Assessing the Indirect Effects of COVID-19 on Healthcare Delivery, Utilization, and Health Outcomes: A Scoping Review

Abstract

Background
The COVID-19 pandemic and global efforts to contain its spread, such as stay-at-home orders and transportation shutdowns, have created new barriers to accessing healthcare, resulting in changes in service delivery and utilization globally. The purpose of this study is to provide an overview of the literature published thus far on the indirect health effects of COVID-19 and to explore the data sources and methodologies being used to assess indirect health effects.

Methods
A scoping review of peer-reviewed literature using three search engines was performed.

Results
One hundred and seventy studies were included in the final analysis. Nearly half (46.5%) of included studies focused on cardiovascular health outcomes. The main methodologies used were observational analytic and surveys. Data was drawn from individual health facilities, multicentre networks, regional registries, and national health information systems. Most studies were conducted in high-income countries with only 35.4% of studies representing low- and middle-income countries.

Conclusion
Healthcare utilization for non-COVID-19 conditions has decreased almost universally, across both high- and lower-income countries. The pandemic’s impact on non-COVID-19 health outcomes, particularly for chronic diseases, may take years to fully manifest and should be a topic of ongoing study. Future research should be tied to system improvement and the promotion of health equity, with researchers identifying potentially actionable findings for national, regional, and local health leadership. Public health professionals must also seek to address the disparity in published data from LMICs as compared to high-income countries.

Full text

European Journal of Public Health, 1–7
ßThe Author(s) 2021. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved.
doi:10.1093/eurpub/ckab047
.........................................................................................................
Assessing the indirect effects of COVID-19 on
healthcare delivery, utilization and health outcomes:
a scoping review
Charlotte M. Roy
1,2
, E. Brennan Bollman
1,2
, Laura M. Carson
2
, Alexander J. Northrop
3
,
Elizabeth F. Jackson
2
, Rachel T. Moresky
1,2
1 Department of Emergency Medicine, Columbia University Irving Medical Center, New York, NY, USA
2 Heilbrunn Department of Population and Family Health, Mailman School of Public Health, Columbia University, New
York, NY, USA
3 Vagelos College of Physicians and Surgeons, Columbia University, New York, NY, USA
Correspondence: Charlotte M. Roy, Department of Emergency Medicine, Columbia University Irving Medical Center, 622
W 168th Street, VC-260, New York, NY 10032, USA, Tel: þ1-212-305-8536, e-mail: charlotteroy.md@gmail.com
Background: The COVID-19 pandemic and global efforts to contain its spread, such as stay-at-home orders and
transportation shutdowns, have created new barriers to accessing healthcare, resulting in changes in service
delivery and utilization globally. The purpose of this study is to provide an overview of the literature published
thus far on the indirect health effects of COVID-19 and to explore the data sources and methodologies being used
to assess indirect health effects. Methods: A scoping review of peer-reviewed literature using three search engines
was performed. Results: One hundred and seventy studies were included in the final analysis. Nearly half (46.5%)
of included studies focused on cardiovascular health outcomes. The main methodologies used were observational
analytic and surveys. Data were drawn from individual health facilities, multicentre networks, regional registries,
and national health information systems. Most studies were conducted in high-income countries with only 35.4%
of studies representing low- and middle-income countries (LMICs). Conclusion: Healthcare utilization for
non-COVID-19 conditions has decreased almost universally, across both high- and lower-income countries. The
pandemic’s impact on non-COVID-19 health outcomes, particularly for chronic diseases, may take years to fully
manifest and should be a topic of ongoing study. Future research should be tied to system improvement and the
promotion of health equity, with researchers identifying potentially actionable findings for national, regional and
local health leadership. Public health professionals must also seek to address the disparity in published data from
LMICs as compared with high-income countries.
.........................................................................................................
Introduction
The World Health Organization announced a cluster of cases of
coronavirus-related pneumonia in Wuhan, China on 9 January
2020. Just over 2 months later, on 11 March, COVID-19 was named
a pandemic.
1
Since then, COVID-19, the disease caused by SARS-
CoV-2, has changed the world in innumerable ways. By the end of
March, many countries around the world had closed their borders
and announced national containment measures including stay-at-
home orders, curfews, public transportation closures and movement
restrictions.
2
The implementation of nationwide lockdowns and
travel restrictions undoubtedly prevented many deaths from
COVID-19. However, restrictions also created barriers that pre-
vented people with medical conditions unrelated to COVID-19
from accessing healthcare.
3,4
In addition, warnings about COVID-
19 incited fears among the public who worried that any clinic or
hospital visit could result in them contracting the virus.
One way to capture the number of deaths caused by COVID-19 is
by calculating excess mortality, defined as the number of deaths
from all causes (all-cause mortality) during a crisis minus the
expected number of deaths over a given period based on historical
trends.
5
Excess mortality is useful because it captures deaths due to
COVID-19 that were not officially categorized as COVID-19-related
(e.g. deaths from COVID-19 that occurred at home or prior to
receiving a diagnostic test). However, a substantial proportion of
these excess deaths are likely due to medical conditions unrelated to
COVID-19 that went undiagnosed or untreated during the pandem-
ic. These are known as indirect deaths. Changes in health service
delivery or utilization and in non-COVID-19 health outcomes can
be termed ‘indirect health effects’ of the pandemic. Figure 1 illus-
trates how health service availability (services offered), utilization
and delivery contribute to indirect effects, including excess mortal-
ity. Health service utilization is moderated by economic, geographic,
immigration status, gender, racial, ethnic and cultural barriers that
affect patients’ access to and interaction with the health system.
Epidemics and pandemics of this magnitude have been shown to
have widespread effects on health systems.
6
Indirect effects lead not
just to deaths but to a wide range of morbidity resulting from the
lack of preventative care, delays in diagnosis of new diseases and
disruptions to treatment of chronic conditions. The impact can be
particularly damaging to already fragile health systems in low- and
middle-income countries (LMICs). For example, it has been esti-
mated that the 2014–15 Ebola epidemic in West Africa caused a 50%
reduction in access to healthcare services including vaccinations and
maternal and child health visits.
7
The epidemic shocked the health-
care system in Guinea so profoundly that these indicators still had
not returned to pre-epidemic levels as of February 2017, nor were
they on a path that suggested this would happen soon thereafter.
8
These findings demonstrate widespread epidemics’ potential to pro-
duce indirect effects with both short- and long-term consequences
for health outcomes.
The purpose of this article is to provide a scoping review of the
literature on the indirect health effects of the COVID-19 pandemic
published thus far. We explore the current data on how COVID-19
has impacted health service delivery and utilization globally, affect-
ing multiple health outcomes. We also appraise the data sources and
methodological approaches used to measure the indirect health
effects of the COVID-19 pandemic, as well as the geographic

distribution of published studies. To our knowledge, this is the first
literature review of the indirect health effects of COVID-19 globally
and across multiple fields of health.
Methods
Given the evolving nature of this pandemic, we decided to pursue a
scoping review rather than a systematic review as our methodology
of research. We adapted the scoping review framework proposed by
Arksey and O’Malley.
9
Research question
This study used a two-part guiding research question: (i) What data
sources, study designs and methods have been used to investigate
the indirect effects of the COVID-19 pandemic on health service
delivery and utilization across various health domains and (ii)
What are the advantages and disadvantages of different methods
of evaluating the indirect health effects of the pandemic? For the
purposes of this study, we defined indirect health effects as identified
changes in the accessibility, delivery, utilization, or outcomes asso-
ciated with healthcare services.
Identification of relevant studies
We conducted an initial literature search over a period of 3 days
from 22 to 24 June 2020 using two electronic databases: Medline/
PubMed and Google Scholar. These databases were selected to iden-
tify articles on a wide range of indirect health effects, focusing on
biomedical literature. Search terms were developed to identify in-
direct effects across a range of health domains (Supplementary ap-
pendix SA1). Our initial search yielded 6119 results. After this initial
review of the literature, the search terms were refined, and we con-
ducted a second review in Medline/PubMed, Google Scholar and the
Scopus database from 10–19 August. This final iteration of search
terms yielded a total of 14 807 articles. A PRISMA flow diagram
depicting this process is shown (figure 2).
Selection process
A preliminary search was conducted prior to initiating the scoping
review to determine the inclusion criteria and establish consistency
between the two reviewers (A.N. and L.C.). Next, two reviewers
completed first and second pass searches of the databases, screening
first by title and abstract. Articles meeting inclusion criteria were
then screened for appropriateness by a second reviewer (C.R. and
B.B.). Reviewers subsequently read the full text of the included
articles, briefly summarized key findings, and categorized the studies
by methodology and data source (A.N., L.C., C.R. and B.B.). Pre-
print articles were excluded. Citations were managed via the Zotero
citation management software.
Inclusion criteria
We included peer-reviewed studies that fell within the following
health categories: cancer, cardiovascular health (including cardiac
disease, stroke and peripheral vascular disease), diabetes, commu-
nicable diseases, maternal health, sexual and reproductive health,
surgical emergencies and child health. Our goal was to determine
what data exist at this point regarding the impact of the pandemic
on healthcare utilization and, where available, health outcomes,
therefore we only included studies with quantitative findings. We
excluded modelling studies that were purely predictive, as well as
studies that attempted to apply findings from data collected prior to
the pandemic to the current context. Furthermore, we excluded
clinical guidelines and commentaries if they did not include primary
data.
We excluded studies on the indirect effects of COVID-19 on the
psychological, social, economic, and environmental dimensions of
health. Although these determinants of health are crucial categories
of indirect effects, the breadth and complex nature of research in
these areas deserves its own review. The relationship between indir-
ect health effects and socioeconomic inequity was not an explicit
focus of this review; nonetheless, it is a critical area of investigation.
As appropriate, we highlight instances of inequity from the included
studies.
Figure 1 Schematic of the impact of COVID-19 on health systems and how this contributes to indirect effects and excess mortality
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Results
A total of 170 articles were included in the final scoping review. A
complete list of included studies is available in Supplementary ap-
pendix SA2. Through our review of the literature, we identified two
dominant methodologies for assessing indirect health effects: obser-
vational analytic (retrospective comparisons of data from the
COVID-19 lockdown period with data from previous months or
years) and observational descriptive (surveys or cross-sectional stud-
ies with no comparison). Studies were categorized as comparing the
COVID-19 time period with the same weeks or months in previous
years (labelled as ‘year-to-year’ comparisons), comparing the
COVID-19 time period with earlier weeks or months within 2020
(‘pre/post’ comparisons), cross-sectional surveys, or other. Studies
categorized as ‘other’ either presented findings with no prior data
for comparison or the methodology was not clear.
The majority (n¼99, 58.2%) of studies reviewed used the year-
to-year methodology, while fewer studies used pre/post (n¼33,
19.4%), survey (n¼31, 18.2%) or other (n¼7, 4.1%) study designs.
The most commonly used data source was medical records from a
single facility (n¼79, 46.5%). Other data sources included national-
level health information systems and registries (n¼23, 13.5%), re-
gional registries or multicentre data (n¼38, 22.4%) and surveys
(n¼30, 17.6%). Papers included in the scoping review are catego-
rized in figure 3 by health category, methodology and data source.
The preponderance of studies published on the indirect health
effects of COVID-19 fell into the cardiovascular category (n¼79,
46.5%). The categories with the fewest articles included in this re-
view were maternal health (n¼6, 3.5%) and diabetes (n¼7, 4.1%).
This is possibly because data on cardiovascular diseases such as
stroke and MI are widely tracked and have meaningful short-term
outcomes. In contrast, it will take years to fully evaluate the impact
of the COVID-19 pandemic on outcomes related to cancer or pre-
ventative measures such as immunization. Additionally, many high-
income countries (HICs) have well-established referral networks for
cardiovascular conditions, as well as disease-specific registries to
track this type of data. Findings from a selection of studies included
in this review are described in Supplementary appendix SA3.
Key substantive findings
During the COVID-19 pandemic, healthcare utilization for non-
COVID-19 conditions has decreased almost universally. Nearly, all
studies reviewed demonstrated this reduction in utilization across
both high- and lower-income countries, and irrespective of the de-
gree of COVID-19 outbreak within that country or region.
Remarkably, these decreases occurred not only for routine services,
such as child health visits or immunizations, but also for emergency
conditions, such as myocardial infarction (MI) and stroke, as well as
chronic, urgent conditions, such as cancer. Studies assessing health
service utilization, or the number of patients who presented to a
facility for a given condition, represented the majority of the
included publications; a minority of reviewed studies (24.1%) meas-
ured health outcomes. At times, particularly via survey approaches,
a subjective decrease in service availability or accessibility was dis-
cussed, typically by either healthcare providers or service users.
10–15
However, these patterns in service delivery were generally not rigor-
ously quantified.
The causes of decreased healthcare utilization during the COVID-19
pandemic remain unclear. For instance, it is unknown whether the
finding of fewer hospital presentations for myocardial infarction or
stroke was due to decreased disease incidence, decreased healthcare-
seeking behaviour or other causes. One hypothesis is that lower
Figure 2 PRISMA flow diagram
Assessing the indirect effects of COVID-19 3of7

healthcare utilization reflects an increased number of people dying at
home from untreated, non-COVID-19 diseases. For example, a study
in the USA suggested that excess mortality in Boston, Massachusetts
could be related to the decrease in hospitalizations for acute cardio-
vascular conditions if more people are dying at home rather than
seeking care.
16
Other potential explanations mentioned by authors
included reduced health facility hours due to national lockdowns
and curfews, reduced human resource availability within healthcare
facilities, and hesitancy to seek care due to fears of contracting the
virus. Decreased service utilization may also reflect the increasing use
of telemedicine, a form of service delivery which may not have been
captured by data collection. Alternately, it is possible that shifting en-
vironmental and social factors could have contributed to decreased
rates of certain diseases.
Despite the global nature of the COVID-19 pandemic, the ma-
jority of studies in our review assessed indirect health effects in HICs
in North America and Europe. Of the articles reviewed, only one-
third (35.4%) included data from an LMIC as classified by the
World Bank. Although countries were in varying stages of the pan-
demic during the time period covered by this review, most countries
initiated some form of lockdown in March 2020.
17
Therefore, one
would expect the impacts of the pandemic to be seen across national
contexts, though perhaps to a greater degree in countries with more
local transmission. Furthermore, many LMICs that COVID-19 has
severely impacted have so far not been the focus of much research
on the pandemic’s indirect effects, in particular India and countries
in Latin America and Africa. These differences may be explained, in
part, due to inequity in data availability and research funding in
LMICs as compared with HICs. Figure 4 depicts the distribution of
articles on indirect health effects by country as compared with the
global distribution of COVID-19 cases. The process used to create
this figure is described in Supplementary appendix SA4.
Methodological approaches
Many of the studies identified in our review employed an observa-
tional analytic approach via a retrospective cohort design, with the
same months in either prior years (‘year-to-year’) or pre-COVID-19
lockdown months within 2020 (‘pre/post’) as the comparison time
period. These approaches each have strengths and weaknesses.
Studies that compared the pre- and post-COVID-19 period within
2020 (usually defined as before and after lockdown) neglect seasonal
variations that could influence healthcare service patterns or health-
seeking behaviours. However, this method minimizes temporal dif-
ferences that could alter healthcare service trends over multiple
years. Conversely, year-to-year comparisons may be affected by tem-
poral differences, including long-term changes in hospital resources
or capabilities, but control for seasonal effects. Finally, studies that
use an observational descriptive design, such as cross-sectional sur-
veys, as their primary methodology are efficient due to their rapid
creation and ease of data collection but are subject to recall bias or
Figure 3 Articles reviewed by (a) health category and methodology and (b) health category and data source
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respondent error. For example, clinician reports about changes in
health services after the onset of the pandemic may be influenced by
personal perceptions. Surveys also focused on subjective health ser-
vice accessibility and availability, rather than objective measures of
utilization or health outcomes.
Data sources
The reviewed studies used a wide range of data sources, including
national demographic surveillance information, regional disease-
specific registries, facility-level data and surveys. Assessing indirect
effects at these multiple levels of health systems helps garner the
most comprehensive and accurate depiction of the pandemic’s
impacts. For example, data analyses of single hospital or clinic
records provide a snapshot of the impact of COVID-19 on a par-
ticular location, whereas national hospital databases can corroborate
if those findings represent changes in healthcare service delivery and
utilization more broadly. Several studies included in this review
drew data from disease-specific registries for stroke and cardiac ar-
rest. Such registries act as an intermediate source between individual
facilities and national-level data that aggregate data across multiple
facilities.
18–22
Finally, LMICs often have a national health information system to
which facilities regularly push data on numerous health indicators,
from the subdistrict to national level.
23
However, depending on
available resources, data quality and completeness may be compro-
mised. In addition, there may be discrepancies between rural and
urban areas in the quality and quantity of available data. Universal
healthcare systems with comprehensive electronic databases can
allow for simplified collection of data across hospitals, clinics and
other lower level facilities. Such systems may enable conclusions
about the indirect effects of COVID-19 to be drawn on a population
level.
Discussion
Continued study of the indirect health effects of the COVID-19
pandemic will be critical to understanding its impact on long-
term health outcomes and to mitigating the effects of the pandemic
moving forward. As previously noted, most studies in this review
demonstrated a decrease in healthcare service utilization across mul-
tiple health conditions globally without delineating possible reasons
for this decline. Future studies should consider examining why these
indirect effects occurred and propose solutions to improve equitable
healthcare access, delivery, and outcomes moving forward. Some of
this work has been done with surveys of health workers and patients
to understand their perceptions of reduced medication access,
delayed diagnostics, transportation barriers and other issues; such
methods have been used particularly for HIV, sexual and reproduct-
ive health, and cancer care.
11–13,24,25
However, research on the in-
direct effects of COVID-19 has not yet rigorously measured changes
in workforce, supplies, demand, access, and quality to understand
how and why the pandemic has so drastically impacted health
systems.
In addition, much of the research on the indirect effects of
COVID-19 presented here focuses on individual facilities or regional
hospital networks or registries. Collecting data at higher levels of the
health system, such as national health information systems, can
demonstrate more robust and generalizable findings if similar effects
are seen across multiple geographic regions. Such cross-cutting
trends were seen in the US Center for Disease Control and
Prevention‘s analysis of the National Syndromic Surveillance
Program, which captured data from a nationally representative sam-
ple of emergency departments and showed a decline in emergency
department visits across all geographic regions.
26,27
Excess all-cause mortality figures that are disproportionate to the
number of documented COVID-19 deaths suggest that indirect health
effects have led to increased mortality. However, there is currently a
Figure 4 Map of the global distribution of (a) indirect effects articles and (b) cumulative incidence of COVID-19
Assessing the indirect effects of COVID-19 5of7

paucity of published data on health outcomes for specific diseases,
with most studies focusing on healthcare delivery and utilization.
28,29
Some fields have shown early outcome findings: for instance, a study
aggregating data from nine hospitals in Nepal found a rise in institu-
tional stillbirth rate and neonatal mortality.
30
In addition, a number
of studies on cardiovascular and surgical emergencies measured in-
hospital mortality and other complications.
31–33
In contrast, data in
the peer-reviewed literature on outcomes related to HIV, tuberculosis,
cancer, and child health (vis-a-vis immunization, nutrition and other
long-term care) remain limited. The pandemic‘s impacts on chronic
conditions and preventative services may take years to demonstrate, as
was seen in Guinea after the 2014–15 Ebola epidemic.
8
Future re-
search should focus on measuring patient-centred outcomes, such
as clinically significant morbidity and mortality, rather than primarily
system metrics like utilization.
As this review demonstrates, there has thus far been a relative pau-
city of published research on the indirect health effects of COVID-19
in LMICs. This may be attributable to a number of factors, including
resource limitations which interfere with data collection, analysis and
publication. In addition, countries were in varying phases of the pan-
demic in the time period covered by this review, which may have
contributed to the disparity in publications, although several studies
demonstrated decreased healthcare service utilization even when
COVID-19 transmission was low. For example, a study in Uganda
demonstrated a 29% decrease in facility deliveries and an 82% in-
crease in maternal mortality in March 2020 compared with January
2020, even though there had been fewer than 50 confirmed cases in
the country at that time.
2,34
This suggests that lockdown restrictions
and fear generated by the pandemic may have caused decreased ser-
vice utilization, regardless of the degree of local transmission. Where
available, we recommend addressing the data disparity between HICs
and LMICs by using existing national health information systems,
such as the open sourced web-based health information system soft-
ware DHIS2, currently in use by ministries of health in 72 LMICs, 58
of these at a national scale.
35
Additionally, these existing data sources
often include maternal, neonatal, and child health information, which
was relatively under-represented in this review.
In addition to variability in access to high-quality data globally,
COVID-19 has also demonstrated inequities in health outcomes
along racial, ethnic and socioeconomic lines. A number of papers
have shown an increased burden of COVID-19 cases and mortality
in racial and ethnic minorities.
36
It is likely that populations with
low socioeconomic status and poor access to healthcare at baseline
will also be disproportionately impacted by the indirect health
effects of COVID-19. Although our search strategy was not specif-
ically designed to capture studies about differences in indirect health
effects along racial, ethnic, or socioeconomic lines, very few of the
papers included in this review made any note of such inequities.
Understanding and addressing the indirect health effects of COVID-
19 experienced by vulnerable groups and the social determinants
that drive such disparities is essential for further research.
This study has several limitations. First, research on COVID-19
has been generated with unprecedented speed and volume. This
scoping review is not intended to be comprehensive and may have
missed studies of indirect health effects not identified by our search
strategy or not falling within the health categories established.
Future studies may systematically review issues raised in this article.
Additionally, this study reviewed only English-language publica-
tions, which may have skewed our findings towards papers from
HICs. As the study of the COVID-19 pandemic’s indirect effects is
new and evolving, methodological approaches were not previously
standardized; therefore, we categorized approaches as seemed most
logical, and future reviews may build on this to identify a new ‘gold
standard’. Finally, some data on the indirect health effects of
COVID-19 in LMICs may currently exist primarily in ‘grey litera-
ture’, such as non-governmental organization or government
reports, and therefore may have been missed in this review.
We recommend that future work should examine COVID-19‘s in-
direct effects longitudinally, particularly as the pandemic’s economic
reverberations affect health-seeking behaviour and healthcare service
delivery over the coming months and years. Importantly, future research
should be tied to system improvement, with researchers identifying
potentially actionable findings for national, regional and local health
leadership. For example, key indicators, or composite indicators, of
disruptions in health service delivery and outcomes could trigger a
multilevel health system response to examine the contextual factors
causing this disruption and create targeted interventions. Such ongoing
research may also help health systems improve resilience for future
epidemics or disasters. Likely, the devastating effect of COVID-19 on
livelihoods and economies will impact health outcomes for years to
come, with disproportionate effects on LMICs and marginalized groups.
Public health professionals must continue to identify these problems,
implement adaptations when possible, and advocate for durable, equit-
ablesolutionsonbehalfofthosemostimpactedbythepandemic.
Supplementary data
Supplementary data are available at EURPUB online.
Conflicts of interest: None declared.
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