Systematic Review of Reported HIV Outbreaks, Pakistan, 2000-2019
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SYNOPSIS
Systematic Review of Reported HIV
Outbreaks, Pakistan, 2000–2019
Elizabeth M. Rabold,1 Hammad Ali,1 Danielle Fernandez, Martha Knuth,
Karl Schenkel, Rana Jawad Asghar, Mirza Amir Baig, Saqib Shaikh, Oliver Morgan
In support of improving patient care, this activity has been planned and implemented by Medscape, LLC and
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Medscape, LLC designates this Journal-based CME activity for a maximum of 1.00 AMA PRA Category 1
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Successful completion of this CME activity, which includes participation in the evaluation component, enables the
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Certification (MOC) program. Participants will earn MOC points equivalent to the amount of CME credits claimed for
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the purpose of granting ABIM MOC credit.
All other clinicians completing this activity will be issued a certificate of participation. To participate in this journal
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and (4) view/print certificate. For CME questions, see page 1256.
Release date: March 19, 2021; Expiration date: March 19, 2022
Learning Objectives
Upon completion of this activity, participants will be able to:
• Distinguish groups at highest risk for HIV infection in Pakistan
• Analyze causes of outbreaks of HIV infection in Pakistan
• Assess factors which might promote unsafe injection practices in Pakistan
CME Editor
Jude Rutledge, BA, Technical Writer/Editor, Emerging Infectious Diseases. Disclosure: Jude Rutledge has disclosed
no relevant financial relationships.
CME Author
Charles P. Vega, MD, Health Sciences Clinical Professor of Family Medicine, University of California, Irvine School
of Medicine, Irvine, California. Disclosure: Charles P. Vega, MD, has disclosed the following relevant financial
relationships: served as an advisor or consultant for GlaxoSmithKline.
Authors
Disclosures: Elizabeth M. Rabold, MD, MPH; Hammad Ali, PhD; Danielle Fernandez, MPH; Martha Knuth, MLIS;
Karl Schenkel, MD; Rana Jawad Asghar, MBBS, MPH; Mirza-Amir Baig, MBBS, MPH; Saqib Ali Shaikh, MSc,
MBBS; and Oliver Morgan, PhD, have disclosed no relevant financial relationships.
Author affiliations: Centers for Disease Control and Prevention, (M.A. Baig); Sindh AIDS Control Program, Larkana, Pakistan
Atlanta, Georgia, USA (E.M. Rabold, H. Ali, D. Fernandez, (S. Shaikh)
M. Knuth); World Health Organization, Geneva, Switzerland
DOI: https://doi.org/10.3201/eid2704.204205
(K. Schenkel, O. Morgan); Global Health Strategists and
Implementers, Karachi, Pakistan (R.J. Asghar); Pakistan
Field Epidemiology and Laboratory Training Program, Karachi
1
These first authors contributed equally to this article.
1040 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 4, April 2021HIV Outbreaks, Pakistan, 2000–2019
of age. A World Health Organization (WHO) report
Unsafe injection practices and injection drug use have
been linked to multiple HIV outbreaks in Pakistan since
cited unsafe medical practices and poor infection
2003; however, few studies have systematically ana- control programs as key risk factors for infection (12)
lyzed the causes of these outbreaks. We conducted a and noted that this outbreak was the fourth HIV out-
systematic review of published English-language litera- break in Larkana since 2003. A cursory review of the
ture indexed in bibliographic databases and search en- literature, however, did not identify peer-reviewed
gines and a focused gray literature review to collate and publications on all of these referenced outbreaks.
analyze all reported HIV outbreaks in Pakistan during The objective of our systematic review was to iden-
2000–2019. Of 774 unique publications reviewed, we tify and collate data from all reported HIV outbreaks
identified 25 eligible publications describing 7 outbreaks. in Pakistan to describe overarching themes and aid
More than half occurred during 2016–2019. The primary in future prevention efforts.
sources of transmission were iatrogenic transmission,
affecting children, persons with chronic medical condi-
tions, and the general population (4 outbreaks); injec-
Methods
tion drug use (2 outbreaks); and a combination of both We followed the PRISMA statement and the Co-
(1 outbreak). In the absence of robust HIV testing and chrane Handbook to conduct this systematic review
surveillance in Pakistan, timely and detailed outbreak (Appendix Table 1, https://wwwnc.cdc.gov/EID/
reporting is important to understand the epidemiology of article/27/4/20-4205-App1.pdf) (13). We searched
HIV in the country. Medline, Embase, CAB Abstracts, Global Health,
PsycInfo, Cochrane Library, Scopus, Academic
T he first cases of HIV in Pakistan were reported
in 1987, with epidemiologic evidence supporting
the importation of cases by migrant workers from the
Search Complete, Cumulative Index to Nursing and
Allied Health Literature, ProQuest Central, PubMed
Central, Virtual Health Library, and Google Schol-
Gulf States (1–3). Since that time, noncontinuous sur- ar to identify English-language publications on re-
veillance assessments have noted high prevalence of ported HIV outbreaks in Pakistan during January
HIV in certain populations; the most recent 2016–2017 1, 2000–December 31, 2019. We limited the search
prevalence estimates were 38.4% among persons who to studies published after January 1, 2000, because
inject drugs (PWID), 7.2% among transgender per- the earliest reported HIV outbreak in Pakistan oc-
sons, and 5.6% among men who have sex with men curred in 2003 (14). To complement the published
(4–8). By comparison, the prevalence in the general literature search, we conducted a comprehensive
population is 0.1%, representing ≈190,000 persons search of the gray literature (i.e., publications not
living with HIV (PLHIV), including 6,100 children published in indexed peer-reviewed journals), in-SYNOPSIS
We systematically screened and reviewed re- Results
sults from the published and gray literature search Our initial search identified 1,653 records published
(Figure). We screened titles and abstracts, and we during January 2000–December 2019. We removed
defaulted to reviewing the abstract if the title had 879 (53%) duplicate reports identified across multi-
an unclear focus and reviewing the full report if no ple databases or search engines through automated
abstract was available, counting it among the num- and manual processes (Figure). Of the remaining 774
ber of abstracts reviewed. We included publications de-duplicated reports, 625 (81%) were excluded af-
that reported data on outbreaks of HIV or sudden ter review of the title and 108 (14%) were excluded
increases in cases in Pakistan. For the purpose of after review of the abstract. We excluded 16 reports
this systematic review, we defined an outbreak as an upon review of the full article, gray literature, or
unexpected number of HIV cases identified through government report, leaving 25 (3%) reports eligible
targeted testing or key population surveillance, la- for inclusion.
beled and reported as an outbreak, and leading to an The 25 reports identified by our search strat-
evaluation or investigation. We excluded abstracts egy described 7 outbreaks: 4 in Punjab Province
without published final reports (unless identified (Sargodha, Sargodha District [2007]; Kot Imrana,
in the gray literature), reports that provided preva- Sargodha District [2018]; Jalalpur Jattan, Gujrat
lence or incidence data only (including key popula- District [2008]; and Faisalabad, Faisalabad District
tion surveys), opinion pieces without mention of a [2019]) and 3 in Sindh Province (Larkana, Larkana
specific outbreak, mathematical modeling studies, District [2003 and 2016] and Ratodero, Larkana Dis-
epidemiologic analyses, reports without quantita- trict [2019]) (Appendix Table 3). Six (24%) reports
tive data, and preprint reports. We also excluded re- described >2 outbreaks.
ports where the author did not define the described Case-positivity rates ranged from 1.3% to
cases as an outbreak or did not provide a discrete 51.8%, varying in part because of sampling meth-
geographic, temporal, or epidemiologic link. If iden- ods. The potential source of 4 of the 7 outbreaks was
tical reports were published in >1 journal, the earli- reported as iatrogenic transmission through unsafe
est publication was included. Similarly, if identical healthcare practices at clinics, hospitals, and dialy-
or nearly identical reports were published in a jour- sis centers; 2 outbreaks were attributed to injection
nal and also included as a conference abstract, we in- drug use, and 1 outbreak was attributed to both.
cluded only the published report. If a report includ- Several reports described a potential association
ed outbreak data as well as a subset of data in a case with unqualified healthcare providers (frequently
control, cohort, or cross-sectional investigation, we designated as quacks in Pakistan [15]), in general,
included data on the larger outbreak and the study. or with a specific provider. Some reports also re-
We reviewed journal submission guidelines to de- ported cultural practices as a contributing factor
termine whether a publication was peer-reviewed. to transmission. Populations most affected by the
We organized eligible publications, gray litera- outbreaks varied by proposed etiology; iatrogenic
ture, and government reports by geographic location causes affected the general community, including
and year of the reported outbreak. We included re- women and children, as well as persons living with
ports describing multiple outbreaks under each ap- specific medical conditions, such as end-stage renal
propriate outbreak heading. We extracted year and disease. Recreational drug use affected primarily
type of report, investigating agency and source or PWID, most frequently men.
reference for primary data, number of persons tested Our review identified 5 reports in peer-reviewed
and diagnosed with HIV, case positivity rate (de- literature, with the remaining reports published as
fined as the percentage of persons positive among letters to the editor or correspondence, nongovern-
the number tested within the period defined by the mental organization and government reports, and
authors of the publication), notable demographic conference abstracts. National or provincial AIDS
and behavioral characteristics of case-patients, ma- control programs led the initial investigations of 4
jor risk factors, and other relevant information (Ap- of the 7 outbreaks; the National Institutes of Health-
pendix Table 3). We noted instances where articles Pakistan and Field Epidemiology Training Pro-
used media reports as their primary citation. One gram–Pakistan and district health departments pro-
author independently reviewed initial data extrac- vided data for the other 3 outbreaks. The Ratodero
tion of all eligible reports for concurrence. If neces- (2019) outbreak had additional support from WHO,
sary, we reached out to corresponding authors of other United Nations agencies, local universities,
individual reports for clarification. and other international and local partners. Of the
1042 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 4, April 2021HIV Outbreaks, Pakistan, 2000–2019
Figure. Identification and selection of studies reporting HIV outbreaks in Pakistan, January 2000–September 2019. CINAHL, Cumulative
Index to Nursing and Allied Health Literature; NGOs, nongovernmental organizations.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 4, April 2021 1043SYNOPSIS
25 reports, 17 (68%) describe this single outbreak. Iatrogenic transmission from unsafe healthcare
Other outbreaks had more limited data, often lim- practices and poor infection prevention and control
ited to case counts and affected population. Authors was identified as the primary or contributing risk
were often not directly affiliated with the primary factor in 5 of the 7 HIV outbreaks (Jalalpur Jattan
data but rather briefly described testing statistics, [2008], Kot Imrana [2018], Larkana [2016], Ratodero
demographic information, and risk factors obtained [2019], and Faisalabad [2019]). From a recent survey
from investigations from government entities, me- in Pakistan, researchers estimated that ≈38% of sur-
dia reports, and other sources. Some discrepancies veyed physicians likely reused syringes (18). Data
were noted across reports pertaining to the same from the latest Demographic Health Survey indicate
outbreak, and many reports did not provide com- that ≈9% of injections given to patients in Pakistan
plete information on case-positivity rates, study are unsafe, and every person receives an average of
period, or method of data collection. Authors occa- 4.1 therapeutic injections per year in Pakistan (19).
sionally (4 [16%]) used media reports as the primary Extrapolating from this frequency and safety data,
source of information. Though most outbreaks had approximately 1 in 3 persons might receive an un-
at least 1 article citing primary data or data directly safe injection every year in Pakistan (19). Further-
from a testing program, the single report found for more, cross-sectional studies of persons with thalas-
the Faisalabad (2019) outbreak cited only a newspa- semia in Pakistan have shown a high prevalence of
per article. Of the 25 reports describing the 7 out- bloodborne infections, including HIV, hepatitis B,
breaks, only 5 reports provided detailed outbreak and hepatitis C, suggestive of infection from blood
investigation information. Despite more extensive transfusions (20,21). Nosocomial or iatrogenic trans-
investigations, these reports still had limited ability mission including unsafe blood transfusions and re-
to draw conclusions or conduct statistical compari- use of medical equipment has contributed to several
sons because of study design (e.g., no comparison HIV outbreaks in other countries, including ≈10,000
group [16] or small sample size [17]). Only 1 of the children in orphanages in Romania (22), >400 chil-
25 reports, describing an outbreak investigation in dren in Libya with frequent co-infection with hep-
Jalalpar Jattan (2008), included phylogenetic infor- atitis B and C (23), and 242 adults and children in
mation (16), which demonstrated that transmission Cambodia (24).
likely occurred over a decade, reflecting endemic Several factors might play a role in the propa-
disease rather than an outbreak. gation of unsafe injection practices in low-income
countries. These factors include sociocultural factors
Discussion such as healthcare providers’ belief that compliance
Our review identified 25 reports describing 7 HIV is better with injections than with oral medication
outbreaks during 2000–2019 in Pakistan: 3 in Sindh and patients might seek healthcare elsewhere if
Province and 4 in Punjab Province. Of these, 4 were not provided injections; financial incentives on the
identified during 2016–2019. In 2019, two outbreaks part of both patient and provider through fee-for-
were reported: a large outbreak primarily affecting injection practices and contingent on provider abil-
children in Ratodero in Larkana, a district with mul- ity to purchase and maintain a supply of injecting
tiple prior outbreaks, and an outbreak in Faisala- equipment; corruption, when money allocated for
bad, primarily infecting PWID. Case-positivity rates healthcare, such as disposable injecting equipment,
ranged from 1.3% to 51.8%, and populations most is used elsewhere, leading to reuse of equipment;
affected varied by outbreak but included PWID; per- lack of policies and procedures around safe injection
sons living with specific medical conditions; and the practices, such that policies forbidding the reuse of
general population, including women and children. injecting equipment are not implemented nor en-
The level of detail pertaining to the description of forced in low-income countries as they are in high-
data collection and investigation methods varied income countries; ready access to injectable medica-
across the publications, and much of the data pro- tions without a prescription; and lack of awareness
vided were collected not by authors but by nation- of risks associated with unsafe injection practices
al, provincial, and district health departments and (25). Given these factors, developing a multi-strat-
other government entities. Iatrogenic transmission egy approach that might be adapted and tailored as
(57%), injection drug use (29%), or both (14%) were necessary might help prevent future outbreaks of
identified as the potential sources of the outbreaks; HIV and other bloodborne pathogens. These strat-
no outbreak solely attributable to sexual transmis- egies include community and healthcare provider
sion was reported. education to address excessive and unnecessary use
1044 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 4, April 2021HIV Outbreaks, Pakistan, running
2000–2019
title
of therapeutic injections, implementation and moni- occurred over a decade (16). Without comprehensive
toring of policies around single-use injecting equip- surveillance and phylogenetic data, ascertaining
ment, and addressing gaps in infection prevention whether new HIV diagnoses or a sudden increase in
and control. diagnoses in an area represent an outbreak or simply
Injection drug use was reported as the primary missed HIV diagnoses with endemic transmission
or contributing cause of HIV transmission in 3 of over time is difficult.
the 7 outbreaks (Larkana [2003], Sargodha [2007], Outbreaks are underrepresented in the litera-
and Faisalabad [2019]). Periodic HIV surveillance ture; those that are published have limited ability to
data are available for key populations in specific characterize the full epidemiologic and phylogenetic
cities from the National AIDS Control Programme footprint of an outbreak. Nonsystematic tracking of
Integrated Biologic and Behavioral Surveillance sur- media reports identified at least 2 other potential
veys, but they are not designed to measure preva- outbreaks known to national or provincial AIDS
lence for the general population or key populations control programs but not described by our system-
in rural areas (4–8). The HIV prevalence among atic review (26,27). Given the frequency of media
PWID documented by each survey increased from reports of HIV outbreaks, albeit without full epi-
10.8% to 38.4%; however, because the survey was demiologic data, and well-documented data on the
expanded to new cities across the different reporting widespread prevalence of unsafe injections across
periods, direct comparison of the change in preva- Pakistan, the paucity of systematic outbreak inves-
lence is not possible. Whether any change in preva- tigations is striking. Of the reports included in our
lence might be attributable to sporadic outbreaks or systematic review, only 5 (20%) were peer-reviewed;
a steady increase in HIV prevalence in this subpopu- the remaining were published as letters to the editor,
lation is unknown. None of the literature describing editorials, general correspondence, abstracts, non-
outbreaks with injection drug use as the primary or government organization publications, and govern-
contributing source of transmission reported a phy- ment reports, without clear description of methods,
logenetic analysis, leaving timelines of infections in study design, and data collection. Given the limited
these outbreaks unclear. outbreak investigations and robust data reporting
Although the Integrated Biologic and Behavioral in peer-reviewed and gray literature, our systematic
Surveillance surveys offer insight into HIV preva- review likely underestimates the frequency of the
lence among key populations, the absence of routine problem and its associated burden of disease.
HIV surveillance in the general population prevents The main strength of our review is that we
understanding of the actual burden of the HIV epi- searched multiple bibliographic databases, with
demic in Pakistan. Considering the high prevalence the addition of Google Scholar and the Virtual
of HIV in PWID, men who have sex with men, and fe- Health Library, nongovernmental organization
male sex workers, as well as unsafe injection practices and government websites, and conference abstracts
as we have described, spillover to the general popula- to ensure all relevant publications were captured.
tion is only a matter of time. Widespread surveillance However, we note several limitations. First, we
of HIV might be challenging and might yield little recognize that the definition of an outbreak is chal-
information given the low general population prev- lenging in the setting of limited phylogenetic and
alence of 0.1% (9). However, adding surveillance of surveillance data. A study by Ansari et al. (16) de-
targeted populations at higher risk, such as pregnant termined that the observed increase in cases was
women, patients at infectious disease or tuberculo- likely a progression of endemic disease only after
sis clinics, and persons requiring frequent transfu- the results of phylogenetic analysis. As such, oth-
sions, might provide early warning signs to changes er outbreaks reported in this review might, if the
in HIV prevalence. Likewise, systematic monitoring same analyses were available, have been deter-
of the blood supply might represent an efficient, less mined not to be outbreaks. Second, our literature
costly approach to surveillance. Currently, routine review was limited to English-language publica-
surveillance is not conducted in any of these settings. tions. Although a potential exists for missing ar-
Although phylogenetic analyses, which assist in un- ticles written in Urdu and other local languages,
derstanding circulating strains and subtypes, might English is one of the official languages in the coun-
contribute to our understanding of a rise in cases, try and is the predominant language for scientific
only 1 publication identified in this review reported a and medical research dissemination in Pakistan
phylogenetic analysis; it showed that, despite prelim- (28,29). Finally, although unlikely, a small chance
inary data suggestive of a new outbreak, transmission exists that a unique outbreak might have been men-
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 4, April 2021 1045SYNOPSIS
tioned in a publication focusing on surveillance or References
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