Received: 24 June 2022 Accepted: 15 September 2022

DOI: 10.1111/hiv.13417

ORIGINAL ARTICLE

The British HIV Association national clinical audit 2021:

Management of HIV and hepatitis C coinfection

Reynie P. Raya 1,2 | Hilary Curtis 3 | Ranjababu Kulasegaram 4 |

3,5 2,6 3,7
Graham S. Cooke | Fiona Burns | David Chadwick |
1,2
Caroline A. Sabin | the BHIVA Audit and Standards Sub-committee

1
National Institute for Health Research
(NIHR) Health Protection Research Unit Abstract
(HPRU) in Blood Borne and Sexually Objectives: We aimed to describe clinical policies for the management of
Transmitted Infections at UCL, Royal
people with HIV/hepatitis C virus (HCV) coinfection and to audit routine
Free Campus, London, UK
2 monitoring and assessment of people with HIV/HCV coinfection attending
Centre for Clinical Research,
Epidemiology, Modelling and Evaluation, UK HIV care.
Institute for Global Health, UCL, Methods: This was a clinic survey and retrospective case-note review. HIV
Royal Free Campus, London, UK
3
clinics in the UK participated in the audit from May to July 2021 by complet-
British HIV Association (BHIVA),
Letchworth, UK ing an online questionnaire regarding their clinic's policies for the manage-
4
Department of Sexual Health, St Thomas ment of people with HIV/HCV coinfection, and by contributing to a case-note
Hospital, London, UK review of people living with HIV with detectable HCV RNA who were under
5
Department of Infectious Disease, the care of their service.
Imperial College London, St Mary's
Campus, London, UK
Results: Ninety-five clinics participated in the clinic survey; of these,
6
Royal Free London NHS Foundation 15 (15.8%) were regional specialist centres, 19 (20.0%) were HIV services
Trust, London, UK with their own coinfection clinics, 40 (42.1%) were HIV services that referred
7
Department of Infectious Diseases, South coinfected individuals to a local hepatology service and 20 (21.1%) were HIV
Tees Hospitals NHS Foundation Trust,
services that referred to a regional specialist centre. Eighty-one clinics pro-
Centre for Clinical Infections,
Middlesbrough, UK vided full caseload estimates; of the approximately 3951 people with a his-
tory of HIV/HCV coinfection accessing their clinics, only 4.9% were believed
Correspondence
Reynie P. Raya, Centre for Clinical
to have detectable HCV RNA, 3.15% of whom were already receiving or
Research, Epidemiology, Modelling and approved for direct-acting antiviral (DAA) treatment. In total, 29 (30.5%) of
Evaluation, Institute for Global Health, the clinics reported an impact of COVID-19 on coinfection care, including
UCL, Royal Free Campus Rowland Hill
Street, London NW3 2PF, UK. delays or reductions in the frequency of services, monitoring, treatment initi-
Email: [email protected] ation and appointments, and changes to the way that treatment was dis-
pensed. Case-note reviews were provided for 283 people with detectable
Funding information
RPR receives funding from the Indonesian HCV RNA from 74 clinics (median age 42 years, 74.6% male, 56.2% HCV
Endowment Fund for Education (LPDP genotype 1, 22.3% HCV genotype 3). Overall, 56% had not received

Members of the BHIVA Audit and Standards Subcommittee

D Chadwick (Chair), H Curtis (Co-ordinator), A Brown, F Burns, E Cheserem, S Croxford, A Freedman, L Haddow, R Kulasegaram, P Khan, N
Larbalestier, N Mackie, R Mbewe, A Mammen-Tobin, F Nyatsanza, E Ong, O Olarinde, T Pillay, S Pires, R Raya, C Sabin, A Sullivan, A Williams, E
Williams.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2022 The Authors. HIV Medicine published by John Wiley & Sons Ltd on behalf of British HIV Association.

HIV Med. 2022;1–9. wileyonlinelibrary.com/journal/hiv 1

2 RAYA ET AL.

Indonesia) and GC from NIHR Research

Professorship and BRC of Imperial College treatment for HCV, primarily due to lack of engagement in care (54.7%)
NHS Trust and/or being uncontactable (16.4%).
Conclusions: Our findings show that the small number of people with HIV
with detectable HCV RNA in the UK should mean that it is possible to achieve
HCV micro-elimination. However, more work is needed to improve engage-
ment in care for those who are untreated for HCV.

KEYWORDS
audit, coinfection, hepatitis C virus, HIV, micro-elimination

INTRODUCTION METHODS

In the UK, there are an estimated 103 800 people living All UK sites known to BHIVA as providers of adult HIV
with HIV, of whom around 5–10% are believed to be care were invited to join the audit between 1 May and
antibody-positive for hepatitis C virus (HCV); those who 31 July 2021. The audit consisted of a clinic survey and a
inject drugs and men who have sex with men (MSM) are retrospective case-note review submitted to BHIVA by an
disproportionately most affected [1–3]. Prior to the avail- online questionnaire (see supplementary material).
ability of interferon-free treatment for HCV, people living For the clinic survey, each site was asked to estimate
with HIV were considered to be a ‘special population’ the total number of people living with HIV attending
due to the poor responses to interferon/ribavirin in this their clinic who were HCV antibody-positive and their
group [4, 5]. However, with the advent of direct-acting arrangements for the management of hepatitis coinfec-
antiviral (DAA) treatment for HCV, sustained virological tion. Respondents were asked to detail any measures
responses to treatment are generally as high in this popu- taken by their site to encourage HCV treatment and to
lation as in others, and thus people living with HIV are describe the impact of the COVID-19 pandemic on their
no longer considered to be a special population [6]. management of coinfection.
The World Health Organization (WHO) has set a As part of the retrospective case-note review, sites were
range of ambitious targets to support the elimination of asked to submit information on people living with HIV aged
viral hepatitis as a public health problem by 2030. These 16 or over with currently detectable HCV RNA. Sites were
include: a 90% reduction in new viral hepatitis infections; asked to report information on the 40 most recent attenders
a 65% reduction in deaths from viral hepatitis; diagnosis or all such individuals, if fewer. Information collected
of 90% of those living with viral hepatitis; and treatment included demographic characteristics, HCV infection man-
of 80% of eligible people with chronic HCV [7]. Given the agement and status, and the management of liver disease.
extensive endeavours and investment required to attain Most questions were pre-coded, but for some, respon-
these targets, it has been proposed that a focus on smaller dents could add free text which was then coded manu-
sub-groups (‘micro-elimination’) may be more realistic ally. Analyses are largely descriptive; median and
[8–10], with people living with HIV being a key group in interquartile ranges (IQR) are presented for numeric
which micro-elimination could be feasible [11, 12]. In values, and percentages for categorical data. Analyses
line with the global situation, in 2018 the British HIV were performed using Stata v.17.0 (StataCorp, College
Association (BHIVA) set a micro-elimination target to Station, TX, USA).
treat all people living with HIV with HCV coinfection in
the UK by 2021 [13].
To demonstrate progress towards this target, BHIVA RESULTS
conducted an audit of clinic policies, and the routine
monitoring and assessment of people with HIV/HCV Clinic survey
coinfection who are attending UK HIV care during the
pandemic and set out to describe clinical policies for the Of 95 clinics that completed the survey, 81 provided full
management of those with HIV/HCV coinfection. This caseload estimates, saying they saw approximately 3951
was planned to take place during 2020 but was postponed (5.8%) HCV antibody-positive individuals among 68 368
to 2021 because of the COVID-19 pandemic, and slightly people living with HIV accessing their clinics. Of these
modified to include information about its impact. 3951, 193 (4.9%) had detectable HCV RNA, including
HIV MEDICINE 3

T A B L E 1 Arrangements for the clinical management of those with HIV/HCV coinfection among HIV clinics participating in the
BHIVA Hepatitis C Coinfection audit 2021

N %
Service arrangement Regional specialist or referral centre 15 15.8
Manage via a coinfection clinic within the HIV 19 20.0
service
Referred to local hepatology service 40 42.1
Referred to regional specialist coinfection clinic 20 21.1
Not relevant 1 1.0
Current access to repeat HCV treatment for Confident that retreatment would be offered in 71 74.7
reinfected individuals following treatment most cases
Retreatment might be offered in some cases 10 10.5
depending on individual circumstances
Not sure 14 14.7
Partner notification for HCV as part of routine Yes, both HCV and HIV 76 80.0
service Routinely for HIV but not for HCV 18 19.0
It is done elsewhere for both HIV and HCV 1 1.0
Local provision of: Peer support for HCV 32 33.7
Home/community visit to encourage care 40 42.1
engagement for people with HCV

Abbreviations: BHIVA, British HIV Association; HCV, hepatitis C.

122 (3.1%) who were already receiving or approved for service, 18 (19%) only for HIV and one (1%) reported that
DAA treatment. Scaling this to the estimated 103 800 this was conducted elsewhere (Table 1).
people living with HIV in the UK suggests that there may Sixty-five out of 95 clinics (68.4%) reported that they
be only a few hundred people with current HIV/HCV had taken specific measures to encourage HCV treatment
coinfection. Almost all clinics were located in England (the 30 (31.6%) clinics that reported that they had not
with only eight in Wales, Scotland or Northern Ireland. taken any such measures saw very few people with coin-
They reported medians of 112 (IQR: 5–37) people who fection). Free text options in this question enabled the
had a positive HCV antibody status, one (1–3) person respondents to report more than one measure that was
with a positive HCV RNA, and one (0–1) person who had taken in their clinics, and thus multiple responses were
been approved for treatment. observed. Clinics generally noted the importance of close
Fifteen (15.8%) of the 95 clinics were regional special- working relationships with hepatology clinics, clearly
ist or referral centres for coinfection, 19 (20.0%) were defined referral pathways (39, or 41.1%), close liaison
HIV services with a dedicated coinfection clinic, with community outreach and specialist services
40 (42.1%) would refer people with HCV coinfection to a (16, 16.8%) and the need for flexibility around appoint-
local hepatology service, and the remaining 20 (21.1%) ments, venues for care and approaches to providing DAA
clinics would refer people to a regional specialist or refer- treatment and monitoring (14, 14.7%) (Table 2).
ral centre. When asked about the offer of repeat HCV Regarding impact of COVID-19 on the clinics’
treatment for people who became reinfected after previ- approaches to managing people with coinfection, 75 out of
ously successful treatment, 71 (74.7%) clinics were confi- 95 of the clinics (78.9%) reported little or no impact, again
dent that repeat treatment would be offered in most because the clinics did not provide care to a large number
cases, 10 (10.5%) said that it might be offered and of people with detectable HCV RNA. Of those clinics that
14 (14.7%) were not sure. Around a third of clinics did report an impact, clinics reported delays or reductions
(32, 33.7%) provided peer support for those with coinfec- in monitoring frequency (8, 8.4%), treatment initiation
tion and 40 (42.1%) provided home or community visits (5, 5.3%), timing of appointments (3, 3.2%) or services gen-
to support engagement with care. The majority (76/95, erally (4, 4.2%), with others reporting changes to the way
80%) of clinics reported that they had a partner notifica- in which treatment was dispensed (5, 5.3%) and a switch
tion programme for HIV and HCV as part of their routine to telemedicine (3, 3.2%) (Table 2).
4 RAYA ET AL.

TABLE 2 Measure to encourage HCV treatment and impact of COVID-19 pandemic towards management of people with HIV/HCV
coinfection

N %
Specific measures to encourage uptake of HCV Close working relationship with hepatology 39 41.1
treatment among people living with HIVa (including nurses) and clearly defined pathways
for referral
Close liaison with community/outreach hepatitis 16 16.8
nurses and specialist services (e.g. drug and
alcohol, prison, homeless)
Flexibility around appointments, venues for care 14 14.7
and approaches to providing DAA treatment
and monitoring
No specific approach – very few patients 30 31.6
Other 3 3.2
Impact of COVID-19 pandemic towards Little or negative impact 75 78.9
management of HIV/HCV coinfectionsa Delayed appointment 3 3.2
Delayed/reduce monitoring 8 8.4
Delayed treatment initiation 5 5.3
Reduce service generally 4 4.2
Changes to way that treatment is dispensed 5 5.3
Switching to telemedicine rather than face-to-face 3 3.2
visits
Other 1 1.5

Abbreviation: DAA, direct-acting antviral; HCV, hepatitis C.

a
Multiple response.

Retrospective case-note review Treatment was already planned for a third of the
159 people who were not currently taking HCV treatment,
Of the 95 clinics that responded to the clinic survey, 11 (6.9%) had either only just recently acquired HCV and
63 also contributed to the case-note review (most of the two (1.3%) had recently been diagnosed with coinfection.
remainder had no cases to report) together with a further Among the others, the main reasons for not taking HCV
11 clinics. In total, the 74 clinics provided information on treatment were generally related to the person's lack of
283 individuals with detectable HCV RNA. The median engagement in care (87, 54.7%) and/or being uncontactable
age was 42 years (IQR: 37–49), and 211 (74.6%) were (26, 16.4%). Clinical judgment about the person's likely
male. It was believed that the most likely modes of acqui- adherence to treatment (10, 6.3%), their risk of reinfection
sition for HIV and HCV were injection drug use 168 (7, 4.4%) or having complex clinical or treatment issues
(59.4%) non-chemsex drugs, 36 (12.7%) chemsex drugs, (6, 3.8%) was also noted as a reason for no treatment. Indi-
sex between men (91, 32.2%) and/or between men and vidual patient wishes not to be treated (22, 13.8%) or beliefs
women (90, 31.8%). Most people (56.2%) had genotype that the treatment would be ineffective (2, 1.3%) or toxic
1 HCV infection, with 22.3% having genotype 3. Overall, (3, 1.9%) were also cited (Table 3). Among those with a
120 out of 283 (42.4%) people had been or were receiving detectable HCV RNA despite having received treatment
HCV treatment, with 63/120 (52.5%) having had previous (n = 62), 17 (27.4%) had been reinfected after successful
treatment, and 57/120 (47.5%) currently being treated. treatment, 25.8% had completed treatment but information
However, the remaining 159 of 283 (56.2%) had not been was unavailable as to its success, 11 (17.7%) had not com-
treated and the treatment status for the other four (1.4%) pleted treatment, 10 (16.1%) had completed treatment but
was unknown. Among those currently receiving or who the results of blood tests were still awaited and seven
had recently finished treatment, drugs taken were sofos- (11.3%) people had started treatment but had subsequently
buvir/ledipasvir with or without ribavirin (27.4%), elbas- disengaged from care or were lost to follow-up.
vir/grazoprevir (21.6%), glecaprevir/pibrentasvir (18.6%), Staging of liver disease had been performed in
and sofosbuvir/velpatasvir with or without ribavirin 170 (60.1%) individuals (75 normal, 50 mild, 13 moderate,
(15.7%) (Table 3). 22 severe fibrosis, 10 not recorded), repeated fibrosis
HIV MEDICINE 5

TABLE 3 Management of HCV infection among people living with HIV with detectable HCV RNA, case-note review

N %
Total number of cases 283 100.0
HCV treatment Has been or is currently being treated 120 42.4
Not been treated for HCV 159 56.2
Not recorded/no response 4 1.4
HCV treatment regimen (n = 102 treatment in Elbasvir/grazoprevir 22 21.6
progress or started during 2018–21) Glecaprevir/pibrentasvir 19 18.6
Sofosbuvir/velpatasvir without ribavirin 16 15.7
Sofosbuvir/velpatasvir with ribavirin 3 2.9
Sofosbuvir/velpatasvir/voxilaprevir 6 5.9
Sofosbuvir/ledipasvir with or without ribavirin 28 27.4
Ombitasvir/paritaprevir/ritonavir + dasabuvir 1 1.0
with or without ribavirin
Not recorded/ not stated 7 6.9
Reason for no HCV treatment (n = 159)
a
Treatment is currently planned 53 33.3
Recently acquired HCV – may clear 11 6.9
spontaneously
Recently diagnosed with HCV and/or re-engaged 2 1.3
in care
Lost to follow-up/switched clinics 1 0.6
Individual is not engaging in care 87 54.7
Individual is not contactable – e.g. no phone 26 16.4
Individual is considered unlikely to adhere well to 10 6.3
treatment
Individual likely to be at significant risk of 7 4.4
reinfection after treatment
Patient has complex clinical or treatment issues 6 3.8
Individual does not wish to be treated 22 13.8
Individual does not believe treatment is effective 2 1.3
Individual believes treatment would be toxic 3 1.9

Abbreviations: BHIVA, British HIV Association; HCV, hepatitis C; RNA, ribonucleic acid.
a
Multiple response.

assessment had been undertaken in 99 (35%) over the DISCUSSION

past 18 months, and HCC screening had been under-
taken in 14 out of 22 (63.6%) with severe fibrosis/cirrho- Our national audit has revealed that, while a sizeable pro-
sis. Other specific auditable outcomes included portion of people living with HIV have acquired HCV coin-
documentation of counselling regarding HCV transmis- fection, a relatively small proportion of people remain to be
sion and safe sex (recorded in 213/283, 75.3%), and treated. The reason for non-treatment was mainly related
annual/biannual anti-HBs screening within 3 years to lack of engagement in healthcare services. A greater
among those who were successfully immunized against understanding of this population, and the challenges/
HBV (recorded in 103/113, 91.2%). Overall, 211 (74.6%) barriers that remain for treatment, will support further
had been offered harm reduction support, 180 (63.6%) steps towards micro-elimination of HCV among people liv-
had a recorded enquiry/discussion about alcohol within ing with HIV in the UK. Our findings provide important
the past 9 months, 207 (73.1%) were recorded as being perspectives on the challenges of achieving micro-
vaccinated against or naturally immune to hepatitis A, elimination in a wider population than other previous stud-
and eight (2.8%) were surface antigen (HBsAg)-positive. ies conducted largely among MSM with HIV [14–20].
6 RAYA ET AL.

Due to the pandemic, a number of clinics changed and three times more likely to start treatment 6 months
their way of providing their service, distributing HCV post-randomization (OR = 3.11, 95% CI: 0.97–10.00) [32].
treatment, and decreasing human resources, with Moreover, in the UK setting, studies on an intervention
delayed tests and monitoring being unavoidable. Over to increase uptake of HCV testing and treatment
this time, many clinics were also forced to rapidly adapt (HepCATT) have shown a promising impact for a better
to new conditions whereby health systems and hospitals HCV cascade of care [33–35].
were primarily utilized for COVID-19 care; this required Another important finding was on reinfection treat-
many to change their arrangements for testing, monitor- ment, where most clinics were confident that they would
ing and delivery of treatment. A preliminary result from be able to offer repeat treatment to most cases if required.
an online survey conducted by WHO showed that 95% of In the UK, particularly England, HCV treatment is coor-
those involved in the provision of HIV, hepatitis and sex- dinated within Operational Delivery Networks (ODNs),
ually transmitted infection testing in 53 European coun- which manage treatment decisions and prescribing.
tries reported a decrease in testing in March–May 2020 Within England, the government provides free DAAs for
compared with the same period in the previous year [21]. those who are newly infected or reinfected [36]. In the
However, such changes to services may also lead to alter- other devolved nations, DAA prescriptions are provided
native solutions in care delivery, for example through the through routine clinical settings. In our clinic survey, we
combination of home testing and telehealth, multi-month were not able to explore further the underlying reasons
prescribing of ART, and development of close relation- for some clinics not being able to offer treatment for
ships of health services with commercial companies and those who were reinfected. However, the existing litera-
non-governmental organizations to support home deliv- ture suggests that provider-related barriers to HCV treat-
ery of medications [22–25]. ment, such as limited knowledge, lack of availability and
Our findings suggest that in most cases, lack of HCV communication issues, may exist for the treatment of
treatment was explained by a lack of engagement, the both new infections and reinfections [37, 38]. Peer sup-
individual's perceptions of treatment (and the need for port has been an important facilitator of the successful
this) or clinical judgment. Lack of engagement in HCV treatment and engagement with healthcare of people
care has been identified as a major barrier to HCV treat- with HIV and HCV [39–42]. Our audit suggested that
ment initiation in other studies [26, 27]; our study did 32 centres provided peer support for engagement, not
not permit a deeper understanding of the reasons for this, only for HIV but also for HCV. Although the current
and future qualitative studies would be helpful in this national standards for peer support in the UK do not spe-
regard. Clinical judgment from health workers has also cifically refer to support for HIV/HCV coinfection [43,
been identified as a treatment barrier in other studies 44], it is evident that peer support for HIV/HCV is
with provider reluctance to prescribe DAAs to individuals already being implemented by many care providers and
with a history of substance use because of a perceived the community.
concern about non-adherence, stigma against substance There are some limitations to our study which should
use, the risk of reinfection or abstinence policies required be acknowledged. First, the setting of the study is in the
by healthcare providers [28, 29]. Willingness to receive UK, where the number of new HIV diagnoses has been
treatment was affected by HCV knowledge status, with declining over the past 10 years and where the proportion
those with high HCV knowledge being more likely to be of people living with HIV with HCV coinfection requir-
very willing to receive treatment than those with lower ing treatment is relatively small. Our findings may there-
levels of HCV knowledge [30]. Therefore, it might be fore not be generalizable to other countries with larger
important to improve education about risks and benefits populations of people with HIV/HCV coinfection or dif-
of treatment for carers and patients. An evidence review ferent health system access. Secondly, compared with a
conducted by Public Health England (PHE) shows that previous BHIVA audit of HIV/HCV coinfection in 2009,
psychosocial and educational interventions to patients fewer clinics participated in the present audit (95 vs.
and nurses might improve adherence and treatment 140 clinics in 2009) [45]. Our audit was undertaken
uptake [31]. One of the studies included is a randomized within the context of a pandemic, and this may have
controlled trial which applied four-session nurse-led resulted in a reduction in participation by clinics which
behavioural intervention for HIV/HCV-coinfected indi- may, in turn, have introduced some bias, particularly if
viduals to overcome barriers of DAA treatment. Its find- participating clinics had managed to treat a greater pro-
ings demonstrate that individuals in the intervention portion of those with coinfection than non-participating
group were four times more likely to prescribe the treat- clinics. However, we believe that our response rate is
ment compared with the control group [odds ratio good given the constraints on people's time for comple-
(OR) = 3.85, 95% confidence interval (CI): 1.23–12.01] tion of audits. We also do not have data on whether only
HIV MEDICINE 7

specific populations – such as MSM or people living with F U N D I N G IN F O R M A T I O N

HIV – were included by each site. As a result of differ- RPR received funding from the Indonesian Endowment
ences in the epidemiology of HIV and HCV in the UK, Fund for Education (LPDP Indonesia Scholarship) during
together with the fact that not all sites provide care to the conduct of the study. GC is supported by NIHR
those with HIV/HCV coinfection, we cannot comment Research Professorship and BRC of Imperial College
on the representativeness of the sample included in the NHS Trust. The funder had no role in study design, data
case-note review. Finally, we did not collect information collection and analysis, decision to publish or preparation
on whether those who had completed treatment had of the manuscript.
experienced an sustained virologic response and on the
number of reinfections per person. Nevertheless, the CONFLICT OF INTEREST
information collected will still support the UK's contin- CAS reports funding from Gilead Sciences, ViiV Health-
ued micro-elimination efforts. care and Janssen-Cilag for membership of Data Safety
and Monitoring Boards, Advisory Boards and for prepara-
tion of educational materials. DC has received research
C O N C L U S IO N S grants from Gilead Sciences and ViiV Healthcare. FB has
received speaker and consultancy fees from Gilead
The small number of people with HIV/HCV coinfection Sciences.
in the UK should mean that it is possible to achieve our
HCV micro-elimination target. Our findings suggest that DA TA AVAI LA BI LI TY S T ATE ME NT
most people who are HCV antibody-positive have been The data that support the findings of this study are avail-
successfully treated. However, a small minority of people able from the corresponding author upon reasonable
continue to have detectable HCV RNA and, of these peo- request.
ple, a smaller group are not currently receiving treatment
or do not have treatment planned. The main reason for ORCID
continued lack of treatment in this group relates to prob- Reynie P. Raya https://orcid.org/0000-0002-4548-6820
lems with engagement in care, although a small minority Ranjababu Kulasegaram https://orcid.org/0000-0002-
of people also held negative views about treatment. The 0472-698X
COVID-19 pandemic has seen creative approaches to the Caroline A. Sabin https://orcid.org/0000-0001-5173-
way that clinics provide services to those with coinfec- 2760
tion. However, continued screening for HCV coinfection/
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