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Ghazzawi et al 2023
1
RESEARCH
Impact of COVID-19 on Hepatitis B Screening in Sierra Leone: Insights from a
Community Pharmacy Model of Care
Manal GHAZZAWI 1, Lawrence S. BABAWO 2, Amir M. MOHAREB 3,4,5, Peter B.
JAMES 6, Sahr A. YENDEWA 7, Samuel P.E. MASSAQUOI 7, Peterlyn E.
CUMMINGS 7, Sulaiman LAKOH 7,8,9, Robert A. SALATA 10,11,
George A. YENDEWA 10,11,12 *
1 KnowHep Foundation, Freetown, Sierra Leone
2 Department of Nursing, School of Community Health Sciences, Njala University, Bo
Campus, Sierra Leone
3 Center for Global Health, Massachusetts General Hospital. Boston, Massachusetts,
USA
4 Division of Infectious Diseases, Massachusetts General Hospital, Boston,
Massachusetts, USA
5 Department of Medicine, Harvard Medical School, Boston, Massachusetts, USA
6 Faculty of Health, Southern Cross University, Lismore, Australia
7 Ministry of Health and Sanitation, Freetown, Sierra Leone
8 College of Medicine and Allied Health Sciences, University of Sierra Leone, Freetown,
Sierra Leone
9 Connaught Hospital, University of Sierra Leone Teaching Hospitals Complex, Ministry
of Health and Sanitation, Freetown, Sierra Leone
10 Department of Medicine, Case Western Reserve University School of Medicine,
Cleveland, Ohio, USA
11 Division of Infectious Diseases and HIV Medicine, University Hospitals Cleveland
Medical Center, Cleveland, Ohio, USA
12 Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
Key words: Hepatitis B virus, Screening, Diagnosis, COVID-19, Sierra Leone
Tables: 1
Figures: 4
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice.
Ghazzawi et al 2023
2
* Corresponding author:
George A. Yendewa, MD, MPH&TM, FACP, FIDSA
Assistant Professor of Medicine (Infectious Diseases)
Case Reserve Western University School of Medicine
Division of Infectious Diseases and HIV Medicine
University Hospitals Cleveland Medical Center
11100 Euclid Ave, Cleveland, OH 44106, USA
Telephone: +1 216-844-1988
Fax: +1 216-844-1632
E-mail: gay7@case.edu
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Ghazzawi et al 2023
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ABSTRACT
Background: There are limited studies evaluating the impact of COVID-19-related
interruptions on hepatitis B virus (HBV) screening in endemic countries in Sub-Saharan
Africa.
Methods: We conducted a retrospective study of HBV testing in a community pharmacy
in Freetown, Sierra Leone, from October 1, 2019, through September 30, 2022. We
compared participant characteristics using Pearson's chi-square test. We evaluated
trends in HBV screening and diagnosis using one-way ANOVA with Tukey’s or Dunnett's
post-test.
Findings: Of 920 individuals screened, 161 had detectable HBsAg (seroprevalence
17.5% [95% CI 14.9-20.4]). There was a 100% decrease in HBV screening during
January-June of 2020; however, screening increased by 27% and 23% in the first and
second year after COVID-19, respectively. Mean quarterly tests showed a significant
upward trend: 55 ± 6 tests during January-March (baseline), 74 ± 16 tests during April-
June, 101 ± 3 tests during July-September, and 107 ± 17 tests during October-December
(one-way ANOVA test for trend, F=7.7, p = 0.0254) but not the mean quarterly number of
people diagnosed with HBV (F = 0.34, p = 0.7992).
Interpretation: Community-based HBV screening dramatically improved following
temporary disruptions related to COVID-19. Seasonal variation in HBV screening, but not
HBV diagnosis, may have implications for HBV elimination efforts in Sierra Leone and
other West African countries.
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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INTRODUCTION
Hepatitis B infection (HBV) affects 296 million people globally, with Sub-Saharan
Africa (SSA) accounting for 25% of chronic cases, i.e., 80 million people [1]. Without
timely diagnosis and treatment, there is an increased risk of developing cirrhosis,
hepatocellular carcinoma, and end-stage liver disease, which collectively caused 820,000
deaths in 2019 [1]. The World Health Organization (WHO) has set a goal of eliminating
HBV globally by 2030 through a 90% reduction in incidence and a 65% decrease in
mortality [2].
Despite the high global burden of HBV, progress towards the elimination goals is
threatened by limited access to HBV screening [2, 3]. Awareness of HBV status is the
first critical step in navigating the HBV cascade of care and facilitates linkage to essential
healthcare services. However, in 2021, only 10% of people with chronic HBV (PWHB)
globally were aware of their status, with an even lower proportion of just 2% in the WHO
African region [4]. Furthermore, many SSA countries lack adequate resources and
infrastructure for delivering affordable HBV services [4, 5], and existing pathways for
accessing these services are largely reliant on hospital- or clinic-based HIV facilities [5-
7]. Additionally, the coronavirus-19 (COVID-19) pandemic has had a notable impact on
healthcare delivery globally and further complicated efforts to eliminate HBV, due to
prioritization of the COVID-19 pandemic response [8-11].
To address the gap in affordable and accessible HBV screening, alternative
models of care delivery such as community pharmacies have emerged in both high- and
low-income countries [12-14]. This has been facilitated by the widespread availability of
point-of-care (POC) tests. Commercially available POC tests for HBV have excellent
diagnostic performance and offer an alternative to laboratory-based testing [15, 16]. The
advantages of POC tests include low cost, ease of use requiring minimal training, quick
results turnaround, and scalability, which increases their accessibility to hard-to-reach
populations [15]. Moreover, there is evidence that nontraditional settings such as
pharmacies, drug and harm reduction services, mobile health units, and community-
based organizations are preferred for HIV, viral hepatitis, and sexually transmitted
infections services by marginalized or stigmatized groups [17, 18], presenting an
opportunity to target populations most in need of care and accelerate HBV elimination
efforts.
Sierra Leone is a West African country with an estimated national prevalence of
HBV surface antigen (HBsAg) of 13% [19]. While there have been notable strides to
implement a national policy for combating HBV, the delivery of HBV care remains
fragmented. There are few viral hepatitis specialty clinics in Sierra Leone, and HBV care
delivery is primarily through hospital-based HIV services [7]. Like elsewhere, the COVID-
19 pandemic has hindered healthcare delivery in the country [20-22], however, its impact
on HBV care has not been evaluated.
The objectives of our study were to: (1) evaluate the impact of COVID-19 on the
utilization of HBV screening services in Sierra Leone and (2) assess trends in HBV
screening and diagnosis using a community-based pharmacy model of care.
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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METHODS
Study setting and context
KnowHep Foundation Sierra Leone is a local non-governmental organization
committed to raising public awareness about viral hepatitis through mass education and
advocacy within communities across Sierra Leone. Established in 2019, the main
objective of the foundation is to improve viral hepatitis care delivery by reaching a
minimum of 80% of the population of Sierra Leone by 2030, through community outreach
initiatives that support the global viral hepatitis elimination agenda. KnowHep Foundation
is affiliated with CitiGlobe Pharmacies Ltd, a network of community-based pharmacies
that provide free or low-cost HBV screening, linkage to care for individuals who test
positive for HBV, and HBV vaccination services.
Study design and key time points
We conducted a retrospective review of pharmacy HBV testing records at
CitiGlobe Pharmacy Ltd in Freetown, Sierra Leone, from October 1, 2019, when
meticulous documenting of all HBV tests performed was commenced, through September
30, 2022. The first confirmed cases of COVID-19 in Sierra Leone were reported in late
March 2020, however, the COVID-19 pandemic had already spread in China, Europe,
and elsewhere since December 2019. This resulted in major disruptions in global supply
chains for medications, testing kits, and other healthcare essentials. Additionally, there
were growing concerns about COVID-19 locally in Sierra Leone, which led to fewer
pharmacy visits by the public. As a result of this, pharmacy services were suspended in
the first quarter of 2020. With the identification of the first COVID-19 cases in Sierra Leone
in March 2020, the Government of Sierra Leone declared a state of emergency, and a
series of population-wide shelter-in-place orders were imposed in the country from April
through June 2020. The suspension of pharmacy services continued throughout this
period. The shelter-in-place orders were lifted at the end of June 2020, which allowed the
resumption of pharmacy services in July 2020.
We divided the study period into the following testing periods: (1) Year 1: October
2019-September 2020; (2) Year 2: October 2020-September 2021; and (3) Year 3:
October 2021-September 2022. We designated Year 1 as the baseline year for HBV
testing and compared it with Years 2 and 3. To assess seasonal trends in HBV screening,
we further divided each year into quarters (i.e., three-month periods).
Data collection and definitions
We used a structured data collection instrument to extract the following data from
screening records: evidence of chronic HBV infection, defined as HBsAg detection, date
of screening, sex, age, highest education attained, and testing episode, i.e., first-time
screening or repeat testing for clinical monitoring of previously diagnosed infection. All
personal identifiers (i.e., name, date of birth, and address) were removed before entering
the data into a password-protected spreadsheet for analysis.
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Ghazzawi et al 2023
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Statistical analysis
We report descriptive statistics as frequencies with percentages, means with
standard deviation, or medians with range. We calculated associations between variables
using Pearson's chi-square test by SPSS Version 29.0 (Armonk, NY; IBM Corp). We
estimated the mean quarterly number of HBV tests as the average of the tests performed
during corresponding quarters in each of Years 1, 2, and 3, respectively. We assessed
seasonal trends in quarterly HBV screening and diagnosis using one-way ANOVA with
Tukey’s or Dunnett's post-test by GraphPad Prism Version 9.5.1 (San Diego, California,
USA). In all analyses, results were considered statistically significant when p < 0.05.
Ethical consideration
We obtained ethical approval to perform the study from Njala University, Bo
Campus, Sierra Leone (approval date 23 January 2023). Informed consent was not
required as this study involved a retrospective analysis of secondary data.
RESULTS
Characteristics of the study participants
A total of 1145 unique individuals underwent HBV screening at the pharmacy from
October 2019 through September 2022. Of these, 920 individuals underwent HBV
screening for the first time, while 225 individuals had repeat HBV testing for clinical
monitoring of previously diagnosed HBV infection. Table 1 presents baseline
sociodemographic characteristics of the population of interest, i.e., first-time testers only.
This consisted of roughly equal proportions of males (51.7%, 476/920) and females
(48.3%, 444/920). The median age was 32 (IQR 27-38) years and the majority were aged
30-39 years. We found that 52.4% (482 of 920) had attained the tertiary level of education.
Seroprevalence of HBsAg
As shown in Table 1, the overall seroprevalence of HBsAg was 17.5% (95% CI
14.9-20.4). When disaggregated by sociodemographic categories, individuals aged 30-
39 years had significantly higher HBsAg seropositivity compared with individuals of other
age groups, i.e., 24.4% (95% 18.9-29.2); p = 0.004. The HBsAg seroprevalence did not
vary based on sex, educational attainment, or year of testing.
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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Impact of COVID-19 on HBV Screening
Overall, 263 individuals were screened for HBV during Year 1, compared with 333
individuals during Year 2 (i.e., a 27% increase from Year 1) and 324 individuals during
Year 3 (i.e., a 23% increase from Year 1). Figure 1 presents the quarterly number of HBV
tests performed, while Figure 2 presents the percentage change in quarterly screenings
compared with the pre-COVID-19 pandemic baseline, i.e., October-December 2019. A
total of 122 HBV tests were performed during the baseline period. Due to the COVID-19-
related suspension of pharmacy services, no HBV screening was offered during January-
June 2020, representing a 100% decrease from the pre-COVID-19 baseline (Figure 2).
Following the lifting of the restrictions, 141 HBV tests were performed during the third
quarter of 2020, representing a 16% increase compared to the pre-COVID-19 baseline.
However, this increase in HBV testing was not sustained over subsequent quarters in
Years 1, 2, or 3 (Figure 2).
Seasonal Trends in HBV Screening and Diagnosis
Figure 3 presents the mean number of HBV tests performed per quarter over Years
1, 2, and 3, after excluding the first, second, and third quarters of 2020 from the analysis
to account for the disruptions in testing patterns due to the COVID-19 pandemic. On
average, 55 ± 6 HBV tests were performed during January-March (baseline), 74 ± 16
tests during April-June, 101 ± 3 tests during July-September, and 107 ± 17 tests during
October-December. One-way ANOVA showed that there was no statistically significant
difference in the number of HBV tests performed between January-March and April-June
(p = 0.4237); however, there were significantly more tests performed during July-
September (p = 0.0380) and October-December (p = 0.0192), respectively, compared
with the January-March baseline. Test of trends between quarterly means by one-way
ANOVA confirmed that HBV testing exhibited a linear seasonal trend, with the lowest
number of tests performed in the first half of the year, which increased significantly
throughout the remainder of the year (F = 7.7, p = 0.0254).
As shown in Figure 4, the mean number of diagnosed cases, i.e., HBsAg positive
tests per quarter, were 11 ± 2 during January-March, 14 ± 5 during April-June, 12 ± 4
during July-September, and 16 ± 2 during October-December. There was no significant
difference in the mean quarterly number of people diagnosed with HBV, i.e., HbsAg
seropositive tests (p > 0.05 for all quarters). Test for trend by one-way ANOVA did not
show a trend in the mean quarterly number of diagnosed cases (F = 0.34, p = 0.7992).
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Ghazzawi et al 2023
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DISCUSSION
In this study of community-based HBV screening in a pharmacy in Freetown,
Sierra Leone, we demonstrate trends in HBV screening and diagnosis. A total of 920
individuals underwent first-time screening for HBV at our pharmacy over the three-year
study period, of whom 17.5% tested positive for HBsAg. The first year of testing coincided
with the onset of the COVID-19 pandemic, which saw major disruptions in service
delivery. As a result, there was a 100% decrease in HBV testing in the first and second
quarters of 2020 compared with the pre-COVID-19 baseline period. This was due to the
fact that in the first quarter of 2020, pharmacy visits decreased considerably partly due to
well-known seasonal variations associated with the Christmas and New Year festivities
in this setting, as well as growing public concerns about the COVID-19 pandemic which
had already spread in China, Europe and elsewhere since December 2019. Due to these
challenges, pharmacy services were suspended in the first quarter of 2020 and remained
so during the population-wide lockdowns implemented in Sierra Leone in the second
quarter of 2020.
Our observations are consistent with research from both high- and low-income
settings, which have reported significant disruptions in HBV service delivery resulting from
the COVID-19 pandemic measures. In a major study sponsored by the European
Association for the Study of the Liver, Kondili et al [10] reported a 35% reduction in HBV
testing between January 2019 and December 2020 in 32 European and 12 non-European
clinical centers. The impact of the COVID-19 pandemic was also observed across
multiple levels of the HBV cascade of care, with a 30% reduction in consultations, a 39%
decrease in referrals, a 29% decline in HBV viral load testing, and a 35% drop in treatment
initiation [10]. Countries in sub-Saharan Africa have faced similar challenges in HBV care
delivery. Lemoine et al [11] reported that between January and April 2020, the monthly
number of visits at hepatitis clinics for new cases declined significantly by 71% in Burkina
Faso, 95% in Tanzania, and 83% in The Gambia, and for patients in follow-up, the
numbers fell by 73%, 77%, and 89% in Burkina Faso, Tanzania, and The Gambia,
respectively. In comparison, the utilization of outpatient services declined by 18% during
the West African Ebola epidemic of 2014 [23], indicating the severity of the impact of
infectious disease outbreaks on routine healthcare delivery.
Despite the pandemic-related disruptions in 2020, we observed an overall 27%
and 23% increase in HBV screening in our pharmacy in the second and third testing
years, respectively, reflecting the healthcare system's ability to address short-term
increases in demand for services. However, it is uncertain whether this trend will continue
in the future. Achieving HBV elimination targets requires a sustained increase in HBV
screening, treatment and prevention, and the healthcare system's resilience in the face
of new public health challenges such as emerging infections is a key factor in achieving
this goal [2]. This will necessitate continuous and sustained investments in capacity-
building of both conventional and complementary healthcare systems such as community
pharmacies to enhance their ability to adapt and respond effectively to the inevitable
increases in demand for HBV services as countries work toward meeting the elimination
targets for 2030.
Another notable finding of our study was that demand for HBV screening was
lowest during the first quarter of each year, increasing linearly during subsequent
quarters, and peaking in the last months of the year. This suggests the presence of
seasonality and temporal patterns that could be further explored to optimize screening
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Ghazzawi et al 2023
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strategies and resource allocation for HBV care delivery in Sierra Leone. Studies from
some settings have reported seasonality in viral hepatitis diagnosis while others have not.
For example, in a study from the United Kingdom, Stewart et al [25] found a higher rate
of HBV testing and diagnosis in the summer months, while Huang et al [26] reported
higher rates of HBV diagnosis during spring and summer in China. Similarly, hepatitis C
virus (HCV) diagnosis has been associated with the summer months in Mexico [27], Egypt
[28], and China [26].
The reasons for seasonality in HBV and HCV diagnosis are not fully understood,
however, since both are blood-borne pathogens, it has been suggested that seasonal
variations in infections may be influenced by behavioral and climatic factors such as
increased sexual activity, injection drug use, tattooing and travel to endemic areas during
the summer months [25-29]. In areas with high HBV endemicity such as Sierra Leone,
seasonal variations in HBV testing and diagnosis may be influenced by an entirely
different set of factors such as cultural practices, differences in access to healthcare,
healthcare policy and awareness campaigns. Low healthcare attendance in the first
quarter may be attributable to the Christmas and New Year festivities in Sierra Leone. Of
note, the KnowHep Foundation is heavily involved in awareness raising and outreach
during the annual World Hepatitis Day in July, which could explain the increase in the
utilization of our services observed in the third and fourth quarters. If this is the case, it
would suggest that community-based advocacy and public awareness campaigns may
successfully improve the frequency of screening in HBV-endemic areas in West Africa.
The overall prevalence of HBsAg was 17.5%, with the highest prevalence (24.4%)
observed among individuals aged 30-39 years. This is in contrast to a recent systematic
review and meta-analysis by Yendewa et al [19], which estimated a national HBsAg
prevalence of 13.0% for Sierra Leone and a regional prevalence of 11.2% for the Western
Area, where the present study was conducted. There are several possible explanations
for this observed difference. Firstly, our pharmacy receives referrals from healthcare
providers for clients with clinical suspicion of liver disease, many of whom are likely to
have HBV infection. Secondly, our outreach and educational activities have attracted a
substantial number of at-risk clients to our free or low-cost services, including those with
family members or sexual partners with known HBV infection, those engaging in
unprotected sexual activity, intravenous drug users, or those sharing personal hygiene
items such as razors or toothbrushes. These groups have a higher pre-test probability of
testing positive for HBV infection, which may partly explain the higher prevalence of
HBsAg seropositivity observed in our study. Our findings are consistent with other studies
that have also reported higher HBsAg seropositivity rates in healthcare settings, including
hepatology clinics, sexually transmitted infection clinics, and hemodialysis centers [30].
These results must be interpreted within the limitations of study design. Firstly, due
to a lack of record keeping, the pre-pandemic period was limited to one quarter, which
may not accurately represent the baseline HBV testing trends. Secondly, the period over
which trends were assessed is relatively short, further research is needed to confirm our
conclusions over a more extended period. Thirdly, the study findings may not be
generalizable to other HBV-endemic regions in Africa, given that the study was conducted
in a single pharmacy in Freetown. Nonetheless, the study's strengths lie in its contribution
to the limited research on the impact of COVID-19 on HBV care delivery in SSA and its
implications for the viral hepatitis elimination goals. Furthermore, our study showcases
the critical, yet underappreciated role community pharmacies serve in resource-limited
settings as primary access points for delivering HBV services to communities in need.
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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CONCLUSION
In summary, the COVID-19 pandemic had a deleterious effect of HBV service
delivery in a community pharmacy setting in Sierra Leone, with a 100% decrease in HBV
screening observed during January to June of 2020 due to disruptions in global supply
chains and population lockdowns. Notwithstanding, the total number of individuals
screened increased modestly by 27% in the first year and by 23% in the second year after
COVID-19-related population restrictions were eased, suggesting resilience in
addressing short-term increases in demand for services. Over the three-year period of
the study, HBV screening appeared to exhibit a seasonal trend, increasing linearly
throughout the year. These findings may have implications for HBV elimination efforts in
Sierra Leone and other highly endemic countries similarly affected by the COVID-19
pandemic.
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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AUTHOR CONTRIBUTIONS
GAY, MG, and RAS conceptualized and designed the study, with contributions
from LSB, AMM, PBJ, SAY, SPEM, PEC, and SL. MG collected the data. GAY conducted
the statistical analysis. All authors contributed to the interpretation of the data. MG, AMM
and GAY wrote the initial manuscript draft. All authors critically reviewed the manuscript,
contributed important intellectual content, and approved of the final version. GAY is acting
as the guarantor of this manuscript.
ACKNOWLEDGMENTS
We wish to acknowledge the pharmacy staff at CitiGlobe Ltd and people living with
HBV in Sierra Leone, without whose help this study would not have been successful.
FUNDING INFORMATION
This research was funded by KnowHep Foundation Sierra Leone and CitiGlobe
Pharmacies Ltd (MG) and grants supporting GAY from the National Institutes of Health
(NIH)/AIDS Clinical Trials Group (ACTG) under Award Numbers 5UM1AI068636-15 and
AI068636 (1560GYD212), the Roe Green Center for Travel Medicine and Global
Health/University Hospitals Cleveland Medical Center Award Number J0713 and the
University Hospitals Minority Faculty Career Development Award/University Hospitals
Cleveland Medical Center Award Number P0603. AMM was supported by the National
Institute for Allergy and Infectious Diseases (NIAID) at NIH (grant K01AI166126) and the
Harvard University Center for AIDS Research (grant P30AI060354). The funders had no
role in the design or authorship of this publication. The article contents are solely the
responsibility of the authors and do not necessarily represent the official views of the
funders.
CONFLICTS OF INTEREST
The authors report no relevant financial disclosures or conflicts of interest.
DATA AVAILABILITY STATEMENT
The data presented in this study are available on request from the corresponding
author upon reasonable request.
ETHICAL APPROVAL
Ethical approval to perform the study was obtained from Njala University, Bo
Campus, Sierra Leone (approval date 23 January 2023). Informed consent was not
required as this study involved a retrospective analysis of secondary data.
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
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REFERENCES
[1] World Health Organization. Hepatitis B, https://www.who.int/news-room/fact-
sheets/detail/hepatitis-b; 2023 [accessed 18 May 2023]
[2] World Health Organization. Final global health sector strategies on respectively, HIV,
viral hepatitis and sexually transmitted infections, 2022-2030,
https://www.who.int/publications/i/item/9789240053779; 2022 [accessed 18 May
2023].
[3] Sonderup MW, Spearman CW. Global Disparities in Hepatitis B Elimination-A Focus
on Africa. Viruses. 2022;14:82. https://doi.org/10.3390/v14010082
[4] World Health Organization. 91 million Africans infected with Hepatitis B or C,
https://www.afro.who.int/news/91-million-africans-infected-hepatitis-b-or-c; 2022
[accessed 18 May 2023].
[5] Ejalu DL, Mutyoba JN, Wandera C, Seremba E, Kambugu A, Muganzi A, et al.
Integrating hepatitis B care and treatment with existing HIV services is possible: cost
of integrated HIV and hepatitis B treatment in a low-resource setting: a cross-
sectional hospital-based cost-minimisation assessment. BMJ Open.
2022;12:e058722. https://doi.org/10.1136/bmjopen-2021-058722
[6] Nankya-Mutyoba J, Ejalu D, Wandera C, Beyagira R, Amandua J, Seremba E, et al.
A training for health care workers to integrate hepatitis B care and treatment into
routine HIV care in a high HBV burden, poorly resourced region of Uganda: the
'2for1' project. BMC Med Educ. 2022;22:297. https://doi.org/10.1186/s12909-022-
03329-3
[7] Nyama ET, Allan-Blitz LT, Bitwayiki R, Swaray M, Lebbie W, Lavalie D, et al.
Challenges of hepatitis B treatment in rural Sub-Saharan Africa: Treatment initiation
and outcomes from a public hospital-based clinic in Kono, Sierra Leone. J Viral
Hepat. 2023;30:455-462. https://doi.org/10.1111/jvh.13812
[8] Ismail Z, Aborode AT, Oyeyemi AA, Khan H, Hasan MM, Saha A, et al. Impact of
COVID-19 pandemic on viral hepatitis in Africa: Challenges and way forward. Int J
Health Plann Manage. 2022;37:547-552. https://doi.org/10.1002/hpm.3317
[9] Kabore HJ, Li X, Allison RD, Avagyan T, Mihigo R, Takashima Y, et al. Effects of
Decreased Immunization Coverage for Hepatitis B Virus Caused by COVID-19 in
World Health Organization Western Pacific and African Regions, 2020. Emerg Infect
Dis. 2022;28:S217-S224. https://doi.org/10.3201/eid2813.212300
[10] Kondili LA, Buti M, Riveiro-Barciela M, Maticic M, Negro F, Berg T, et al. Impact of
the COVID-19 pandemic on hepatitis B and C elimination: An EASL survey. JHEP
Rep. 2022;4:100531. https://doi.org/10.1016/j.jhepr.2022.100531
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
13
[11] Lemoine M, Kim JU, Ndow G, Bah S, Forrest K, Rwegasha J, et al. Effect of the
COVID-19 pandemic on viral hepatitis services in sub-Saharan Africa. Lancet
Gastroenterol Hepatol. 2020;5:966-967. https://doi.org/10.1016/S2468-
1253(20)30305-8
[12] Freeland C, Ventricelli DJ. The Role of the Pharmacist in Preventing Hepatitis B in
the Context of the Opioid Crisis. Prev Chronic Dis. 2020;17:E88.
https://doi.org/10.5888/pcd17.200062
[13] Bahap M, Kara E, Cagla Sonmezer M, Inkaya AC, Aydin-Hakli D, Unal S, et al.
Pharmacist intervention to improve patients' knowledge and attitude towards
hepatitis B infection. Int J Clin Pract. 2021;75:e13952.
https://doi.org/10.1111/ijcp.13952
[14] Berenbrok LA, Gessler C, Kirisci L, Herrera-Restrepo O, Coley KC. Impact of
pharmacist motivational interviewing on hepatitis B vaccination in adults with
diabetes. J Am Pharm Assoc (2003). 2023;63:66-73.e1.
https://doi.org/10.1016/j.japh.2022.08.013
[15] Xiao Y, Thompson AJ, Howell J. Point-of-Care Tests for Hepatitis B: An Overview.
Cells. 2020;9:2233. https://doi.org/10.3390/cells9102233
[16] Njai HF, Shimakawa Y, Sanneh B, Ferguson L, Ndow G, Mendy M, et al. Validation
of rapid point-of-care (POC) tests for detection of hepatitis B surface antigen in field
and laboratory settings in the Gambia, Western Africa. J Clin Microbiol.
2015;53:1156-63. https://doi.org/10.1128/JCM.02980-14
[17] European Centre for Disease Prevention and Control. Public health guidance on
HIV, hepatitis B and C testing in the EU/EEA – An integrated approach. Stockholm:
ECDC; 2018. https://www.ecdc.europa.eu/sites/default/files/documents/hiv-hep-
testing-guidance_0.pdf [accessed 24 May 2023].
[18] Chandrasekar E, Kaur R, Song S, Kim KE. A comparison of effectiveness of
hepatitis B screening and linkage to care among foreign-born populations in clinical
and nonclinical settings. J Multidiscip Healthc. 2015;8:1-9.
https://doi.org/10.2147/JMDH.S75239
[19] Yendewa GA, Wang GM, James PB, Massaquoi SPE, Yendewa SA, Ghazzawi M,
et al. Prevalence of Chronic Hepatitis B Virus Infection in Sierra Leone, 1997-2022:
A Systematic Review and Meta-Analysis. Am J Trop Med Hyg. 2023 (in press).
https://doi.org/10.4269/ajtmh.22-0711
[20] Sevalie S, Youkee D, van Duinen AJ, Bailey E, Bangura T, Mangipudi S, et al. The
impact of the COVID-19 pandemic on hospital utilisation in Sierra Leone. BMJ Glob
Health. 2021;6:e005988. https://doi.org/10.1136/bmjgh-2021-005988
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
14
[21] Parmley LE, Hartsough K, Eleeza O, Bertin A, Sesay B, Njenga A, et al. COVID-19
preparedness at health facilities and community service points serving people living
with HIV in Sierra Leone. PLoS One. 2021;16:e0250236.
https://doi.org/10.1371/journal.pone.0250236
[22] Lakoh S, Jiba DF, Baldeh M, Adekanmbi O, Barrie U, Seisay AL, et al. Impact of
COVID-19 on Tuberculosis Case Detection and Treatment Outcomes in Sierra
Leone. Trop Med Infect Dis. 2021;6:154. https://doi.org/10.3390/tropicalmed6030154
[23] Wilhelm JA, Helleringer S. Utilization of non-Ebola health care services during Ebola
outbreaks: a systematic review and meta-analysis. J Glob Health. 2019;9:010406.
https://doi.org/10.7189/jogh.09.010406
[24] Kazmi SK, Khan FMA, Natoli V, Hunain R, Islam Z, Costa ACDS, et al. Viral
hepatitis amidst COVID-19 in Africa: Implications and recommendations. J Med
Virol. 2022;94:7-10. https://doi.org/10.1002/jmv.27330
[25] Stewart JS, Farrow LJ, Clifford RE, Lamb SG, Coghill NF, Lindon RL, et al. A three-
year survey of viral hepatitis in West London. Q J Med. 1978;47:365-84.
[26] Huang P, Ye G, Zhong J, Sha Q. Assessment of current epidemiological status of
viral hepatitis in Guangdong Province, China. Southeast Asian J Trop Med Public
Health. 2002; 33:832-6.
[27] Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths JK.
Seasonality in six enterically transmitted diseases and ambient temperature.
Epidemiol Infect. 2007;135:281-92. https://doi.org/10.1017/S0950268806006698
[28] Talaat M, El-Sayed N, Kandeel A, Azab MA, Afifi S, Youssef FG, et al. Sentinel
surveillance for patients with acute hepatitis in Egypt, 2001-04. East Mediterr Health
J. 2010;16:134-40.
[29] Fares A. Seasonality of hepatitis: a review update. J Family Med Prim Care.
2015;4:96-100. https://doi.org/10.4103/2249-4863.152263
[30] Tan M, Bhadoria AS, Cui F, Tan A, Van Holten J, Easterbrook P, et al. Estimating
the proportion of people with chronic hepatitis B virus infection eligible for hepatitis B
antiviral treatment worldwide: a systematic review and meta-analysis. Lancet
Gastroenterol Hepatol. 2021;6:106-119. https://doi.org/10.1016/S2468-
1253(20)30307-1
. CC-BY-NC 4.0 International licenseIt is made available under a
is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
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Table 1. Seroprevalence rates of HBsAg by baseline characteristics and testing periods
Characteristics
Overall
(%)
HBsAg Screening
HBsAg
Seropositivity
(95% CI)
p-Value
Positive
Negative
Total
920
161
759
17.5 (14.9-20.4)
Gender
Male
476 (51.7)
92
384
19.3 (15.8-22.9)
0.131
Female
444 (48.3)
69
375
15.5 (12.2-18.9)
Age, years
10-20
57 (6.2)
5
52
8.8 (1.2-16.3)
0.004
20-29
266 (28.9)
64
202
24.4 (18.9-29.2)
30-39
482 (52.4)
80
402
16.6 (13.3-19.9)
40-49
66 (7.2)
6
60
9.1 (2.0-16.2)
≥50
49 (5.3)
6
43
12.2 (2.7-21.8)
Education
None
104 (11.3)
16
88
15.4 (8.3-22.4)
0.436
Primary
123 (13.4)
17
106
13.8 (7.6-20.0)
Secondary
148 (16.1)
31
117
20.9 (14.3-27.6)
Tertiary
545 (59.2)
97
448
17.8 (14.6-21.0)
Testing Period
Year 1
(Oct 2019-Sep 2020)
263 (28.6)
58
205
22.1 (17.0-27.1)
0.069
Year 2
(Oct 2020-Sep 2021)
333 (36.2)
51
282
15.3 (11.4-19.2)
Year 3
(Oct 2021-Sep 2022)
324 (35.2)
52
272
16.0 (12.0-20.1)
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Ghazzawi et al 2023
16
FIGURE LEGENDS
Figure 1. Temporal trends in HBV testing and HBsAg seroprevalence from October 2019
to September 2022
Abbreviations: HBV, hepatitis B virus; HBsAg, hepatitis B surface antigen
Figure 2. Changes in HBV screening from October 2019 to September 2022
Abbreviations: HBV, hepatitis B virus
Figure 3. Quarterly trends in HBV testing
Abbreviations: HBV, hepatitis B virus
Figure 4. Quarterly trends in HBV diagnosis
Abbreviations: HBV, hepatitis B virus
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Figure 1. Ghazzawi et al 2023
Oct-Dec 2019
Jan-Mar 2020
Apr-Jun 2020
Jul-Sep 2020
Oct-Dec 2020
Jan-Mar 2021
Apr-Jun 2021
Jul-Sep 2021
Oct-Dec 2021
Jan-Mar 2022
Apr-Jun 2022
Jul-Sep 2022
0
25
50
75
100
125
150
175
Frequency
HBV tests performed
Positive HBsAg cases
122
141
88
59
85
101 109
50
62
103
25 32
14
5
17 17
15 16 10 9
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Figure 2. Ghazzawi et al 2023
0
27 23
0
-100 -100
16
-28
-52
-30
-17
-11
-59
-49
-16
Year 1
Year 2
Year 3
Oct-Dec 2019
Jan-Mar 2020
Apr-Jun 2020
Jul-Sep 2020
Oct-Dec 2020
Jan-Mar 2021
Apr-Jun 2021
Jul-Sep 2021
Oct-Dec 2021
Jan-Mar 2022
Apr-Jun 2022
Jul-Sep 2022
-100
-75
-50
-25
0
25
50
Change in HBV Tes t i ng ( %)
Year l y
Baseline
Quarterly
Baseline
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Figure 3. Ghazzawi et al 2023
Jan-Mar
Apr-Jun
Jul-Sep
Oct-Dec
0
25
50
75
100
125
150
Quarters
Quarterly HBV Tests
P = 0.4237
P = 0.0380
P = 0.0192
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint
Figure 4. Ghazzawi et al 2023
Jan-Mar
Apr-Jun
Jul-Sep
Oct-Dec
0
5
10
15
20
25
30
35
Quarters
Postive HBV Tests
P = 0.8878
P = 0.9816
P = 0.6799
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is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) The copyright holder for this preprint this version posted May 28, 2023. ; https://doi.org/10.1101/2023.05.24.23290418doi: medRxiv preprint