COVID-19 related disruption and resilience in immunisation activities in LMICs: a rapid review

Abstract

Objectives
We conducted a rapid review to determine the extent that immunisation services in low-income and middle-income countries (LMICs) were disrupted by the COVID-19 pandemic and synthesised the factors that can be used to build resilience in future.

Design
Rapid review reported in accordance with the Preferred reporting for Systematic reviews and Meta-Analyses (PRISMA) guidelines.

Data sources
PubMed and Web of Science were searched through 6 October 2023.

Eligibility criteria for selecting studies
We included studies that focused on disruption to immunisation activities due to the COVID-19 pandemic in LMICs. Outcomes included routine vaccine coverage, supplementary immunisation activities, vaccine doses, timing of vaccination, supply chain changes, and factors contributing to disruption or resilience.

Data extraction and synthesis
Two independent reviewers used standardised methods to search, screen and code studies. Quality assessment was performed using a modified version of the Critical Appraisal Skills Programme for qualitative research. Findings were summarised qualitatively.

Results
Of 4978 identified studies, 85 met the eligibility criteria. Included studies showed declines in immunisation activities across LMICs related to the COVID-19 pandemic. These included reductions in achieved routine coverage, cancellation or postponement of campaigns and underimmunised cohorts. Immunisation was most disrupted in the early months of the pandemic; however, recovery varied by country, age-group and vaccine. Though many countries observed partial recovery in 2020, disruption in many countries continued into 2021. It has also been noted that clinician staff shortages and vaccine stock-outs caused by supply chain disruptions contributed to immunisation delays, but that concern over COVID-19 transmission was a leading factor. Key resiliency factors included community outreach and healthcare worker support.

Conclusions
There is limited information on whether reductions in vaccination coverage or delays have persisted beyond 2021. Further research is needed to assess ongoing disruptions and identify missed vaccine cohorts.

Full text

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HartnerA- M, etal. BMJ Open 2024;14:e076607. doi:10.1136/bmjopen-2023-076607
Open access
COVID- 19 related disruption and
resilience in immunisation activities in
LMICs: a rapid review
Anna- Maria Hartner ,1,2 Xiang Li,1 Katy Gaythorpe1
To cite: HartnerA- M, LiX,
GaythorpeK. COVID- 19 related
disruption and resilience in
immunisation activities in LMICs:
a rapid review. BMJ Open
2024;14:e076607. doi:10.1136/
bmjopen-2023-076607
►Prepublication history
and additional supplemental
material for this paper are
available online. To view these
les, please visit the journal
online (https://doi.org/10.1136/
bmjopen-2023-076607).
Received 12 June 2023
Accepted 19 July 2024
1MRC Centre for Global
Infectious Disease Analysis,
Jameel Institute, School of
Public Health, Imperial College
London, London, UK
2Centre for Articial Intelligence
in Public Health Research,
Robert Koch Institute, Wildau,
Germany
Correspondence to
Ms Anna- Maria Hartner;
a. hartner@ imperial. ac. uk
Original research
© Author(s) (or their
employer(s)) 2024. Re- use
permitted under CC BY.
Published by BMJ.
ABSTRACT
Objectives We conducted a rapid review to determine
the extent that immunisation services in low- income and
middle- income countries (LMICs) were disrupted by the
COVID- 19 pandemic and synthesised the factors that can
be used to build resilience in future.
Design Rapid review reported in accordance with the
Preferred reporting for Systematic reviews and Meta-
Analyses (PRISMA) guidelines.
Data sources PubMed and Web of Science were
searched through 6 October 2023.
Eligibility criteria for selecting studies We included
studies that focused on disruption to immunisation
activities due to the COVID- 19 pandemic in LMICs.
Outcomes included routine vaccine coverage,
supplementary immunisation activities, vaccine doses,
timing of vaccination, supply chain changes, and factors
contributing to disruption or resilience.
Data extraction and synthesis Two independent
reviewers used standardised methods to search, screen
and code studies. Quality assessment was performed
using a modied version of the Critical Appraisal Skills
Programme for qualitative research. Findings were
summarised qualitatively.
Results Of 4978 identied studies, 85 met the eligibility
criteria. Included studies showed declines in immunisation
activities across LMICs related to the COVID- 19
pandemic. These included reductions in achieved routine
coverage, cancellation or postponement of campaigns
and underimmunised cohorts. Immunisation was most
disrupted in the early months of the pandemic; however,
recovery varied by country, age- group and vaccine.
Though many countries observed partial recovery in 2020,
disruption in many countries continued into 2021. It has
also been noted that clinician staff shortages and vaccine
stock- outs caused by supply chain disruptions contributed
to immunisation delays, but that concern over COVID- 19
transmission was a leading factor. Key resiliency factors
included community outreach and healthcare worker
support.
Conclusions There is limited information on whether
reductions in vaccination coverage or delays have
persisted beyond 2021. Further research is needed to
assess ongoing disruptions and identify missed vaccine
cohorts.
INTRODUCTION
The COVID- 19 pandemic began on 12
December 2019 and quickly spread globally,
adding to the strain on existing healthcare
provision and creating unique problems
in terms of service delivery.1 Throughout
2020, there were disruptions to screening
for cancer, maternal health services, care for
chronic conditions and immunisations.2 This
strain on health services has continued past
2020, as even those that have recovered to
pre- COVID levels of visits and surveillance
have to catch- up missed cohorts and delayed
treatments.
Low- income and middle- income countries
(LMICs) disproportionately bear the burden
of vaccine preventable diseases3; however,
globally, vaccination has seen a plateau in
coverage, with zero- dose children an ongoing
concern. The issue of zero- dose or underim-
munised children is particularly important, as
it can hint at wider heterogeneity in healthcare
access which may have been exacerbated by
the pandemic.4 It is estimated that 67 million
children missed vaccinations between 2019
and 2021; of those, 48 million were zero- dose
children.5 Furthermore, targeting zero- dose
children can be more difficult as they are
often in harder- to- reach areas, particularly in
LMICs, where 1one in six children living in
rural areas are zero- dose.5
STRENGTHS AND LIMITATIONS OF THIS STUDY
⇒The rapid synthesis of ndings through the decision
to structure the paper methodologically as a rapid
review allows for key insights to target missed co-
horts and identify research gaps related to immuni-
sation disruption and recovery to- date.
⇒We include a narrative analysis of disruption across
low- income and middle- income countries; this re-
view benets from the inclusion of barriers, enablers
and resilience to/in service provision.
⇒The search strategy was limited to English- language
studies identied from databases PubMed and Web
of Science up to 6 October 2023, meaning not all
relevant research meeting inclusion criteria may
have been captured.

2HartnerA- M, etal. BMJ Open 2024;14:e076607. doi:10.1136/bmjopen-2023-076607
Open access
Resilient healthcare systems can withstand additional
and unusual strains while maintaining priority services.
Yet, it is still uncertain what factors contributed to disrup-
tion or resilience in light of the COVID- 19 pandemic,
which was a unique test on global healthcare systems.
These factors and considerations may be instrumental
in preparing for future healthcare strains such as those
potentially caused by other epidemics, climate change, or
antimicrobial resistance. As such, understanding the key
factors for disruption due to the COVID- 19 pandemic is
critical for future planning in order to minimise the nega-
tive consequences of disruptions.
In order to understand the current state of vaccination
coverage disruption, and highlight factors contributing
to resilience, we undertook a rapid review (RR) of the
existing literature. This focused on LMICs as they bear
the majority of burden of vaccine preventable diseases.
We included studies that not only discuss the quantitative
measures of disruption, such as reduced immunisation
coverage and cancelled campaigns, but also more quali-
tative discussions of the factors contributing to disruption
or characteristics of resilient systems.
AIM AND RESEARCH QUESTIONS
The aim of this review was to understand the extent of
disruptions in vaccination coverage due to the COVID- 19
pandemic and the factors that contributed to the disrup-
tion or resilience. Specifically, our research questions
were:
RQ1: To what extent were immunisation services in
LMICs disrupted by the COVID- 19 pandemic?
RQ2: How did disruption vary by geography, demogra-
phy, or socioeconomic group?
RQ3: What factors contributed to coverage disruption
or resilience?
METHODS
A RR was conducted using streamlined systematic review
methods and reported in accordance with the Preferred
Reporting Items for Systematic Reviews and Meta- Analyses
(PRISMA) guidelines.6 The full PRISMA checklist can be
found in the online supplemental material on pages 1–5.
Procedure
We searched PubMed and Web of science up to 6 October
2023 for studies published after 1 December 2019 in the
English- language with search terms (((COVID- 19) OR
(SARS- CoV- 2))) AND (immunisation OR vaccination)
AND (disruption OR delay* OR postpon*). Studies
were included if they focused on disruption to vaccina-
tion activities due to the COVID- 19 pandemic in LMICs.
Studies were excluded if they focused on high- income
countries only, examined disruption due to other
factors, that is, not related to the pandemic, or were
reviews, commentaries, or modelling studies without
novel data.
Study selection, data extraction and quality assessment
Search results were imported into the Covidence (www.
covidence.org) systematic review management tool
where duplicates were removed. Titles and abstracts were
screened by one reviewer, full- text review was completed by
two reviewers with conflicts resolved through consensus.
Each study was extracted by one reviewer into a Google
sheet. We extracted information on (1) last date of
included data, (2) countries studied, (3) qualitative find-
ings related to the research questions RQ1, RQ2 and
RQ3 and (4) binary data on whether routine immunisa-
tion, SIAs, doses, schedule timing or supply chains were
mentioned in the study. A second reviewer was consulted
where there was uncertainty concerning the extracted
data.
The quality of studies was assessed through a modi-
fied, nine question checklist of the Critical Appraisal
Skills Programme (CASP) for qualitative studies. The
10th question, ‘how valuable is the research’, was omitted
given the aim to assess quality based on binary indicators
and given no studies were excluded based on determina-
tions of value. Results were listed as N/A if not applicable
for the study. All CASP results are available in the online
supplemental material on pages 6–8.
Synthesis
There were two main types of evidence to synthe-
sise: quantitative information (ie, percentage drops in
coverage achieved, doses administered, or supplemen-
tary immunisation activities (SIAs) postponed) and qual-
itative information on contributing factors informed by
surveys or questionnaires. We grouped results by research
question. Finally, we collate characteristics of the studies
themselves, such as countries studied or dates of included
data. For these, we have prepared summary statistics. The
full list of included studies and outcomes provided are
included in the online supplemental material.
Patient and public involvement
There was no patient or public involvement in this study.
RESULTS
Characteristics of studies
We found 4978 studies where 85 met the inclusion
criteria (figure 1). The majority of studies were published
in either 2021 (n=30; 35.29%) or 2022 (n=32; 37.65%),
though most studies only reported on data from 2020
(n=52; 61.18%). Fourteen (16.47%) studies included data
during the first 6 months of 2021; a further 15 (17.64%)
included data between July and December of 2021. Only
four (4.71%) studies included data from 2022; the most
recent of these covered data through November of 2022.
Most (n=20; 23.53%) of the studies considered multiple
LMICs. Of those that only considered one country, India
(n=12; 14.11%), Ethiopia (n=7; 8.24%), Pakistan (n=5;
5.88%) and Brazil (n=4; 4.71%) were the most frequently
studied. The African continent was the most represented.

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Most (n=57; 67.05%) studies examined the effect of the
COVID- 19 pandemic on routine immunisation coverage,
with an additional seven (8.24%) reporting pandemic
effects on SIAs. The change in the number of admin-
istered doses (n=19; 22.35%) or the timing of doses
(n=15; 17.64%) was also reported by several studies; eight
(9.41%) reported disruptions in the vaccine supply chain.
Extent of disruption
We divide this section into a few main areas: supply chains
and vaccine availability, the delivery of routine immuni-
sation (as doses given, coverage and/or delays), SIAs
and finally, signs of recovery (to prepandemic achieved
coverage in any of the disrupted activities mentioned
previously).
Vaccine supply
Following the declaration of COVID- 19 as a pandemic,
there was a reduction of vaccine sales and periods
of stock- out and low availability of vaccines in some
countries,7–11 though one study in Northern Nigeria
found that states experienced less stock- outs in 2020
as compared with 2019.12 More globally, vaccine sales
between April and August 2020 fell by 9.5% across 84
countries,13 but some losses in vaccine receipt after stock-
outs were recouped by catch- up activities, such as in
Uganda.8
Routine immunisation
We divide insight by WHO region or country.
In the WHO African Region, there was a varied picture
of disruption. In Ethiopia, minimal disruptions were
found up to August 2020.10 14–18 Similarly, in the Demo-
cratic Republic of Congo (DRC), disruptions in Kinshasa
were minimal up to December 2020, with one study
even finding increases in diphtheria tetanus toxoid and
pertussis dose 3 (DTP3) and measles- containing- vaccine
first- dose (MCV1) doses administered.19 20 In Kenya21–23
and Burkina Faso,24 immunisation services were largely
Figure 1 Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) ow of study selection.

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unaffected. Zambia saw a mixed picture, in which esti-
mates during the first 6 months of 2020 varied month-
to- month, with both disruptions and positive increases
as compared with previous years; overall, however, the
number of additional children missed was found to be
minimal.25 In South Africa, however, full immunisation
dropped in the first months of the pandemic, especially in
April, where it dropped by 30%.26 27 Ghana,28–30 Nigeria,31
Uganda,8 20 Liberia,32 Sierra Leone20 33 and Somalia11 all
saw drops in coverage in 2020, and while some countries
had begun to see recovery in coverage achieved, this was
not enough to compensate for missed cohorts.20 34
In the WHO region of the Americas, there were declines
in coverage reported for the Dominican Republic,
Mexico, Ecuador and Brazil. The Dominican Republic
saw a drop of 10 percentage points,35 while vaccinations
were reduced by 36% in Mexico,36 37 and 14% fewer doses
administered were in Ecuador.38 In Brazil, approximately
20% of children missed vaccinations, with an 18% overall
decline in doses administered in the first year of the
pandemic.39–41 However, one study found no significant
evidence of COVID- 19 isolation measures on vaccines per
child in Brazil.42
In the Eastern Mediterranean WHO region, drops in
coverage were seen for Lebanon, Afghanistan, Jordan
and Pakistan43–47 of 31%, 21%, 6%–16% and 30%–48%,
respectively, over the initial stages of the pandemic. Paki-
stan additionally reported that as of September 2021,
18% of parents had delayed routine immunisation for
their children during the pandemic; an additional 2%
received no immunisations.48
In the South East Asian WHO region, there were signifi-
cant disruptions.49 50 In India, six studies found substantial
drops in coverage across the majority of districts (88%51)
especially in lockdown and early in the pandemic.52–56
As a result, children born in India after COVID- 19 had a
2%–10% lower probability of timely vaccination compared
with earlier cohorts.57 58 Two studies, one conducted among
the Armed Forces population in Mumbai, the other across
India, found disruptions continued into 2021.56 58 Only
one study found that the number of immunisation sessions
in India increased in 2020 and 2021 compared with 2019.59
In Nepal and Bangladesh, the most severe disruptions were
also seen earlier in the pandemic, particularly in Bangla-
desh, where 20%–25% of planned outreach immunisations
were cancelled between April and May 2020.60 61 In Indo-
nesia, one study reported that 27.4% of parents delayed
compulsory immunisation in 2020.62
In the WHO European region, in Armenia, there were
only small declines in coverage achieved.63 In the Western
Pacific WHO Region, one study from China found that
immunisation coverage dropped drastically in January
2020, but had recovered to pre- pandemic levels by June.64
However, a second study conducted in Beijing found
pandemic effects to continue into 2021, staying below
2019 levels despite catch- up activities.65
Globally, there were substantial drops in routine
immunisations in 2020.9 Overall, it was estimated that
there were 31% fewer vaccine doses given.66 In middle-
income countries, 14% of individuals delayed or missed
vaccinations in the first 6 months of the pandemic,67
and there was a 20% increase in children who had not
completed the three- dose DTP series.68 While disrup-
tion varied by vaccine,69 70 most saw the most severe
declines in the 6 months of the pandemic followed by
variable recovery71 which may affect control and elimi-
nation efforts.72
It was not only the total number of doses administered
that was affected, but also when those doses were given.
In China and India, the majority of interviewed caregivers
delayed vaccination57 67 73–75 and in Ecuador and Sierra
Leone, this delay was worse for last doses.33 38
Supplementary immunisation activities
Overall, we found fewer studies focusing on SIAs or
campaigns specifically; however, there are compre-
hensive records kept by the WHO campaign tracker
as part of the immunisation repository.76 In 57 coun-
tries, SIAs were more disrupted in the early stages of
the pandemic, with 57% of planned campaigns globally
postponed or cancelled because of COVID- 19 by May
2020.76 By December 2020, this had fallen to 26% and
many campaigns were reinstated from July 2020 onwards.
By December 2021, in 54 countries, this had fallen again
to 16% of scheduled campaigns delayed or cancelled.76
Overall, of those campaigns disrupted between March
2020 and December 2021, 59% had been reinstated.76
Factors leading to postponement or cancellation of SIAs
included non- pharmaceutical interventions, such as
national lockdowns,77 and stock- outs or increased demand
for general healthcare supplies.8 78 One study found that
the national policy guidance of Mozambique and Uganda
recommend the halting of campaigns in 2020.79 Addition-
ally, while some SIAs had been reinstated, and there were
plans for catch- up activities, there are still large missed
cohorts.9 53 72 80
Recovery
Information on recovery is limited by the date ranges
of the included studies, which mainly focused on 2020
and 2021. A key finding is that while there were signs of
improvement in routine immunisation coverage achieved
and reinstated vaccination campaigns, there was not the
positive increase needed to catch- up missed cohorts, that
is, a sufficient return to prepandemic levels of immunisa-
tion.33 34 37 61 65 66 70 81 It was also noted that pre- COVID- 9
levels of coverage had not been reached in many coun-
tries by the end of 2022.72
Heterogeneity in disruption
Heterogeneity in immunisation disruption was found
across several factors, including geography, demography,
wealth and education; these are further detailed below.
Variations in the extent of disruption by antigen were
similarly reported in several studies.10 13 18 20 38 44 49 64 65 75

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Geographical heterogeneity
Despite significant overall decreases in immunisation
in LMICs, there was geographical heterogeneity in the
extent of disruption and in the regions and/or indi-
viduals affected. On a national level, several studies
reported differences in the extent of disruption as a
result of economic income classification49 67 68 by WHO
region,68 69 78 by global burden of disease super- region,66
or by Gavi eligibility,68 with greater pandemic impact
observed in LMICs compared with high- income coun-
tries, affecting the primarily African Region, the Amer-
icas and Asia. The reverse trend was seen for vaccine sales
early in the pandemic (ie, April to August 2020), with
high- income countries experiencing a 20% decline and
low- income countries observing a 10% increase.13
On a subnational level, many countries observed statis-
tically significant differences between regions, provinces
or districts in regards to the change in health service util-
isation,37 51 56 59 82 routine immunisation coverage38 44 55 or
complete vaccination.24 In some countries, certain prov-
inces reported increases in immunisation service provi-
sion or doses for some vaccines, such as in the Southern
Province of Rwanda, where measles and rubella immuni-
sation increased.82 Geographical heterogeneity was also
observed in the subsequent recovery of services.27 51
While some countries reported differences in disrup-
tion between urban and rural areas, there was significant
heterogeneity in the extent of disruption. One study
found that the odds of immunisation in Ethiopia were
higher in rural areas,14 while another observed greater
initial declines in urban and periurban areas in South
Africa, followed by recovery in these areas and declines
in rural areas as the pandemic progressed.27 In Paki-
stan, lockdown affected rural areas more than urban
areas.46 Geographical heterogeneity was also observed
between Ethiopia’s hospitals and health centres, in
which vaccine- related supplies were twice as likely to be
affected by COVID- 19 in hospitals7 10; in Nigeria, activi-
ties coordinated at the state level were impacted less than
healthcare facilities.12 In China, immunisation services
continued in hospitals, even when immunisation clinics
were suspended.64
In India, children residing in ‘COVID- 19 red zones’
were more likely to face immunisation disruption.55 Simi-
larly, a study on polio outreach services in 33 African and
Eastern Mediterranean countries found services neces-
sary for ‘reaching their most vulnerable populations’
were partially or severely disrupted.78
Demographic heterogeneity
Few studies focused on the effects of demographic hetero-
geneity on COVID- 19- related immunisation disruption,
including factors such as gender, age, birth order or caste.
Only two studies looked at differences by gender; one
found greater declines in females than males, though this
decline was not significant.44 The second, conducted in
Brazil, also found no significant differences, but did find
that infants were less likely to experience immunisation
disruptions or delays compared with 1- year- old chil-
dren.39 This finding was similar to two studies, conducted
in Eastern India and in China, where increasing age of
the child was found to be associated with immunisation
delays.74 75 A study conducted in South- East Asia and
the Western Pacific found similar results, in which early
infancy was less disrupted than infancy, school- entry
age and adolescent immunisation.49 However, greater
disruption was seen among infants compared with adult/
elderly immunisation.49 Additionally, one study in Jordan
found that children older than 12 months were less likely
to experience delays.45 Finally, one study conducted in
China found firstborn children were less likely to expe-
rience delays,75 while another paper in India examined
heterogeneity as a result of ethnicity or caste, finding
lower castes had lower likelihoods of full immunisation
and greater immunisation disruption, though these find-
ings were not significant.55
While even fewer articles examined the demographic
heterogeneity of disruption based on the characteristics
of parents or caregivers, two studies stratified results by
maternal or caregiver age; one finding that increasing
maternal age was associated with delayed vaccination,74
the other finding no association.45 Only one study exam-
ined other contributing factors of parents, finding that
women were more likely to delay vaccination for their
children than men; presence of a chronic illness, prior
influenza vaccination, or experience with COVID- 19
diagnosis were also associated with delays in childhood
vaccination.62
Socioeconomic heterogeneity
Contributors to socioeconomic heterogeneity in immu-
nisation disruption largely included measures of house-
hold income and education. Two studies, one in Brazil
and the other in India, found that missed vaccine doses
were more likely in children from poorer households39 55;
in India it was additionally found that there were greater
declines in immunisation among poorer subgroups.55
A study in South Africa found mixed results, finding
declines in full immunisation and first dose of measles
greater in wealthier quintiles at the start of the pandemic,
but with faster positive recovery and continued declines
among poorer subgroups as the pandemic progressed.27
Another study in Iraq found that low socioeconomic
status was associated with an increase in missed vaccine
appointments.83 Two studies, one conducted in Iraq and
one conducted in Indonesia, similarly found that the type
of employment changed the odds of vaccination during
the pandemic62 83; in Indonesia, healthcare workers
(HCWs) especially were more likely to delay vaccination
in their children.62
Only two studies, one in India and one in Iraq, focused
on education, similarly finding higher probability of
incomplete immunisation and greater declines in house-
holds without formal education.55 83

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Factors contributing to coverage disruption and resilience
We divide this section into three key areas: health system
barriers, vaccine demand, and resilience.
Health system barriers
Many of the initial challenges in maintaining immunisa-
tion services in LMICs were the result of health system and
supply barriers during the early stages of the pandemic.
Many countries reported issues with vaccine supply
delays or stock- outs7–9 11 32 37 58 81 84–86 and lack of personal
protective equipment (PPE) for HCWs, including masks,
gloves and other drugs and supplies.7 12 31 32 51 51 53 54 84 85 87
Disruption caused by vaccine stock- outs or supplies was
found to vary by WHO region9 or by geographical subre-
gion10 31 49 87; notably one study in Southeast Asia and the
Western Pacific found vaccine stock- outs to be among the
least important reasons for service provision delays.49 A
lack of logistical support impacting routine services or
outreach, such as a lack of fuel or water, was reported by
three studies in the WHO African region.31 32 84
Similarly, HCWs availability posed a significant chal-
lenge, with countries citing difficulties due to the diversion
of staff to COVID- 19 response, staff illness and transporta-
tion difficulties, among others.9 12 18 31 31 32 51 53 54 85 One study
in Kenya further reported disruption due to a HCW strike
from December 2020 to January 2021.23 On an individual
level, HCWs reported that pandemic- related stigma, stress
or fears impacted service delivery,7 31 51 54 60 85 with some
additionally reporting harassment by law enforcement or
by patients themselves.31 51 Only one study, conducted at
a tertiary health centre in Ghana, found no disruptions in
vaccine supply or in HCW availability.29
COVID- 19 lockdowns and restrictions also resulted
in cancelled immunisation services, clinic closures
or reduced healthcare access or services avail-
able,7 31 32 45 46 49 55 62 67 77 83 86 88 89 with some reporting diffi-
culties maintaining COVID- 19 prevention rules, such as
social distancing, due to non- compliant patients or a lack
of space.12 31 54 84
Competing priorities also meant some countries faced
declines in funding for immunisation services or supplies,
resulting in financial constraints.12 53 87
Vaccine demand and acceptance
Many of the challenges in maintaining routine immu-
nisation services during the COVID- 19 pandemic also
resulted from declining vaccine demand and increasing
fear or stigma surrounding COVID- 19 among caregivers.
Declines in vaccine demand were frequently attributed
to travel barriers or difficulties in reaching immunisation
services or clinics,9 12 16–18 32 48 49 53–55 60 65 75 83 89 COVID- 19
restrictions or requirements, including testing require-
ments, mask requirements or lockdowns,45 47 60 67 84 85 88
and financial constraints.16 53 60 67 One study, conducted
in South East Asia and the Western Pacific, reported
that while affordability issues contributed to immunisa-
tion service utilisation, it was among the lowest ranked
reasons.49 Some caregivers additionally reported low or
no awareness of the availability of immunisation services,
often believing clinics and hospitals were closed for
routine immunisation services.29 53 74 84
Declines in vaccine demand due to fears of contracting
COVID- 19 at clinics or hospitals were pervasive,
and one of the most reported causes across several
studies.9 12 16 18 29 32 45 47–49 53–55 58 60 67 74 84 85 89 Many others
reported additional fear or stigma against healthcare
providers, including fears that staff might be infected
by the virus.29 32 54 60 85 One survey of 100 caregivers at a
tertiary health centre in Eastern India found that 83%
of respondents agreed that ‘safety (was) more important
than vaccination’.74 Further unspecified declines in
vaccine demand were noted by several studies.9 46 81
Vaccine hesitancy factors were less commonly reported;
misinformation and misbeliefs contributed to declines
in demand in just two studies,9 60 while fears specifically
about vaccine side effects were found in just one study in
a tertiary hospital in North Ghana.29 One additional study
in Liberia reported declines due to vaccine conspiracies,
where parents believed their children would be injected
with COVID- 19.32 Only one in Ethiopia study reported
fewer declines in vaccine demand as a result of COVID- 19
pandemic misinformation, including that they were not
susceptible to the disease, the disease was not severe, or
that the pandemic did not exist.18
Resiliency
Though few papers highlighted resiliency factors
or enablers to immunisation during the COVID- 19
pandemic, two key focuses included community outreach
to address declining vaccine demand and acceptance and
the importance of improved HCW support to increase
service provision. In Jordan and China, alternative
arrangements for childhood vaccination (ie, outside of
the standard service provision within healthcare clinics)
were found to be key to maintaining immunisation
demand, though in Jordan this insight was based on a
survey of caregiver beliefs.45 73 Similarly, a community
intervention highlighting the importance of maintaining
timely vaccination, despite the pandemic, was crucial in
Jordan, India and Ethiopia.16 18 45 58 Ethiopia addition-
ally reported decreased fear of COVID- 19 as an enabling
factor.16 In India, adequate access to PPE, overcoming
barriers to transportation for HCWs, community and/or
family support and training on COVID- 19 management
were crucial to support HCWs in maintaining immuni-
sation service provision.85 Similarly, proactive communi-
cation and coordination on all levels of the healthcare
system was essential in Ethiopia in maintaining health
system resiliency.87 In India, capacity building to ensure a
trained workforce assisted in maintaining immunisation
programmes,58 89 while in Nigeria, one study found the
supply chain logistics to be the most important factor for
maintaining immunisation services.12 Finally, in Zambia,
community awareness through the National Immu-
nization Campaign assisted in catching up pandemic
declines.25

7
HartnerA- M, etal. BMJ Open 2024;14:e076607. doi:10.1136/bmjopen-2023-076607
Open access
DISCUSSION
Despite the challenges faced by health systems during
the COVID- 19 pandemic, the WHO has continued to
emphasise the importance of routine immunisation,
noting that the last effects of immunisation declines can
lead to higher burdens of disease and/or excess deaths.90
This review highlights the extent of disruption faced by
LMICs, finding significant heterogeneity between and
within regions, countries and individual demographics,
but nevertheless showing declines in routine immunisa-
tion in 2020 and 2021 that had not often not recovered to
pre- COVID- 19 levels.
SIAs and campaigns were postponed with few regions
reporting full recovery. Many LMICs rely on outreach
services to reach vulnerable populations, especially where
access to health clinics or services is limited.9 COVID- 19
response efforts or mitigation strategies, including lock-
downs, resulted in additional disruption to transportation
services, logistical support or supplies, often hindering
additional outreach activities and limiting the services
that were available. This has resulted in a deepening of
existing coverage inequalities, with studies noting greater
disruptions among households with lower incomes,
formal education or those situated in informal housing
or in some regions, rural areas, emphasising the hetero-
geneity that existed prior to the pandemic.91
We used a RR format for this study, which includes some
limitations. We included only two databases for the time
period and only studies in English. As a result, we may
be missing studies stored in other databases or in other
languages. Additionally, RRs may have additional risks of
bias, given the single- reviewer extraction and synthesis of
findings.
The findings in this study are limited by the data avail-
able—the majority of studies used data from 2020, limiting
much of our understanding of how routine immunisation
services have recovered since countries lifted lockdown
or other COVID- 19 response policies. Our study includes
only articles and does not include grey literature. Never-
theless, this study expands on the findings of a systematic
review of available literature on childhood disruptions to
immunisation using data from 2020, which included 39
studies and found an overall median decline of 10.8%.92
Additionally, our study only focuses on LMICs; this is in
contrast to high- income countries, which, according to
one study on 26 middle- income and high- income coun-
tries, saw considerably less missed vaccination.67 Our
study highlights the findings through 2022 and empha-
sises the ongoing heterogeneity in immunisation, along-
side the barriers and enablers to service provision.
Our findings also emphasise the urgency required
to target individuals and cohorts who may have missed
out on routine immunisation or campaigns during the
COVID- 19 pandemic, ensuring the barriers highlighted
by staff and caretakers, including low staff or service
availability, vaccine or supply stock- outs and transporta-
tion barriers are mitigated. Importantly, approaches to
combat fears, misinformation or misbeliefs, including
those surrounding COVID- 19 transmission and risk, are
critical. Though few studies touched on vaccine hesitancy,
declining vaccine acceptance has become a formative
issue, and additional strategies are required to prevent
additional backsliding.5
Rebuilding immunisation services in LMICs will
require a greater focus on healthcare resilience, so that
the disruption caused by future epidemics or disasters
on routine immunisation services is minimal, and that
recovery and performance are rapid and improved
through an adaptation to real- world events.93 Many of
the countries that showed service delivery resilience
during the COVID- 19 pandemic highlighted the need
for proactive and ongoing communication and coor-
dination across multiple interconnected systems, espe-
cially between the community and healthcare system.
One study, published in May of 2023, offers an updated
framework to address the idea of epidemic- ready primary
healthcare. Importantly, this framework offers solutions
to many of the observed barriers found in this review,
focusing on adequate training, compensation and protec-
tion for HCWs, reliable logistic and supply- chain infra-
structure and linkages to the community.94 Given the
reliance on primary healthcare and outreach systems for
immunisation in LMICs, this approach may be a benefi-
cial starting point, though notably, it will require a shift
in how healthcare currently interacts with public health,
alongside strong political commitment and financing.94
Further research will be required to understand how
postpandemic disruption and recovery in immunisation
services has progressed, especially in regards to vulner-
able communities.
CONCLUSION
This review highlights the extent and heterogeneity
of immunisation disruption in LMICs as a result of the
COVID- 19 pandemic and the factors contributing to
disruption and resilience in immunisation programmes.
Given there is limited information on whether reductions
in vaccination coverage or delays have persisted beyond
2021, further research is needed to assess ongoing disrup-
tions, identify missed vaccine cohorts and examine factors
contributing to resilience. Furthermore, these findings
highlight the need for immunisation programmes to
provide support for HCWs and proactive communication
within the health system and with the wider community
to ensure the effect of future disasters on vulnerable
communities is minimal.
Contributors AMH: conceptualisation, methodology, formal analysis, writing—
original draft, writing—review and editing. XL: conceptualisation, methodology,
writing—review and editing. KAMG: guarantor, supervision, conceptualisation,
methodology, formal analysis, writing—original draft, writing—review and editing.
Funding This work was supported, in whole or in part, by the Bill & Melinda
Gates Foundation, via the Vaccine Impact Modelling Consortium [Grant Number
INV- 034281], previously (OPP1157270 / INV- 009125) and Gavi, the Vaccine
Alliance. Under the grant conditions of the Foundation, a Creative Commons
Attribution 4.0 Generic License has already been assigned to the Author Accepted

8HartnerA- M, etal. BMJ Open 2024;14:e076607. doi:10.1136/bmjopen-2023-076607
Open access
Manuscript version that might arise from this submission. AMH, XL, and KAMG also
acknowledge funding from the MRC Centre for Global Infectious Disease Analysis
(reference MR/R015600/1), jointly funded by the UK Medical Research Council
(MRC) and the UK Foreign, Commonwealth Development Ofce (FCDO), under
the MRC/FCDO Concordat agreement and is also part of the EDCTP2 programme
supported by the European Union; and acknowledge funding by Community Jameel.
Competing interests KAMG reports speaker fees from Sano Pasteur outside the
submitted work.AMH and XL declare no competing interests.
Patient and public involvement Patients and/or the public were not involved in
the design, or conduct, or reporting or dissemination plans of this research.
Patient consent for publication Not applicable.
Ethics approval Not applicable.
Provenance and peer review Not commissioned; externally peer reviewed.
Data availability statement All data relevant to the study are included in the
article or uploaded as supplementary information.
Supplemental material This content has been supplied by the author(s). It has
not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been
peer- reviewed. Any opinions or recommendations discussed are solely those
of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and
responsibility arising from any reliance placed on the content. Where the content
includes any translated material, BMJ does not warrant the accuracy and reliability
of the translations (including but not limited to local regulations, clinical guidelines,
terminology, drug names and drug dosages), and is not responsible for any error
and/or omissions arising from translation and adaptation or otherwise.
Open access This is an open access article distributed in accordance with the
Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits
others to copy, redistribute, remix, transform and build upon this work for any
purpose, provided the original work is properly cited, a link to the licence is given,
and indication of whether changes were made. See:https://creativecommons.org/
licenses/by/4.0/.
ORCID iD
Anna- MariaHartner http://orcid.org/0000-0002-8502-9915
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