International Journal of Gynecology and Obstetrics 128 (2015) 165–168
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
The prevalence of sexually transmitted infections among migrant female patients in Italy Antonio S. Laganà a,⁎, Valeria Gavagni b, Justine V. Musubao a, Alfonsa Pizzo a a b
Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences, University of Messina, Messina, Italy Department of Infectious Diseases, University of Messina, Messina, Italy
a r t i c l e
i n f o
Article history: Received 19 March 2014 Received in revised form 25 July 2014 Accepted 24 September 2014 Keywords: Epidemiology Migrants Screening Sexually transmitted infections
a b s t r a c t Objective: To evaluate the prevalence of several sexually transmitted infections (STIs) among migrant women incoming to Italy. Methods: A single-center, prospective, observational study was conducted of migrant women who had attended an outpatient clinic in Messina, Italy, between January 1, 2003, and December 31, 2013. Participants underwent a gynecologic examination and a cervical smear test. Patients who showed cytologic alterations underwent human papillomavirus (HPV) typing by PCR and allele-specific hybridization. Routine tests for hepatitis B virus (HBV), hepatitis C virus (HCV), HIV, and syphilis were done for pregnant participants. Results: Overall, 724 women were enrolled, of whom 320 (44.2%) were pregnant. The mean ± SD age was 33.1 ± 9.8 years. Cytologic abnormalities were recorded for 76 (10.5%) participants. Among 46 who attended a follow-up clinic, 32 (69.6%) tested positive for HPV serotypes. Among the pregnant women, 9 (2.8%) had HBV infection, 3 (0.9%) had HCV infection, and 1 (0.3%) had HIV infection. No cases of syphilis were recorded. Conclusion: The prevalence of STIs among migrant women in Messina is similar to that among nonmigrants. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction An analysis of the findings of the Italian National Institute of Health reported 18 000 cases of sexually transmitted infections (STIs) among migrant patients in Italy between 1990 and 2008 [1]. The annual proportion of migrants in Italy (who are mostly of European and African origin) affected by an STI rose from 10% in 1994 to 35% in 2008; this increase is directly proportional to the growth of the migrant population in Italy within the same timeframe [1]. In Italy, most migrant patients diagnosed with STIs are heterosexual and have a low level of education [1]. Only 1.2% use illicit drugs, and one-fifth have previously had an STI [1]. Compared with nonmigrant patients, more migrant patients have gonorrhea (9.3% vs 4.1%), latent syphilis (15.6% vs 6.9%), and Chlamydia trachomatis infection (8.1% vs 5.7%) [1]. By contrast, the prevalence of HIV infection is lower in migrants (5.3%) than in nonmigrants (8.8%) [1,2]. Trends in the main STIs require continuous monitoring, particularly because the prevalences of STIs are an indicator of living conditions (e.g. poverty, housing, and habits) and access to prevention. The continuous incoming migratory flow in Italy requires detailed analysis of the epidemiology of STIs to assess whether different health policies should be adopted. This analysis should be as accurate and transparent ⁎ Corresponding author at: Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences, University of Messina, Via C. Valeria 1, 98125 Messina, Italy. Tel.: +39 0902212183; fax: +39 0902937083. E-mail address: [email protected] (A.S. Laganà).
as possible because the perception of risk could be negatively emphasized by the media without any medical correlation, which might potentially lead to a stereotype of migrants as disease carriers, with the resulting effect of creating and reinforcing suspicion and diffidence against what might be perceived as diversity. The Italian health service guarantees that all individuals within the national territory have the right to healthcare, so such care should be readily available to the migrant population. The aim of the present study was to evaluate the prevalence of several STIs—syphilis and infections with HPV, hepatitis B virus (HBV), hepatitis C (HCV), and HIV—among migrant female patients in a dedicated outpatient clinical setting in Italy.
2. Materials and methods The present single-center, prospective, observational study was conducted at an outpatient clinic for migrant women at the Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences of the University Hospital “G. Martino” in Messina, Italy. All female patients who attended the outpatient clinic were informed about the medical procedures that would be done and were asked to enroll in the study. Women who attended the clinic between January 1, 2003, and December 31, 2013, were included in the study if they had voluntarily chosen to participate and signed informed consent for both the procedures and data collection. The study was designed in accordance with the Helsinki Declaration, conformed to the Committee on
http://dx.doi.org/10.1016/j.ijgo.2014.08.013 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
166
A.S. Laganà et al. / International Journal of Gynecology and Obstetrics 128 (2015) 165–168
Publication Ethics guidelines [3], and was approved by the institutional review board of the hospital. Information about the age and nationality of each participant was recorded. A gynecologic exam and cervical smear test were performed. If the patient was pregnant, routine infectology tests for infectious markers of HBV, HCV, HIV, and syphilis were also done. The cervical smear was performed with a thin-layer cytology preparation (ThinPrep, Cytyc Corporation, Boxborough, MA, USA). Patients who showed cytologic alterations according to the Bethesda classification [4] also underwent a test for HPV genotypes by nested PCR, amplification of the L1 region, and typing by allele-specific hybridization. To eliminate bias, all clinical gynecologic procedures were performed by one operator (A.P.), and every examination was conducted in the same laboratory. The study design, analysis, interpretation of data, and manuscript drafting and revisions followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement [5]. For data reporting, parametric values are expressed as mean ± SD, whereas nonparametric values are expressed as number (percentage).
3. Results During the study period, 724 migrant women were enrolled, of whom 320 (44.2%) were pregnant. The mean age of the participants was 33.1 ± 9.8 years. Their countries of origin are shown in Table 1. Among the 724 patients who underwent cervical screening, 76 (10.5%) showed cytologic abnormalities. More than one-fifth of Table 1 Origin of participants (n = 724). Country of origin
No. (%)
Sri Lanka Romania Philippines Morocco Poland Ukraine Russia China Cuba Colombia Tunisia Albania Senegal Belarus India Mauritius Nigeria Moldova Bangladesh Israel Kosovo Brazil Argentina Ecuador Venezuela El Salvador Ghana Slovakia Bosnia Greece Dominican Republic Peru Guinea Libya Ethiopia Serbia Dominican Republic Slovenia Croatia Hungary Bulgaria
236 (32.6) 139 (19.2) 113 (15.6) 88 (12.2) 21 (2.9) 14 (1.9) 14 (1.9) 11 (1.5) 9 (1.2) 9 (1.2) 9 (1.2) 5 (0.7) 5 (0.7) 5 (0.7) 4 (0.6) 4 (0.6) 3 (0.4) 3 (0.4) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1)
participants of Polish, Russian, and Ukrainian origins had positive cervical smear tests (Table 2). Only 46 (60.5%) of the 76 patients with a positive smear test returned to the clinic for the recommended HPV DNA test. Among those tested, 32 (69.6%) tested positive for HPV infection. The genotype was not identified in 9 (28.1%) patients because they dropped out before genotyping. Eight multiple infections were identified. The most frequent identified genotype was HPV16 (identified in 8 [25.0%] patients), followed by HPV31 (5 [15.6%]), HPV6 (5 [15.6%]), HPV18 (2 [6.3%]), HPV31 (2 [6.3%]), and HPV66 (2 [6.3%]). Other high-risk (HPV35, HPV51, HPV53, and HPV58) and low-risk (HPV54, HPV70, HPV72, and HPV73) genotypes were identified less frequently (Fig. 1). The genotypes HPV16, HPV6, and HPV31 were prevalent among the 10 Romanian women who tested positive for HPV (Table 3). Multiple infections were not recorded for women of Moroccan, Polish, or Russian origin (Table 3). Among the 320 pregnant patients, 9 (2.8%) had HBV infection, 3 (0.9%) had HCV infection, and 1 (0.3%) had HIV infection (Table 4). No cases of syphilis were recorded (Table 4). Ten (3.1%) of 320 pregnant women had been immunized against HBV. The proportion of women who were immunized varied by country, from 3 (5.8%) of 52 women from the Philippines and 2 (5.0%) of 40 from Romania, to 3 (2.1%) of 140 from Sri Lanka.
4. Discussion In the present study, one-tenth of female migrants had a positive cervical smear, with proportions varying by country of origin. Approximately 70% of participants who went on to be tested were positive for HPV infection. Few pregnant participants had positive tests for other STIs. Infection with HPV is common among the general population worldwide: evidence suggests that more than 75% of sexually active women have at least one HPV infection during their lifetime and more than 59% have a high-risk HPV genotype [6–10]. In Italy, the prevalence of any type of HPV among women aged between 17 and 70 years varies from 7% to 16% [11]. The prevalence of HPV infection in the present study population was 4.4% overall, but rose to 69.6% among participants whose cervical smear results showed cytologic abnormalities. Among women diagnosed with cervical cancer worldwide, the most common HPV genotype is HPV16, which is identified in 50% (43.4%– 56.0%) of patients [7,8]. HPV18 has a prevalence of 15% (10.6%–22.1%) [7,8]. Notably, HPV16 and HPV18 together are responsible for 70% of the cases of cervical cancer [7,8]. Other genotypes (e.g. HPV31, HPV33, HPV35, HPV45, HPV52, HPV56, HPV58, and HPV59) are observed with varying frequency across countries [7,8]. In the present study’s migrant population, the most frequent genotype was HPV16, which is the same as in nonmigrants in Italy [9]. However, approximately 40% of the participants with cytologic abnormalities did not return to the clinic for a HPV test and the HPV genotypes were not identified in more than one-quarter of those participants who did undergo HPV testing. Table 2 Origin of patients with cytologic abnormalities.a Country of origin
No. of patients
Positive cervical smear
Negative cervical smear
Sri Lanka Romania Philippines Morocco Poland Russia Ukraine China Colombia Others Total
236 139 113 88 21 14 14 11 9 79 724
12 (5.1) 20 (14.4) 7 (6.2) 8 (9.1) 5 (23.8) 4 (28.6) 3 (21.4) 2 (18.2) 1 (11.1) 14 (17.7) 76 (10.5)
224 (94.9) 119 (85.6) 106 (93.8) 80 (90.9) 16 (76.2) 10 (71.4) 11 (78.6) 9 (81.8) 8 (88.9) 65 (82.3) 648 (89.5)
a
Values are given as number (percentage) unless stated otherwise.
A.S. Laganà et al. / International Journal of Gynecology and Obstetrics 128 (2015) 165–168
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Fig. 1. HPV genotypes among the 32 study participants who tested positive for HPV DNA. Abbreviation: HPV, human papillomavirus.
The epidemiology of HBV infection in Italy has changed significantly in past decades, in line with the introduction of compulsory vaccineprophylaxis. Infection with HBV is now present at a very low endemic level, having decreased from 12 cases per 100 000 inhabitants in 1985 to 0.9 cases per 100 000 inhabitants in 2010 (0.0, 0.5, and 1.2 cases per 100 000 people aged 0–14, 15–24 and ≥ 25 years, respectively) [12]. Analysis of the seroprevalence of infectious markers of HBV among the 320 pregnant women showed that almost 3% were infected with this virus, which is higher than the 12.5% reported for nonmigrant women in Italy [13]. The difference increases further if the women coming from areas endemic for HBV are considered—e.g. the seroprevalence of HBV among Romanian women was 12.5%. Furthermore, the present data demonstrated the low prevalence of immunization for HBV among migrant women: only 3% of the pregnant participants had been vaccinated. This low prevalence of immunization in the study sample of migrant women, coupled with new cases of infections affecting any age group, emphasizes the need to improve monitoring and to provide opportunities to vaccinate all individuals who seem to be unprotected, including close relatives.
The epidemiology of HCV also seems to have changed considerably in the past two decades, with a progressive decrease in its incidence and a change in risk factors since the introduction of screening tests for blood donors. The prevalence of HCV remains high in Italy, with a gradient that increases from 2%–4% in northern Italy to 5%–8% in central Italy and more than 8% in southern Italy, and with age [13–16]. The prevalence of infection with HCV among pregnant participants in the present study was 0.9%, which is lower than the national average. However, the difference is smaller for women coming from regions with a high prevalence of HCV infection—e.g. 5.0% of participants from Romania had this infection. Several other studies [13,17–19] have compared the prevalence of anti-HCV antibodies among migrants in a specific country with that among nonmigrants. These studies showed that, for all migrant groups and for every country except Italy, the prevalence of anti-HCV was higher among immigrants than among the general population [13,17–19]. With regard to HIV infection, approximately 2.6 million new cases were recorded worldwide in 2009, which is a reduction of 20% from the number observed in 1999 [20]. Between 2001 and 2009, the
Table 3 HPV infections by country of origin. Country of origin
No. of HPV-positive women
Romania
10
Sri Lanka Morocco
5 4
Poland
3
Philippines Russia Belarus Albania Colombia Slovakia Slovenia Ukraine
2 2 1 1 1 1 1 1
Abbreviation: HPV, human papillomavirus.
Single infection
Multiple infection
Not identified
Type
No. (%)
Type
No. (%)
HPV6 HPV16 HPV31 HPV35 HPV73 HPV31 HPV6 HPV6 HPV16 HPV33 HPV53 HPV16 – – – – – –
1 (10) 3 (30) 1 (10) 1 (10) 1 (20) 2 (50) 1 (25) 1 (33.3) 1 (33.3) 1 (33.3) 1 (50) 1 (50) 0 0 0 0 0 0
HPV6 + HPV72 HPV33 + HPV51 HPV6 + HPV31 + HPV6 6 HPV18 + HPV70 –
1 (10) 1 (10) 1 (10)
1 (10)
1 (20) 0
3 (60) 1 (25)
–
0
0
1 (50) 0 1 (100) 1 (100) 1 (100) 0 0 0
0 1 (50) 0 0 0 1 (100) 1 (100) 1 (100)
HPV16 – HPV16 HPV16 HPV31 – – –
+ HPV66 + HPV54 + HPV18 + HPV58
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A.S. Laganà et al. / International Journal of Gynecology and Obstetrics 128 (2015) 165–168
Table 4 Prevalence of infections with HBV, HCV, and HIV, and of syphilis among pregnant patients.a Country of origin
No. of women
HBV
HCV
HIV
Syphilis
Sri Lanka Philippines Morocco Romania Poland Tunisia Belarus Others Total
140 52 45 40 7 4 1 31 320
0 0 2 (4.4) 5 (12.5) 1 (14.3) 0 1 (100) 0 9 (2.8)
1 (0.7) 0 0 2 (5.0) 0 0 0 0 3 (0.9)
0 0 0 1 (2.5) 0 0 0 0 1 (0.3)
0 0 0 0 0 0 0 0 0
Abbreviations: HBV, hepatitis B virus; HCV, hepatitis C virus. a Values are given as number (percentage) unless indicated otherwise.
incidence of HIV infection decreased by 25% in 33 countries, 22 of which are in Sub-Saharan Africa, which retains the highest number of infections [20]. However, some regions do not reflect the general trend: from 2001 to 2009, the incidence of HIV rose by over 25% in seven countries of eastern Europe and central Asia [20]. In Italy in 2012, the incidence of new diagnoses of HIV infection was 22.3 per 100 000 migrant residents as compared with five new cases per 100 000 Italian residents [21]. The incidence of HIV infection among nonmigrants as compared with migrants is not distributed uniformly across the country: in 2012, a high incidence among migrants was observed in central-south Italy (20–24 per 100 000 residents), whereas the highest incidences among nonmigrants were recorded in central-north Italy (0–8 per 100 000 residents) [21]. The prevalence of HIV infection among the 320 pregnant women in the present study was 0.3% (the only positive result was found for a woman of Romanian origin). This result agrees with the recent trend in the prevalence of HIV infection in central and western Europe (0.1% to b0.5%) [20]. Although no cases of syphilis were recorded in the present sample, latent syphilis is more frequently diagnosed among migrants than among nonmigrants in Italy (15.6% vs 6.9%) [1]. One of the limitations of the present analysis is that the more prevalent STIs (chlamydia and gonorrhea) were not evaluated, which could represent a source of bias. Health protection in Italy is enshrined in Article 32 of the Constitution, which, identifying health as a “fundamental right of the individual and collective interest”, does not base this right on Italian citizenship or status (regular or irregular) of residence. From this principle stems current legislation that establishes the right of any migrant incoming to Italy to take advantage of public health services irrespective of their administrative or judicial situation [22]. Health care for migrants coming into Italy is regulated by legislative decree no. 286 of 1998—the “Consolidation Act on concerning immigration and the status of foreigners” [23]—which for the first time offers a modern legal approach to guarantee the right of ordinary inclusion of migrants in the Italian National Health System (NHS). Concerning this Consolidation Act, Article 34 addresses the topic of foreigners enrolled in the Italian NHS, who are therefore legally residing in Italy. Article 35 is dedicated to those who are not enrolled in the Italian NHS (e.g. short-term migrants such as students or tourists), or who do not meet the criteria for regular entry and residence. In conclusion, the present epidemiologic approach has revealed that the prevalences of various STIs among migrants in Italy are not higher than those of nonmigrants. The infections could be a result of marginalization and poverty upon arrival in Italy, their place of stay, and immigration policies. The present data analysis may help, at least in part, to address health policies management: given the results, it seems unnecessary that migrant female patients incoming to Italy should undergo STI screening different from that undergone by Italian women. It would be better to use any available resources to avoid—or at least reduce—the serious situations of marginality and poverty that migrants very often have to face.
Conflict of interest The authors have no conflicts of interest. References [1] Italian National Institute of Health, Migration and Health. Migration: the reception system towards the immigrant population health services and verification of the right to health of these populations. (in Italian) http://www.iss.it/binary/pres/cont/ SINTESI_PROGETTOMigrazione_e_Salute_CONVEGNO.pdf. Published June 2010. Accessed September 20, 2014. [2] Bisoffi Z, Panebianco R. Infectious diseases of the migrant: the perspective of hospital. Epidemiology and risks associated with health and prevention. (in Italian) Ital J Public Health 2011;8(3 Suppl.):S23–33. [3] Wager E, Kleinert S. Responsible research publication: international standards for authors. http://publicationethics.org/files/International%20standards_authors_for% 20website_11_Nov_2011.pdf. Published 2011. Accessed September 20, 2014. [4] Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, et al. The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 2002;287(16):2114–9. [5] von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007;370(9596): 1453–7. [6] Frazer IH, Cox JT, Mayeaux Jr EJ, Franco EL, Moscicki AB, Palefsky JM, et al. Advances in prevention of cervical cancer and other human papillomavirus-related diseases. Pediatr Infect Dis J 2006;25(2 Suppl.):S65–81. [7] Clifford G, Franceschi S, Diaz M, Muñoz N, Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine 2006;24(Suppl. 3) S3/26–34. [8] Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjose S, Bruni L, et al. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 2008;26(Suppl. 10):K1–K16. [9] Clifford GM, Gallus S, Herrero R, Muñoz N, Snijders PJ, Vaccarella S, et al. Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis. Lancet 2005;366(9490):991–8. [10] International Agency for Research on Cancer. All Cancers (excluding non-melanoma skin cancer): Estimated Incidence, Mortality and Prevalence Worldwide in 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx. Published 2013. Accessed September 23, 2014. [11] Epicentro, National Center for Epidemiology, Surveillance and Health Promotion. HPV infection. http://www.epicentro.iss.it/problemi/hpv/epid.asp#Italia. (in Italian). Published 2014. Accessed September 20, 2014. [12] Zuccaro O, Tosti ME, Mele A, Spada E, SEIEVA Collaborative Group. Epidemiology of acute viral hepatitis in Italy: results of the surveillance through SEIEVA (Sistema Epidemiologico Integrato dell’Epatite Virale Acuta). http://www.iss.it/binary/publ/ cont/12_4_web.pdf. Published 2012. Accessed July 26, 2014. [13] European Centre for Disease Prevention and Control (ECDC). Technical Report. Hepatitis B and C in the EU neighbourhood: prevalence, burden of disease and screening policies. http://ecdc.europa.eu/en/publications/Publications/TER_100914_Hep_B_C% 20_EU_neighbourhood.pdf. Published September 2010. Accessed July 26, 2014. [14] Fusco M, Girardi E, Piselli P, Palombino R, Polesel J, Maione C, et al. Epidemiology of viral hepatitis infections in an area of southern Italy with high incidence rates of liver cancer. Eur J Cancer 2008;44(6):847–53. [15] Alberti A, Noventa F, Benvegnù L, Boccato S, Gatta A. Prevalence of liver disease in a population of asymptomatic persons with hepatitis C virus infection. Ann Intern Med 2002;137(12):961–4. [16] Kondili LA, Chionne P, Costantino A, Villano U, Lo Noce C, Pannozzo F, et al. Infection rate and spontaneous seroreversion of anti-hepatitis C virus during the natural course of hepatitis C virus infection in the general population. Gut 2002;50(5): 693–6. [17] Chironna M, Germinario C, Lopalco PL, Quarto M, Barbuti S. HBV, HCV and HDV infections in Albanian refugees in Southern Italy (Apulia region). Epidemiol Infect 2000;125(1):163–7. [18] Chironna M, Germinario C, Lopalco PL, Carrozzini F, Quarto M. Prevalence of hepatitis virus infections in Kosovar refugees. Int J Infect Dis 2001;5(4):209–13. [19] Majori S, Baldo V, Tommasi I, Malizia M, Floreani A, Monteiro G, et al. Hepatitis A, B, and C infection in a community of sub-Saharan immigrants living in Verona (Italy). J Travel Med 2008;15(5):323–7. [20] Joint United Nations Programme on HIV/AIDS (UNAIDS). Global Report. UNAIDS Report on the global AIDS epidemic 2010. www.unaids.org/documents/20101123_ GlobalReport_em.pdf. Published 2010. Accessed January 7, 2014. [21] Italian National Institute of Health. Update on new diagnoses of HIV infection and cases of AIDS in Italy to December 31, 2012. http://www.iss.it/binary/ccoa/cont/ Dicembre_2013.pdf. Published December 2013. Accessed September 20, 2014. [22] Italian Parliament, Chamber of Deputies. Regulations governing immigration and the status of foreigners. Law 6 March 1998 n. 40. http://www.camera.it/parlam/leggi/ 98040l.htm. Published March 12, 1998. Accessed July 27, 2014. [23] President of the Italian Republic. Consolidation act of provisions governing immigration and regulations the status of foreigners. Legislative Decree July 25 no. 286. http://www.interno.gov.it/mininterno/export/sites/default/it/assets/files/22/0732_ decreto_legislativo_286-1998.pdf. Published August 18, 1998. Accessed July 27, 2014.
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
The prevalence of sexually transmitted infections among migrant female patients in Italy Antonio S. Laganà a,⁎, Valeria Gavagni b, Justine V. Musubao a, Alfonsa Pizzo a a b
Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences, University of Messina, Messina, Italy Department of Infectious Diseases, University of Messina, Messina, Italy
a r t i c l e
i n f o
Article history: Received 19 March 2014 Received in revised form 25 July 2014 Accepted 24 September 2014 Keywords: Epidemiology Migrants Screening Sexually transmitted infections
a b s t r a c t Objective: To evaluate the prevalence of several sexually transmitted infections (STIs) among migrant women incoming to Italy. Methods: A single-center, prospective, observational study was conducted of migrant women who had attended an outpatient clinic in Messina, Italy, between January 1, 2003, and December 31, 2013. Participants underwent a gynecologic examination and a cervical smear test. Patients who showed cytologic alterations underwent human papillomavirus (HPV) typing by PCR and allele-specific hybridization. Routine tests for hepatitis B virus (HBV), hepatitis C virus (HCV), HIV, and syphilis were done for pregnant participants. Results: Overall, 724 women were enrolled, of whom 320 (44.2%) were pregnant. The mean ± SD age was 33.1 ± 9.8 years. Cytologic abnormalities were recorded for 76 (10.5%) participants. Among 46 who attended a follow-up clinic, 32 (69.6%) tested positive for HPV serotypes. Among the pregnant women, 9 (2.8%) had HBV infection, 3 (0.9%) had HCV infection, and 1 (0.3%) had HIV infection. No cases of syphilis were recorded. Conclusion: The prevalence of STIs among migrant women in Messina is similar to that among nonmigrants. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction An analysis of the findings of the Italian National Institute of Health reported 18 000 cases of sexually transmitted infections (STIs) among migrant patients in Italy between 1990 and 2008 [1]. The annual proportion of migrants in Italy (who are mostly of European and African origin) affected by an STI rose from 10% in 1994 to 35% in 2008; this increase is directly proportional to the growth of the migrant population in Italy within the same timeframe [1]. In Italy, most migrant patients diagnosed with STIs are heterosexual and have a low level of education [1]. Only 1.2% use illicit drugs, and one-fifth have previously had an STI [1]. Compared with nonmigrant patients, more migrant patients have gonorrhea (9.3% vs 4.1%), latent syphilis (15.6% vs 6.9%), and Chlamydia trachomatis infection (8.1% vs 5.7%) [1]. By contrast, the prevalence of HIV infection is lower in migrants (5.3%) than in nonmigrants (8.8%) [1,2]. Trends in the main STIs require continuous monitoring, particularly because the prevalences of STIs are an indicator of living conditions (e.g. poverty, housing, and habits) and access to prevention. The continuous incoming migratory flow in Italy requires detailed analysis of the epidemiology of STIs to assess whether different health policies should be adopted. This analysis should be as accurate and transparent ⁎ Corresponding author at: Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences, University of Messina, Via C. Valeria 1, 98125 Messina, Italy. Tel.: +39 0902212183; fax: +39 0902937083. E-mail address: [email protected] (A.S. Laganà).
as possible because the perception of risk could be negatively emphasized by the media without any medical correlation, which might potentially lead to a stereotype of migrants as disease carriers, with the resulting effect of creating and reinforcing suspicion and diffidence against what might be perceived as diversity. The Italian health service guarantees that all individuals within the national territory have the right to healthcare, so such care should be readily available to the migrant population. The aim of the present study was to evaluate the prevalence of several STIs—syphilis and infections with HPV, hepatitis B virus (HBV), hepatitis C (HCV), and HIV—among migrant female patients in a dedicated outpatient clinical setting in Italy.
2. Materials and methods The present single-center, prospective, observational study was conducted at an outpatient clinic for migrant women at the Department of Paediatric, Gynaecological, Microbiological and Biomedical Sciences of the University Hospital “G. Martino” in Messina, Italy. All female patients who attended the outpatient clinic were informed about the medical procedures that would be done and were asked to enroll in the study. Women who attended the clinic between January 1, 2003, and December 31, 2013, were included in the study if they had voluntarily chosen to participate and signed informed consent for both the procedures and data collection. The study was designed in accordance with the Helsinki Declaration, conformed to the Committee on
http://dx.doi.org/10.1016/j.ijgo.2014.08.013 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
166
A.S. Laganà et al. / International Journal of Gynecology and Obstetrics 128 (2015) 165–168
Publication Ethics guidelines [3], and was approved by the institutional review board of the hospital. Information about the age and nationality of each participant was recorded. A gynecologic exam and cervical smear test were performed. If the patient was pregnant, routine infectology tests for infectious markers of HBV, HCV, HIV, and syphilis were also done. The cervical smear was performed with a thin-layer cytology preparation (ThinPrep, Cytyc Corporation, Boxborough, MA, USA). Patients who showed cytologic alterations according to the Bethesda classification [4] also underwent a test for HPV genotypes by nested PCR, amplification of the L1 region, and typing by allele-specific hybridization. To eliminate bias, all clinical gynecologic procedures were performed by one operator (A.P.), and every examination was conducted in the same laboratory. The study design, analysis, interpretation of data, and manuscript drafting and revisions followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement [5]. For data reporting, parametric values are expressed as mean ± SD, whereas nonparametric values are expressed as number (percentage).
3. Results During the study period, 724 migrant women were enrolled, of whom 320 (44.2%) were pregnant. The mean age of the participants was 33.1 ± 9.8 years. Their countries of origin are shown in Table 1. Among the 724 patients who underwent cervical screening, 76 (10.5%) showed cytologic abnormalities. More than one-fifth of Table 1 Origin of participants (n = 724). Country of origin
No. (%)
Sri Lanka Romania Philippines Morocco Poland Ukraine Russia China Cuba Colombia Tunisia Albania Senegal Belarus India Mauritius Nigeria Moldova Bangladesh Israel Kosovo Brazil Argentina Ecuador Venezuela El Salvador Ghana Slovakia Bosnia Greece Dominican Republic Peru Guinea Libya Ethiopia Serbia Dominican Republic Slovenia Croatia Hungary Bulgaria
236 (32.6) 139 (19.2) 113 (15.6) 88 (12.2) 21 (2.9) 14 (1.9) 14 (1.9) 11 (1.5) 9 (1.2) 9 (1.2) 9 (1.2) 5 (0.7) 5 (0.7) 5 (0.7) 4 (0.6) 4 (0.6) 3 (0.4) 3 (0.4) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 2 (0.3) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 1 (0.1)
participants of Polish, Russian, and Ukrainian origins had positive cervical smear tests (Table 2). Only 46 (60.5%) of the 76 patients with a positive smear test returned to the clinic for the recommended HPV DNA test. Among those tested, 32 (69.6%) tested positive for HPV infection. The genotype was not identified in 9 (28.1%) patients because they dropped out before genotyping. Eight multiple infections were identified. The most frequent identified genotype was HPV16 (identified in 8 [25.0%] patients), followed by HPV31 (5 [15.6%]), HPV6 (5 [15.6%]), HPV18 (2 [6.3%]), HPV31 (2 [6.3%]), and HPV66 (2 [6.3%]). Other high-risk (HPV35, HPV51, HPV53, and HPV58) and low-risk (HPV54, HPV70, HPV72, and HPV73) genotypes were identified less frequently (Fig. 1). The genotypes HPV16, HPV6, and HPV31 were prevalent among the 10 Romanian women who tested positive for HPV (Table 3). Multiple infections were not recorded for women of Moroccan, Polish, or Russian origin (Table 3). Among the 320 pregnant patients, 9 (2.8%) had HBV infection, 3 (0.9%) had HCV infection, and 1 (0.3%) had HIV infection (Table 4). No cases of syphilis were recorded (Table 4). Ten (3.1%) of 320 pregnant women had been immunized against HBV. The proportion of women who were immunized varied by country, from 3 (5.8%) of 52 women from the Philippines and 2 (5.0%) of 40 from Romania, to 3 (2.1%) of 140 from Sri Lanka.
4. Discussion In the present study, one-tenth of female migrants had a positive cervical smear, with proportions varying by country of origin. Approximately 70% of participants who went on to be tested were positive for HPV infection. Few pregnant participants had positive tests for other STIs. Infection with HPV is common among the general population worldwide: evidence suggests that more than 75% of sexually active women have at least one HPV infection during their lifetime and more than 59% have a high-risk HPV genotype [6–10]. In Italy, the prevalence of any type of HPV among women aged between 17 and 70 years varies from 7% to 16% [11]. The prevalence of HPV infection in the present study population was 4.4% overall, but rose to 69.6% among participants whose cervical smear results showed cytologic abnormalities. Among women diagnosed with cervical cancer worldwide, the most common HPV genotype is HPV16, which is identified in 50% (43.4%– 56.0%) of patients [7,8]. HPV18 has a prevalence of 15% (10.6%–22.1%) [7,8]. Notably, HPV16 and HPV18 together are responsible for 70% of the cases of cervical cancer [7,8]. Other genotypes (e.g. HPV31, HPV33, HPV35, HPV45, HPV52, HPV56, HPV58, and HPV59) are observed with varying frequency across countries [7,8]. In the present study’s migrant population, the most frequent genotype was HPV16, which is the same as in nonmigrants in Italy [9]. However, approximately 40% of the participants with cytologic abnormalities did not return to the clinic for a HPV test and the HPV genotypes were not identified in more than one-quarter of those participants who did undergo HPV testing. Table 2 Origin of patients with cytologic abnormalities.a Country of origin
No. of patients
Positive cervical smear
Negative cervical smear
Sri Lanka Romania Philippines Morocco Poland Russia Ukraine China Colombia Others Total
236 139 113 88 21 14 14 11 9 79 724
12 (5.1) 20 (14.4) 7 (6.2) 8 (9.1) 5 (23.8) 4 (28.6) 3 (21.4) 2 (18.2) 1 (11.1) 14 (17.7) 76 (10.5)
224 (94.9) 119 (85.6) 106 (93.8) 80 (90.9) 16 (76.2) 10 (71.4) 11 (78.6) 9 (81.8) 8 (88.9) 65 (82.3) 648 (89.5)
a
Values are given as number (percentage) unless stated otherwise.
A.S. Laganà et al. / International Journal of Gynecology and Obstetrics 128 (2015) 165–168
167
Fig. 1. HPV genotypes among the 32 study participants who tested positive for HPV DNA. Abbreviation: HPV, human papillomavirus.
The epidemiology of HBV infection in Italy has changed significantly in past decades, in line with the introduction of compulsory vaccineprophylaxis. Infection with HBV is now present at a very low endemic level, having decreased from 12 cases per 100 000 inhabitants in 1985 to 0.9 cases per 100 000 inhabitants in 2010 (0.0, 0.5, and 1.2 cases per 100 000 people aged 0–14, 15–24 and ≥ 25 years, respectively) [12]. Analysis of the seroprevalence of infectious markers of HBV among the 320 pregnant women showed that almost 3% were infected with this virus, which is higher than the 12.5% reported for nonmigrant women in Italy [13]. The difference increases further if the women coming from areas endemic for HBV are considered—e.g. the seroprevalence of HBV among Romanian women was 12.5%. Furthermore, the present data demonstrated the low prevalence of immunization for HBV among migrant women: only 3% of the pregnant participants had been vaccinated. This low prevalence of immunization in the study sample of migrant women, coupled with new cases of infections affecting any age group, emphasizes the need to improve monitoring and to provide opportunities to vaccinate all individuals who seem to be unprotected, including close relatives.
The epidemiology of HCV also seems to have changed considerably in the past two decades, with a progressive decrease in its incidence and a change in risk factors since the introduction of screening tests for blood donors. The prevalence of HCV remains high in Italy, with a gradient that increases from 2%–4% in northern Italy to 5%–8% in central Italy and more than 8% in southern Italy, and with age [13–16]. The prevalence of infection with HCV among pregnant participants in the present study was 0.9%, which is lower than the national average. However, the difference is smaller for women coming from regions with a high prevalence of HCV infection—e.g. 5.0% of participants from Romania had this infection. Several other studies [13,17–19] have compared the prevalence of anti-HCV antibodies among migrants in a specific country with that among nonmigrants. These studies showed that, for all migrant groups and for every country except Italy, the prevalence of anti-HCV was higher among immigrants than among the general population [13,17–19]. With regard to HIV infection, approximately 2.6 million new cases were recorded worldwide in 2009, which is a reduction of 20% from the number observed in 1999 [20]. Between 2001 and 2009, the
Table 3 HPV infections by country of origin. Country of origin
No. of HPV-positive women
Romania
10
Sri Lanka Morocco
5 4
Poland
3
Philippines Russia Belarus Albania Colombia Slovakia Slovenia Ukraine
2 2 1 1 1 1 1 1
Abbreviation: HPV, human papillomavirus.
Single infection
Multiple infection
Not identified
Type
No. (%)
Type
No. (%)
HPV6 HPV16 HPV31 HPV35 HPV73 HPV31 HPV6 HPV6 HPV16 HPV33 HPV53 HPV16 – – – – – –
1 (10) 3 (30) 1 (10) 1 (10) 1 (20) 2 (50) 1 (25) 1 (33.3) 1 (33.3) 1 (33.3) 1 (50) 1 (50) 0 0 0 0 0 0
HPV6 + HPV72 HPV33 + HPV51 HPV6 + HPV31 + HPV6 6 HPV18 + HPV70 –
1 (10) 1 (10) 1 (10)
1 (10)
1 (20) 0
3 (60) 1 (25)
–
0
0
1 (50) 0 1 (100) 1 (100) 1 (100) 0 0 0
0 1 (50) 0 0 0 1 (100) 1 (100) 1 (100)
HPV16 – HPV16 HPV16 HPV31 – – –
+ HPV66 + HPV54 + HPV18 + HPV58
168
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Table 4 Prevalence of infections with HBV, HCV, and HIV, and of syphilis among pregnant patients.a Country of origin
No. of women
HBV
HCV
HIV
Syphilis
Sri Lanka Philippines Morocco Romania Poland Tunisia Belarus Others Total
140 52 45 40 7 4 1 31 320
0 0 2 (4.4) 5 (12.5) 1 (14.3) 0 1 (100) 0 9 (2.8)
1 (0.7) 0 0 2 (5.0) 0 0 0 0 3 (0.9)
0 0 0 1 (2.5) 0 0 0 0 1 (0.3)
0 0 0 0 0 0 0 0 0
Abbreviations: HBV, hepatitis B virus; HCV, hepatitis C virus. a Values are given as number (percentage) unless indicated otherwise.
incidence of HIV infection decreased by 25% in 33 countries, 22 of which are in Sub-Saharan Africa, which retains the highest number of infections [20]. However, some regions do not reflect the general trend: from 2001 to 2009, the incidence of HIV rose by over 25% in seven countries of eastern Europe and central Asia [20]. In Italy in 2012, the incidence of new diagnoses of HIV infection was 22.3 per 100 000 migrant residents as compared with five new cases per 100 000 Italian residents [21]. The incidence of HIV infection among nonmigrants as compared with migrants is not distributed uniformly across the country: in 2012, a high incidence among migrants was observed in central-south Italy (20–24 per 100 000 residents), whereas the highest incidences among nonmigrants were recorded in central-north Italy (0–8 per 100 000 residents) [21]. The prevalence of HIV infection among the 320 pregnant women in the present study was 0.3% (the only positive result was found for a woman of Romanian origin). This result agrees with the recent trend in the prevalence of HIV infection in central and western Europe (0.1% to b0.5%) [20]. Although no cases of syphilis were recorded in the present sample, latent syphilis is more frequently diagnosed among migrants than among nonmigrants in Italy (15.6% vs 6.9%) [1]. One of the limitations of the present analysis is that the more prevalent STIs (chlamydia and gonorrhea) were not evaluated, which could represent a source of bias. Health protection in Italy is enshrined in Article 32 of the Constitution, which, identifying health as a “fundamental right of the individual and collective interest”, does not base this right on Italian citizenship or status (regular or irregular) of residence. From this principle stems current legislation that establishes the right of any migrant incoming to Italy to take advantage of public health services irrespective of their administrative or judicial situation [22]. Health care for migrants coming into Italy is regulated by legislative decree no. 286 of 1998—the “Consolidation Act on concerning immigration and the status of foreigners” [23]—which for the first time offers a modern legal approach to guarantee the right of ordinary inclusion of migrants in the Italian National Health System (NHS). Concerning this Consolidation Act, Article 34 addresses the topic of foreigners enrolled in the Italian NHS, who are therefore legally residing in Italy. Article 35 is dedicated to those who are not enrolled in the Italian NHS (e.g. short-term migrants such as students or tourists), or who do not meet the criteria for regular entry and residence. In conclusion, the present epidemiologic approach has revealed that the prevalences of various STIs among migrants in Italy are not higher than those of nonmigrants. The infections could be a result of marginalization and poverty upon arrival in Italy, their place of stay, and immigration policies. The present data analysis may help, at least in part, to address health policies management: given the results, it seems unnecessary that migrant female patients incoming to Italy should undergo STI screening different from that undergone by Italian women. It would be better to use any available resources to avoid—or at least reduce—the serious situations of marginality and poverty that migrants very often have to face.
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