Hepatitis A, B, and C Infection in a Community of Sub‐Saharan Immigrants Living in Verona (Italy)

Silvia Majori MD, Vincenzo Baldo MD, Irene Tommasi MD, Maria Malizia MD, Annarosa Floreani MD, Geraldo Monteiro MD, Aladino Ferrari MD, Augusto Accordini BD, Patrizia Guzzo BD, Tatjana Baldovin BD, PhD
DOI: http://dx.doi.org/10.1111/j.1708-8305.2008.00230.x 323-327 First published online: 1 September 2008


Background In Italy, about 5% of the population is represented by immigrants. The epidemiology of hepatitis A virus (HAV), hepatitis B virus (HBV), and hepatitis C virus (HCV) infection in Africa is very different from Europe; the present study aimed to assess the seroprevalence of viral hepatitis infections in sub‐Saharan African immigrants living in Verona.

Methods A total of 182 illegal immigrants were interviewed concerning sociodemographic characteristics and epidemiological information. Their serum was tested for anti‐HAV [immunoglobulin (Ig) G and IgM], HBV (HBsAg, anti‐HBs, anti‐HBc, HBeAg, and anti‐HBe), and HCV (anti‐HCV) markers.

Results The immigrants (age: 3 mo–60 y) were mostly single and males, with a higher education; only 50% of them declared having a regular job. Anti‐IgG HAV+ prevalence was 99.5% (100% HAV positivity in the younger age bracket). As for HBV, 67.6% (123) of the immigrants were naturally infected and 9.3% had chronic infection; 4.4% were anti‐HBs+ isolated (vaccinated). For HBV infection (any HBV marker), a significant difference was only found for increasing age ( p< 0.01) and married people ( p< 0.001). A statistically significant prevalence of HBsAg was found among the unemployed ( p< 0.001) and those with a lower education ( p< 0.05). Five cases (2.7%) resulted in HCV+ with no reported specific risk factors and with no significantly different sociodemographic features; these people tended to report a low level of education and unemployment.

Conclusions HAV and HBV positivity is higher than in the autochthonous population. While HAV positivity merely represents past infection, the high prevalence of HBsAg in immigrants and the presence of HBsAg/HBeAg in the same group may represent a risk for HBV transmission. The HCV positivity rate resulted similar to the prevalence of the Italian population.

In the past years, immigration flows to Italy have increased enormously, passing from 140,000 immigrants in 1970 to beyond 1 million in 1997 and nearly 3 million in 2005, representing nowadays about 5% of the country’s population and ranking Italy in an intermediate position for immigration within the European Union. 1,2 The majority of Italy’s immigrants come from Europe (47.3%), Africa (23.7%), and Asia (17.3%), and their distribution throughout the country depends on the demand for work: approximately 60% live in the north, 30% in central Italy, and 10% in the south. Such a distribution is related to the level of wealth and job opportunities. Since the 1990s, the rate of immigration has been the highest in northeast Italy. The north‐to‐south gradient of immigration explains also a different risk of transmission of infectious agents from an infected individual to susceptible contacts in the resident population.

Considering in particular immigrants coming from Africa, and especially from the sub‐Saharan area, it cannot be ignored that the social and sanitary situation (prevention, diagnosis, and medical care) and the epidemiology of hepatitis infections in general are very different from the situation in Europe.

Hepatitis B virus (HBV) infection is endemic in sub‐Saharan Africa and is usually acquired in early childhood, either at birth or by early horizontal transmission, 3,4 with an 8% to 20% prevalence of chronic carriers (HBsAg positivity), which is consistently higher compared with Western and Central Europe (0.2%–0.5%) 4 including Italy where the actual rate prevalence is under 2%. 5

The prevalence of hepatitis C virus (HCV) infection is very high in many African countries, averaging between 5 and 10%, in sharp contrast with the majority of Europe, where it is around 1%. 6,7 In northeastern Italy, pregnant women have shown a prevalence of HCV infection of 1.9% and an HBsAg positivity rate of 1%. 8

In developing countries, most people are infected with hepatitis A virus (HAV) early in life, and more than 90% of people are anti‐HAV positive. In the past few decades, HAV has progressively decreased in Italy: nowadays, people under 40 years old are generally anti‐HAV negative, and the interepidemic incidence of symptomatic hepatitis A is less than 3/100,000 population. 5

Economic difficulties and transport development drive migration to developed countries, and this could theoretically facilitate the spread of pathogenic microorganisms. Hence, the importance of an adequate social, economic, and cultural integration and the need for an efficient health service with an effective prevention policy are proven.

Our knowledge of the state of health of Italian immigrants is still insufficient owing to the numbers of illegal immigrants, the dynamics of the migratory flow, and the lack of adequate observation and research tools. 9

Though they are not evenly distributed throughout the country, several voluntary associations have played a fundamental part in providing health care for illegal immigrants. In a group of illegal immigrants from sub‐Saharan Africa living in Verona (northeast Italy) and attending a health care center run by a group of medical volunteers, this study assessed the seroprevalence of viral hepatitis infections and its possible impact on the immigrants’ own communities and on the autochthonous population.


The study was conducted in Verona (Italy) between March 2004 and December 2005 on 182 illegal immigrants from sub‐Saharan Africa attending a volunteer health center predisposed specially for illegal immigrants, as these subjects cannot use the standard national medical advices. After a medical checkup, all subjects consecutively enrolled gave their informed consent to join the study and were interviewed by a member of the medical staff in accordance with Italian law on privacy. Their sociodemographic characteristics (nationality, age, sex, marital status, the number of cohabitants in their accommodation, their level of education, and employment), vaccinations, and epidemiological information on the risk of parenteral/sexual transmission of infections [history of intravenous drug use (IVDU) and surgery] were collected using a standard questionnaire designed by a research doctor with expertise in educational programs. The languages used for interviews were English and French, and in any case, some cultural mediators were present. Each interviewer was trained during a meeting performed with all medical staff. Refusal rate of participation was around 50%, probably for fear of being identified by Italian authorities.

A blood sample for serological tests was collected in a territorial laboratory of the Verona Local Public Health Unit (ULSS 20). Serum samples were divided into two aliquots, one was immediately processed and the other (10 mL) was stored at −70°C.

All samples were tested for anti‐HAV [immunoglobulin (Ig) G and IgM], HBV (HBsAg, anti‐HBs, anti‐HBc, HBeAg, and anti‐HBe), and HCV (anti‐HCV) serum markers using a third‐generation enzyme immunoassay (Abbott Diagnostic, North Chicago, IL, USA) according to the manufacturer’s recommendations. Anti‐HCV enzyme‐linked immunosorbent assay immunoreactivity was confirmed by immunoblotting (Western Blotting, Bio‐Rad, Marnes la Coquette, France). The study was approved by the local ethic committee.

Analyses were performed using the EPI‐Info 2002 package supplied by the Centers for Disease Control and Prevention (Atlanta, GA, USA), assessing statistical significance with the chi‐square test and Fisher’s exact test as appropriate. Chi‐square for trend and t‐test were also applied. A p value of ≤ 0.05 was considered significant.


Among the 182 immigrants enrolled in the study, 34.1% (n= 62) came from Nigeria, 9.3% (n= 17) from Ghana, 6.6% (n= 12) from Guinea‐Bissau, and the other 50% (n= 91) from other sub‐Saharan countries.

Of the 182 naturally HBV infected, 17 (9.3%) had a chronic infection (HBsAg or HBsAg/HBeAg positivity) and 106 (58.2%) resulted in anti‐HBc isolated or anti‐HBs/anti‐HBc positive.

Eight (4.4%) were anti‐HBs+ isolated and reported having been vaccinated: two of them were under 29 years old and six were between 30 and 39 years old (Table 1).

View this table:
Table 1

Prevalence of HBV markers infection in 182 sub‐Saharan immigrants

MarkersN subjects (182)%
HBsAg+16Embedded Image
HBsAg+/HB Ag+1
anti‐HBs/anti‐HBc6435.2Embedded Image
anti‐HBc isolated4223.1
anti‐HBs isolated84.4

Positivity to HBV, HCV, and HAV infections in the 182 subjects according to their sociodemographic features is shown in Table 2.

View this table:
Table 2

Rate of positivity to HBV, HCV, and HAV infection in 182 sub‐Saharan immigrants according to sociodemographic characteristics

HBsAg/HBeAgAny marker*Anti‐HCVAnti‐HAV
CharacteristicsSubjects, NN%N%N%N%
Age class
 00–243126.52064.5 26.531100.0
 25–293625.61747.2 12.836100.0
 30–3453611.33260.4 11.95298.1
 35–3950510.04284.0 00.050100.0
 ≥4012216.712100.0 18.312100.0
Civil status
 Married641421.95585.9 11.66398.4
 Single11832.56857.6 43.4118100.0
 Employed9544.2 6366.322.195100.0
 Unemployed871314.9 6069.033.48698.9
Educational level
 Primary/secondary school671116.4§ 5176.146.067100.0
 High school11565.27262.610.911499.1
  • * 123 subjects (excluding vaccinated).

  • Chi‐square for linear trend p< 0.01.

  • p< 0.001.

  • § p< 0.05.

Immigrants were mostly young (age range 3 mo–60 y; mean 31.7 ± 7.94 y), male, and single, with a higher education; only about 50% officially declared they had a job.

Among HBV‐infected subjects, 17 were HBsAg positive: 1 was a 28‐year‐old unemployed single woman and 16 were men (31 ± 8 years old), 2 of them married; 1 was a 4‐year‐old also positive to HBsAg, HBeAg, and HBcAb, with a history of HAV hepatitis but no HCV coinfection. This child lived in a family of five, and no parenteral risk factor was recorded. A statistically significant prevalence of HBsAg/HBeAg markers was found among the unemployed ( p< 0.001) and the people with a lower educational level ( p< 0.05). HBsAg positivity did not correlate with marital status or age. The global rate of HBV infection (any HBV marker) with wild strands showed a significant tendency to increase with age ( p< 0.01) and a positive correlation with married status ( p< 0.001) but not with gender, employment, or educational level.

Of the 182 people enrolled, 5 males (2.7%) who had been in Italy since 2003 were HCV positive. Two of them had a history of HBV infection. No specific parenteral risk factors emerged for these subjects, nor were there any significant differences in their sociodemographic characteristics, though they mostly declared a lower educational level and unemployment.

The overall prevalence of anti‐HAV (all were anti‐IgG HAV+ and none were anti‐IgM HAV+) was 99.5%, and no statistically significant differences emerged in relation to marital status, job, or schooling. The prevalence was evenly distributed in all age brackets, with a 100% of anti‐HAV positivity in the youngest age group.


The constant increase of the migratory flows from developing nations may lead to public health problems such as an increased risk of transmission of some infections to the local population, especially because of the immigrants’ lifestyle (poverty, overcrowded dwellings, and possibility of sexual promiscuity) and the insurgence of new, latent, or subclinical pathologies often deriving from their difficult condition and/or illegal status.

This study reports the prevalence of past or active A, B, and C hepatitis infections in irregular African immigrants without considering further clinical evaluation done elsewhere by specialists.

The people enrolled in this study had a prevalence of HAV infection evenly distributed among the age groups that reached 100% already in the youngest group, confirming that HAV is still rampant in sub‐Saharan Africa, as in the majority of developing nations. 10–15 Anti‐HAV IgM were always negative, however, indicating past infection and the flimsiness of the risk of HAV transmission to the autochthonous population.

Infection early in life explains why there are no differences in the prevalence of HAV in relation to marital status, sex, occupation, or schooling, but it also points to the importance of improving the sanitary conditions and counseling in developing countries.

As for HBV, our sample had a rate of positivity similar to that of the geographical area the people came from, where markers of HBV infection (any marker) and chronic HBV infection are, respectively, 70% to 90% and 8% to 20%, 16 showing a strong circulation of the virus, with infection early in life and a high lifelong risk of HBV transmission to nonimmune subjects.

In Italy, anti‐HBsAg positivity in young people is now around 1.2% to 2.0%, 17 thanks mainly to the compulsory vaccination introduced in 1991, so the presence of HBs/HBeAg positivity and the high HBsAg positivity rate (globally 9.3%) among studied immigrants might represent a public health problem as risk of HBV transmission.

In fact, economically disadvantaged groups, such as illegal immigrants, represent categories that need more attention. People with low socioeconomic status are also people with low educational level and with less awareness of their rights. Thus, they are even more likely at risk of missing facilities. Some HbsAg‐positive subjects are married or cohabiting and are more likely to spread the infection. Finally, the influx of immigrants from undeveloped countries poses the threat of increasing incidence of chronic HBV infection in Western countries.

More vaccination programs are needed to reduce HBV transmission in highly endemic countries: only 4.4% of our sample was anti‐HBs+ isolated. Better hygiene would also be necessary to prevent iatrogenic transmission, 18 as well as better education and the provision of sanitary information.

HCV infection prevalence (2.7%) in studied sub‐Saharan African immigrants is a little higher than that reported in a similar study (0.9%) carried out in the mid‐1990s by Chiaramonte and colleagues, 19 but it is substantially the same as the estimated prevalence in their geographical area of origin (on average around 3.0%). 20 In any case as the most recent Italian data show an HCV incidence rate of 0.5/100,000 and a prevalence rate that ranges from 3% to 26%, 5 at this moment, there is no evidence of any particular impact of this infection on the autochthonous population. 5

The rise in IVDU and prostitution in Western countries might contribute to the maintenance and to the increasing rates of HBV and HCV circulation in subjects coming from developing countries as some authors 18 believe that HCV and HBV infection is mainly transmitted by sexual and family routes.

The small number of HCV‐positive cases (5 of 182) in our sample prevents any further epidemiological analysis: the subjects reported no specific risk factors, and little can be learnt from their demographic data. The lack of a vaccine makes it indispensable to provide counseling for HCV‐positive subjects and their cohabitants, which is also useful for other parenterally or sexually transmitted infections.

Our findings show that Central African immigrants do not currently represent an important health problem for the autochthonous population in terms of hepatitis A or C infection because all the immigrants in our sample had been infected and recovered from HAV infection, and their HCV positivity rate was much the same as it was in northeast Italy (1.9%). 5,8,21

Conversely, their HBsAg positivity was higher than in the local population, and the chronically infected subjects (9.3%) might transmit HBV to other members of the general population in the event of a risk‐related lifestyle for the transmission of parenteral infections or to nonimmune cohabitants or contacts, who should be offered vaccination. A constant seroepidemiological surveillance appears to be essential to monitor the prevalence of the main hepatitis and other infections to control their transmission by means of counseling and vaccination programs wherever possible. Illegal immigrants, compared to legal ones, are more often subject to poverty and inability to access health services. This may lead to reactivation of latent infections or appearance of new ones. 22,23

A disease anywhere is a problem everywhere. Therefore, disease, illness, and health are universally important to everyone. When problems such as newcomer health are national problems, they demand national solutions and approaches. Public health services should not ignore this situation and should take appropriate actions.

Declaration of interests

The authors state that they have no conflicts of interest.


We are very grateful to Franco Dalle Pezze, Morena Nicolis, and Monica Riondato for their technical support.


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