impact on mortality, morbidity, and hospitalization, burden of disease, immunogenicity, effectiveness, efficacy, safety, cost-effectiveness, compliance	All other outcomes than those specified as eligible
Study design	Primary peer-reviewed research* Observational studies • Cohort studies • Case–control studies • Pre-/post-vaccine introduction time series • Cross-sectional studies • Ecological study Interventional studies • Randomized studies • Non-randomized studies • Cost-effectiveness or health economics studies • Surveys	Non-primary research • Systematic reviews** • Meta-analyses** • Narrative reviews (without methods) Non-human data (e.g. animal models, in-vitro, in-silico) or predictions via modeling methods Case reports Letter to editor Newspaper Editorial Comment Opinions Molecular studies Pilot studies Protocols/pre-clinical studies Studies with insufficient methodological details
Limits
Publication date	January 1, 2000 to February 1, 2020	All publications outside the eligible time period
Geographic scope	Mexico	All other countries
Language	English, Spanish	All other languages

BHRV, bovine-human reassortant vaccine; HRV, human attenuated vaccine.

^±For interventional studies.

*References cited by screened articles were manually reviewed for relevance (i.e. snowballing) **References of included articles in these systematic reviews/meta-analyses were manually screened for additional relevant original articles (as deemed necessary by the reviewer).

Table 2. Overview of main results from the included studies (N = 22)

Reference	Country/state	Time period	Study design	Vaccine	Sample size	Age of study population (years)	Clinical outcome	Main findings
Impact on mortality (n = 5)
Richardson 2020^Citation37	Mexico	Pre: 2003–2007 Post: 2007–2017	Observational Study (Database Analysis)	HRV/BHRV	n/a	Children <5 yoa	Acute diarrheal disease	Post universalization period: Mortality decreased by 52.6% During rotavirus seasons: Mortality reduced by 66.9%
Paternina-Caicedo 2015^Citation32	Mexico (LATAM Study)	Pre: 2002–2005 Post: 2006–2009	Observational Study (Database Analysis)	HRV	n/a	Children <5 yoa	All-cause diarrhea	Relative reduction in death rates: <1 yoa: 35.6 (32.6 to 38.4); <5 yoa: 33.9 (31.4 to 36.3); 702 deaths prevented
Gastañaduy 2012^Citation24	Mexico	2002–2011; 2003–2006	Observational Study (Database Analysis)	HRV	4,677,341	Children <5 yoa	All-cause diarrhea	Diarrhea Mortality rate reduced: Northern Mexico 45%; Central Mexico 55%; Southern Mexico 43%
Richardson 2010^Citation35	Mexico	Pre: 2003–2006 Post: 2008–2009	Observational Study (Database Analysis)	HRV	n/a	Children <5 yoa	All-cause diarrhea	December 2007, 74% ≤11 months of age received one dose of rotavirus vaccine. 2008: 1,118 diarrhea-related deaths among <5 yoa; a reduction of 675 from the annual median of 1,793 deaths during the 2003–2006 period. Diarrhea-related mortality, overall: Baseline – 18.1 deaths per 100,000 children 2008: 11.8 per 100,000 children (rate reduction, 35%; 95% CI: 29–39; P < .001). Diarrhea-related mortality, ≤11 months of age: Baseline – 61.5 deaths per 100,000 children 2008–36.0 per 100,000 children (rate reduction, 41%; 95% CI: 36–47; P < .001). Diarrhea-related mortality between 12 and 23 months: 2008–29% lower for children Mortality among unvaccinated children between the ages of 24 and 59 months was not significantly reduced.
Esparza-Aguilar 2009^Citation26	Mexico	2000–2007	Observational Study (Database Analysis)	HRV	n/a	Infants (<4 yoa)	Acute diarrheal disease	Deaths in children >5 years of age dropped 42%. Mortality decreased in states that received the vaccine in 2006: 22.7% in >1 yoa 15.8% in 1–4 yoa
Impact on morbidity (n = 3)
Richardson 2020^Citation37	Mexico	Pre: 2003–2007 Post: 2007–2017	Observational Study (Database Analysis)	HRV/BHRV	n/a	Children <5 yoa	Acute diarrheal disease	Post universalization period: Hospitalizations decreased by 46% New cases decreased by 15.5% During rotavirus seasons Hospitalizations reduced by 64.7% New cases reduced by 28.7%
Leboreiro 2013^Citation29	Mexico	2008–2010	Observational Study (Database Analysis)	HRV/BHRV	2,289	Infants (<2 yoa)	All-cause diarrhea	Decrease in the number and severity of rotavirus cases treated in the hospital (OR 0.18, p = .01)
Quintanar-Solares 2011^Citation33	Mexico	Pre: 2003–2006 Post: 2008–2009	Observational Study (Database Analysis)	HRV	Data from 306 censia hospitals	Children <5 yoa	All-cause diarrhea	<5 yoa: Decrease by 11% (N = 9,836) in 2008; decrease by 40% (N = 6,597) in 2009. <1 yoa: Decrease by 25% in 2008, 52% in 2009
Real-world vaccine effectiveness (n = 1)
Yen 2011^Citation43	Mexico (Chiapas)	March 2010 – May 2010	Observational (Case-Control)	HRV	14 cases, 29 controls	Children <5 yoa	Severe RVGE	94% effective (95% CI: 16%-100%) after 2nd dose against G9P rotavirus-related hospitalization
Immunogenicity (n = 3)
Ciarlet 2008^Citation24	Mexico (LATAM Study)	2005–2006	RCT	BHRV	363	Infants (<2 yoa)	Antibody Responses to OPV and RV	Concomitant administration of BHRV with OPV does not interfere with immunogenicity of each of the poliovirus types 1, 2, and 3.98% of subjects achieved serum-neutralizing antibody titer >1:8 against Poliovirus types (1,2,3) Reduction in the anti-RV IgA titers when given at the same time as OPV, yet children met criteria for seroconversion.
Ruiz-Palacios 2007^Citation38	Mexico (San Pedro Martir)	June 2001-May 2003	RCT (Phase IIb)	HRV	405	Infants (<2 yoa)	RVGE	Immunogenicity: Seroconversion rates range 34.2–63.9% 2 months after 1st dose and increased to 50–70.6% 2 months after 2nd dose GMC (U/mL) Dose 1 (after 2 months): 36.9 (27.7–49.2); Dose 2 (after 4 months): 58.3 (43.8–77.5); (after 10 months): 102.8 (82.5–128.0)
Salinas 2005^Citation40	Mexico (LATAM Study)	May 2001 – April 2002	RCT	HRV	2,155	Infants (<1 yoa)	RVGE	Seroconversion rates range 61% (10^4.Citation7 FFU group) – 65% (10^Citation5,Citation8 FFU group) 2 months after 2nd dose
Efficacy (n = 4)
Salinas 2005^Citation40	Mexico (LATAM Study)	May 2001 – April 2002	RCT	HRV	2,155	Infants (<1 yoa)	RVGE	Against Hospitalization – 79% (95% CI: 48–92%) Severe GE – 86% (95% CI: 63–96%) Any GE – 70% (95% CI: 46–84%) Severe GE (G9 serotypes) – 77% (95% CI: 18–96%)
Ruiz-Palacios 2006^Citation39	Mexico (LATAM Study)	Pre: 2003–2004	RCT (Phase 3)	HRV	63,225 (safety cohort) 20,169 (efficacy cohort)	Infants (<2 yoa)	Severe RVGE	Severe RVGE and hospitalizations: 85% reduction More Severe RVGE: 100% reduction Hospitalization for diarrhea of any cause: 42% reduction
Ruiz-Palacios 2007^Citation38	Mexico (San Pedro Martir)	June 2001-May 2003	RCT (Phase IIb)	HRV	405	Infants (<2 yoa)	RVGE	Any GE: 80% (95% CI: 46.3–93.5) Severe GE: 95% (95% CI: 61.0–99.8)
Linhares 2008^Citation31	Mexico (LATAM Study)	2-year period	RCT	HRV	15,183 (4,335 Mexican)	Infants (<2 yoa)	Severe RVGE	Vaccine Efficacy: Year 1: 82.1% Year 2: 97.3% Year 3: 100%
Safety (n = 7)
Linhares 2008^Citation31	Mexico (LATAM Study)	2-year period	RCT	HRV	15,183 (4,335 Mexican)	Infants (<2 yoa)	Severe RVGE	Relative Risk (vaccinated vs placebo) for definite intussusception diagnosed during the first 2 years of life after administration of first vaccine dose was 0.36 (95% CI 0.12–1.06). Intussusception was reported in 4/7,669 (vaccine group) and 11/7,514 (placebo group). No increased risk of definite intussusception was seen in the vaccinated group vs the placebo group during the 2-years’ follow-up (p 0.065)
Salinas 2005^Citation40	Mexico (LATAM Study)	May 2001 – April 2002	RCT	HRV	2,155	Infants (<1 yoa)	RVGE	The reactogenicity profile of HRV was similar to the placebo, and no vaccination-related serious adverse events were reported. Only 1 intussusception case was reported 6 months after the second dose of HRV (10^4.Citation7 FFU in a 10-month-old boy)
Ruiz-Palacios 2006^Citation39	Mexico (LATAM Study)	Pre: 2003–2004	RCT (Phase 3)	HRV	63,225 (safety cohort) 20,169 (efficacy cohort)	Infants (<2 yoa)	Severe RVGE	During the 31-day window after each dose: 6 vaccinated and 7 placebo recipients had definite intussusception (difference in risk: −0.32 per 10,000 infants; 95% CI: −2.91 to 2.18; P = .78)
Ruiz-Palacios 2007^Citation38	Mexico (San Pedro Martir)	June 2001-May 2003	RCT (Phase IIb)	HRV	405	Infants (<2 yoa)	RVGE	SAEs were reported for 31 (8%) of the 405 children, and 2 deaths not related to vaccination
Velázquez 2012^Citation42	Mexico	January 2008 – October 2010	Observational (Active Surveillance and Controlled Case-Series Analysis)	HRV	221 hospitals (IMSS) 1.5 million infants under surveillance during the study period of almost 3 years	Infants (<1 yoa)	Intussusception	753 episodes of intussusception reported in 750 infants, 701 were in vaccinated infants Post-dose 1: 34.5% Post-dose 2: 65.5% Relative incidence of intussusception within 31 days of vaccination: Post-dose 1: 1.75 (95.5% CI: 1.24–2.48; P = .001) Post-dose 2: 1.06 (95.5% CI: 0.75–1.48; P = .75) Relative incidence of intussusception within 7 days of vaccination: Post-dose 1: 6.49 (95.5% CI: 4.17–10.09; P < .001) Post-dose 2: 1.29 (95.5% CI: 0.80–2.11; P = .29)
Baay 2017^Citation22	Mexico (LATAM Study)	15 February 2016 (Last Accessed) Vaccine Study (Between August 5, 2003, and March 12, 2004)	Observational Study (Database Analysis)	HRV	63,225 (Mexico 13,246)	Infants (<2 yoa)	3 most common SAEs: Gastroenteritis Pneumonia Bronchiolitis	Overall rate of SAEs of 1.05% in all Latin American countries combined (Rate: Min (48.1/10.000 person-years; Max 296.2/10,000 person-years) Overall SAE rates (>1/10,000 person-years) in Mexico: Gastroenteritis – 16.8 Pneumonia – 1.9 Bronchiolitis – 19.5 Bronchopneumonia – 7.5 Bronchitis – 0.2 Bronchospasm – 0.2 Dehydration – 1.9 Urinary Tract Infection – 1.1 Head injury – 1.3 Asthma – 0.2 Febrile Convulsion – 1.5 Pertussis – 0.2 Diarrhea – 0.7 Convulsion – 0.6 Any Preferred Term – 74.3
Ciarlet 2008^Citation24	Mexico (LATAM Study)	2005–2006	RCT	BHRV	363	Infants (<2 yoa)	Antibody Responses to OPV and RV	Adverse experiences reported within 14 days after any visit: 92.6% in the OPV+RV (concomitant) group vs 89.6% in the RV-OPV (staggered use) group Most commonly reported events (concomitant vs staggered group): Diarrhea (40.2% vs 39.8%) Elevated temperature (24.3% vs 25.8%) Vomiting (21.3% vs 24.9%) Irritability (4.6% vs 6.7%) Vaccine related SAE (concomitant vs staggered group): Intussusception that occurred 3 days after administration of the third dose of RV vaccination in a male infant aged 25 weeks in the staggered use group
Burden of disease (n = 2)
Linhares 2012^Citation30	Mexico (LATAM Study)	Mexico: Jan-June 2003	Observational (Active Surveillance Study)	None	Total in Study: 8,031 In Mexico: 1,306 Samples tested: 1,154	Infants (<3 yoa)	Acute and Severe RVGE	For Mexico: Study Duration: 179 days Children enrolled: 1,306 N (samples tested): 1,154 Rota Positive stool samples: 59% (overall)
Granados 2011^Citation28	Mexico	2001–2006	Observational Study (Database Analysis)	None	n/a	Children <5 yoa	Rotavirus diarrhea	2001: Estimates of DALYS were 19,426 2006: Estimated DALYS decreased by 28.9% Costs of treatment were relatively constant, estimated at US$ 38.7 million and increased only by 5%.
Health economics of rotavirus vaccination (n = 4)
Carlos 2013^Citation23	Mexico	5-year period	Health Economic Model	HRV/BHRV	n/a	All ages	Rotavirus infection	Routine immunization with both HRV and BHRV is a highly cost-effective intervention in Mexico. Among the vaccines, HRV was most cost-effective strategy. Without vaccination: 760,559 cumulative rotavirus events in Mexico, entailing direct medical costs of 529.3 million MXN and loss of 5,036 QALYs With HRV: Net Savings of 74 million and gains of 553 QALY with respect to BHRV
Constenla 2009^Citation25	Mexico	5-year period	Health Economic Model	HRV	The annual birth cohort considered was 2,285,000 children	All Ages	Cost and Health Benefits	Prevent: 651 deaths 13,833 hospitalizations 414,927 outpatient visits Economic Burden: Reduced by US$ 14 million At a vaccine price US$ 16, Cost-Effectiveness Ratio would be US$ 1,139 per DALY
Valencia-Mendoza 2008^Citation41	Mexico	Projected: 2002–2006 (Unclear)	Health Economic Model	BHRV	Assumption of all birth cohort (2 million)	Children <5 yoa	RVGE	Prevent: 71,464 medical visits (59%) 5,040 hospital admissions (66%) 612 deaths from rotavirus gastroenteritis (70%) Total medical costs prevented: US$74,663.91 (−79,624 to −62,049) At US$10 per dose and a cost of administration of US$13.70 per 3-dose regimen, vaccination would cost: US$122,058 per death prevented US$4,383 per discounted life-year saved Total net cost of US$74.7 million dollars to the healthcare system
Rheingans 2007^Citation34	Mexico (LATAM Study)	Projected: 2003–2008	Health Economic Model	HRV	n/a	Children <5 yoa	RVGE	Averted with Vaccination vs no Vaccination: Hospitalizations: 651 Deaths: 11,758 Outpatient visits: 412,267 Medical costs: US$11,881,594 (69% reduction) DALYs: 22,330 (70% reduction) ICER (Cost per DALY averted): US$2,070/DALY Meaning: very cost-effective (ICER < US$6,121/DALY), is more than 95%
Compliance (n = 1)
Luna-Casas 2019^Citation14	Mexico	2010: HRV 2012: BHRV	Observational Study (Database Analysis)	HRV/BHRV	n/a	All ages	n/a	More eligible infants received all doses with HRV vs BHRV (p < .001). Among infants vaccinated with HRV vs BHRV, 93.7% vs 71.1% completed full series (p < .001), and 75.5% vs 70.9% completed full series on schedule (p = .105), respectively.

BHRV, bovine-human reassortant vaccine; CI, confidence interval; DALY, disability-adjusted life-years; FFU, focus-forming units; GE; gastroenteritis; GMC, geometric mean concentration; HRV, human attenuated vaccine; ICER, incremental cost–effectiveness ratio; IMSS, Mexican Social Security; LATAM, Latin America; n/a, not available; OPV, oral polio vaccine; OR, odds ratio; p, percentage value; QALY, quality-adjusted life-years; RCT, randomized controlled trial; RV, rotavirus vaccination; RVGE, rotavirus gastroenteritis; SAE, serious adverse event; yoa, years of age.

Figure 1. PRISMA flowchart

n, sample size; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-analyses; yoa, years of age.

Figure 2. Distribution of studies by (a) Study design, (b) Age of study population, (c) Study outcome, and (d) Clinical endpoint

RTC, randomized control trial; yoa, years of age.

Figure 3. Summary characteristics of studies by vaccine and study outcome*

*Numbers do not add to N = 22 as a study can count toward more than one category (>1 endpoint per study).

Figure 4. Risk of bias assessment of observational studies using STROBE checklist.^18,19

STROBE, Strengthening the Reporting of Observational studies in Epidemiology.

Figure 5. Risk of bias assessment of RCTs using Cochrane risk bias of tool.²⁰

RCT, randomized controlled trial.

Figure 6. Plain Language Summary

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