Outcomes of hepatitis C screening programs targeted at risk groups hidden in the general population: a systematic review

Zuure, Freke R; Urbanus, Anouk T; Langendam, Miranda W; Helsper, Charles W; van den Berg, Charlotte HSB; Davidovich, Udi; Prins, Maria

doi:10.1186/1471-2458-14-66

Table 3 Integrated screening programs at general practitioner (GP) clinics

From: Outcomes of hepatitis C screening programs targeted at risk groups hidden in the general population: a systematic review

Program characteristics									Program outcomes
First author, year of publication	Calendar year of data collection	Population	Country and HCV prevalence according to CDC[23]	Setting of screening	Duration of screening program	Other tests	Pre-screening selection	Media activities	Screening uptake and anti-HCV prevalence (95% CI)	Risk profile of identified HCV cases/Risk factors associated with HCV	Follow-up of HCV-infected individuals
Monnet et al. 2000, 2009 [70]	1997-1998	Patient of GP clinics, health centres, occupational physicians, prison health service, public laboratories	France (1.1%): Le Doubs	GP clinics, health centre, occupational physicians, prison health service, public laboratories	1 year	None	Yes, no previous positive HCV serology, and at least having one risk factor: transfusion before 1991, (ex-)IDU, (ex-)snorting cocaine, tattoo, HCV diagnosis in living environment	Yes	Scr. uptake: 82.5% (782/948) Prevalence: 4.0% (31/782; 95% CI: 2.8-5.6)*	Multivariable regr. analysis: - Age 30+ - Drug use	70.9% (22/31) attended the hepatologist for HCV RNA testing. Of those who tested HCV RNA positive, 10 had elevated ALAT of which 8 had a biopsy. Based on the results, 5 were indicated for treatment (no results reported).
Monnet et al. 2000, 2009 [70]	1997-1998		France (1.1%): Le Doubs		1 year	None		Yes		Multivariable regr. analysis: - Age 30+ - Drug use	Outcomes: RNA rate: 86.4% (19/22) Start treatment: NR SVR: NR
Anderson et al. 2009 [71]	2003-2004	GP patients aged 30–54 yrs	Scotland (1.1%): socio-economically deprived area of Glasgow	GP clinics (intervention clinic and comparison clinic)	6 months	None	No; in intervention practice all individuals aged 30–54 yrs who attended non-urgent appointments were offered HCV screening. In comparison practice, no intervention was carried out.	Eligible patients in intervention practice received information leaflet	Scr. uptake: Intervention clinic: 27.8% (117/421) Comparison clinic: not applicable Prevalence: Intervention clinic: 12.8% (15/117; 95% CI: 7.9-20.0) Comparison clinic: No individuals were tested during study period.**	Multivariable regr. analysis - History of IDU	HCV RNA positive patients (n = 11) were referred to a specialist and all attended ≥1 appointment. Four years later, 8 were lost to follow-up, 2 started treatment, and 1 achieved an SVR. Outcomes: RNA rate: 73.3% (11/15) Start treatment: 18.2% (2/11) SVR: 50.0% (1/2)
Pauti et al. 2008 [44]	2007	People with poor access to health care, mostly migrants	France (1.1%): Saint-Denis and Paris areas	Health care and advice centers of Médecins du Monde^b	4 years, but data from 1 year are reported	HIV, HBV	No	No	Scr. uptake: NR Prevalence: 5.9% (70/1196; 95% CI: 4.7-7.3)**	Listed risk factors: - North and Middle Africa - Sub-Saharan Africa - Eastern Europe	The objective of the project was to offer full access to treatment, but actual results are not reported
Pauti et al. 2008 [44]	2007	People with poor access to health care, mostly migrants	France (1.1%): Saint-Denis and Paris areas	Health care and advice centers of Médecins du Monde^b	4 years, but data from 1 year are reported	HIV, HBV	No	No			Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Uddin et al. 2010 [46]^a	NR	GP patients	UK (1.1%): East London, West London, Walsall, Sandwell, Bradford	GP clinic (and at community centers, see Additional file 1: Table S1)	NR	HBV	Yes, immigrants from the Indian sub-continent (India, Bangladesh or Pakistan)	No	Scr. uptake: NR	Not applicable	Not applicable
Uddin et al. 2010 [46]^a	NR	GP patients			NR	HBV		No	Prevalence: 0% (0/171; 95% CI: 0–2.19 )**	Not applicable	Not applicable
Kallman et al. 2010 [47]^a	NR	GP patients	USA (1.9%): Northern Virginia	GP clinic (and general health screening at Asian health fairs, see Additional file 1: Table S1)	NR	HBV	Yes, Vietnamese	NR	Scr. uptake: NR Prevalence: 1.2% (3/245; 95% CI: 0.4-3.5) at GP clinic**	Univariable regr. analysis: - Elevated AST	Patients were seen by their primary care givers for further management, or referred for further follow-up and treatment (no results reported).
Kallman et al. 2010 [47]^a	NR	GP patients	USA (1.9%): Northern Virginia		NR	HBV	Yes, Vietnamese	NR		Univariable regr. analysis: - Elevated AST	Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Ouzan, D, 2003 [72]	2000	GP patients aged over 18 years	France (1.1%): Alpes-Maritimes district	GP clinic	1 month	None	Yes: unknown HCV serology status, and at least one risk factor: blood transfusion before 1991, injecting or nasal DU, incarceration. Previously diagnosed HCV positives that visited the GP in the screening period were also followed-up.	No	Scr. uptake: 66.0% (233/353) Prevalence:3.9% (9/233; 95% CI: 2.0-7.02) 9 were newly identified through screening; 229 were found with a previous diagnosis**	NR for newly identified	Patients were followed-up by their GP, referred to a specialist, or a hospital unit.
											Follow-up data are reported for newly and previously diagnosed patients together and available for 159/238. HCV RNA test results were known for n = 106, and 82 were HCV RNA positive. A liver biopsy was performed in 62, of which 31 received treatment. Treatment was effective for 10, fairly effective for 12, and ineffective for 7.
											Outcomes: RNA rate: 77.4% (82/106) Start treatment: 37.8% (31/82) SVR: NR
Josset et al. 2004 [73]	1997	GP patients aged 18–70 yrs	France (1.1%): Haute-Normandie	GP clinic	10 days	None	Yes, no previous HCV serology performed, and at least one of the traditional risk factors present ^c	No	Scr. uptake: 72.7% (3550/4883) Prevalence: 1.4% (49/3550; 95% CI: 1.0-1.8%)**	An evaluation of screening strategies based on risk factor data showed that screening those with a history of blood transfusion or drug use appeared to be the most efficient approach.	NR Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Pradat et al. 2001 [74]	1997	GP patients aged 18–69 yrs	France (1.1%): Lyon area	GP clinics	6 months; each GP clinic offered HCV screening for 5 days	None	No	NR	Scr. uptake: 59.0% 6876/11646 Prevalence: 0.4% (30/6876; 95% CI: 0.3-0.6)***	Listed risk factors: - History of IDU - Transfusion <1990 - Other risk factors	NR Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Altman et al. 1999 [75]	1997	GP patients	France (1.1%): Val-de-Marne and Hauts-de-Seine	GP clinics	2 weeks	None	Yes, no previous HCV serology performed, and a history of IDU or transfusion before 1991	No	Scr. uptake:	NR	NR
									Transfusion group: 76.9% (226/294) History of IDU group: 50.0% (13/26)		Outcomes: RNA rate: NR Start treatment: NR SVR: NR
									Prevalence: Transfusion group: 3.1% (7/226, 95% CI: 1.5-6.3) History of IDU group: 30.8% (4/13; 95% CI: 12.7-57.6)*		Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Helsper et al. 2010 [76]	2007-2008	GP patients	Netherlands (1.1%): Amersfoort and Apeldoorn	GP clinics in intervention region with primary care practice support, and GP clinics in control region without practice support	4 months	None	Yes, individual risk estimation by GP	Yes	Scr. uptake: NR	Data not available	NR
Helsper et al. 2010 [76]	2007-2008	GP patients	Netherlands (1.1%): Amersfoort and Apeldoorn		4 months	None	Yes, individual risk estimation by GP	Yes	Prevalence: Intervention: 1.7% (3/172; 95% CI: 0.6-5.0) Control: 0.8% (1/118; 95% CI: 0.04-4.6)**	Data not available	Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Sahajian et al. 2004 [77]	2000-2001	GP, private practitioners, and specialist patients	France (1.1%): Lyon area	GP clinics Intervention: A campaign including training aimed at GPs was designed to improve screening practices. The campaign also reached the public. Comparison: Data were compared to the 12-months period preceding the campaign.	12 months	None	Yes, history of IDU, blood products before 1991, or elevated serum transaminase levels	Yes	Scr. uptake: NR	NR	NR
Sahajian et al. 2004 [77]	2000-2001	GP, private practitioners, and specialist patients	France (1.1%): Lyon area		12 months	None		Yes	Prevalence: Intervention: 1.73% (276/15952; 95% CI: 1.53-1.94) Comparison: 1.67% (231/13799; 95% CI:1.47-1.90)**	NR	Outcomes: RNA rate: NR Start treatment: NR SVR: NR
Roudot-Thoraval et al. 2000 [78]	1997-1998	GP patients aged 6–85 years	France (1.1%): Le Doubs and n^o 6 d’Ile-de-France	GP clinics Intervention 1: GPs asked their patients for risk factors for HCV and offered screening to those at risk. Intervention 2: Posters and leaflets in GPs waiting rooms, motivating those with a risk to discuss testing with their GP.	15 months	None	Yes, several risk factors (not all are listed), among which a history of IDU, transfusion, tattoo, HCV in social environment	Yes (intervention 2)	Scr. uptake: NR Prevalence: Intervention 1: 5.7% (15/261; 95% CI: 3.51-9.26) Intervention 2: 4.4% (10/228; 95% CI: 2.40-7.88)**	Listed risk factors: - History of IDU - Transfusion before 1991 - Elevated ALT or symptoms - Tattoo - Other	NR Outcomes: RNA rate: NR Start treatment: NR SVR:

Note: CI = confidence interval; NR = not reported; IDU = injecting drug use; HCV = hepatitis C virus; HBV = hepatitis B virus; HIV = human immunodeficiency virus; ALT = alanine aminotransferase; AST = aspartate aminotransferase; SVR = sustained virological response.
*HCV-antibody prevalence is considered suboptimal (data were collected before 1994 when sensitivity/specificity of tests was not optimal, or reactive HCV-antibody test results were not confirmed by immunoblot).
**The reliability of the reported HCV-antibody prevalence is undecided (data were collected after 1993, but the diagnostic tests are unspecified, or other than described below, or dried blood spots or oral fluid samples were used).
***HCV-antibody prevalence is considered valid; data were collected after 1993, and reactive HCV-antibody test results were confirmed by second or higher generation immunoblot assays from Ortho, Chiron, Novartis (RIBA), Innogenetics (LiaTek), Pasteur (DECISCAN HCV), Genelabs Diagnostics (HCV BLOT), or Mikrogen (recomBlot HCV IgG 2.0).
^aThese programs combined a nonintegrated screening approach with integrated screening at the GP clinic (see Additional file 1: Table S1). Here only results of the integrated screening are presented.
^bMédecins du Monde (‘Doctors of the World’) is an international humanitarian organization providing medical care to vulnerable populations.
^cTransfusion before 1991, history of drug use, history of gastroscopy, contact with HCV infected person (spouse or other family member, occupational exposure, active or former imprisonment, history of invasive procedures (catheterism, fluid aspiration/cytology, biopsy), history of colonoscopy, history of surgery.

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