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A systematic review of community based hepatitis C treatment

  • Amanda J. Wade1, 2Email author,
  • Vanessa Veronese1, 2,
  • Margaret E. Hellard1, 2, 3 and
  • Joseph S. Doyle1, 3, 4
BMC Infectious DiseasesBMC series – open, inclusive and trusted201616:202

https://doi.org/10.1186/s12879-016-1548-5

Received: 27 November 2015

Accepted: 6 May 2016

Published: 16 May 2016

Abstract

Background

Hepatitis C virus (HCV) treatment uptake globally is low. A barrier to treatment is the necessity to attend specialists, usually in a tertiary hospital. We investigate the literature to assess the effect of providing HCV treatment in the community on treatment uptake and cure.

Methods

Three databases were searched for studies that contained a comparison between HCV treatment uptake or sustained virologic response (SVR) in a community site and a tertiary site. Treatment was with standard interferon with or without ribavirin, or pegylated interferon and ribavirin. A narrative synthesis was conducted.

Results

Thirteen studies fulfilled the inclusion criteria. Six studies measured treatment uptake; three demonstrated an increase in uptake at the community site, two demonstrated similar rates between sites and one demonstrated decreased uptake at the community site. Nine studies measured SVR; four demonstrated higher SVR rates in the community, four demonstrated similar SVR rates, and one demonstrated inferior SVR rates in the community compared to the tertiary site.

Conclusion

The data available supports the efficacy of HCV treatment in the community, and the potential for community based treatment to increase treatment uptake. Whilst further studies are required, these findings highlight the potential benefit of providing community based HCV care – benefits that should be realised as interferon-free therapy become available.

(PROSPERO registration number CRD42015025505).

Keywords

Hepatitis C Community-based Opioid substitution Treatment Models of care

Background

Each year in Australia less than 2 % of people infected with hepatitis C virus (HCV) are treated and globally treatment uptake rates are similarly low [1]. Barriers to HCV treatment include; difficulty in accessing a treatment service, not being offered treatment once in a treatment service and toxic pegylated interferon based treatment with poor efficacy [25]. Stigma is also a significant barrier to treatment in health care settings [6].

Fortunately the HCV treatment landscape is changing; pegylated interferon, ribavirin and protease inhibitor regimens of 6–12 months duration, which generate serious adverse effects in about 10 % of people and achieve cure in only 70 % are being replaced by all oral, well tolerated interferon free, direct acting antiviral (DAA) therapy, often for 12 weeks duration, with cure in more than 95 % [7, 8]. Although treatment tolerability and efficacy as a barrier to HCV treatment has been overcome, in the vast majority of countries HCV antiviral costs remain prohibitive. For DAA therapy to have maximum impact on the HCV epidemic, it must be affordable and accessible. To date, in most developed and many developing countries specialist physicians have provided HCV treatment, usually from tertiary hospital outpatient clinics. Such clinics often have rigid appointment scheduling and do not always provide multidisciplinary care. The reassuring safety profile and high efficacy of DAA therapy means HCV treatment could now be provided in a diverse range of clinical settings. HCV treatment could be provided in community-based clinics, including opioid substitution therapy (OST) clinics or using telehealth, with a variety of service providers including nurses, general practitioners and specialists. Increasing treatment accessibility may significantly improve HCV treatment uptake and cure, but a key issue is a lack of quality information about which model of care is most efficacious.

The Australian government has recently made a landmark decision to fund DAA therapy for every Australian infected with hepatitis C from 1st March 2016 [9]. In addition, a new model of care will be implemented in order to facilitate access to treatment. General practitioners will be able to prescribe DAA, albeit after authorization from a specialist [10]. As the new Australian model of care unfolds, it is timely to reflect upon the available evidence regarding hepatitis C treatment in the community.

To gain data that may inform HCV service delivery policy, we reviewed the literature to compare treatment uptake rates in community based treatment services with conventional tertiary services, and to compare sustained virological response (SVR) outcomes in patients treated with standard interferon with or without ribavirin, or pegylated interferon and ribavirin, in the community with patients treated in conventional tertiary settings.

Methods

Published research was scanned by formal searches of three electronic databases (Medline, EMBASE and CINAHL) from January 2000 to July 2015. Search terms included “hepatitis C”, “antiviral agents”, “patient care management” and “healthcare delivery”. The full search strategy is detailed in the Additional file 1. Citations were screened and evaluated using the established inclusion and exclusion criteria at the abstract level by two operators (AW and VV), and relevant studies were retrieved as full manuscripts. Articles were restricted to English language.
  1. 1.1.

    Eligibility criteria

     
Inclusion criteria were:
  1. (i)

    people with chronic HCV infection and;

     
  2. (ii)

    provision of treatment for hepatitis C in the community and;

     
  3. (iii)

    comparison with tertiary based services and;

     
  4. (iv)

    measuring and reporting either treatment uptake or SVR outcomes.

     

Treatment could include pegylated interferon and ribavirin, with or without DAA or interferon-free. Health care provider could be a specialist or general practitioner or nurse; the use of telehealth was permitted.

Exclusion criteria were defined as:
  1. (i)

    treatment of custodial populations or;

     
  2. (ii)

    treatment of HIV-HCV co-infected populations or;

     
  3. (iii)

    treatment of children or;

     
  4. (iv)

    treatment in residential facilities (i.e. inpatient rehabilitation) or;

     
  5. (v)

    modeling studies or;

     
  6. (vi)

    papers assessing patient or practitioner knowledge or attitudes or;

     
  7. (vii)

    papers published before 2000 because interferon ribavirin combination therapy was only licensed in 1998 and antiviral treatment was exclusively delivered in tertiary care.

     
  1. 1.2.

    Definitions and end-points

    A community service was defined as a medical service that was not a tertiary hospital or academic facility, including primary care clinics that may provide opiate substitution therapy (OST) and private practice. Treatment uptake was defined as proportion of HCV infected patients at service that received a prescription for HCV treatment. Cure was defined as sustained virologic response (SVR) at week 12 or 24 post cessation or completion of HCV treatment.

     
  1. 1.3.

    Study selection

    Using inclusion and exclusion criteria, identified abstracts were assessed for relevance by two researchers (AW and VV). Variations in citation assessment were resolved by a third reviewer (JD). Full text papers were then retrieved for review. If further data were required to classify a full text paper the authors were contacted. The following information was obtained for each article; authors, year of publication, country of origin, number of subjects, healthcare delivery structure, treatment uptake rate, SVR rate. For studies that measured SVR rate the following additional data was extracted: proportion with genotype 1 infection, proportion with HIV co-infection, prior treatment history and proportion with advanced fibrosis.

     

A narrative review of the included studies was performed. This review is registered with the PROSPERO database (registration number CRD42015025505).

Results

The flow diagram of the study analysis is shown in Fig. 1. The search generated 1499 citations, 413 duplicates were then deleted. Of the remaining 1086 citations, 967 were excluded based on the abstract. Full text articles were retrieved for 119 citations. A further 8 articles were included after citations searching. Thirteen of the 127 articles fulfilled the inclusion criteria. A summary of data from included articles is shown in Table 1, below.
Fig. 1

Flow diagram of study analysis

Table 1

Summary of included studies

Study

Year

Country

Design

Intervention

Facility

n

Rx uptake

SVR

n (%)

n (%)

Arora

2011

USA

Prospective cohort study of treatment outcome

Telehealth to support primary care (in community and prison)

Tertiary

146

 

84/146 (58)

Primary total (Prisoners)

261 (106)

 

152/261 (58)

Bruce

2012

USA

Randomised controlled trial of treatment uptake and outcome

Directly observed therapy in OST clinic vs self administered treatment in tertiary clinic

Tertiary

9

4/9 (44)

1/4 (33)

Primary

12

12/12 (100)

6/12 (75)

Chen

2014

Taiwan

Prospective cohort study of treatment outcome

Telecare

Tertiary

150

 

99/150 (66)

Telecare

148

 

102/148 (69)

Gigi

2013

Greece

Retrospective cohort study of treatment uptake

Rx in OST clinic

Tertiary

643 Ab+

276/643 (43)

 

Primary

204 Ab+

17/204 (8)

 

Jou

2013

USA

Retrospective cohort study of treatment outcome

Analysis of data by Rx site

Academic

1905

 

760/1905 (40)

Community

1165

 

455/1165 (39)

Kramer

2010

USA

Retrospective cohort study of treatment uptake

 

Specialist clinic

24,853

3537 (14)

 

Primary Care clinic

1929

251 (13)

 

Kuo

2015

Taiwan

Prospective cohort study of treatment uptake and outcome

Rx in community

Pre intervention

18

4/18 (22)

2/4 (50)

Post intervention

3/16 (19)

3/3 (100)

Moriarty

2001

New Zealand

Observational study of treatment uptake

Rx co-located at NSP site

Tertiary

51

1 (2)

 

Primary

4 (8)

 

Moussalli

2010

France

Observational study of treatment uptake

Rx in OST clinic

Pre intervention

337

2/337 (0.6)

 

Post intervention

85/335 (25)

37/85 (44)

Myers

2011

Canada

Observational study of treatment outcomes

 

Academic

133

 

79/133 (59)

Community

250

 

120/250 (48)

Nazareth

2013

Australia

Retrospective cohort study of treatment outcomes

Telehealth

Tertiary

528

 

311/528 (59)

Telehealth

50

 

36/50 (72)

Niederau

2014

Germany

Prospective cohort study of treatment outcome

Analysis of adherence to guidelines by Rx site

Hospital based

621

 

290/621 (47)

Private practice

3778

 

1744/3778 (46)

Rossaro

2013

USA

Retrospective cohort study of treatment outcomes

Telehealth

Tertiary

40

 

16/37 (43)

Telehealth

40

 

21/38 (55)

Rx treatment, OST opioid substitution therapy, Ab + HCV antibody positive

Five of the included studies were from the US, two were from Taiwan and there was one study each from Australia, New Zealand, Greece, France, Germany and Canada. The interventions to provide treatment in the community were diverse and included telehealth and treatment provision from primary care clinics, opioid substitution therapy (OST) clinics or needle exchange programs. Treatment consisted of pegylated interferon and ribavirin in all studies but for Moriarty [11] and Gigi [12], in which standard interferon with or without ribavirin was also included.

Studies which measured treatment uptake only (see Table 2)

Table 2

Summary of studies which investigated treatment uptake

Study

Study population and policy for initiating treatment (if included in publication)

Facility

N

OST (%)

Active illicit substance use

Treatment uptake

n (%)

Bruce

HCV infection +/− HIV

Attendance at OST clinic

Rx according to published guidelines and the same in both facilities

Tertiary

9

100

Opioid negative on urine toxicology in past 30 days

4 (44)

Primary

12

100

Opioid negative on urine toxicology in past 30 days

12 (100)

Gigi

HCV antibody positive

Attended Liver clinic or OST clinic

Policy for Rx initiation not published

Tertiary

643

0

Nil

276 (43)

Primary

204

100

Nil

17 (8)

Kramer

HCV infection

Designated Primary Care Provider

Majority of care from one Veterans Affairs facility

Rx indicated if more than portal fibrosis and no contraindications (including no active illicit drug use)

Specialist clinic

24,853

N/P

N/P

3537 (14)

Primary clinic

1929

N/P

N/P

251 (13)

Kuo

HCV antibody positive

Participation in screening program

Pre-intervention Rx if: ALT >40 (once) and > F1 or HCV RNA positive

Post intervention Rx if ALT >80 (twice) and > F1

Pre intervention

18

N/P

N/P

4 (22)

Post intervention

N/P

N/P

3 (19)

Moriarty

HCV infection

Attendance at outreach clinic

Policy for Rx initiation not published

Tertiary

51

N/P

N/P

1 (2)

Primary

N/P

N/P

4 (8)

Moussalli

HCV infection

Attendance at OST Primary healthcare facility

Rx if > F2 fibrosis

Pre-intervention

337

N/P

N/P

2 (0.6)

Post intervention

N/P

N/P

85 (25)

OST opioid substitution therapy, N/P not provided, Rx treatment

Two studies investigated the outcome of treatment provision in opioid substitution clinics, and had different results. Moussalli et al. noted an increase in treatment uptake when provided at an OST clinic. Before treatment was available in the OST clinic two of 337 patients had commenced treatment for HCV. After treatment was made available in the OST clinic 85 patients commenced therapy, and of those patients 37 (44 %) achieved an SVR [13]. However, in a retrospective cohort study in Greece, only 17 of 204 HCV antibody positive patients (8 %) commenced treatment in an OST setting, compared to 276 of 643 patients (43 %) in a tertiary liver unit [12]. Of note, few HCV antibody positive patients in the OST clinic had HCV RNA testing performed - 33 of 204, of which 28 were positive. In comparison, 498 of the 643 HCV antibody positive patients in the tertiary liver unit were known to be HCV RNA positive.

A retrospective study of treatment uptake in a needle and syringe exchange program (NSEP) centre in New Zealand found of 51 HCV infected patients, four commenced treatment at the needle exchange centre, whilst only one patient commenced treatment at the hospital [11].

A large retrospective study in the US demonstrated that treatment uptake in primary care clinics 251 of 1929 patients (13 %) was similar to treatment uptake in specialist clinics 3537 of 24,853 (14 %) [14].

Studies which measured treatment outcome only (see Table 3)

Table 3

Summary of trials which investigated treatment outcome

Study

Facility

N

Age (years)

Gender (% male)

Genotype 1 (%)

HIV infected n (%)

Prior treatment

Fibrosis assessment

Fibrosis result

SVR

Mean or %

n (%)

Arora

Tertiary

146

45

45

57

0

Naive

APRI

0.938

84 (58)

Telehealth

261

42

73

56

0

0.935

152 (58)

Bruce

Tertiary

9

43

67

67 (G1&4)

3 (33)

N/P

Biopsy (G1 only)

F4 33 %

1 (33)

Primary

12

40

42

67 (G1&4)

3 (25)

F4 25 %

6 (75)

Chen

Tertiary

150

52

N/P

58

0

Naive

 

N/P

99 (66)

Primary

148

47

N/P

61

0

N/P

102 (69)

Jou

Academic

1905

48

59

100

0

Naive

Biopsy

F3/4 10 %

760 (40)

Community

1165

47

61

100

0

F3/4 11 %

455 (39)

Kuo

Preintervention

18

57

33

N/P

N/P

N/P

 

N/P

2 (50)

Post intervention

3 (100)

Myers

Academic

133

46

70

49

0

Naïve & experienced

Biopsy

F4 14 %

79 (59)

Community

250

46

64

55

0

F4 10 %

120 (48)

Nazareth

Tertiary

528

43

65

N/P

N/P

Naïve & experienced

Biopsy or Hepascore

F4 19 %

311 (59)

Telehealth

50

46

50

60

N/P

Hepascore

F4 20 %

36 (72)

Niedaerau

Hospital based

621

N/P

N/P

100

N/P

N/P

 

N/P

290 (47)

Private practice

3778

N/P

N/P

100

N/P

N/P

1744 (46)

Rossaro

Tertiary

40

54

55

65

0

Naive

Biopsy

F4 45 %

16 (43)

Telehealth

40

51

48

65

0

F4 28 %

21 (55)

N/P not provided

Three cohort studies compared SVR rates obtained by standard care in a tertiary hospital with SVR rates obtained using telehealth (video-conferencing) to populations with poor access to specialist care i.e. in rural or remote areas, or prison. A large prospective study in the US demonstrated no difference in SVR between patients treated in tertiary care and patients treated by their primary care clinician with telehealth support (58 % in both groups) [15]. A smaller retrospective study in the US demonstrated similar results, with 43 % of tertiary patients obtaining an SVR compared to 55 % patients treated via telehealth [16]. A retrospective Australian study found 72 % of telehealth treated patients had an SVR compared to 59 % of tertiary treated patients [17]. All three studies demonstrate SVR rates achieved in telehealth care were similar or higher when compared to SVR rates achieved in tertiary care.

Chen et al., performed a study in which patients selected treatment delivered via telephone consultations provided from a health communication center, or treatment delivered conventionally in a hospital outpatient clinic, and detected no difference in SVR outcomes [18].

Three observational studies examined SVR outcomes of community based treatment. Jou retrospectively analysed results from a randomized control drug trial according to treatment site. SVR outcome were the same in the academic (40 %) and the community (39 %) sites [19]. Niederau also found similar SVR outcomes between treatment provided in a hospital with 290 of 621 patients (47 %) attaining SVR, and 1744 of 3778 patients (46 %) attaining SVR in private practice [20]. However, in an observational study in Canada lower rates of SVR were seen in community settings 120 of 250 patients (48 %), when compared to academic centres, 79 of 133 patients (59 %) [21]. Further analysis demonstrated the difference was due to lower SVR rates in patients infected with genotype 1 treated in the community.

Studies which measured treatment uptake and outcome (see Tables 2 and 3)

Bruce et al. conducted a randomized clinical trial in which subjects on methadone in an OST clinic were randomized to receive modified directly observed treatment at the OST clinic or standard of care therapy at a tertiary liver clinic. Subjects treated at the OST clinic had directly observed therapy (DOT) for methadone, pegylated interferon and morning ribavirin doses, but self administered evening ribavirin. All 12 patients randomized to the OST clinic started treatment and six of eight patients (75 %) eligible to be assessed for SVR achieved SVR. In comparison four of the nine patients (44 %) randomized to standard of care commenced treatment and one of three patients (33 %) eligible to be assessed for SVR achieved an SVR [22].

A small Taiwanese study showed similar treatment uptake rates with tertiary care, four of eighteen patients (22 %) compared to three of 16 patients (19 %) commencing treatment when it was made available in the community [23]. SVR was achieved in two of four patients (50 %) in the tertiary facility and three of three patients (100 %) in the community facility.

Discussion

This systematic review has identified publications, which contain a comparison between HCV treatment uptake rates or SVR outcomes in community and tertiary treatment services. Of the thirteen publications included, only one was a randomized controlled trial and the remainder were observational studies. The interventions that resulted in HCV treatment provision in the community were diverse, and included; telehealth, integrated HCV services in OST clinics or NSEP services, private medical practice and outreach services staffed by specialists or nurses.

Of the six studies that measured treatment uptake as an outcome (see Table 2), three demonstrated an increase in uptake at the community site [11, 13, 22]. Interestingly, two of these studies were conducted in OST clinics, and the third in a NSEP service. Two studies demonstrated similar treatment uptake rates between the community and tertiary services [14, 23]. The large study by Kramer et al. investigated the treatment uptake within the Veterans Affairs Healthcare in the United States according to whether treatment was provided from a primary care provider clinic or a specialist clinic. It is not known what proportion of the primary care provider clinics may have been OST providers as well. One study demonstrated decreased treatment uptake at the community site [12]. The authors attributed this difference to a difficulty in collaboration between OST staff and hospital based specialists.

The factors contributing to increased treatment uptake in the community sites varied according to the study; provision of non invasive fibrosis assessment (Fibrotest-Actitest) (Mousalli), multidisciplinary services (Mousalli, Moriarty, Bruce), modified directly observed therapy (Bruce) and gaining trust (Moriarty), led to improved management of HCV in the community setting.

Of the nine studies that measured SVR as an outcome (see Table 3), four demonstrated higher SVR rates in the community group [16, 17, 22, 23]. Possible reasons for this include that the community services were more convenient for the patients and offered a “one stop shop” where multiple needs could be met, or that HCV treatment was integrated into a developed patient-provider relationship. Another explanation is that the availability of multidisciplinary services may have helped mitigate factors associated with poor adherence or SVR outcomes in PWID such as unstable housing, poor social functioning and ongoing drug use [24]. Four studies demonstrated similar outcomes between the two treatment settings [15, 1820]. One study from Canada in which 250 patients were treated in the community and 133 in an academic centre, demonstrated lower SVR rates in patients treated in the community [21]. The difference was due to SVR outcomes in genotype one patients only. Patient characteristics including level of fibrosis, rates of dose modification and treatment cessation for genotype one infected patients were similar in the community and academic sites, and an explanation for the difference in SVR between treatment sites was not apparent.

Modelling studies indicate that treatment uptake is the major limiting factor to substantial reductions in disease burden. Current treatment rates in Australia of 3 per 1000 PWID annually would need to be scaled up to 40 per 1000 PWID annually to halve HCV prevalence by 2030. [25]. The advent of DAA therapy has made the elimination of HCV a tangible concept since treatment is simple and well tolerated, but for this to be achieved a significant change in service delivery would be required, and has been undertaken.

Nine of ten studies reporting SVR outcomes demonstrated similar or superior SVR rates were achieved in the community. Further, findings in this review suggest that decentralising HCV services and providing HCV treatment in the community, particularly OST clinics, may increase treatment uptake. Numerous cohort studies conducted in OST clinics indicate that HCV treatment in this setting can be successful, even in the peginterferon based treatment era [19, 26, 27]. The key components of successful HCV treatment delivery in the community need to be identified, to inform policy and ensure that integrated services are adequately resourced.

This review was limited by the lack of published data that compares outcomes of HCV treatment delivered in the community with treatment delivered in conventional tertiary settings. Some studies included in the review have a small number of participants and therefore lack statistical power. There was only one small randomised controlled trial comparing community and tertiary based treatment, and this study also provided DOT to the patients in the community arm, rendering the relative contribution of both interventions difficult to assess. This review investigated interferon based HCV treatment and therefore the findings may not be applicable to HCV treatment with DAA. A large randomised controlled trial addressing the effect of community provision of HCV DAA treatment – the Prime Study based in Melbourne, Australia – is underway (clinicaltrials.gov NCT02555475). It is likely that any treatment outcome difference between hospital and community care may become less pronounced as treatment becomes easier with DAA therapy.

Conclusion

In conclusion, this review demonstrates that the limited data available supports the safety of peginterferon based HCV treatment in the community, and the potential for community based treatment to increase treatment uptake. The paucity of high quality data available to assess the effect of HCV treatment in the community on HCV treatment uptake is striking. This variable is a key component in the hepatitis C cascade of care, and further studies are warranted to clarify how best to structure HCV service delivery in the era of DAA.

Ethics approval and consent

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

The search strategy used to generate data, which supports the conclusions of this article, is included as an Additional file 1.

Abbreviations

DAA: 

direct acting antivirals

DOT: 

directly observed therapy

HCV: 

hepatitis C virus

NSEP: 

needle and syringe exchange program

OST: 

opioid substitution therapy

PWID: 

people who inject drugs

SVR: 

sustained virologic response

Declarations

Acknowledgements

The authors gratefully acknowledge the contribution to this work of the Victoria Operational Infrastructure Support Program funding for the Burnet Institute.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Centre for Population Health, Burnet Institute
(2)
School of Public Health and Preventive Medicine, Monash University
(3)
Department of Infectious Diseases, The Alfred Hospital
(4)
Department of Medicine, University of Melbourne

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© Wade et al. 2016