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Citation: Suárez-Rodríguez, G.L.;
Salazar-Loor, J.; Rivas-Condo, J.;
Rodríguez-Morales, A.J.; Navarro,
J.-C.; Ramírez-Iglesias, J.R. Routine
Immunization Programs for Children
during the COVID-19 Pandemic in
Ecuador, 2020—Hidden Effects,
Predictable Consequences. Vaccines
2022,10, 857. https://doi.org/
10.3390/vaccines10060857
Academic Editors: Valentina
Baccolini and Giuseppe Migliara
Received: 1 April 2022
Accepted: 17 May 2022
Published: 27 May 2022
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Article
Routine Immunization Programs for Children during the
COVID-19 Pandemic in Ecuador, 2020—Hidden Effects,
Predictable Consequences
Gianina Lizeth Suárez-Rodríguez 1,2 , JoséSalazar-Loor 1,3, Jackson Rivas-Condo 4,
Alfonso J. Rodríguez-Morales 5,6 , Juan-Carlos Navarro 1,2 and JoséRubén Ramírez-Iglesias 1, 2, *
1Research Group of Emerging and Neglected Diseases, Ecoepidemiology and Biodiversity, Health Sciences
Faculty, Universidad Internacional SEK (UISEK), Quito 170120, Ecuador;
gianina.suarez@uisek.edu.ec (G.L.S.-R.); jose.salazar@uisek.edu.ec (J.S.-L.);
juancarlos.navarro@uisek.edu.ec (J.-C.N.)
2Program of Master in Biomedicine, Health Sciences Faculty, Universidad Internacional SEK (UISEK),
Quito 170120, Ecuador
3
Faculty of Engineering and Applied Sciences, Universidad Internacional SEK (UISEK), Quito 170120, Ecuador
4Secretaría de Salud del Distrito Metropolitano de Quito, Quito 170136, Ecuador; jackrivas88@hotmail.com
5Grupo de Investigación Biomedicina, Faculty of Medicine, Fundación Universitaria Autónoma de las
Américas, Pereira 660001, Risaralda, Colombia; alfonso.rodriguez@uam.edu.co
6Program of Master in Clinical Epidemiology and Biostatistics, Universidad Científica del Sur,
Lima 150142, Peru
*Correspondence: jose.ramirez@uisek.edu.ec
Abstract:
The COVID-19 pandemic has led to a global disruption of several services, including routine
immunizations. This effect has been described in several countries, but there are few detailed studies
in Latin America and no reports in Ecuador. Therefore, this work aims to quantify the reduction
in routine immunizations for infants during the 2020 COVID-19 pandemic in Ecuador. 2018, 2019,
and 2020 data were obtained from the Ministry of Health, Ecuador. The number of doses and the
extent of immunization coverage was descriptively compared for four vaccines: rotavirus (ROTA),
poliovirus (PV), pneumococcal (PCV), and pentavalent (PENTA) vaccines. There was no significant
difference in doses applied during the 2018 and 2019 years. However, a significant
(p< 0.05)
drop
of 137,000 delivered doses was observed in 2020 compared to the pre-pandemic years. Reductions
in the percentage of coverage were more pronounced for the PENTA vaccine (17.7%), followed
by PV (16.4%), ROTA (12%), and PCV vaccines (10.7%). Spatial analysis shows a severe impact
on vaccination coverage on provinces from the Coast and Highland regions of the country. The
pandemic has significantly impacted the immunization programs for infants across Ecuador. This
retrospective analysis shows an urgent need to protect vulnerable zones and populations during
public health emergencies.
Keywords: routine immunization; vaccination; infants; pandemic; COVID19; preventable diseases
1. Introduction
An outbreak of atypical pneumonia was reported in December 2019 in Wuhan, China,
caused by the novel coronavirus SARS-CoV-2 which produced the coronavirus disease in
2019 (COVID-19) [
1
]. On 11 March, the WHO declared the COVID-19 a pandemic [
2
] and,
by October 2020, the virus had spread all over the world [
3
]. In this scenario, and with no
treatments or vaccines available during the initial months of the pandemic, several non-
pharmaceutical intervention measures were taken to control the spread of
SARS-CoV-2,
mitigate its effects on populations, and reduce the burden on healthcare systems. These
measures included the everyday use of personal protective equipment, diligent hand
hygiene practices, social distancing, stay-at-home orders, and movement restrictions at
Vaccines 2022,10, 857. https://doi.org/10.3390/vaccines10060857 https://www.mdpi.com/journal/vaccines
Vaccines 2022,10, 857 2 of 12
several geographical levels [
4
,
5
]. However, disruption in health services, particularly
in low-income and middle-income countries (LMIC), has been reported, including the
redirection of services to the COVID-19 response, healthcare facility closures, negative
impacts on medical supply chains, and interruptions to routine immunization programs [
6
].
Vaccination is one of the most successful measures to reduce infant morbidity and mortality
and confers protection across childhood. Securing programs for timely immunizations is
critical to preventing outbreaks of vaccine-preventable diseases (VPD) and to decreasing
the risk of re-emerging diseases in countries susceptible to natural disasters [
7
,
8
]. Despite
the worldwide efforts to maintain essential services related to healthcare settings, several
LMIC and some high-income countries reported severe disruptions in their routine immu-
nization programs for infants in 2020, with a significant decline in the number of doses
administered and the extent of vaccination coverage in the USA, the United Kingdom,
Spain, Pakistan, Sierra Leone, and the region of South-East Asia and the Western Pacific,
among others [
9
–
15
]. Similarly, the Global Alliance for Vaccines and Immunization (GAVI)
reported that 13.5 million people in the least-developed countries of the world would not be
protected against diseases such as measles, polio, and human papillomavirus [
16
]. Multiple
factors such as a concern about leaving home and being exposed to COVID-19 as well
as interruptions in transport systems have been associated with delayed immunizations
during the pandemic [17,18].
The first case of COVID-19 in the South American country of Ecuador was reported on
29 February 2020. Subsequently, a state of national emergency was declared on 11 March,
with measures implemented for mitigating the transmission of SARS-CoV-2 at the popula-
tion level [
19
]. These measures consisted of pedestrian and vehicle mobility restrictions,
the suspension of mass events, national and international flight disruptions, the closing
of borders, stay-at-home orders, and remote working for non-essential services [
20
]. Most
of these directions were nationally reduced by October–November 2020, although some
measures were maintained according to the situation of specific provinces and cities. The
Ecuadorian immunization program for infants (children under one year) is comprised of
meningococcal, hepatitis B, rotavirus, poliovirus, pneumococcal, pentavalent (diphtheria,
pertussis, tetanus, hep B, Hemophilus), and influenza vaccines [
21
]. However, there are
few studies of the impact of the COVID-19 pandemic on routine immunizations for infants
in South America, and no detailed studies about the variations in the vaccine-administered
doses for children in Ecuador. The progressively adopted measures for controlling trans-
mission of SARS-CoV-2 in Ecuador represent an important context to analyze the routine
vaccination process. Therefore, this study aims to evaluate the effects of the COVID-19
mitigation measures on routine immunization programs for infants in Ecuador.
2. Materials and Methods
2.1. Study Population and Databases
Ecuador is classified as an LMIC [
22
] and its territory comprises 24 provinces within
3 regions. The coastal region, consisting of Esmeraldas, Manabi, Los Ríos, Santa Elena,
Guayas, Santo Domingo de los Tsáchilas and El Oro; the highlands region, consisting of
Azuay, Bolívar, Cañar, Carchi, Cotopaxi, Chimborazo, Imbabura, Loja, Pichincha and Tun-
gurahua; and the Amazon region, consisting of Morona Santiago, Napo, Orellana, Pastaza,
Sucumbíos and Zamora Chinchipe, and the Insular region comprising Galapagos islands.
The databases of all provinces were provided and approved for use under the au-
thorizations MSP-DNEPC-2021-0003-O and MSP-DNEAIS-2021-0069-O by the National
Direction of Statistics and Health Information Analysis of the Ministry of Health (MSP),
Ecuador, which is the only department in charge that centralizes national public registries.
Vaccination campaigns led by the Ministry of Health represent nearly 95% of the doses
administered in the country. These immunization data contain information about vaccines
exclusively. Doses applied, years, months, general geographical locations, and no personal
information. A total of four types of vaccines within the Ecuadorian routine immunization
programs for infants under one year were compared: the ROTA, PV, PCV, and PENTA
Vaccines 2022,10, 857 3 of 12
vaccines for the pre-pandemic years 2018–2019 and for the initial year of the COVID-19
pandemic in 2020. The national program recommends applying two doses for the ROTA
vaccine at 2 and 4 months and three doses for the PV, PCV, and PENTA vaccines at 2, 4,
and 6 months.
The data were compared from March–at the beginning of the lockdown declaration
in Ecuador–to December, for the 2018 and 2020 years. Information about the population
of infants for each region and province was also obtained from the MSP (Table 1). The
vaccination coverage calculated in this study is the proportion of children in the Region
receiving the recommended vaccines [
23
]. This indicator is the result of the ratio between
the number of doses administered with a specific antigen and the number of infants in
a locality.
Table 1. Total population of infants from the 24 Ecuadorian provinces.
Region Province
Year
2018 2019 2020
Coast
Esmeraldas 13,382 13,293 13,211
Manabí29,803 29,499 29,207
Los Ríos 18,982 18,897 18,888
Santa Elena 8772 8834 8897
Guayas 79,639 79,543 79,535
Santo Domingo 10,532 10,535 10,537
El Oro 12,597 12,526 12,464
Subtotal 173,707 173,127 172,739
Highlands
Azuay 15,962 15,943 15,700
Bolívar 4387 4338 4223
Cañar 5670 5680 5660
Carchi 3280 3258 3236
Cotopaxi 10,408 10,355 10,304
Chimborazo 10,005 9863 9762
Imbabura 9202 9173 9141
Loja 10,031 9978 9,923
Pichincha 56,493 56,768 57,062
Tungurahua 10,207 10,159 10,111
Subtotal 135,645 135,515 135,122
Amazon
Morona Santiago 4886 4865 4842
Napo 3320 3341 3361
Orellana 3952 3883 3821
Pastaza 2618 2639 2659
Sucumbíos 4920 4940 4958
Zamora Chinchipe 2840 2839 2837
Subtotal 22,536 22,498 22,478
Insular Galápagos 617 624 631
Total 332,505 331,773 330,970
Due to the absence of personal information in the dataset or direct intervention on the
aimed population, no bioethical approval was required.
2.2. Statistical and Spatial Analysis
We used the Kruskal Wallis test, which is a nonparametric approach, to compare three
or more groups by a dependent variable that is measured on at least an ordinal level. Here
we compare the doses administered and the extent of vaccination coverage from 2018,
2019, and 2020, at national and provincial scales. The variation in the vaccination coverage
between the analyzed years was calculated using the following formula: vaccination
coverage percentage = (Year 1 Coverage
−
Year 2 Coverage/Year 1 Coverage)
×
100. In
the case of doses administered, the variation was calculated as the difference between
Vaccines 2022,10, 857 4 of 12
two years. A specific analysis was performed using the data for the doses applied during
April, a month with strict measures imposed by the local government, and November,
which saw a flexibilization in the adopted restrictions. The differences were significant,
with p< 0.05. The IBM SPSS v25 (Armonk, NY, USA) software was used for graphs and
statistical tests. To explore possible differences in the influence of the COVID-19 pandemic
context on the vaccination process in the Ecuadorian territory, a spatial clustering analysis
was performed to establish the potential heterogeneity of vaccination coverage in all the
evaluated years at the provincial and cantonal levels, using the Global Moran’s I and
Getis–Ord Gi statistics [24,25].
The Global Moran’s I indicate the degree to which points are like their spatial neigh-
bors. Negative values indicate strong negative autocorrelation (high spatial dispersion),
values higher than two indicate a positive correlation or clustering, and data between 0
and 2 are considered random patterns. The Getis–Ord Gi was used for the hotspot and
clustering analysis, where cold spots are low values clustered in areas and hot spots are high
values clustered in a location. The statistics were obtained using the ArcGIS Pro 10.8 soft-
ware. Additionally, to evaluate the trend in the vaccination process across 2018–2020,
and to detect specific breakpoints in immunizations administered in Ecuador, a Joinpoint
analysis [
26
] was performed with the number of last vaccination doses administered for
all the antigens studied. The Joinpoint Regression Software v4.9.1.0. was used for this
trend analysis.
3. Results
3.1. Population of Study and Changes in the National Administered Doses and
Vaccination Coverage
The infant population of the pre-pandemic and pandemic years was analyzed to
determine if any alteration in the national vaccination program was due to changes in the
newborn registration. According to the MSP data, the number of infants registered was
332,505 (2018), 331,773 (2019), and 330,970 (2020), with no statistical differences between
the analyzed years.
The total numbers of the last vaccine doses administered in Ecuador were 947,722 and
920,808, during 2018 and 2019, with a mean for pre-pandemic years of 934,265. In 2020, the
number dropped to 797,234, with a significant reduction of 137,031 and a variation of 14% in
the vaccination coverage percentage compared to the 2018/2019 mean for the last doses at
the national scale (Figure 1). The detailed last administered doses and vaccination coverage
percentages are shown in Table 2, where the pre-pandemic years presented similar behavior.
Vaccines 2022, 10, x FOR PEER REVIEW 5 of 13
Figure 1. Administered doses and vaccination coverage percentages for the ROT, PV, PCV, and
PENTA vaccines in Ecuador. The graph shows the total number of final doses and the coverage:
second dose for ROT, and third dose for the rest of the antigens.
Table 2. Variation of last administered vaccination doses and coverage percentage for infants in
Ecuador.
Vaccine
Number of Last Doses
(Coverage Percentage) Variation
2018–2019
p-Value
2018–2019
Variation
2018–2020
p-Value
2018–2020
Variation
2019–2020
p-Value
2019–2020
Variation Pre-Pan-
demic Years–2020
2018 2019 2020
ROTA 234,000
(70.37)
231,167
(69.68)
203,911
(61.61)
2833
(0.98) 0.617 30,089
(12.45) 0.000 27,256
(11.58) 0.000 28,672
(12.01)
PV 240,473
(72.32)
230,950
(69.61)
196,322
(59.32)
9523
(3.75) 0.412 44,151
(17.98) 0.000 34,628
(14.78) 0.000 39,389
(16.38)
PCV 236,881
(71.24)
226,515
(68.27)
206,205
(62.3)
10,366
(4.17) 0.166 30,676
(12.55) 0.000 20,310
(8.74) 0.010 25,493
(10.65)
PENTA 236,368
(71.09)
232,176
(68.98)
190,796
(57.65)
4192
(2.97) 0.762 45,572
(18.91) 0.000 41,380
(16.43) 0.000 43,476
(17.67)
However, 2020 shows a significant disruption for all four antigens evaluated with
mean reduction values of 43,476 (17.67%), 39,389 (16.38%), 28,672 (12.01%), and 25,493
(10.65%) for the PENTA, PV, ROTA, and PCV vaccines, respectively (Table 2). This reduc-
tion shown in 2020 is observed for the three mandatory doses for PENTA, PV, PCV, and
the two doses in the case of the ROTA vaccine (Figure 2, panels A; B; C; D). Interestingly,
the last doses were the most affected for all the antigens. The third administered dose and
vaccination coverage percentage for PENTA (190,796/57.65%) and PCV (206,205/62.3%)
were the most and least affected vaccines analyzed in this study, respectively.
Figure 1.
Administered doses and vaccination coverage percentages for the ROT, PV, PCV, and
PENTA vaccines in Ecuador. The graph shows the total number of final doses and the coverage:
second dose for ROT, and third dose for the rest of the antigens.
Vaccines 2022,10, 857 5 of 12
Table 2.
Variation of last administered vaccination doses and coverage percentage for infants
in Ecuador.
Vaccine
Number of Last Doses
(Coverage Percentage) Variation
2018–2019
p-Value
2018–2019
Variation
2018–2020
p-Value
2018–2020
Variation
2019–2020
p-Value
2019–2020
Variation
Pre-Pandemic
Years–2020
2018 2019 2020
ROTA 234,000
(70.37)
231,167
(69.68)
203,911
(61.61)
2833
(0.98) 0.617 30,089
(12.45) 0.000 27,256
(11.58) 0.000 28,672
(12.01)
PV 240,473
(72.32)
230,950
(69.61)
196,322
(59.32)
9523
(3.75) 0.412 44,151
(17.98) 0.000 34,628
(14.78) 0.000 39,389
(16.38)
PCV 236,881
(71.24)
226,515
(68.27)
206,205
(62.3)
10,366
(4.17) 0.166 30,676
(12.55) 0.000 20,310
(8.74) 0.010 25,493
(10.65)
PENTA 236,368
(71.09)
232,176
(68.98)
190,796
(57.65)
4192
(2.97) 0.762 45,572
(18.91) 0.000 41,380
(16.43) 0.000 43,476
(17.67)
However, 2020 shows a significant disruption for all four antigens evaluated with
mean reduction values of 43,476 (17.67%), 39,389 (16.38%), 28,672 (12.01%), and 25,493
(10.65%) for the PENTA, PV, ROTA, and PCV vaccines, respectively (Table 2). This reduction
shown in 2020 is observed for the three mandatory doses for PENTA, PV, PCV, and the
two doses in the case of the ROTA vaccine (Figure 2, panels A; B; C; D). Interestingly, the
last doses were the most affected for all the antigens. The third administered dose and
vaccination coverage percentage for PENTA (190,796/57.65%) and PCV (206,205/62.3%)
were the most and least affected vaccines analyzed in this study, respectively.
Vaccines 2022, 10, x FOR PEER REVIEW 6 of 13
Figure 2. Changes in administered vaccination doses and coverage percentages. The graph shows
the detailed number of every dose administered and the vaccination coverage in Ecuador during
the three analyzed years. Panels: (A) ROTA; (B) PV; (C) PCV; (D) PENTA.
In general, we registered an average reduction of 14.18% of vaccination coverage for
the antigens evaluated here.
3.2. Spatial Pattern Analysis of Vaccination Coverage
Due to the statistical differences displayed by the doses administered and immun-
ization coverage percentages in 2020 compared to 2018–2019, we decided to perform a
spatial analysis to detect possible clustering areas and specific patterns for the vaccination
coverage rates in 2020.
The interannual analysis shows high and random clustering values for the coverage
of evaluated vaccines in the pre-pandemic years, indicated by the Global Moran’s I index.
Changes in the pattern of high vaccination coverage for all the antigens in 2020 were de-
tected, especially in the Orellana and Pastaza provinces, located in the eastern region of
the country (Figure 3). The average coverage registered for these provinces was 97.48%
and 91.17% in 2018–2019, which were superior values compared to the 86.42% and 79.03%,
registered in 2020. Similarly, the Esmeralda province, located in northwestern Ecuador,
presents changes in the clustering of hot spots, with average coverage values of 93.98% in
2018–19 and 80.03% in 2020. The intra-annual analysis of 2020 indicates highly dispersed
data regarding the vaccination coverage values for all types of antigens, and a few hot and
cold spots of clustering across the Ecuadorian territory, except for the analysis of the
PENTA vaccine (Figure 3). This general lack of clustering, observed in the maps as areas
without color, indicates that immunizations with ROTA, PV, and PCV vaccines were sim-
ilarly affected in the cantons and provinces of the territory. This result is also indicated by
the Global Moran’s I index, whose values oscillated between 0 and 2 for these antigens.
Figure 2.
Changes in administered vaccination doses and coverage percentages. The graph shows
the detailed number of every dose administered and the vaccination coverage in Ecuador during the
three analyzed years. Panels: (A) ROTA; (B) PV; (C) PCV; (D) PENTA.
In general, we registered an average reduction of 14.18% of vaccination coverage for
the antigens evaluated here.
3.2. Spatial Pattern Analysis of Vaccination Coverage
Due to the statistical differences displayed by the doses administered and immu-
nization coverage percentages in 2020 compared to 2018–2019, we decided to perform a
spatial analysis to detect possible clustering areas and specific patterns for the vaccination
coverage rates in 2020.
Vaccines 2022,10, 857 6 of 12
The interannual analysis shows high and random clustering values for the coverage
of evaluated vaccines in the pre-pandemic years, indicated by the Global Moran’s I index.
Changes in the pattern of high vaccination coverage for all the antigens in 2020 were
detected, especially in the Orellana and Pastaza provinces, located in the eastern region
of the country (Figure 3). The average coverage registered for these provinces was 97.48%
and 91.17% in 2018–2019, which were superior values compared to the 86.42% and 79.03%,
registered in 2020. Similarly, the Esmeralda province, located in northwestern Ecuador,
presents changes in the clustering of hot spots, with average coverage values of 93.98% in
2018–19 and 80.03% in 2020. The intra-annual analysis of 2020 indicates highly dispersed
data regarding the vaccination coverage values for all types of antigens, and a few hot
and cold spots of clustering across the Ecuadorian territory, except for the analysis of
the PENTA vaccine (Figure 3). This general lack of clustering, observed in the maps as
areas without color, indicates that immunizations with ROTA, PV, and PCV vaccines were
similarly affected in the cantons and provinces of the territory. This result is also indicated
by the Global Moran’s I index, whose values oscillated between 0 and 2 for these antigens.
Vaccines 2022, 10, x FOR PEER REVIEW 7 of 13
Figure 3. Spatial analysis of vaccination coverage rates for infants in 2018, 2019, and 2020 in Ecuador.
The maps show patterns of high (red) and low (blue) vaccination coverage areas compared to their
neighboring locations. Numbers in the superior square indicate the Global Moran’s I index, calcu-
lated using the coverage of the last dose of every vaccine applied.
Cold spots in the 2020 maps indicate low vaccination coverage percentages for these
three antigens in the Guayas province, with a 76.25% vaccination coverage. In the case of
Figure 3.
Spatial analysis of vaccination coverage rates for infants in 2018, 2019, and 2020 in Ecuador.
The maps show patterns of high (red) and low (blue) vaccination coverage areas compared to their
neighboring locations. Numbers in the superior square indicate the Global Moran’s I index, calculated
using the coverage of the last dose of every vaccine applied.
Vaccines 2022,10, 857 7 of 12
Cold spots in the 2020 maps indicate low vaccination coverage percentages for these
three antigens in the Guayas province, with a 76.25% vaccination coverage. In the case of
the PENTA vaccine, the cold spots include the Los Rios, Manabí, Bolivar, and Chimborazo
provinces, with coverage values of 74.54%, 78.80%, 67.85%, and 69.18%, respectively. The
vaccination coverage values for these five provinces in the pre-pandemic years were 88.51%,
84.51%, 90.04%, 68.58%, and 73.18%.
The insular region was not included in this analysis due to the absence of neighboring
counterparts. The general percentages of vaccination coverage in 2020 calculated for
the Amazon, Coast, Highland, and Insular regions were 84.53%, 75.74%, 70.36%, and
69.33%, respectively.
3.3. Yearly Trend Analysis and Administered Vaccine Doses during April and
November 2018–2020
The Joinpoint analysis used to detect specific breakpoints and changes related to
immunizations is displayed in Figure 4, which shows all antigens with a stable trend,
around 22,000 to 25,000 immunizations, in the administered doses from month 0 (January
2018) to nearly month 26 (February 2020). The only exception was the PCV vaccine, for
which the breakpoint begins on month 23 (November 2019). The lowest point in the
vaccination trend is observed in month 28 (April 2020) for the four antigens, with doses
oscillating between 14,000 and 16,000 immunizations. Subsequently, all administered
doses presented an increasing trend with higher doses administered around months 32
(August 2020) to 34 (November 2020). The PENTA and PV vaccines presented a marked
decreasing trend, showing new low immunization levels between 10,000 and 14,000 doses
administered, respectively.
Vaccines 2022, 10, x FOR PEER REVIEW 8 of 13
the PENTA vaccine, the cold spots include the Los Rios, Manabí, Bolivar, and Chimborazo
provinces, with coverage values of 74.54%, 78.80%, 67.85%, and 69.18%, respectively. The
vaccination coverage values for these five provinces in the pre-pandemic years were
88.51%, 84.51%, 90.04%, 68.58%, and 73.18%.
The insular region was not included in this analysis due to the absence of neighboring
counterparts. The general percentages of vaccination coverage in 2020 calculated for the
Amazon, Coast, Highland, and Insular regions were 84.53%, 75.74%, 70.36%, and 69.33%,
respectively.
3.3. Yearly Trend Analysis and Administered Vaccine Doses during April and November 2018–
2020
The Joinpoint analysis used to detect specific breakpoints and changes related to im-
munizations is displayed in Figure 4, which shows all antigens with a stable trend, around
22,000 to 25,000 immunizations, in the administered doses from month 0 (January 2018)
to nearly month 26 (February 2020). The only exception was the PCV vaccine, for which
the breakpoint begins on month 23 (November 2019). The lowest point in the vaccination
trend is observed in month 28 (April 2020) for the four antigens, with doses oscillating
between 14,000 and 16,000 immunizations. Subsequently, all administered doses pre-
sented an increasing trend with higher doses administered around months 32 (August
2020) to 34 (November 2020). The PENTA and PV vaccines presented a marked decreasing
trend, showing new low immunization levels between 10,000 and 14,000 doses adminis-
tered, respectively.
Figure 4. Yearly Joinpoint analysis of immunizations administered for infants in Ecuador. The four
graphs show the number of the last doses administered of rotavirus, poliovirus, pneumococcal, and
Figure 4.
Yearly Joinpoint analysis of immunizations administered for infants in Ecuador. The four
graphs show the number of the last doses administered of rotavirus, poliovirus, pneumococcal, and
pentavalent vaccines. Months (January to December) and years (2018 to 2020) covered: 0–12, 2018;
13–24, 2019; 25–36, 2020.
Vaccines 2022,10, 857 8 of 12
The following specific analysis aimed to determine the possible influence of the
government measures against the COVID-19 pandemic imposed during April 2020 on the
national vaccination process and its subsequent flexibilization in November of the same
year. During April, the pre-pandemic years show similar numbers, between 21,000 and
24,000 administered doses, with the highest variation around 2600 for the PCV vaccine.
In 2020, the significant difference with 2018–2019 in the last applied dose was maintained
for all the antigens. In this case, immunization with the PV vaccine was the most affected,
followed by the PCV, PENTA, and ROTA antigens, with reduction means of 18,468, 12,449,
12,310, and 9672, respectively (Table 3).
Table 3. Last administered vaccination doses for infants during April 2018–2020 in Ecuador.
Vaccine Administered Doses Variation
2018–2019
p-Value
2018–2019
Variation
2018–2020
p-Value
2018–2020
Variation
2019–2020
p-Value
2019–2020
Variation
PrePandemic
Years–2020
2018 2019 2020
ROTA 21,121 23,802 12,789 2681 0.304 8332 0.000 11,013 0.000 9,672
PV 23,770 24,590 5712 820 0.811 18,058 0.000 18,878 0.000 18,468
PCV 22,956 24,656 11,357 1700 0.582 11,599 0.000 13,299 0.000 12,449
PEN TA 22,712 24,512 11,302 1800 0.474 11,410 0.000 13,210 0.000 12,310
However, there was no statistical difference between November 2020 and the two
other evaluated years, with around 20,000 administered doses for all the antigens in the
initial year of the pandemic (Table 4). Despite this apparent recovery, the mean drops of
applied doses oscillated between 1365 for ROTA and 3865 for PCV as the least and most
affected administered vaccines.
Table 4. Last administered vaccination doses for infants during November 2018–2020 in Ecuador.
Vaccine Administered Doses Variation
2018–2019
p-Value
2018–2019
Variation
2018–2020
p-Value
2018–2020
Variation
2019–2020
p-Value
2019–2020
Variation
PrePandemic
Years–2020
2018 2019 2020
ROTA 24,882 21,968 22,060 2914 0.689 2822 0.689 92 0.689 1365
PV 23,831 21,783 20,892 2048 0.548 2939 0.548 891 0.548 1915
PCV 23,603 20,316 18,084 3287 0.167 5519 0.167 2232 0.167 3875
PEN TA 23,310 22,174 19,017 1136 0.051 4293 0.051 3157 0.051 3725
4. Discussion
In this study, we analyzed the influence of the COVID-19 pandemic on routine im-
munization programs for infants during 2020 in Ecuador. The size of the population to be
vaccinated (infants under one year of age) did not vary significantly in the three years ana-
lyzed, including 2020, the year of the pandemic that was evaluated; therefore, the reduction
in vaccination coverage in this age group in 2020 might not have been the consequence
of a reduction of infants to be immunized but another independent effect. Overall, the
data show a severe disruption for the four antigens evaluated at the national scale, for
both administered doses and coverage percentages. The reduction of the doses in 2020 was
137,031, about 14% fewer vaccines administered compared to 2018/2019.
Similarly, we described the national percentage coverage reduction, with the PENTA
vaccine as the most affected antigen within the routine program. These values indicate
that a specific population of infants missed the ROTA, PV, PCV, and PENTA vaccinations
during the months between March and December of 2020.
To the best of our knowledge, this is the first detailed research analyzing the impact
of the pandemic on infant immunization in Ecuador, and it is among only few studies
published in Latin America. A global study estimating the disruption in routine immuniza-
tions in several regions reported a general 7.7% and 7.9% reduction for the measles and
diphtheria-tetanus-pertussis (DTP3) vaccines [
27
]; the last one includes three out of the five
antigens presented in the PENTA vaccine applied in Ecuador. Specifically, a 6.6% reduction
for the DTP3 coverage is described in the Latin American region and 6.7% in the case of
Ecuador [27].
Vaccines 2022,10, 857 9 of 12
Our reported values suggest a more drastically affected vaccination process and indi-
cate the importance of measuring the extent of the disruption of immunizations, especially
in LMIC countries. The benefits of vaccination across childhood are only guaranteed if
the appropriate immunization schedule is completed at the correct time [
8
]. However, the
vaccination coverage values of the last doses for all the antigens were the most reduced
in 2020. Although there is no direct explanation for these results, this may be related to
several reasons, such as the misconception that good immunity can be achieved by partial
immunization, general parental choices, or even using alternative methods, as determined
in other studies [28,29].
Although disruptions in routine immunization have been described in several coun-
tries and regions of the world, the reduced levels of administered immunizations could be
different depending on the province, canton, or subdistrict evaluated in a specific country.
The lack of clustering observed in the intra-annual spatial analysis performed for Ecuador
suggests that the vaccination coverage was generally affected across the territory. Despite
this, specific cold spots were determined in the Guayas province for all the antigens. In
fact, the cities in this coastal province presented the highest morbidity and mortality rates
during the initial months of the pandemic [
30
], which lead to the tightening of COVID-19
related domestic measures to control the transmission in this and other provinces [31].
Moreover, the disruption of the PENTA vaccine was more drastic for several provinces
of the Coast and Highlands regions of the territory. Conversely, several provinces in the
Amazon region presented hot spots, suggesting a high vaccination coverage compared
to the other two regions. Nevertheless, it is essential to highlight that the population of
the Amazon provinces is significantly less (739,814) compared to the Coast (7,236,822) and
the Highlands (6,449,355) regions [
32
]. Similarly, the specific population behavior of each
province and the compliance with the generally adopted measures could be responsible for
the differences detected in the immunization processes described in this section. This con-
text and other socio-cultural factors could have influenced the pattern of better vaccination
coverage observed in the Amazon area.
Although the Galapagos Islands were not included in this analysis, this region showed
the lowest vaccination coverage in this study. The COVID-19 pandemic could be worsened
in this area due to its being located outside of the mainland and problems related to
shortages and disruptions of medical supply chains, which also affected the global vaccine
distribution for routine immunizations [
6
]. Other studies carried out in Sierra Leone,
Pakistan [
11
], and the Dominican Republic [
33
] highlighted the importance of detecting
vulnerable zones to the impact of immunization programs, which are usually rural areas
and subnational locations where inequities affect access to vaccination. Based on this,
every country should evaluate its performance during this pandemic to strengthen its
public health services and avoid possible outbreaks of several VPDs such as polio, whose
eradication may be delayed in several parts of the world due to the pandemic in the
current context [
34
], and measles, which is the main threat due to its high reproduction
number [35,36].
Like several countries, Ecuador adopted non-pharmaceutical measures to mitigate
viral transmission among its population. The measures were appointed colors according
to the level of mobilization restrictions: red for the highest level of restriction, imposed
from March 2020 and mainly associated with the movement of vehicles and persons, and
green for more flexible measures from October to December 2020. The trend analysis
showed similar behavior in the immunizations applied during 2018, and in 2019 until the
declaration of the COVID-19 pandemic, in March 2020. Subsequently, the trend indicates
a severe decrease in immunizations, which is in concordance with the red stage in April
2020, when the national last administered vaccination doses were significantly lower than
pre-pandemic years.
Mobilization restriction, national lockdowns, and stay-at-home orders may be related
to these results, although other social factors could be playing specific roles. Surveys applied
to parents and caretakers indicate that the fear of contracting the virus, the overburdened
Vaccines 2022,10, 857 10 of 12
health care systems of the countries, the shortage of vaccines, and the lack of protective
equipment are among the alternative reasons for the disruption of the vaccination described
in various studies [
14
,
15
,
17
,
37
]. Interestingly, in November 2020, with the green stage
implemented, the number of doses administered is similar to 2018/2019, indicating a
similar vaccination process for the three evaluated years.
However, it is difficult to suggest a recovery in the the vaccination doses administered
in November 2020 due to the overall reduction of immunizations, calculated with the
general data from March to December 2020. Similarly, the last doses applied of some
antigens such as the PCV and PENTA vaccines presented a decrease towards December
2020. Although no special measures were imposed during this month, this may be related
to a shortage in vaccine supplies in the country, an effect that has been reported in other
works [
6
]. Nevertheless, the increasing number of immunizations applied in the last months
of 2020 is a behavior observed in several countries and regional studies [27,38].
Based on this scenario, implementing tailored catch-up strategies for unvaccinated
children is imperative to prevent possible outbreaks of these diseases, especially when
returning to normal activities. Some of the recommendations listed in several studies are
recognizing the most affected zones, contacting and identifying those who missed specific
immunizations, implementing social media campaigns for the general public, and creating
opportunities for vaccination services [12,14].
For this study, we used the best-verified source of information in the country, which
was obtained from the Ecuadorian MSP. However, we must emphasize that this data comes
from the periodic official vaccination report carried out by each health establishment in the
country. Based on this fact, the main limitations in this study are related to the intrinsic
bias in the public data, which may contain gaps or erroneous entries. Moreover, it is
necessary to clarify that the MSP does not report data from the private sector, which only
allows for the analysis of data from public health institutions. Additionally, our approach
was mainly based on the number of administered doses to the total yearly population of
infants, due to the lack of data supplied and authorized for use by the MSP about this
population for specific months of the evaluated years. Based on the design of this study,
certain confounding factors remained unadjusted. Thus, we can only hypothesize about
the possible reasons for the vaccination disruption in the country and associate the data
with the policy restriction during 2020.
5. Conclusions
In conclusion, the COVID-19 pandemic caused unprecedented interruptions in vaccine
delivery in several countries worldwide. For example, our study reports that there was
a reduction in the number of vaccine doses in Ecuador and the vaccination coverage for
children under one year of age for the analyzed vaccines (ROTA, PV, PCV, and PENTA).
This scenario could be explained by the imminent fear of contagion and the public health
measures implemented to mitigate the direct effects of the pandemic. In this sense, the
COVID-19 pandemic has disrupted essential health care services around the globe. As a
result, several countries with high mortality and morbidity rates due to COVID-19 are still
unable to recover from the direct effects of the pandemic. Therefore, Ecuador must restore
the systematic efforts to ensure the fulfilment of its childhood immunization schedule.
Otherwise, this could initiate the spread of vaccine-preventable diseases in children.
Author Contributions:
Conceptualization, G.L.S.-R. and J.R.R.-I.; methodology, G.L.S.-R., J.S.-L. and
J.R.R.-I.; software, G.L.S.-R. and J.S.-L.; investigation, G.L.S.-R., J.S.-L., A.J.R.-M., J.R.-C.,
J.-C.N.
and
J.R.R.-I.; data curation, G.L.S.-R., J.R.-C. and J.S.-L.; writing—original draft preparation, G.L.S.-R.,
A.J.R.-M., J.-C.N. and J.R.R.-I.; writing—review and editing A.J.R.-M., J.-C.N. and J.R.R.-I.; supervision,
J.-C.N. and J.R.R.-I.; project administration, J.R.R.-I. and J.-C.N. All authors have read and agreed to
the published version of the manuscript.
Funding:
This work was supported by a grant from DII-P011617_2 (JCN, JRRI, JGS), Directorate of
Research and Innovation, Universidad Internacional SEK (UISEK).
Vaccines 2022,10, 857 11 of 12
Institutional Review Board Statement:
Ethical review and approval were waived for this study, due
to REASON: the database only contained the number of doses applied in the Ecuadorian territory
and did not contain personal information. The National Directorate of Health Intelligence of the
Ecuadorian MSP, under the document MSP-DIS-2021-0027-O indicates that this research does not
require approval of this Directorate, nor the Ethics Committee for the Expedited Review of Research
in COVID-19 in Ecuador.
Informed Consent Statement: Not Applicable.
Data Availability Statement:
Restrictions apply to the availability of these data. Data was obtained
from the National Direction of Statistics and Health Information Analysis of the Ministry of Health
(MSP) under the authorizations MSP-DNEPC-2021-0003-O and MSP-DNEAIS-2021-0069-O, and are
available from the authors with the permission of the MSP.
Acknowledgments:
To Ministery of Health, Ecuador (Ministerio de Salud Pública, MSP). To review-
ers for the helpful suggestions and comments to improve the final version.
Conflicts of Interest: The authors declare no conflict of interest.
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