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Hepatitis C: an epidemiological review M. I. Memon 1 and M. A. Memon 2 1 Department of Community Health, Guild NHS Trust, Honorary Lecturer Lancashire Post Graduate Medical School, Preston and Professor of Ethnicity and Community Health, Bolton Institute, Bolton, and 2 Department of Surgery, Queen’s Medical Centre, Nottingham, UK Received March 2001; accepted for publication July 2001 EPIDEMIOLOGY OF HEPATITIS C VIRUS Hepatitis C virus (HCV), a positive strand RNA virus which is related to flavi and pestiviruses family, was first identified in the USA in 1989 as a major causative agent of post trans- fusion non-A, non-B hepatitis [1]. According to WHO esti- mates, approximately 3% of the world population, or about 170 million people, may be infected with hepatitis C virus [2,3]. In the USA, antibodies to HCV are encountered in between 0.1% to 1.8% of the general population (Table 1). In healthy volunteer blood donors the incidence of HCV in the USA varies between 0.17% to 1.4% and in the UK is 0.35% (Table 2). However in other parts of the world the incidence HCV infection both in the general population and blood donors may be much higher (Tables 1 and 2). Although the annual incidence of newly acquired HCV has declined substantially in the USA, from 180 000 to 30 000 in the past decade, there still remains a large reservoir of chronically infected Americans (estimated to be 3.9 million) who can serve as a source of transmission to others and who are at risk of severe consequences of chronic liver disease [4]. HCV infections leads to acute hepatitis in 20% of cases and chronic hepatitis in 50% of cases, 20% of who develop cir- rhosis [5,6]. There is also a strong relationship between HCV and hepatocellular carcinoma [7,8]. HCV is transmitted primarily by exposure to infected blood. However, in up to 50% of cases no recognizable transmission factor/route could be identified [9]. Therefore, a number of other routes of transmission such as sexual or household exposure to an infected contact are postulated but not widely accepted. This is because conflicting data has emerged regarding the presence of HCV in body fluids other than blood. Some authors have found total absence of the virus in sperm, saliva, vaginal secretions and other body fluids [9]. However, others have documented the presence of HCV-specific antigens in semen of infected individuals [10,11]. Risk factors for HCV infection include intravenous drug abuse, haemodialysis, transfusion of blood products, tattooing, high sexual behaviour, exposure to healthcare and organ transplants from HCV-positive donors and use of blood contaminated straws for cocaine snorting [12,13]. As far back as 1981, two separate American studies showed that there was increased risk of acquiring post-transfusion non-A, non-B infection (PTH-NANB) following blood trans- fusion if the donors have elevated ALT levels compared with normal ALT levels [14–16]. Furthermore the exclusion of blood donors with antibodies to the hepatitis B core antigen was found to prevent another 20–30% of the PTH-NANB, Abbreviations: HCC, hepatocellular carcinoma; HCV, hepatitis C virus; PTH-NANB, post-transfusion non-A, non-B infection. Correspondence: Professor M. I. Memon, Oakwood, Whitehall Road, Darwen, Lancashire BB3 2LH, UK. E-mail: [email protected] Journal of Viral Hepatitis, 2002, 9, 84–100 Ó 2002 Blackwell Science Ltd SUMMARY. The aim of the study was to analyse the current literature regarding the mode of transmission of HCV and its global prevalence in different groups of people. A systematic review of the literature on the epidemiology of hepatitis C from 1991 to 2000 using computerized bibliographic data- bases which include Medline, Current Content and Embase. The prevalence of hepatitis C virus (HCV) varies tremen- dously in different parts of the world, with the highest inci- dence in the Eastern parts of the globe compared with the Western parts. Furthermore, certain groups of individuals such as intravenous drug users are at increased risk of ac- quiring this disease irrespective of the geographical location. Although the main route of transmission is via contamin- ated blood, curiously enough in up to 50% of the cases no recognizable transmission factor/route could be identified. Therefore, a number of other routes of transmission such as sexual or household exposure to infected contacts have been investigated with conflicting results. Hepatitis C in- fection is an important public health issue globally. Better understanding of routes of transmission will help to combat the spread of disease. In order to prevent a world wide epidemic of this disease, urgent measures are required to (i) develop a strategy to inform and educate the public re- garding this disease and (ii) expedite the efforts to develop a vaccine. Keywords: epidemiology, etiology, hepatitis C, prevention and control, risk factors, statistics and numerical data.
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Page 1: Hepatitis C: an epidemiological review

Hepatitis C: an epidemiological reviewM. I. Memon1 and M. A. Memon2 1Department of Community Health, Guild NHS Trust, Honorary Lecturer Lancashire Post

Graduate Medical School, Preston and Professor of Ethnicity and Community Health, Bolton Institute, Bolton, and 2Department of Surgery, Queen's

Medical Centre, Nottingham, UK

Received March 2001; accepted for publication July 2001

EPIDEMIOLOGY OF HEPATITIS C VIRUS

Hepatitis C virus (HCV), a positive strand RNA virus which is

related to ¯avi and pestiviruses family, was ®rst identi®ed in

the USA in 1989 as a major causative agent of post trans-

fusion non-A, non-B hepatitis [1]. According to WHO esti-

mates, approximately 3% of the world population, or about

170 million people, may be infected with hepatitis C virus

[2,3]. In the USA, antibodies to HCV are encountered in

between 0.1% to 1.8% of the general population (Table 1).

In healthy volunteer blood donors the incidence of HCV in

the USA varies between 0.17% to 1.4% and in the UK is

0.35% (Table 2). However in other parts of the world the

incidence HCV infection both in the general population and

blood donors may be much higher (Tables 1 and 2).

Although the annual incidence of newly acquired HCV has

declined substantially in the USA, from 180 000 to 30 000

in the past decade, there still remains a large reservoir of

chronically infected Americans (estimated to be 3.9 million)

who can serve as a source of transmission to others and who

are at risk of severe consequences of chronic liver disease [4].

HCV infections leads to acute hepatitis in 20% of cases and

chronic hepatitis in 50% of cases, 20% of who develop cir-

rhosis [5,6]. There is also a strong relationship between HCV

and hepatocellular carcinoma [7,8].

HCV is transmitted primarily by exposure to infected

blood. However, in up to 50% of cases no recognizable

transmission factor/route could be identi®ed [9]. Therefore, a

number of other routes of transmission such as sexual or

household exposure to an infected contact are postulated but

not widely accepted. This is because con¯icting data has

emerged regarding the presence of HCV in body ¯uids other

than blood. Some authors have found total absence of the

virus in sperm, saliva, vaginal secretions and other body

¯uids [9]. However, others have documented the presence of

HCV-speci®c antigens in semen of infected individuals

[10,11]. Risk factors for HCV infection include intravenous

drug abuse, haemodialysis, transfusion of blood products,

tattooing, high sexual behaviour, exposure to healthcare

and organ transplants from HCV-positive donors and use of

blood contaminated straws for cocaine snorting [12,13].

As far back as 1981, two separate American studies showed

that there was increased risk of acquiring post-transfusion

non-A, non-B infection (PTH-NANB) following blood trans-

fusion if the donors have elevated ALT levels compared with

normal ALT levels [14±16]. Furthermore the exclusion of

blood donors with antibodies to the hepatitis B core antigen

was found to prevent another 20±30% of the PTH-NANB,

Abbreviations: HCC, hepatocellular carcinoma; HCV, hepatitis C

virus; PTH-NANB, post-transfusion non-A, non-B infection.

Correspondence: Professor M. I. Memon, Oakwood, Whitehall

Road, Darwen, Lancashire BB3 2LH, UK.

E-mail: [email protected]

Journal of Viral Hepatitis, 2002, 9, 84±100

Ó 2002 Blackwell Science Ltd

SUMMARY. The aim of the study was to analyse the current

literature regarding the mode of transmission of HCV and its

global prevalence in different groups of people. A systematic

review of the literature on the epidemiology of hepatitis C

from 1991 to 2000 using computerized bibliographic data-

bases which include Medline, Current Content and Embase.

The prevalence of hepatitis C virus (HCV) varies tremen-

dously in different parts of the world, with the highest inci-

dence in the Eastern parts of the globe compared with the

Western parts. Furthermore, certain groups of individuals

such as intravenous drug users are at increased risk of ac-

quiring this disease irrespective of the geographical location.

Although the main route of transmission is via contamin-

ated blood, curiously enough in up to 50% of the cases no

recognizable transmission factor/route could be identi®ed.

Therefore, a number of other routes of transmission such as

sexual or household exposure to infected contacts have

been investigated with con¯icting results. Hepatitis C in-

fection is an important public health issue globally. Better

understanding of routes of transmission will help to combat

the spread of disease. In order to prevent a world wide

epidemic of this disease, urgent measures are required to (i)

develop a strategy to inform and educate the public re-

garding this disease and (ii) expedite the efforts to develop a

vaccine.

Keywords: epidemiology, etiology, hepatitis C, prevention

and control, risk factors, statistics and numerical data.

Page 2: Hepatitis C: an epidemiological review

Table 1 Global Prevalence of Anti-HCV in the general population of different geographical locations

Author(s) Year(s)

Geographical

location

Type of

subjects

Number

tested

Percentage

positive (%)

Fairley et al. [127] 1990 Australia Antenatal women 252 0.4

Garner et al. [128] 1997 Australia Pregnant women 1537 1.1

Tao et al. [129] 1991 China Normal subjects 438 2.1

Darwish et al. [130] 1996 Egypt Nonrandom selected

residents

155 51

Dubois et al. [131] 1997 France Randomly selected

individuals undergoing

routine medical check-up

in social security

medical centres

6283 1.1

Richard-Lenoble et al. [132] 1995 Gabon Cross-sectional study 109 22

Martinson et al. [133] 1996 Ghana Cross-sectional children

and adolescence study

803 5.4

Jeannel et al. [134] 1998 Guinea Urban and rural population 459 1.1

Burkina Faso 965 4.9

Nekata et al. [135] 1994 Ho Chi Minh Pregnant women and

tropical disease patients

292 3.8

Chan et al. [136] 1992 Hong Kong Health exhibition attendants 382 0.5

Reddy et al. [137] 1995 India Random sample 91 5.5

Marranconi et al. [138] 1994 Italy Pregnant women 5672 0.7

Osella et al. [139] 1997 Italy Random sample of

population of a small town

in southern Italy

1969 26

Guadagnino et al. [140] 1997 Italy General population of a town 1352 14.4

Tajima et al. [141] 1991 Japan Normal subjects 971 5.1±49

Tibbs et al. [142] 1991 Kiribati Tropical communities 385 4.8

Vanuatu 138 <1

Zaire 173 6.4

Kim et al. [143] 1992 Korea Normal subjects > 20-year-old 4917 1.7

Morvan et al. [144] 1994 Madagascar Healthy subjects 643 3.3

Ahmed et al. [145] 1998 Malawi Descriptive study, Pregnant

women (both HIV positive

and negative)

150 16.5

Miller et al. [146] 1993 New Zealand Maori and Paci®c islanders 3483 0.49

Perez et al. [147] 1996 Nicaragua Cross-sectional study 399 0

Oshita et al. [148] 1993 Osaka Normal subjects 298 2

Luby [149] 1997 Pakistan Randomly selected subjects 309 6.5

Baumgart et al. [150] 1993 Papua New Guinea,

Central

Leprosy and HBV survey 253 1

Turner [151] 1993 Papua New Guinea,

Western

Remote, rural and

capital subjects

180 1±12

Hyams et al. [152] 1992 Peru Northern jungle region 2111 0

Bahakim et al. [153] 1991 Saudi Arabia Pregnant women 260 4.6

Healthy subjects 760 5.3

al-Faleh et al. [154] 1991 Saudi Arabia Children 4496 0.9

al Nasser et al. [155] 1992 Saudi Arabia Healthy subjects 380 3.6

al Karawi et al. [156] 1992 Saudi Arabia Antenatal women 385 1

al-Faleh et al. [157] 1995 Saudi Arabia Healthy subjects 1482 1.8

Chen et al. [158] 1991 Taiwan Pregnant women 294 0.34

Lee et al. [159] 1991 Taiwan Hepatitis B vaccination

program

1419 0.28

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 85

Page 3: Hepatitis C: an epidemiological review

though this was not con®rmed by other European studies

[16±18]. The screening of donors for ALT and anti-HBc for

prevention of PTH-NANB was termed surrogate testing.

Before 1986, the incidence of post-transfusion HCV ran-

ged from 5% to 13% which declined to between 1.5% to 9%

from 1986 to 1990 [19±25]. Since 1990, when anti-HCV

screening of blood donors became mandatory, the incidence

of post-transfusion HCV declined to < 1% but not completely

eliminated. This is because the ®rst generation ELISA may

not become positive for months after infection with HCV

[26]. Furthermore, seronegative HCV carriers were respon-

sible for 10±15% of HCV transmission [26]. The new gen-

eration of various tests will further reduce the risk of

transfusion-transmitted HCV as they are able to detect a

number of additional antigens and are more sensitive.

It has been suggested that HCV can down-regulate the

pace of replication in order to escape viral clearance by the

host immune system, yet can still exist in a quiescent or low

replicative state within hepatocytes which in part is

responsible for the high degree of viral persistence in HCV

infection [26]. HCV displays a high mutation rate like many

RNA viruses which (i) provides protection against immu-

nological detection and destruction which leads to its per-

sistence, ¯are up and transmission of disease; (ii) can lead to

unreliability of antibody tests; (iii) higher reinfection rate due

to incomplete immunity; (iv) variable clinical expression;

(v) variable and unpredictable response to treatment; and,

lastly, (vi) dif®culty in development of a reliable vaccine

[27±29].

RECIPIENTS OF BLOOD AND BLOOD PRODUCTS

The incidence of acquiring post-transfusion HCV infection is

directly related to the number and amount of blood products

received [30±32]. Therefore, haemophilics have a very high

incidence of HCV infection, 46±90% [33±35]. Similarly

patients receiving > 100 000 U of cryoprecipitate per year

compared with those receiving < 100 000 U have a signi®-

cantly higher chance of become infected (76% vs 46%) [35].

Although virucidal procedures for blood products such as

heat treatment, pasteurization and solvent-detergent treat-

ment have nearly totally eliminated the risk of HCV trans-

mission, they nonetheless do not guarantee complete

security [35±37]. This is because there have been a number

of incidences of HCV transmission via intravenous immu-

noglobulin preparations [36,38±40]. However, a recent

Dutch study [41], failed to show any seroconversion

amongst 57 patients who received clotting products between

1989 and 1993 following virucidal treatment.

In children receiving multiple blood transfusion for tha-

lassemia, the incidence of HCV infection varies from 55% to

83% [30±42]. The outcome of HCV infection in these chil-

dren was variable; resolution in 20%, chronic infection in

69% and recurrent attacks of acute infection in 11%. In a

European multicentre study [43] of paediatric population

with chronic hepatitis C with no underlying systemic

disease, with a mean period of follow-up of 6 years, it

emerged that most children remain asymptomatic and some

even achieved sustained biochemical remission. This study

Table 1 Continued

Author(s) Year(s)

Geographical

location

Type of

subjects

Number

tested

Percentage

positive (%)

Pregnant women 793 0.4

Chien et al. [160] 1993 Taiwan Check-up program 108 5.6

Chang et al. [161] 1993 Taiwan Healthy infants 748 0

Chuang et al. [162] 1993 Taiwan Healthy subjects 275 2.9

Chang et al. [163] 1996 Taiwan Bunun aboriginal community 712 16.9

Triki et al. [164] 1997 Tunisia Young male military recruits,

healthy individuals (all age

groups from 6 Months onward)

33 363 0.4

Doganci et al. [165] 1992 Turkey High socioeconomic group in

Belgium

116 0

Hyams et al. [166] 1992 USA Military recruits 1538 0.3

Jonas et al. [167] 1997 USA Adolescent medicine clinic

or school-based clinics

869 0.1

Alter et al. [168] 1999 USA 3rd National health and

nutrition examination

survey (1998±94)

21 241 1.8

Blitz-Dorfman et al. [169] 1996 Venezuela Randomly selected subjects 293 0

Scott et al. [170] 1992 Yemen Cross-sectional survey 348 2.6

Oshitani et al. [171] 1995 Zambia Adult hospital patients with

and without jaundice

495 0.6

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

86 M. I. Memon & M. A. Memon

Page 4: Hepatitis C: an epidemiological review

Table 2 Prevalence of anti-HCV in both volunteer and professional blood donors

Author(s) Year(s)

Geographical

location Type of donors

Number

of donors

Percentage

positive (%)

Allain et al. [172] 1991 Australia Voluntary 167 511 0.78

Archer et al. [173] 1992 Australia Not speci®ed (all) 94 970 0.45

Mison [174] 1997 Australia Voluntary 34 725 0.29

Khan et al. [175] 1993 Bangladesh Professional 163 2.4

Voluntary 83 0

Japanese voluntary 7479 0.6

Jeannel et al. [134] 1998 Benin (W. Africa) Not speci®ed 582 1.4

Vasconcelos et al. [176] 1994 Brazil Not speci®ed ±random selection 5000 1.14

Ito et al. [177] 1993 China Not speci®ed 451 0.7

Wang et al. [178] 1994 China Voluntary 1909 0.3

Professional 1017 5.7

Arthur et al. [179] 1997 Egypt Not speci®ed 2644 24.8

Schottstedt et al. [180] 1998 Germany Not speci®ed 428 896 0.005

Song et al. [181] 1994 Ho Chi Minh Not speci®ed 491 20.6

Hanoi Not speci®ed 499 0.8

Lin et al. [182] 1992 Hong Kong Voluntary 5000 0.4,1.2,3.8*

Panigrahi et al. [183] 1997 India Voluntary 15 922 1.85

Budihusodo et al. [184] 1991 Indonesia Voluntary 243 24.3

Amirudin et al. [185] 1991 Indonesia Not speci®ed 196 3.1

Sulaiman et al. [186] 1995 Indonesia Voluntary 7572 2.1

Darmadi et al. [187] 1996 Indonesia Voluntary 2233 2.3

Prati et al. [188] 1997 Italy Not speci®ed (repeat donors) 16 515 0.03

Tanaka et al. [189] 1992 Japan Voluntary 34 989 0.56

Watanabe et al. [190] 1993 Japan Not speci®ed (all) 16 500 2.2

Sasaki et al. [191] 1996 Japan Not speci®ed (all) 114 266 0.19

Tanaka et al. [192] 1998 Japan Not speci®ed (four age groups) 448 020 0.3

Kim et al. [193] 1993 Korea Not speci®ed 150 1.3

Araj et al. [194] 1995 Lebanon Not speci®ed (random selection) 536 0.7

Morris et al. [195] 1998 Northern Ireland Not speci®ed (all) 231 321 0.01

Kakepoto et al. [196] 1996 Pakistan Voluntary 16 705 1.18

Arguillas et al. [197] 1991 Philippines Not speci®ed 392 2.2

Abdourakhmanov et al. [198] 1998 Russia Voluntary 10 682 0.93

Paid 267 7.5

al Karawi [156] 1992 Saudi Arabia Voluntary 4818 1.5

Abdelaal et al. [199] 1994 Saudi Arabia Not speci®ed (random selection) 744 3.2

Crawford et al. [200] 1994 Scotland Not speci®ed (all) 180 658 0.088

Wang [201] 1995 Singapore Not speci®ed (all) 65 208 0.37

Tucker et al. [202] 1997 South Africa Voluntary 66 314 0.41

Lissen et al. [203] 1993 Spain Voluntary 400 1.2

Munoz-Gomez et al. [204] 1996 Spain Voluntary 55 587 0.93

Chen et al. [205] 1990 Taiwan Voluntary 420 0.95

Lee et al. [159] 1991 Taiwan Paid 500 0.4

Songsivilai et al. [206] 1997 Thailand Voluntary 3255 5.6

Mutimer et al. [207] 1995 UK Voluntary 287 332 0.35

Stevens et al. [208] 1990 USA Voluntary 874 1.4

Anderson et al. [209] 1995 USA Voluntary 21 431 0.5

Murphy et al. [210] 1996 USA Voluntary 862 398 0.36

Chuang et al. [211] 1999 USA Voluntary 149 756 0.17

el Guneid et al. [212] 1993 Yemen Not speci®ed (all) 294 1

Oshitani et al. [171] 1995 Zambia Not speci®ed (all) 240 0

*ALT £ SD, ALT raised 2±3 SD, ALT > 3 SD.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 87

Page 5: Hepatitis C: an epidemiological review

concluded on the basis of repeated liver biopsies, that severe

hepatitis and cirrhosis are infrequently encountered with

chronic hepatitis C infection in children and adolescence.

The risk of developing hepatic decompensation in HCV

patients in the presence of coinfection with HIV is 21 times

higher compared with those who are HIV negative [44,45].

OTHER IATROGENIC ROUTESOF TRANSMISSION

There is increased prevalence of HCV infections amongst

certain groups of patients which include: (i) long-term can-

cer survivors (20%); (ii) bone marrow transplant recipients

(29%); (iii) renal dialysis patients (15±20%); (iv) renal

transplant patients ± which is directly related to the fre-

quency and duration of haemodialysis received prior to their

transplant [29,32,46±54]. However, the prevalence of HCV

infection differs greatly between different countries and even

between different dialysis centres in the same country, the

highest has been reported from Brazil (82%) and the lowest

from Europe (4%) [55]. There is a direct correlation with the

duration of dialysis and number of blood transfusions

received and the incidence of acquiring HCV infection [55].

Other possible mechanisms of transmission include sharing

dialysis machines between HCV positive and negative

patients [56,57] and nosocomial transmission by the dialysis

staff [58±61]. It is clear from various studies that rigorously

applied universal infection precautions during dialysis by the

staff signi®cantly decrease the nosocomial transmission of

HCV infections [55,59,60,62,63]. The nosocomial trans-

mission has also been documented from a cardiac surgeon

(to ®ve patients), via anaesthetic tubing, and via syringes for

intravenous catheter ¯ushing [64±66].

RISK TO HEALTHCARE PROFESSIONALS

Healthcare professionals dealing with blood and blood

products are at a greater risk of contracting HCV via need

stick injury. The risk of acquiring HCV infection following a

single needle stick injury with contaminated blood is low as

determined by anti-HCV seroconversion using second gen-

eration assay and PCR [67±69]. High risk groups include

surgeons, obstetricians, haemodialysis nurses/technicians,

oral surgeons, emergency department workers and intensive

care workers (Table 3). The risk factors include: (i) type of

needle, i.e. hollow vs solid; (ii) the frequency of occupational

blood contacts; (iii) the type of patients, i.e. acute infection vs

chronic carriers; and (iv) prevalence of HCV amongst

patients. Three European studies [70±72] failed to show any

HCV seroconversion in healthcare workers following anti-

HCV positive needle prick injuries following at least

10 months of follow-up. In contrast, two Japanese pros-

pective studies revealed a seroconversion rate of between

3.3% and 5.6% amongst 90 and 56 healthcare workers,

respectively, following needle-stick injury [73,74]. Use of

blunt needles, use of double gloving in high-risk patients, use

of protective goggles and passing of sharp instruments via a

tray rather than directly are important precautionary

measures in minimizing iatrogenic transmission of HCV. It is

clear from the various studies that the risk of occupational

risk of HCV transmission does exist and preventive measures

as outlined above are currently the mainstay of healthcare

workers against HCV infection.

INTRAFAMILIAL TRANSMISSION

There is some evidence that intrafamilial spread of HCV also

occur as seropositivity for anti-HCV is 5±10-fold in individ-

uals living with an HCV-positive patient compared with

general population (Table 4). A number of studies [75±80]

totalling 335 patients, found the prevalence of HCV infection

in household (nonsexual) contacts to be between 0% to 11%

(average 3.6%). Children are less effected than spouses. The

nonsexual household transmission of HCV is speculative and

include sharing of toothbrushes, dental appliances, razors

and nail-grooming equipment.

The low rates of transmission may be due to low serum

titre of virus in HCV carriers during HCV infection [81].

However, no conclusive data exists as to the threshold

concentration of HCV required to transmit infection [29].

The prevalence of anti-HCV among the sexual and

household contacts of chronic hepatitis C patients ranges

between 0% to 27% (Table 4). Caporaso et al. [82] published

one of the largest studies evaluating the intrafamilial spread

of HCV among 1370 household contacts of 585 HCV pos-

itive subjects (index cases). By using third generation ELISA

and PCR techniques they found the incidence of anti-HCV to

be 7.3% (15.6% spouses, 3.2% in other relatives). After

adjusting for various confounders, the study failed to show

any correlation between spouses vs other relatives and

length of marriage and acquiring HCV infection. The

authors concluded that sexual transmission does not seem to

play a role in the intrafamilial spread of HCV infection. In

contrast to this study Guadagnino et al. [83] showed that

spouses who had been married to the index cases longer

than 20 years had a 7.5-fold risk of HCV seropositivity as

compared with those married less than 20 years. They

concluded that sexual contact plays an independent role in

the spread of HCV infection in the family setting.

A study from Japan [84] found spouses with anti-HCV-

positive partners to be twice as likely to have anti-HCV than

spouses with anti-HCV-negative partners. However, 50% of

the couples presented discordant HCV genotypes. The authors

concluded that the clustering of HCV infection among speci®c

couples within this endemic population may not be attribut-

able to heterosexual transmission. In contrast a study from

Taiwan [85] showed direct correlation with the duration of

marriage (> 20 years vs < 20 years) and duration of actual

exposure to the index patients but not with serum HCV titres.

The infected couples had more frequent sexual contacts and

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

88 M. I. Memon & M. A. Memon

Page 6: Hepatitis C: an epidemiological review

more commonly shared toothbrushes than those with unin-

fected spouses. The authors concluded that spouses of patients

with chronic hepatitis C have a higher risk of acquiring HCV

that increases with longer marriage and duration of exposure,

and they should be educated about how to avoid contracting

HCV infection from their spouses.

One study showed a higher prevalence of anti-HCV in

female partners for positive males but not vice versa [86]. As

the data is so con¯icting, some experts believe that in long-

standing monogamous relationships no modi®cation in

sexual practices is required except during menstruation and

if one or the other partners have overt genital ulceration. In

other situations safe sex practices may help prevent the

transmission of HCV.

SEXUAL TRANSMISSION IN HIGH-RISK GROUPS

Sexual transmission of HCV occurs, but infrequently. The

prevalence of HCV infection is higher amongst heterosexual

individuals attending sexually transmitted diseases clinics,

male homosexuals, prostitutes and partners of intravenous

drug abusers (Table 5). There seems to be a positive

correlation with the overall number of sexual partners, not

using a condom, receptive anal intercourse, sexual activity

Table 3 Prevalence of anti-HCV in the healthcare professional of different geographical locations

Author(s) Year(s)

Geographical

location Type of subject

Number

tested

Percentage

positive (%)

Frider et al. [213] 1994 Argentina Healthcare workers 439 2.7

Jadoul et al. [214] 1994 Belgium Dialysis nurses 120 4.1

Vanderborght et al. [215] 1995 Brazil Healthcare workers 242 2.7

Germanaud [216] 1994 France Healthcare workers 430 0.9

Schlipkoter et al. [217] 1992 Germany Dialysis staff 121 1.6

Jochen et al. [218] 1992 Germany Hospital staff 1033 0.6

Ribero et al. [219] 1991 Italy Dentists 526 6.3

Campello et al. [220] 1992 Italy Healthcare workers 407 1.2

Petrosillo et al. [221] 1995 Italy Healthcare workers 5813 2

Nakashima et al. [222] 1993 Japan Hospital staff & acupuncturist 1077 1

Fujiyama et al. [223] 1995 Japan Dialysis staff 216 2.3

Rehman et al. [224] 1996 Pakistan Healthcare workers 95 4

Mujeeb et al. [225] 1998 Pakistan Operating room personnel 104 4.4

Hyams et al. [152] 1992 Peru Healthcare workers 148 0

Arguillas et al. [197] 1991 Philippines Physicians and lab staff 123 1.6

Soni et al. [226] 1993 South Africa Healthcare workers 212 0

Struve et al. [227] 1994 Sweden Healthcare staff 880 0.7

Liaw et al. [228] 1991 Taiwan Hospital administrative staff 123 0.8

Oge et al. [229] 1998 Turkey Urologist 24 12.5

Mortimer et al. [230] 1989 UK Healthcare workers 100 0

Herbert et al. [231] 1992 UK Dentist 94 0

Zuckerman et al. [70] 1994 UK Healthcare workers 1053 0.3

Neal et al. [232] 1997 UK Healthcare workers 1949 0.2

Lodi [233] 1997 UK Dental healthcare workers 167 1.2

Klein [69] 1991 USA Dentists 456 1.8

Abb [234] 1991 USA Healthcare workers 1018 0.6

Shapiro et al. [235] 1992 USA Orthopaedic surgeons 3262 0.8

Cooper et al. [236] 1992 USA Hospital staff 243 1.6

Thomas et al. [237] 1993 USA Teaching hospital healthcare personnel 943 0.7

Polish et al. [238] 1993 USA Community hospital healthcare

personnel

1677 1.4

Niu et al. [239] 1993 USA Dialysis staff 142 1.4

Forseter et al. [240] 1993 USA Dialysis nurses 51 1.9

Gerberding [241] 1994 USA Hospital care providers 976 1.4

Goetz et al. [242] 1995 USA Liver transplantation personnel 57 5.3

Panlilio et al. [243] 1995 USA Hospital-based Surgeons in moderate

to high AIDS areas

770 0.9

Tokars et al. [244] 1998 USA Dialysis staff 54 194 2

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 89

Page 7: Hepatitis C: an epidemiological review

involving a trauma, history of other sexually transmitted

diseases and those coinfected with HIV [81,86±89].

PERINATAL OR VERTICAL OR MOTHER-TO-OFFSPRING TRANSMISSION

Perinatal transmission of HCV infection occurs between 0

and 15% of cases [55]. There remains a debate as to the exact

role of this route of HCV spread [90]. Vertical transmission

from mother to child has been reported in a number of studies

[91±100] on the basis of asymptomatic biochemical abnor-

malities of liver function tests in particular ALT and transient

anti-HCV seropositivity using either ELISA or PCR in the

majority of infants born to mothers with HCV infection.

Persistence of anti-HCV has been noted with HIV coinfection

suggesting facilitatory role of HIV in HCV transmission

[91,92,94,97,101]. RT-PCR although have con®rmed ver-

tical transmission of HCV infection, has also generated a

contradictory data when mother-infant pairs were evaluated.

Some studies have shown no detectable anti-HCV despite

detectable anti-HCV [102±106], whereas others have shown

the prevalence of anti-HCV to be between 5% and 80%

[94,96,100,107±113]. There is a positive correlation with

HCV-RNA titre in the mother and subsequent development of

HCV infection in children [110,111,114,115]. Furthermore,

acute HCV infection during pregnancy even in the absence of

HIV carries an increased risk of vertical transmission

[101,107,114]. What remain controversial is the route and

timing of HCV transmission. It seems logical to think that

selective vertical transmission of certain subsets of HCV

variants either in utero or in the immediate postnatal period is

a possibility [116]. A study from Taiwan showed that elective

cesarean sections were associated with lowest microtrans-

fusion from mother to fetus compared with spontaneous

vaginal delivery or emergency cesarean sections [111,117].

In the light of the current available knowledge, no effective

way of preventing transmission of HCV infection from mother

to child exists. Similarly, transmission of HCV by breast milk

has been suggested but never proved [93,118,119]. It has

been insinuated that there might be some correlation be-

tween the duration of breastfeeding by HCV-RNA-positive

mother and the acquiring of HCV infection by the baby. In

view of this inconclusive data, it is premature to advise anti-

HCV-positive mothers against breastfeeding.

INTRAVENOUS DRUG USERS

Intravenous drug abusers not only have the highest pre-

valence of HCV infection but also constitute a potential

reservoir of HCV in the community. The incidence varies

between 31% to as high as 98% in different parts of the

world (Table 6). The prevalence of HCV infection increases

proportionally with the duration of intravenous drug abuse

[120±122]. Other risk factors include male gender, being

older, sex trade worker, risky sexual behaviour, multiple

sexual partners, needle sharing and history of being in pri-

son [120,122±126]. Oral drug abusers, when compared

with intravenous drug abusers, were found to have far less

incidence of HCV infections in two studies, one from New

Zealand (4% vs 73%) and Taiwan (5.4% vs 53%) [123].

CONCLUSIONS

Better understanding of the mode of spread of the disease will

assist in minimizing HCV spread globally. The overall burden

on the society both ®nancially and socially to support and

manage individuals with HCV is a time bomb waiting to

explode unless urgent measures are undertaken to (i) develop

Table 4 Prevalence of anti-HCV in sexual partners

Author(s) Year(s) Geographical location Number tested Percentage positive (%)

Davis et al. [245] 1996 Australia 19 0

Kolho et al. [246] 1991 Finland 30 3.3

Meisel et al. [247] 1995 Germany 94 0

Brettler et al. [248] 1992 International 106 2.7

Power et al. [249] 1995 Ireland 393 0.5

Scotto et al. [250] 1996 Italy 83 8.4

Caporaso et al. [82] 1998 Italy 11 379 15.6

Guadagnino et al. [83] 1998 Italy 267 11.3

Akahane et al. [251] 1994 Japan 154 27

Koda et al. [252] 1996 Japan 121 17.4

Mauser-Bunschoten et al. [253] 1995 Netherlands 75 0

Win et al. [254] 1994 Scotland 75 5.3

Diago et al. [255] 1996 Spain 394 7.6

Kao et al. [85] 1996 Taiwan 100 17

Saltoglu et al. [256] 1998 Turkey 38 7.8

Gordon et al. [257] 1992 UK 42 4.7

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

90 M. I. Memon & M. A. Memon

Page 8: Hepatitis C: an epidemiological review

a strategy to inform and educate the lay public and press

regarding this disease (HCV awareness programs); (ii) set up

clinical information system(s) to monitor trends, occurrence

and effectiveness of intervention programs; (iii) identify the

route of spread for sporadic cases of HCV which accounts for

almost 50% of cases; (iv) develop inexpensive sensitive and

speci®c tests for detection of HCV infection at an early stage;

(v) make available these diagnostic tests universally and in

particular for the poorer countries where HCV is reaching

epidemic proportions; and (vi) lastly to expedite the efforts to

develop a vaccine. Individuals who have been unfortunate to

have acquired the HCV can be supported by appropriate

therapeutic drug regimes, which at present vary from centre

to centre. Therefore, multicentre clinical trials are needed

urgently to de®ne the role of interferon alone or in combi-

nation with other antiviral agents for both symptomatic

and asymptomatic individuals. Furthermore, the exact

interaction of interferon with the virus, host and the inter-

feron regimens (dynamic tripartite interaction) in producing

a variable response needs to be elucidate so that optimal

Table 5 Prevalence of anti-HCV in the high sexual risk groups of different geographical locations

Author(s) Year(s)

Geographical

location Type of subjects

Number

tested

Percentage

positive (%)

Fairley et al. [127] 1990 Australia STD subjects 177 6.2

Quaranta et al. [258] 1994 France Heterosexual STD subjects 82 18

van Doornum et al. [259] 1991 Holland Heterosexual STD subjects 468 1.3

Corona et al. [260] 1991 Italy Heterosexual STD subjects 1130 1.7

Weinstock et al. [261] 1993 USA Heterosexual STD subjects 1162 3.4

Weinstock et al. [261] 1993 USA Inner city clinics for STD 1292 7.7

Thomas et al. [262] 1994 USA Heterosexual STD subjects 1257 10

Gust et al. [263] 1989 Australia Homosexual men 148 9

Fairley et al. [127] 1990 Australia Homosexual men 330 22.7

Bodsworth et al. [89] 1996 Australia Homosexual men 1038 7.6

Melbye et al. [264] 1990 Denmark Homosexual men 259 4.1

Westh et al. [265] 1993 Denmark Homosexual men 147 1

Westh et al. [265] 1993 Denmark Homosexual men 147 1.4

Quaranta et al. [258] 1994 France Homosexual men 68 3

Hadziyannis et al. [266] 1993 Greece Homosexual men 426 4±9

Corona et al. [260] 1991 Italy Homosexual men 195 2

Gasparini et al. [267] 1991 Italy Homosexual men 212 4

Ricchi et al. [268] 1992 Italy Homo-bisexual men 622 6.9

Donahue et al. [269] 1991 North America Homosexual men 926 1.6

Hyams et al. [152] 1992 Peru Homosexual men 103 1

Tor et al. [270] 1990 Spain Homosexual men 105 17

Sanchez-Quijano et al. [271] 1990 Spain Homosexual men 146 5.4

Lissen et al. [203] 1993 Spain Homosexual men 168 4.2

Sonnerborg et al. [272] 1990 Sweden Homosexual men 48 0

Osmond et al. [273] 1993 USA Homosexual men 589 1.5

Buchbinder et al. [274] 1994 USA Homosexual men 343 5

Thomas et al. [86] 1995 USA Homosexual men 35 18

Ndimbie et al. [275] 1996 USA Homosexual men 1058 2.9

Osella et al. [276] 1998 USA Homosexual men 228 12.7

Fairley et al. [127] 1990 Australia Prostitutes 212 10.4

Wu et al. [277] 1993 China Prostitutes 622 12

Hadziyannis et al. [266] 1993 Greece Prostitutes 203 4

Develoux et al. [278] 1994 Niger Prostitutes 250 7.6

Mast et al. [3] 1991 North America Prostitutes 535 12

Hyams et al. [152] 1993 Peru Prostitutes 966 0.7

Sanchez-Quijano et al. [271] 1990 Spain Prostitutes 78 8.9

Gutierrez et al. [279] 1992 Spain Prostitutes 227 9

Lissen et al. [203] 1993 Spain Prostitutes 310 6.4

STD, sexually transmitted disease.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 91

Page 9: Hepatitis C: an epidemiological review

anti-HCV therapy can be formulated. This coupled with

patients orientated surveys to identify quality of life issues

whilst on treatment will guide the physicians in tailoring a

treatment regime most suitable for these patients. Because

there is a wide variation in the disease prevalence rate which

may re¯ect (i) small sample size and (ii) variation in meth-

odology and serological testing, it is paramount that multi-

centre trials address the issue of the true global prevalence of

HCV infection in various groups of people using an up to

date single most sensitive and speci®c test. This task can only

be undertaken through the auspices of WHO, Center for

communicable diseases in Atlanta, GA, USA and the health

Departments of various countries which one hopes will

achieve an effective control of global spread of HCV.

REFERENCES

1 Choo QL et al. Isolation of a cDNA clone derived from a

blood-borne non-A, non-B viral hepatitis genome. Science

1989; 244: 359±362.

2 Anonymous. Hepatitis C: global prevalence. Weekly Epi-

demiol Record 1997; 72: 341±344.

3 Mast EE et al. Strategies to prevent and control hepatitis B

and C virus infections: a global perspective. Vaccine 1999;

17: 1730±1733.

4 Alter MJ. Epidemiology of hepatitis C in the West. Semin

Liver Dis 1995; 15: 5±14.

5 van der Poel CL et al. Hepatitis C virus six years on. Lancet

1994; 344: 1475±1479.

6 Di Bisceglie AM et al. Long-term clinical and histopatho-

logical follow-up of chronic posttransfusion hepatitis.

Hepatology 1991; 14: 969±974.

7 Saito I et al. Hepatitis C virus infection is associated with

the development of hepatocellular carcinoma. Proc Natl

Acad Sci USA 1990; 87: 6547±6549.

8 Lee HS et al. Predominant etiologic association of hepatitis

C virus with hepatocellular carcinoma compared with

hepatitis B virus in elderly patients in a hepatitis B-endemic

area. Cancer 1993; 72: 2564±2567.

9 Van Damme P et al. Epidemiology of hepatitis B and C

in Europe. Acta Gastroenterologica Belgica 1998; 61: 175±

182.

10 Fried MW et al. Absence of hepatitis C viral RNA from

saliva and semen of patients with chronic hepatitis C.

Gastroenterology 1992; 102: 1306±1308.

Table 6 Prevalence of anti-HCV in the intravenous drug users of different geographical locations

Author(s) Year(s) Geographical location Number tested Percentage positive (%)

Gust et al. [263] 1989 Australia 149 58

Fairley et al. [127] 1990 Australia 431 61.9

Bell et al. [121] 1990 Australia 172 84

Crofts et al. [280] 1993 Australia 303 68

Crofts et al. [281] 1997 Australia 1741 66.7

van Beek et al. [282] 1998 Australia 1078 75.6 (< 20 years)

Chang et al. [283] 1999 China 899 67.2

Westh et al. [265] 1993 Denmark 126 98

Smyth et al. [284] 1998 Dublin 733 61.8

Stark et al. [125] 1995 Germany 405 83

Stark et al. [285] 1996 Germany 324 94

Van den Hoek et al. [286] 1990 Holland 304 74

Van Ameijden [287] 1995 Holland 305 65

Galeazzi et al. [288] 1995 Italy 227 75

Guadagnino et al. [126] 1995 Italy 146 68

Wood®eld et al. [289] 1993 New Zealand 110 73

Robinson et al. [290] 1995 New Zealand 92 77

Kemp et al. [291] 1998 New Zealand 241 64.7

Hagan et al. [292] 1999 North America 2462 85.7

Bolumar et al. [293] 1996 Spain 1056 85.5

Santana Rodriguez et al. [294] 1998 Spain 122 87.6

Chen et al. [205] 1990 Taiwan 58 81

Lee et al. [159] 1991 Taiwan 115 53

Lamden et al. [120] 1998 UK 773 67

Donahue et al. [269] 1991 USA 225 85

Garfein et al. [295] 1998 USA 229 37.6

Nakata et al. [135] 1994 Vietnam (Ho Chi Minh) 67 87

Vietnam (Hanoi) 200 31

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

92 M. I. Memon & M. A. Memon

Page 10: Hepatitis C: an epidemiological review

11 Kotwal GJ et al. Detection of hepatitis C virus-speci®c

antigens in semen from non-A, non-B hepatitis patients.

Dig Dis Sci 1992; 37: 641±644.

12 Sharara AI et al. Hepatitis C. Ann Intern Med 1996; 125:

658±668.

13 Conry-Cantilena C et al. Routes of infection, viremia, and

liver disease in blood donors found to have hepatitis C virus

infection. N Engl J Med 1996; 334: 1691±1696.

14 Alter HJ et al. Donor transaminase and recipient hepatitis.

Impact on blood transfusion services. JAMA 1981; 246:

630±634.

15 Aach RD et al. Serum alanine aminotransferase of donors

in relation to the risk of non-A,non-B hepatitis in recipi-

ents: the transfusion-transmitted viruses study. N Engl

J Med 1981; 304: 989±994.

16 Widell A et al. Relation between donor transaminase and

recipient hepatitis non-A, non-B in Sweden. Vox Sang

1988; 54: 154±159.

17 Reesink HW et al. HCV and blood transfusion. Arch Virol

Suppl 1992; 4: 241±243.

18 Aymard JP et al. Post-transfusion non-A, non-B hepatitis

after cardiac surgery. Prospective analysis of donor blood

anti-HBc antibody as a predictive indicator of the occur-

rence of non-A, non-B hepatitis in recipients. Vox Sang

1986; 51: 236±238.

19 Esteban JI et al. Evaluation of antibodies to hepatitis C virus

in a study of transfusion-associated hepatitis. N Engl J Med

1990; 323: 1107±1112.

20 Aach RD et al. Hepatitis C virus infection in post-transfu-

sion hepatitis. An analysis with ®rst- and second-genera-

tion assays. N Engl J Med 1991; 325: 1325±1329.

21 Barrera JM et al. Incidence of non-A, non-B hepatitis after

screening blood donors for antibodies to hepatitis C virus and

surrogate markers. Ann Intern Med 1991; 115: 596±600.

22 Elia GF et al. Incidence of anti-hepatitis C virus antibodies

in non-A, non-B post-transfusion hepatitis in an area of

northern Italy. Infection 1991; 19: 336±339.

23 Mattsson L et al. Seroconversion to hepatitis C virus anti-

bodies in patients with acute posttransfusion non-A, non-B

hepatitis in Sweden. Infection 1991; 19: 309±312.

24 Jullien AM et al. Impact of screening donor blood for

alanine aminotransferase and antibody to hepatitis B core

antigen on the risk of hepatitis C virus transmission. Eur J

Clin Microbiol Infect Dis 1993; 12: 668±672.

25 Donahue JG et al. The declining risk of post-transfusion

hepatitis C virus infection. N Engl J Med 1992; 327:

369±373.

26 Farci P et al. A long-term study of hepatitis C virus repli-

cation in non-A, non-B hepatitis. N Engl J Med 1991; 325:

98±104.

27 Houghton M et al. Molecular biology of the hepatitis C

viruses: implications for diagnosis, development and con-

trol of viral disease. Hepatology 1991; 14: 381±388.

28 Bukh J et al. Sequence analysis of the core gene of 14

hepatitis C virus genotypes. Proc Natl Acad Sci USA 1994;

91: 8239±8243.

29 Nowicki MJ et al. The hepatitis C virus: identi®cation, epi-

demiology, and clinical controversies. J Pediatr Gastro-

enterol Nutrition 1995; 20: 248±274.

30 Lai ME et al. Evaluation of antibodies to hepatitis C virus in

a long-term prospective study of posttransfusion hepatitis

among thalassemic children: comparison between ®rst-

and second-generation assay. J Pediatr Gastroenterol

Nutrition 1993; 16: 458±464.

31 Khalifa AS et al. Prevalence of hepatitis C viral antibody in

transfused and nontransfused Egyptian children. Am J Trop

Med Hyg 1993; 49: 316±321.

32 Fink FM et al. Association of hepatitis C virus infection

with chronic liver disease in paediatric cancer patients. Eur

J Pediatr 1993; 152: 490±492.

33 Kanesaki T et al. Hepatitis C virus infection in children

with hemophilia: characterization of antibody response to

four different antigens and relationship of antibody

response, viremia, and hepatic dysfunction. J Pediatr 1993;

123: 381±387.

34 Eyster ME et al. Natural history of hepatitis C virus infec-

tion in multitransfused hemophiliacs: effect of coinfection

with human immunode®ciency virus. The Multicenter

Hemophilia Cohort Study. J Acquir Immune De®c Syndr

1993; 6: 602±610.

35 Makris M et al. Hepatitis C antibody and chronic liver

disease in haemophilia. Lancet 1990; 335: 1117±1119.

36 Pawlotsky JM et al. Chronic hepatitis C after high-dose

intravenous immunoglobulin. Transfusion 1994; 34: 86±87.

37 Maisonneuve P et al. Antibody to hepatitis C (anti C 100±3)

in French hemophiliacs. Nouvelle Revue Francaise D Hema-

tologie 1991; 33: 263±266.

38 Yu MW et al. Hepatitis C transmission associated with intra-

venous immunoglobulins. Lancet 1995; 345: 1173±1174.

39 Schneider LC et al. Intravenous immunoglobulin and

hepatitis C virus: the Boston episode. Clin Ther 1996; 18

(suppl B): 108±109.

40 Bresee JS et al. Hepatitis C virus infection associated with

administration of intravenous immune globulin. A cohort

study. JAMA 1996; 276: 1563±1567.

41 Mauser-Bunschoten EP et al. Hepatitis C infection and

viremia in Dutch hemophilia patients. J Med Virol 1995;

45: 241±246.

42 Resti M et al. Prevalence of hepatitis C virus antibody in

beta-thalassemic polytransfused children in a long-term

follow-up. Vox Sang 1991; 60: 246±247.

43 Bortolotti F et al. Posttransfusion and community-acquired

hepatitis C in childhood. J Pediatr Gastroenterol Nutr 1994;

18: 279±283.

44 Tagariello G et al. Hepatitis C virus genotypes and severity

of chronic liver disease in haemophiliacs. Br J Haematol

1995; 91: 708±713.

45 Makris M et al. The natural history of chronic hepatitis C in

haemophiliacs. Br J Haematol 1996; 94: 746±752.

46 Locasciulli A et al. Hepatitis C virus serum markers and

liver disease in children with leukemia during and after

chemotherapy. Blood 1993; 82: 2564±2567.

47 Ribas A et al. How important is hepatitis C virus (HCV)-

infection in persons with acute leukemia? Leukemia Res

1997; 21: 785±788.

48 Cesaro S et al. Chronic hepatitis C virus infection after

treatment for pediatric malignancy. Blood 1997; 90:

1315±1320.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 93

Page 11: Hepatitis C: an epidemiological review

49 Locasciulli A et al. Hepatitis C virus infection and liver fail-

ure in patients undergoing allogeneic bone marrow trans-

plantation. Bone Marrow Transplant 1995; 16: 407±411.

50 Diego JM et al. Hepatitis C in dialysis and transplantation.

Curr Opin Nephrol Hypertens 1996; 5: 497±503.

51 Fabrizi F et al. Detection of de novo hepatitis C virus

infection by polymerase chain reaction in hemodialysis

patients. Am J Nephrol 1999; 19: 383±388.

52 Izopet J et al. Molecular evidence for nosocomial trans-

mission of hepatitis C virus in a French hemodialysis unit.

J Med Virol 1999; 58: 139±144.

53 Sandhu J et al. Hepatitis C prevalence and risk factors in

the northern Alberta dialysis population. Am J Epidemiol

1999; 150: 58±66.

54 Lettau LA. The A, B, C, D, and E of viral hepatitis: spelling

out the risks for healthcare workers. Infect Control Hosp

Epidemiol 1992; 13: 77±81.

55 van der Poel CL et al. Hepatitis C virus: epidemiology,

transmission and prevention. Curr Stud Hematol Blood

Transfus 1998: 208±236

56 Pru CE et al. Hepatitis C transmission through dialysis

machines. ASAIO J 1994; 40: M889±91.

57 McLaughlin KJ et al. Nosocomial transmission of hepatitis

C virus within a British dialysis centre. Nephrol Dialysis

Transplant 1997; 12: 304±309.

58 Irish DN et al. Identi®cation of hepatitis C virus serocon-

version resulting from nosocomial transmission on a hae-

modialysis unit: implications for infection control and

laboratory screening. J Med Virol 1999; 59: 135±140.

59 Okuda K et al. Mode of hepatitis C infection not associated

with blood transfusion among chronic hemodialysis

patients. J Hepatol 1995; 23: 28±31.

60 Fabrizi F et al. Incidence of seroconversion for hepatitis C

virus in chronic haemodialysis patients: a prospective

study. Nephrol Dialysis Transplant 1994; 9: 1611±1615.

61 Schneeberger PM et al. Infection control of hepatitis C in

Dutch dialysis centres [news]. Nephrol Dialysis Transplant

1998; 13: 3037±3040.

62 Huraib S et al. High prevalence of and risk factors for

hepatitis C in haemodialysis patients in Saudi Arabia: a

need for new dialysis strategies. Nephrol Dialysis Transplant

1995; 10: 470±474.

63 Gilli P et al. Prevention of hepatitis C virus in dialysis units.

Nephron 1995; 70: 301±306.

64 Esteban JI et al. Transmission of hepatitis C virus by a

cardiac surgeon. N Engl J Med 1996; 334: 555±560.

65 Schvarcz R et al. Nosocomial transmission of hepatitis C

virus. Infection 1997; 25: 74±77.

66 Allander T et al. Frequent patient-to-patient transmission

of hepatitis C virus in a haematology ward. Lancet 1995;

345: 603±607.

67 Mitsui T et al. Hepatitis C virus infection in medical per-

sonnel after needlestick accident. Hepatology 1992; 16:

1109±1114.

68 Kelen GD et al. Hepatitis B and hepatitis C in emergency

department patients. N Engl J Med 1992; 326: 1399±1404.

69 Klein RS et al. Occupational risk for hepatitis C virus

infection among New York City dentists. Lancet 1991; 338:

1539±1542.

70 Zuckerman J et al. Prevalence of hepatitis C antibodies

in clinical health-care workers. Lancet 1994; 343:

1618±1620.

71 Petrosillo N et al. Prevalence of hepatitis C antibodies in

health-care workers. Italian Study Group on Blood-borne

Occupational Risk in Dialysis [letter; comment]. Lancet

1994; 344: 339±340.

72 Hernandez ME et al. Risk of needle-stick injuries in the

transmission of hepatitis C virus in hospital personnel.

J Hepatol 1992; 16: 56±58.

73 Sodeyama T et al. Detection of hepatitis C virus markers

and hepatitis C virus genomic-RNA after needlestick acci-

dents. Arch Intern Med 1993; 153: 1565±1572.

74 Arai Y et al. A prospective study of hepatitis C virus infec-

tion after needlestick accidents. Liver 1996; 16: 331±334.

75 Everhart JE et al. Risk for non-A, non-B (type C) hepatitis

through sexual or household contact with chronic carriers.

Ann Intern Med 1990; 112: 544±545.

76 Deny P et al. Low rate of hepatitis C virus (HCV) trans-

mission within the family. J Hepatol 1992; 14: 409±410.

77 Mondello P et al. Anti-HCV antibodies in household con-

tacts of patients with cirrhosis of the liver ± preliminary

results. Infection 1992; 20: 51±52.

78 Bellobuono A et al. Intrafamilial spread of hepatitis C virus.

Transfusion 1991; 31: 475.

79 Scaraggi FA et al. Intrafamilial and sexual transmission of

hepatitis C virus [letter; comment]. Lancet 1993; 342:

1300±1302.

80 Camarero C et al. Horizontal transmission of hepatitis C

virus in households of infected children. J Pediatr 1993;

123: 98±99.

81 Esteban JI et al. Hepatitis C virus antibodies among risk

groups in Spain. Lancet 1989; 2: 294±297.

82 Caporaso N et al. Spread of hepatitis C virus infection

within families. Investigators of an Italian Multicenter

Group. J Viral Hepat 1998; 5: 67±72.

83 Guadagnino V et al. Hepatitis C virus infection in family

setting. Eur J Epidemiol 1998; 14: 229±232.

84 Tanaka K et al. Heterosexual transmission of hepatitis C

virus among married couples in southwestern Japan. Int J

Cancer 1997; 72: 50±55.

85 Kao JH et al. Transmission of hepatitis C virus between

spouses: the important role of exposure duration. Am J

Gastroenterol 1996; 91: 2087±2090.

86 Thomas DL et al. Sexual transmission of hepatitis C virus

among patients attending sexually transmitted diseases

clinics in Baltimore ± an analysis of 309 sex partnerships.

J Infect Dis 1995; 171: 768±775.

87 Hess G et al. Hepatitis C virus and sexual transmission.

Lancet 1989; 2: 987.

88 Tedder RS et al. Hepatitis C virus: evidence for sexual

transmission. BMJ 1991; 302: 1299±1302.

89 Bodsworth NJ et al. Hepatitis C virus infection in a large

cohort of homosexually active men: independent associa-

tions with HIV-1 infection and injecting drug use but not

sexual behaviour. Genitourin Med 1996; 72: 118±122.

90 Koff RS. The low ef®ciency of maternal-neonatal trans-

mission of hepatitis C virus: how certain are we? [Editorial

comment] Ann Intern Med 1992; 117: 967±969.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

94 M. I. Memon & M. A. Memon

Page 12: Hepatitis C: an epidemiological review

91 Weintrub PS et al. Hepatitis C virus infection in infants

whose mothers took street drugs intravenously. J Pediatr

1991; 119: 869±874.

92 Giovannini M et al. Maternal-infant transmission of hepa-

titis C virus and HIV infections: a possible interaction.

Lancet 1990; 335: 1166.

93 Wejstal R et al. Mother to infant transmission of hepatitis C

virus infection. J Med Virol 1990; 30: 178±180.

94 Wejstal R et al. Mother-to-infant transmission of hepatitis

C virus. Ann Intern Med 1992; 117: 887±890.

95 Novati R et al. Mother-to-child transmission of hepatitis C

virus detected by nested polymerase chain reaction. J Infect

Dis 1992; 165: 720±723.

96 Thaler MM et al. Vertical transmission of hepatitis C virus.

Lancet 1991; 338: 17±18.

97 Paccagnini S et al. Perinatal transmission and manifesta-

tion of hepatitis C virus infection in a high risk population.

Pediatr Infect Dis J 1995; 14: 195±199.

98 Tanzi E et al. Is HCV transmitted by the vertical/perinatal

route? Arch Virol Suppl 1993; 8: 229±234.

99 Aizaki H et al. Mother-to-child transmission of a hepatitis C

virus variant with an insertional mutation in its hyper-

variable region. J Hepatol 1996; 25: 608±613.

100 Matsubara T et al. Mother-to-infant transmission of hepa-

titis C virus: a prospective study. Eur J Pediatr 1995; 154:

973±978.

101 Maggiore G et al. Vertical transmission of hepatitis C [let-

ter; comment]. Lancet 1995; 345: 1122.

102 Uehara S et al. The incidence of vertical transmission of

hepatitis C virus. Tohoku J Exp Med 1993; 171: 195±202.

103 Marcellin P et al. Prevalence of hepatitis C virus infection

in asymptomatic anti-HIV1 negative pregnant women and

their children. Dig Dis Sci 1993; 38: 2151±2155.

104 Roudot-Thoraval F et al. Lack of mother-to-infant trans-

mission of hepatitis C virus in human immunode®ciency

virus-seronegative women: a prospective study with

hepatitis C virus RNA testing. Hepatology 1993; 17:

772±777.

105 Reinus JF et al. Failure to detect vertical transmission of

hepatitis C virus. Ann Intern Med 1992; 117: 881±886.

106 Fischler B et al. Vertical transmission of hepatitis C virus

infection. Scand J Infect Dis 1996; 28: 353±356.

107 Sabatino G et al. Vertical transmission of hepatitis C virus:

an epidemiological study on 2,980 pregnant women in

Italy. Eur J Epidemiol 1996; 12: 443±447.

108 Kuroki T et al. Vertical transmission of hepatitis C virus

(HCV) detected by HCV-RNA analysis. Gut 1993; 34:

S52±53.

109 Lam JP et al. Infrequent vertical transmission of hepatitis C

virus. J Infect Dis 1993; 167: 572±576.

110 Ohto H et al. Transmission of hepatitis C virus from

mothers to infants. The Vertical Transmission of Hepatitis

C Virus Collaborative Study Group. N Engl J Med 1994;

330: 744±750.

111 Lin HH et al. Possible role of high-titer maternal viremia in

perinatal transmission of hepatitis C virus. J Infect Dis

1994; 169: 638±641.

112 Ni YH et al. Temporal pro®le of hepatitis C virus antibody

and genome in infants born to mothers infected with

hepatitis C virus but without human immunode®ciency

virus coinfection. J Hepatol 1994; 20: 641±645.

113 Gonzalez A et al. Ef®cacy of screening donors for antibodies

to the hepatitis C virus to prevent transfusion-associated

hepatitis: ®nal report of a prospective trial. Hepatology

1995; 22: 439±445.

114 Resti M et al. Mother to child transmission of hepatitis C

virus: prospective study of risk factors and timing of

infection in children born to women seronegative for

HIV-1. Tuscany Study Group on Hepatitis C Virus Infec-

tion. BMJ 1998; 317: 437±441.

115 Zanetti AR et al. A prospective study on mother-to-infant

transmission of hepatitis C virus. Intervirology 1998; 41:

208±212.

116 Weiner AJ et al. A unique, predominant hepatitis C virus

variant found in an infant born to a mother with multiple

variants. J Virol 1993; 67: 4365±4368.

117 Lin HH et al. Least microtransfusion from mother to fetus

in elective cesarean delivery. Obstet Gynecol 1996; 87:

244±248.

118 Nagata I et al. Mother-to-infant transmission of hepatitis C

virus. J Pediatr 1992; 120: 432±434.

119 Ogasawara S et al. Hepatitis C virus RNA in saliva and

breastmilk of hepatitis C carrier mothers. Lancet 1993;

341: 561.

120 Lamden KH et al. Hepatitis B and hepatitis C virus infec-

tions: risk factors among drug users in Northwest England.

J Infect 1998; 37: 260±269.

121 Bell J et al. Hepatitis C virus in intravenous drug users. Med

J Aust 1990; 153: 274±276.

122 Medin C et al. Seroconversion to hepatitis C virus in

dialysis patients: a retrospective and prospective study.

Nephron 1993; 65: 40±45.

123 Mansell CJ et al. Epidemiology of hepatitis C in the East.

Semin Liver Dis 1995; 15: 15±32.

124 Chang CJ et al. Seroepidemiology of hepatitis C virus

infection among drug abusers in southern Taiwan. J For-

mosan Med Assoc 1998; 97: 826±829.

125 Stark K et al. Prevalence and determinants of anti-HCV

seropositivity and of HCV genotype among intravenous

drug users in Berlin. Scand J Infect Dis 1995; 27: 331±337.

126 Guadagnino V et al. Relevance of intravenous cocaine use

in relation to prevalence of HIV, hepatitis B and C virus

markers among intravenous drug abusers in southern

Italy. J Clin Lab Immunol 1995; 47: 1±9.

127 Fairley CK et al. Epidemiology and hepatitis C virus in

Victoria. Med J Aust 1990; 153: 271±273.

128 Garner JJ et al. Prevalence of hepatitis C infection in

pregnant women in South Australia. Med J Aust 1997;

167: 470±472.

129 Tao QM et al. Seroepidemiology of HCV and HBV infection

in northern China. Gastroenterol Japon 1991; 26 (Suppl. 3):

156±158.

130 Darwish MA et al. High seroprevalence of hepatitis A, B, C,

and E viruses in residents in an Egyptian village in The Nile

Delta: a pilot study. Am J Trop Med Hyg 1996; 54:

554±558.

131 Dubois F et al. Hepatitis C in a French population-

based survey, 1994 seroprevalence, frequency of viremia,

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 95

Page 13: Hepatitis C: an epidemiological review

genotype distribution, and risk factors. The Collaborative

Study Group. Hepatology 1997; 25: 1490±1496.

132 Richard-Lenoble D et al. Hepatitis B, C, D, and E markers in

rural equatorial African villages (Gabon). Am J Trop Med

Hyg 1995; 53: 338±341.

133 Martinson FE et al. Seroepidemiological survey of hepatitis

B and C virus infections in Ghanaian children. J Med Virol

1996; 48: 278±283.

134 Jeannel D et al. Evidence for high genetic diversity and

long-term endemicity of hepatitis C virus genotypes 1 and

2 in West Africa. J Med Virol 1998; 55: 92±97.

135 Nakata S et al. Hepatitis C and B virus infections

in populations at low or high risk in Ho Chi Minh and

Hanoi. Vietnam J Gastroenterol Hepatol 1994; 9: 416±

419.

136 Chan GC et al. Prevalence of hepatitis C infection in Hong

Kong. J Gastroenterol Hepatol 1992; 7: 117±120.

137 Reddy PH et al. Hepatitis virus markers in the Baiga tribal

population of Madhya Pradesh, India. Trans R Soc Trop Med

Hyg 1995; 89: 620.

138 Marranconi F et al. Prevalence of anti-HCV and risk factors

for hepatitis C virus infection in healthy pregnant women.

Infection 1994; 22: 333±337.

139 Osella AR et al. Epidemiology of hepatitis C virus infection

in an area of Southern Italy. J Hepatol 1997; 27: 30±35.

140 Guadagnino V et al. Prevalence, risk factors, and genotype

distribution of hepatitis C virus infection in the general

population: a community-based survey in southern Italy.

Hepatology 1997; 26: 1006±1011.

141 Tajima K et al. Natural horizontal transmission of HCV

in microepidemic town in Japan. Lancet 1991; 337:

1410±1411.

142 Tibbs CJ et al. Prevalence of hepatitis C in tropical com-

munities: the importance of con®rmatory assays. J Med

Virol 1991; 34: 143±147.

143 Kim YS et al. Prevalence of hepatitis C virus antibody

among Korean adults. J Korean Med Sci 1992; 7: 333±336.

144 Morvan JM et al. Anti-HCV antibody prevalence among an

asymptomatic population living in two villages in

Madagascar. Trans R Soc Trop Med Hyg 1994; 88: 657.

145 Ahmed SD et al. Seroprevalence of hepatitis B and C and

HIV in Malawian pregnant women. J Infect 1998; 37:

248±251.

146 Miller J et al. The epidemiology and control of hepatitis C in

New Zealand. Commun Dis NZ 1993; 93: 33±41 (Abstract).

147 Perez OM et al. Prevalence of antibodies to hepatitis A, B,

C, and E viruses in a healthy population in Leon. Nicaragua

Am J Trop Med Hyg 1996; 55: 17±21.

148 Oshita M et al. Prevalence of hepatitis C virus in family

members of patients with hepatitis C. J Med Virol 1993; 41:

251±255.

149 Luby SP et al. The relationship between therapeutic injec-

tions and high prevalence of hepatitis C infection in

Ha®zabad. Pakistan Epidemiol Infect 1997; 119: 349±356.

150 Baumgart KW et al. Hepatitis C virus in the central prov-

ince of Papua New Guinea [letter; comment]. Med J Aust

1993; 159: 284±285.

151 Turner PF. Hepatitis C virus in the Western Province of

Papua New Guinea. Med J Aust 1993; 158: 140.

152 Hyams KC et al. Seroprevalence of hepatitis C antibody in

Peru. J Med Virol 1992; 37: 127±131.

153 Bahakim H et al. Hepatitis C virus antibodies in high-risk

Saudi groups. Vox Sang 1991; 60: 162±164.

154 al-Faleh FZ et al. Prevalence of antibody to hepatitis C virus

among Saudi Arabian children: a community-based study.

Hepatology 1991; 14: 215±218.

155 al Nasser MN et al. Seropositivity to hepatitis C virus in

Saudi haemodialysis patients. Vox Sang 1992; 62: 94±97.

156 al Karawi MA et al. Hepatitis C virus infection in chronic

liver disease and hepatocellular carcinoma in Saudi Ara-

bia. J Gastroenterol Hepatol 1992; 7: 237±239.

157 al-Faleh FZ et al. Pro®le of hepatitis C virus and the possible

modes of transmission of the virus in the Gizan area of

Saudi Arabia: a community-based study. Ann Trop Med

Parasitol 1995; 89: 431±437.

158 Chen DS et al. Hepatitis C virus infection in Taiwan. Gas-

troenterol Japon 1991; 26 (Suppl. 3): 164±166.

159 Lee SD et al. Seroepidemiology of hepatitis C virus infection

in Taiwan. Hepatology 1991; 13: 830±833.

160 Chien RN et al. Low prevalences of HBV and HCV infection

in patients with primary biliary cirrhosis in Taiwan: a case

control study. J Gastroenterol Hepatol 1993; 8: 574±576.

161 Chang MH et al. Minimal role of hepatitis C virus infection

in childhood liver diseases in an area hyperendemic for

hepatitis B infection. J Med Virol 1993; 40: 322±325.

162 Chuang WL et al. The role of hepatitis C virus in chronic

hepatitis B virus infection. Gastroenterol Japon 1993; 28

(Suppl. 5): 23±27.

163 Chang SJ et al. Risk factors of hepatitis C virus infection in

a Taiwanese aboriginal community. Kao-Hsiung I Hsueh Ko

Hsueh Tsa Chih [Kaohsiung J Med Sci] 1996; 12: 241±247.

164 Triki H et al. Seroepidemiology of hepatitis B, C and delta

viruses in Tunisia. Trans R Soc Trop Med Hyg 1997; 91:

11±14.

165 Doganci L et al. Prevalence of hepatitis A, B and C in

Turkey. Eur J Clin Microbiol Infect Dis 1992; 11: 661±662.

166 Hyams KC et al. Seroprevalence of hepatitis A, B, and C in

a United States military recruit population. Military Med

1992; 157: 579±582.

167 Jonas MM et al. Low prevalence of antibody to hepatitis C

virus in an urban adolescent population. J Pediatr 1997;

131: 314±316.

168 Alter MJ et al. The prevalence of hepatitis C virus infection

in the United States, 1988 through 1994. N Engl J Med

1999; 341: 556±562.

169 Blitz-Dorfman L et al. Serological survey of markers of

infection with viral hepatitis among the Yukpa Amerindi-

ans from western Venezuela. Ann Trop Med Parasitol 1996;

90: 655±657.

170 Scott DA et al. The epidemiology of hepatitis C virus anti-

body in Yemen. Am J Trop Med Hyg 1992; 46: 63±68.

171 Oshitani H et al. Low prevalence of hepatitis C virus

infection in Lusaka. Zambia Trans R Soc Trop Med Hygiene

1995; 89: 380.

172 Allain JP et al. Prediction of hepatitis C virus infectivity

in seropositive Australian blood donors by supplemental

immunoassays and detection of viral RNA. Blood 1991;

78: 2462±2468.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

96 M. I. Memon & M. A. Memon

Page 14: Hepatitis C: an epidemiological review

173 Archer GT et al. Prevalence of hepatitis C virus antibod-

ies in Sydney blood donors. Med J Aust 1992; 157:

225±227.

174 Mison LM et al. Prevalence of hepatitis C virus and geno-

type distribution in an Australian volunteer blood donor

population. Transfusion 1997; 37: 73±78.

175 Khan M et al. Comparison of seroepidemiology of hepatitis

C in blood donors between Bangladesh and Japan. Gas-

troenterol Japon 1993; 28 (suppl 5): 28±31.

176 Vasconcelos HC et al. Hepatitis B and C prevalences among

blood donors in the south region of Brazil. Memorias Do

Instituto Oswaldo Cruz 1994; 89: 503±507.

177 Ito S et al. Epidemiological characteristics of the incidence

of hepatitis C virus (C100±3) antibodies in patients with

liver diseases in the inshore area of the Yangtze River.

J Gastroenterol Hepatol 1993; 8: 232±237.

178 Wang Y et al. Hepatitis C virus RNA and antibodies among

blood donors in Beijing. J Hepatol 1994; 21: 634±640.

179 Arthur RR et al. Hepatitis C antibody prevalence in blood

donors in different governorates in Egypt. Trans R Soc Trop

Med Hyg 1997; 91: 271±274.

180 Schottstedt V et al. PCR for HBV, HCV and HIV-1 experi-

ences and ®rst results from a routine screening programme

in a large blood transfusion service. Biologicals 1998; 26:

101±104.

181 Song P et al. Markers of hepatitis C and B virus infections

among blood donors in Ho Chi Minh City and Hanoi.

Vietnam Clin Diagnostic Lab Immunol 1994; 1: 413±418.

182 Lin CK et al. A study of hepatitis C virus antibodies and

serum alanine amino transferase in blood donors in Hong

Kong Chinese. Vox Sang 1992; 62: 98±101.

183 Panigrahi AK et al. Magnitude of hepatitis C virus infection

in India: prevalence in healthy blood donors, acute and

chronic liver diseases. J Med Virol 1997; 51: 167±174.

184 Budihusodo U et al. Seroepidemiology of HBV and HCV

infection in Jakarta, Indonesia. Gastroenterol Japon 1991;

26 (Suppl. 3): 196±201.

185 Amirudin R et al. Hepatitis B and C virus infection in Ujung

Pandang, Indonesia. Gastroenterol Japon 1991; 26 (Suppl.

3): 184±188.

186 Sulaiman HA et al. Prevalence of hepatitis B and C viruses

in healthy Indonesian blood donors. Trans R Soc Trop Med

Hyg 1995; 89: 167±170.

187 Darmadi S et al. Hepatitis C virus infection-associated

markers in sera from blood donors in Surabaya. Indonesia

Microbiol Immunol 1996; 40: 401±405.

188 Prati D et al. The incidence and risk factors of community-

acquired hepatitis C in a cohort of Italian blood donors.

Hepatology 1997; 25: 702±704.

189 Tanaka E et al. Prevalence of antibody to hepatitis C virus

in Japanese schoolchildren: comparison with adult blood

donors. Am J Trop Med Hyg 1992; 46: 460±464.

190 Watanabe J et al. Predictive value of screening tests for

persistent hepatitis C virus infection evidenced by viraemia.

Japanese experience. Vox Sang 1993; 65: 199±203.

191 Sasaki F et al. Very low incidence rates of community-

acquired hepatitis C virus infection in company employees,

long-term inpatients, and blood donors in Japan. J Epi-

demiol 1996; 6: 198±203.

192 Tanaka H et al. The risk of hepatitis C virus infection

among blood donors in Osaka. Japan J Epidemiol 1998; 8:

292±296.

193 Kim BS et al. Prevalence of hepatitis C virus related to liver

diseases in Korea. Gastroenterol Japon 1993; 28 (Suppl. 5):

17±22.

194 Araj GF et al. Hepatitis C virus: prevalence in Lebanese

blood donors and brief overview of the disease. J Med

Libanais ± Lebanese Med Journal 1995; 43: 11±16.

195 Morris K et al. Completed hepatitis C lookback in Northern

Ireland. Transfusion Med 1997; 7: 269±275.

196 Kakepoto GN et al. Epidemiology of blood-borne viruses: a

study of healthy blood donors in Southern Pakistan.

Southeast Asian J Trop Med Public Health 1996; 27:

703±706.

197 Arguillas MO et al. Seroepidemiology of hepatitis C virus

infection in the Philippines: a preliminary study and

comparison with hepatitis B virus infection among blood

donors, medical personnel, and patient groups in Davao.

Philippines Gastroenterol Japon 1991; 26 (Suppl. 3):

170±175.

198 Abdourakhmanov DT et al. Epidemiological and clinical

aspects of hepatitis C virus infection in the Russian

Republic of Daghestan. Eur J Epidemiol 1998; 14: 549±553.

199 Abdelaal M et al. Epidemiology of hepatitis C virus: a study

of male blood donors in Saudi Arabia. Transfusion 1994;

34: 135±137.

200 Crawford RJ et al. Prevalence and epidemiological char-

acteristics of hepatitis C in Scottish blood donors. Trans-

fusion Med 1994; 4: 121±124.

201 Wang JE. A study on the epidemiology of hepatitis C

infection among blood donors in Singapore. J Public Health

Med 1995; 17: 387±391.

202 Tucker TJ et al. Hepatitis C virus infection rate in volunteer

blood donors from the Western Cape ± comparison of

screening tests and PCR. South African Med J 1997; 87:

603±605.

203 Lissen E et al. Hepatitis C virus infection among sexually

promiscuous groups and the heterosexual partners of

hepatitis C virus infected index cases. Eur J Clin Microbiol

Infect Dis 1993; 12: 827±831.

204 Munoz-Gomez R et al. Hepatitis C virus infection in Span-

ish volunteer blood donors: HCV RNA analysis and liver

disease. Eur J Gastroenterol Hepatol 1996; 8: 273±277.

205 Chen DS et al. Hepatitis C virus infection in an area

hyperendemic for hepatitis B and chronic liver disease: the

Taiwan experience. J Infect Dis 1990; 162: 817±822.

206 Songsivilai S et al. High prevalence of hepatitis C infection

among blood donors in northeastern Thailand. Am J Trop

Med Hyg 1997; 57: 66±69.

207 Mutimer DJ et al. Hepatitis C virus infection in the

asymptomatic British blood donor. J Viral Hepat 1995; 2:

47±53.

208 Stevens CE et al. Epidemiology of hepatitis C virus. A pre-

liminary study in volunteer blood donors. JAMA 1990;

263: 49±53.

209 Anderson SC et al. Comparison of two second-generation

anti-hepatitis C virus ELISA on 21431 US blood donor

samples. J Viral Hepat 1995; 2: 55±61.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 97

Page 15: Hepatitis C: an epidemiological review

210 Murphy EL et al. Demographic determinants of hepatitis C

virus seroprevalence among blood donors. JAMA 1996;

275: 995±1000.

211 Chuang TY et al. Porphyria cutanea tarda and hepatitis C

virus: a case-control study and meta-analysis of the lit-

erature. J Am Acad Dermatol 1999; 41: 31±36.

212 el Guneid AM et al. Prevalence of hepatitis B, C, and D

virus markers in Yemeni patients with chronic liver dis-

ease. J Med Virol 1993; 40: 330±333.

213 Frider B et al. Prevalence of hepatitis C in health care

workers investigated by 2nd generation enzyme-linked and

line immunoassays. Acta Gastroenterol Latinoamericana

1994; 24: 71±75.

214 Jadoul M et al. Prevalence of hepatitis C antibodies in health-

care workers [letter; comment]. Lancet 1994; 344: 339.

215 Vanderborght BO et al. High prevalence of hepatitis C

infection among Brazilian hemodialysis patients in Rio de

Janeiro: a one-year follow-up study. Revista Do Instituto

Med Trop Sao Paulo 1995; 37: 75±79.

216 Germanaud J et al. The occupational risk of hepatitis C

infection among hospital employees. Am J Public Health

1994; 84: 122.

217 Schlipkoter U et al. Transmission of hepatitis C virus (HCV)

from a haemodialysis patient to a medical staff member.

Scand J Infect Dis 1990; 22: 757±758.

218 Jochen AB. Occupationally acquired hepatitis C virus

infection [letter; comment]. Lancet 1992; 339: 304.

219 Ribero ML et al. Prevalence of HCV antibody among Italian

dental practitioners. Third Int Symp HCV, Strasbourg, 96

(Abstract), 1991.

220 Campello C et al. Prevalence of HCV antibodies in health-

care workers from northern Italy. Infection 1992; 20:

224±226.

221 Petrosillo N et al. Hepatitis B virus, hepatitis C virus and

human immunode®ciency virus infection in health care

workers: a multiple regression analysis of risk factors.

J Hosp Infect 1995; 30: 273±281.

222 Nakashima K et al. Low prevalence of hepatitis C virus

infection among hospital staff and acupuncturists in

Kyushu. Japan J Infect 1993; 26: 17±25.

223 Fujiyama S et al. Changes in prevalence of anti-HCV

antibodies associated with preventive measures among

hemodialysis patients and dialysis staff. Hepato-Gastroen-

terology 1995; 42: 162±165.

224 Rehman K et al. Prevalence of seromarkers of HBV and

HCV in health care personnel and apparently healthy

blood donors. JPMA ± J Pakistan Med Assoc 1996; 46:

152±154.

225 Mujeeb SA et al. Frequency of parenteral exposure and

seroprevalence of HBV, HCV, and HIV among operation

room personnel. J Hosp Infect 1998; 38: 133±137.

226 Soni PN et al. Hepatitis C virus antibodies among risk

groups in a South African area endemic for hepatitis B

virus. J Med Virol 1993; 40: 65±68.

227 Struve J et al. Prevalence of antibodies against hepatitis C

virus infection among health care workers in Stockholm.

Scand J Gastroenterol 1994; 29: 360±362.

228 Liaw YF et al. Hepatitis C virus infection in patients with

chronic liver diseases in an endemic area for hepatitis B

virus infection. Gastroenterol Japon 1991; 26 (suppl 3):

167±169.

229 Oge O et al. Occupational risk of hepatitis B and C infec-

tions in urologists. Urol Intis 1998; 61: 206±209.

230 Mortimer PP et al. Hepatitis C virus antibody. Lancet 1989;

2: 798.

231 Herbert AM et al. Occupationally acquired hepatitis C virus

infection. Lancet 1992; 339: 305.

232 Neal KR et al. Prevalence of hepatitis C antibodies among

healthcare workers of two teaching hospitals. Who is at

risk? BMJ 1997; 314: 179±180.

233 Lodi G et al. Prevalence of HCV infection in health care

workers of a UK dental hospital. Br Dental J 1997; 183:

329±332.

234 Abb J. Prevalence of hepatitis C virus antibodies in hospital

personnel. Zentralblatt Fur Bakteriologie 1991; 274:

543±547.

235 Shapiro CN et al. Use of the hepatitis-B vaccine and infec-

tion with hepatitis B and C among orthopaedic surgeons.

The American Academy of Orthopaedic Surgeons Sero-

survey Study Committee. J Bone Joint Surg Am 1996; 78:

1791±1800.

236 Cooper BW et al. Seroprevalence of antibodies to hepatitis

C virus in high-risk hospital personnel. Infect Control Hosp

Epidemiol 1992; 13: 82±85.

237 Thomas DL et al. Viral hepatitis in health care personnel at

The Johns Hopkins Hospital. The seroprevalence of and

risk factors for hepatitis B virus and hepatitis C virus

infection. Arch Intern Med 1993; 153: 1705±1712.

238 Polish LB et al. Risk factors for hepatitis C virus infection

among health care personnel in a community hospital. Am

J Infect Control 1993; 21: 196±200.

239 Niu MT et al. Multicenter study of hepatitis C virus infec-

tion in chronic hemodialysis patients and hemodialysis

center staff members. Am J Kidney Dis 1993; 22: 568±573.

240 Forseter G et al. Hepatitis C in the health care setting. II.

Seroprevalence among hemodialysis staff and patients in

suburban New York City. Am J Infect Control 1993; 21: 5±8.

241 Gerberding JL. Incidence and prevalence of human

immunode®ciency virus, hepatitis B virus, hepatitis C

virus, and cytomegalovirus among health care personnel

at risk for blood exposure: ®nal report from a longitudinal

study. J Infect Dis 1994; 170: 1410±1417.

242 Goetz AM et al. Prevalence of hepatitis C infection in health

care workers af®liated with a liver transplant center.

Transplantation 1995; 59: 990±994.

243 Panlilio AL et al. Serosurvey of human immunode®ciency

virus, hepatitis B virus, and hepatitis C virus infection

among hospital-based surgeons. Serosurvey Study Group.

J Am College Surgeons 1995; 180: 16±24.

244 Tokars JI et al. National surveillance of dialysis associated

diseases in the United States. 1995 ASAIO J 1998; 44:

98±107.

245 Davis AR et al. Hepatitis C virus transmission to hetero-

sexual partner: bedroom or bathroom hazard? Med J Aust

1996; 164: 126.

246 Kolho E et al. Transmission of hepatitis C virus to sexual

partners of seropositive patients with bleeding disorders: a

rare event. Scand J Infect Dis 1991; 23: 667±670.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

98 M. I. Memon & M. A. Memon

Page 16: Hepatitis C: an epidemiological review

247 Meisel H et al. Transmission of hepatitis C virus to children

and husbands by women infected with contaminated anti-

D immunoglobulin. Lancet 1995; 345: 1209±1211.

248 Brettler DB et al. The low risk of hepatitis C virus trans-

mission among sexual partners of hepatitis C-infected

hemophilic males: an international, multicenter study.

Blood 1992; 80: 540±543.

249 Power JP et al. Hepatitis C infection from anti-D immuno-

globulin [letter; comment]. Lancet 1995; 346: 372±373.

250 Scotto G et al. Sexual transmission of hepatitis C virus

infection. Eur J Epidemiol 1996; 12: 241±244.

251 Akahane Y et al. Hepatitis C virus infection in spouses of

patients with type C chronic liver disease. Ann Intern Med

1994; 120: 748±752.

252 Koda T et al. Hepatitis C transmission between spouses.

J Gastroenterol Hepatol 1996; 11: 1001±1005.

253 Mauser-Bunschoten EP et al. Transmission of hepatitis C

virus to spouses [letter; comment]. Ann Intern Med 1995;

122: 154±155.

254 Win N et al. The low risk of hepatitis C virus transmission

among sexual partners of con®rmed HCV-positive blood

donors. Transfusion Med 1994; 4: 243±244.

255 Diago M et al. Intrafamily transmission of hepatitis C virus:

sexual and non-sexual contacts. J Hepatol 1996; 25:

125±128.

256 Saltoglu N et al. Sexual and non-sexual intrafamilial

spread of hepatitis C virus: intrafamilial transmission of

HCV. Eur J Epidemiol 1998; 14: 225±228.

257 Gordon SC et al. Lack of evidence for the heterosexual

transmission of hepatitis C. Am J Gastroenterol 1992; 87:

1849±1851.

258 Quaranta JF et al. Prevalence of antibody to hepatitis C

virus (HCV) in HIV-1-infected patients (nice SEROCO

cohort). J Med Virol 1994; 42: 29±32.

259 van Doornum GJ et al. Prevalence of hepatitis C virus

infections among heterosexuals with multiple partners.

J Med Virol 1991; 35: 22±27.

260 Corona R et al. Heterosexual and homosexual transmission

of hepatitis C virus: relation with hepatitis B virus and

human immunode®ciency virus type 1. Epidemiol Infect

1991; 107: 667±672.

261 Weinstock HS et al. Hepatitis C virus infection among

patients attending a clinic for sexually transmitted diseases.

JAMA 1993; 269: 392±394.

262 Thomas DL et al. Hepatitis C, hepatitis B, and human

immunode®ciency virus infections among non-intraven-

ous drug-using patients attending clinics for sexually

transmitted diseases. J Infect Dis 1994; 169: 990±995.

263 Gust I et al. Prevalence of infection with hepatitis C virus in

Australia. Med J Aust 1989; 151: 719±18.

264 Melbye M et al. Sexual transmission of hepatitis C virus:

cohort study 1981±9 among European homosexual men.

BMJ 1990; 301: 210±212.

265 Westh H et al. Hepatitis C virus antibodies in homosexual

men and intravenous drug users in Denmark. Infection

1993; 21: 115±117.

266 Hadziyannis SJ et al. Hepatitis C virus infection in Greece

and its role in chronic liver disease and hepatocellular

carcinoma. J Hepatol 1993; 17 (suppl 3): S72±7.

267 Gasparini V et al. Hepatitis C virus infection in homosexual

men: a seroepidemiological study in gay clubs in north-

east Italy. Eur J Epidemiol 1991; 7: 665±669.

268 Ricchi E et al. Anti-hepatitis C virus antibodies amongst

Italian homo-bisexual males. Eur J Epidemiol 1992; 8:

804±807.

269 Donahue JG et al. Antibody to hepatitis C virus among

cardiac surgery patients, homosexual men, and intraven-

ous drug users in Baltimore. Maryland Am J Epidemiol

1991; 134: 1206±1211.

270 Tor J et al. Sexual transmission of hepatitis C virus and its

relation with hepatitis B virus and HIV. BMJ 1990; 301:

1130±1133.

271 Sanchez-Quijano A et al. Hepatitis C virus infection in

sexually promiscuous groups. Eur J Clin Microbiol Infect Dis

1990; 9: 610±612.

272 Sonnerborg A et al. Hepatitis C virus infection in individ-

uals with or without human immunode®ciency virus type

1 infection. Infection 1990; 18: 347±351.

273 Osmond DH et al. Comparison of risk factors for hepatitis C

and hepatitis B virus infection in homosexual men. J Infect

Dis 1993; 167: 66±71.

274 Buchbinder SP et al. Hepatitis C virus infection in sexually

active homosexual men. J Infect 1994; 29: 263±269.

275 Ndimbie OK et al. Hepatitis C virus infection in a male

homosexual cohort: risk factor analysis. Genitourin Med

1996; 72: 213±216.

276 Osella AR et al. Hepatitis B and C virus sexual transmission

among homosexual men. Am J Gastroenterol 1998; 93:

49±52.

277 Wu JC et al. Prevalence, infectivity, and risk factor analysis

of hepatitis C virus infection in prostitutes. J Med Virol

1993; 39: 312±317.

278 Develoux M et al. Hepatitis C virus antibodies in prostitutes

in Niger. Trans R Soc Trop Med Hyg 1994; 88: 536.

279 Gutierrez P et al. Prevalence of anti-hepatitis C virus anti-

bodies in positive FTA-ABS non-drug abusing female

prostitutes in Spain. Sex Transm Dis 1992; 19: 39±40.

280 Crofts N et al. Hepatitis C virus infection among a cohort of

Victorian injecting drug users. Med J Aust 1993; 159:

237±241.

281 Crofts N et al. Methadone maintenance and hepatitis C

virus infection among injecting drug users. Addiction 1997;

92: 999±1005.

282 van Beek I et al. Infection with HIV and hepatitis C virus

among injecting drug users in a prevention setting: retro-

spective cohort study. BMJ 1998; 317: 433±437.

283 Chang CJ et al. Hepatitis C virus infection among short-

term intravenous drug users in southern Taiwan. Eur

J Epidemiol 1999; 15: 597±601.

284 Smyth BP et al. Bloodborne viral infection in Irish injecting

drug users. Addiction 1998; 93: 1649±1656.

285 Stark K et al. Frontloading: a risk factor for HIV and

hepatitis C virus infection among injecting drug users in

Berlin. AIDS 1996; 10: 311±317.

286 Van den Hoek JA et al. Prevalence, incidence, and risk

factors of hepatitis C virus infection among drug users in

Amsterdam. J Infect Dis 1990; 162: 823±826.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

Epidemiological review of hepatitis C 99

Page 17: Hepatitis C: an epidemiological review

287 Van Ameijden EJ et al. A longitudinal study on the inci-

dence and transmission patterns of HIV, HBV and HCV

infection among drug users in Amsterdam. Eur J Epidemiol

1993; 9: 255±262.

288 Galeazzi B et al. Hepatitis C virus infection in Italian

intravenous drug users: epidemiological and clinical

aspects. Liver 1995; 15: 209±212.

289 Wood®eld DG et al. Hepatitis C virus infections in

oral and injectable drug users. NZ Med J 1993; 106:

332±334.

290 Robinson GM et al. Hepatitis C prevalence and needle/

syringe sharing behaviours in recent onset injecting drug

users. NZ Med J 1995; 108: 103±105.

291 Kemp et al. Injecting behaviours and prevalence of hepa-

titis B, C and D markers in New Zealand injecting drug user

populations. NZ Med J 1998; 111: 50±53.

292 Hagan H et al. Syringe exchange and risk of infection

with hepatitis B and C viruses. Am J Epidemiol 1999; 149:

203±213.

293 Bolumar F et al. Prevalence of antibiotics to hepatitis C in a

population of intravenous drug users in Valencia, Spain.

1990±92. Int J Epidemiol 1996; 25: 204±209.

294 Santana Rodriguez OE et al. Prevalence of serologic

markers of HBV, HDV, HCV and HIV in non-injection drug

users compared to injection drug users in Gran Canaria,

Spain. Eur J Epidemiol 1998; 14: 555±561.

295 Garfein RS et al. Prevalence and incidence of hepatitis C

virus infection among young adult injection drug users.

JAIDS 1998; 18 (suppl 1): S11±9.

Ó 2002 Blackwell Science Ltd, Journal of Viral Hepatitis, 9, 84±100

100 M. I. Memon & M. A. Memon