Scotto, Gaetano MD*†; Saracino, Annalisa MD*†; Palumbo, Emilio MD‡; Angarano, Gioacchino MD§; Italian Group for Immigrants Infectious Diseases Study
Migration has probably become one of the most important determinants of global health and social development; it is not a new phenomenon, of course, but is increasing all over the world, and people are moving in larger numbers faster and further than at any other time in history.1,2 Italy, as other European countries and the United States, has recently seen an increase in the number of immigrants; in fact, 85,337 persons were admitted to our country in 1997 and 306,000 in 2001.3 Actually, the total number of legal immigrants can be estimated at 2,600,000 people (4.2% of all Italian population), apart from the illegal clandestine subjects, who are not easily quantifiable.4 In this context, the health service for immigrants, particularly if clandestine, is ineffective and is supported above all by the religious or lay volunteers' associations. Only lately, hospitals and local health services have started on creating outpatient departments for immigrated people, where they can find interpreters, too.5-7 Immigrant people are often considered a source of many infectious diseases (tuberculosis, human immunodeficiency virus [HIV], viral hepatitis) and, in particular, of tropical diseases, such as malaria, schistosomiasis, dengue, virus hepatitis E infection, and so on, endemic in their original countries, but not present in our nation. They are also suspiciously seen by a lot of people as spreading diseases not completely known, for example, Ebola, severe acute respiratory syndrome, and so on. These prejudices cause indifference and "apartheid."8,9
Some international recent studies have effectively demonstrated an increase in cases of tropical infections, particularly malaria, diagnosed in many European operative units of infectious diseases, and the major part of these diseases occurred in immigrant people, coming from countries endemic for these infections.10-12
In light of these considerations, with the cooperation of The Italian Society of Infectious and Tropical Diseases (SIMIT), a retrospective, multicenter, epidemiological survey has been performed, whose aim was to investigate the prevalence of tropical infections in immigrated patients hospitalized in 48 Italian operative units of infectious diseases during 2002.
PATIENTS AND METHODS
The main Italian infectious disease clinics were invited to contribute to the analysis. Each participating center was requested to fill a questionnaire regarding the discharge diagnosis, the country of origin, and demographic features (age, sex, resident status, and inscription in the National Health Service) of each hospitalized immigrant, as reported by the registers of each hospital during 2002. Data were received from 48 Italian infectious disease clinics (12 in the north, 22 in the center, and 12 in the south), with a total of 2255 immigrants hospitalized during 2002. Among this population, we have evaluated the prevalence of patients affected by imported tropical diseases. For each patient, we have also evidenced the following data: age, sex, country of provenience, resident status, time in Italy. In addition, we have compared our experience with previously published Italian and international reports regarding this problem.
Descriptive statistics were calculated for demographic and clinical characteristics of all cases.
Data were collected for 2255 immigrants, representing 5.98% of all patients (N = 37,661), followed by the Infectious Diseases Department cooperating in the study during 2002. Among this population, imported tropical diseases were found in 120 patients, representing 6% of the total of immigrated hospitalized patients. The major part of these subjects were men (n = 77, 64.1%), and the mean age was 28.1 years (range, 17-57 years), with any case observed in pediatric people; 77 patients (64.2%) were hospitalized in the north of Italy (36 in Lombardy), 30 (25%) in the center (20 in Lazio), and the remaining 13 (10.8%) in the south (11 in Apulia). All patients were hospitalized in ordinary regimens. Most patients (108, 90%) come from Africa, whereas only 3 subjects come from South America and 9 from Asia. The mean time of residence in Italy of these patients was 5 months (range, 15 days-13 months); only 22 (18.3%) people had a regular residence permit and were covered by the National Health Service. All these data are summarized in Table 1.
The prevalent disease was malaria (95 cases [79.2%] with 60 men and 35 women), followed by schistosomiasis with 15 cases (12.5%, 10 men and 5 women), amebiasis with 8 cases (6.6%, 7 men and 1 woman), and dengue with 2 cases, both in women (1.6%) (Table 2). The patients affected by malaria (90 cases of infection by Plasmodium falciparum, 4 by Plasmodium vivax, and one by Plasmodium malaria) come principally from Africa (21 from Nigeria, 19 Ghana, 16 Senegal, 7 Burkina Faso, 6 Kenya, 5 Cameroon, Uganda, and Ethiopia), whereas the remaining 10 patients come from Brazil (3 cases), China (4 cases), and India (3 cases) (Table 3). The 4 patients infected by P. vivax come from Ethiopia, whereas the case of infection by P. malaria was evidenced in a Brazilian patient. The 2 patients affected by dengue, both women, come from Sri Lanka, and they arrived in Italy 4 and 6 days ago, respectively. Among the subjects affected by schistosomiasis (6 infected by Schistosoma haematobium and 9 by Schistosoma mansoni), 7 come from Egypt, and all presented an infection by S. mansoni, 6 from Burkina Faso (4 infected by S. haematobium and 2 by S. mansoni), and 2 from Tanzania (infected by S. haematobium). The diagnosis of schistosomiasis was made by serological tests, and all cases of schistosomiasis were chronic disease. Eight patients were affected by amebiasis, and in 5 cases, the localization was intestinal, and in 3, hepatic. All these patients come from Africa (5 Morocco, all with intestinal localization, 2 Senegal, and 1 Cameroon). Human immunodeficiency virus testing was routinely carried out on all hospitalized immigrants, and only 3 patients, all infected by P. falciparum, presented also HIV infection: 2 come from Senegal and one from Nigeria.
The aim of this retrospective, multicenter, epidemiological study was to investigate the prevalence of tropical diseases in immigrated patients hospitalized in Italian infectious disease clinics during 2002. Imported tropical diseases were found in only a few patients, representing 6% of the total of hospitalized immigrants, with a prevalence of malaria (95 cases [79.2%]), whereas prevalent infectious diseases included HIV infection (16%), tuberculosis (13%), and acute or chronic viral hepatitis (12%). We have compared our data with the results evidenced in other Italian and European reports, and we have observed that also in these studies, the rate of tropical diseases in immigrants was very low, with an evident prevalence of malaria.10,11,13-15 The only difference concerned the proportion of patients arriving from Asia and South America; in fact, although in our and in the other Italian studies, the major part of patients come from Africa (90% in our experience), in some European studies, the distribution of patients according to country of origin was different, with many cases of malaria, particularly caused by P. vivax, not only in subjects coming from Africa, but also in patients coming from Asia and South America. Italy, in fact, is the most important reference point for immigrants from Africa and East Europe, although in the last 10 years, the migratory flow toward our country of Asiatic and South American subjects is decreased, and it is increased in other European countries, such as Germany and France.3,4 Thus, our experience, in accordance with literature, evidences that only a few tropical diseases have been imported, and therefore, immigrants should not be considered as infectious disease carriers. Economic need is the principal factor of immigration movement, and these people come to Italy principally to work and it justified the need for relatively young and healthy workers; for this reason, most immigrated people are healthy when they arrive in Italy, whereas ill subjects are unable to enterprise the migratory flow. The range of health issues in these people became inevitably broad after their arrival in Italy, and it included infectious diseases such as HIV infection, tuberculosis, hepatitis, and other diseases such as respiratory or gastrointestinal disorders, directly correlated with the condition of poverty present in many immigrant communities (deficiency of food, unhealthy condition of life, promiscuous sexual relationships).5,6,8
Malaria has represented the prevalent tropical infection, and in literature, it is evident that cases of imported malaria in immigrants are likely to increase in the next few years in many European countries, with the emergence of increasing resistance of parasites to several antimalarial drugs.16 Reports of malaria are increasing in many countries and in areas thought free of the disease, as Italy, and actually it is endemic in 92 countries, with each year having 300 million to 500 million clinical new cases of infection, particularly in the African regions (80%-90% of the total cases in the world).17 In Italy, there are about 500 to 600 new cases per year of imported malaria, and half of these cases are observed in immigrated subjects, whereas the other cases concerned Italian people with a recent temporary stay in an endemic area.18 Thus, the most important factor contributing to the reemergence of this historical disease is human migration. For this reason, it is necessary that any immigrant, or Italian subject, with fever who has traveled to a malaria-endemic area in the last year should be screened with a blood smear for malaria as soon possible.
Most patients affected by tropical diseases were hospitalized in the northern regions of Italy (64.2%) versus 25% in the central regions and 8.5% in southern area. This simply reflects the disparity of immigrant distribution in Italy and indicates that southern Italy is only an arrival point leading to a location in the northern regions.4,5 Another important result regards the resident status of all patients (clandestine or legal resident). In fact, in our population, most of the patients were clandestine, and only 22 (18.3%) people had a regular residence permit and were covered by the National Health Service. These data are in contradiction with other studies that evidenced that most immigrants hospitalized in Italy, independent of the admission diagnosis, have a regular residence permit, whereas clandestine prevents, if possible, any relationship with public structure.9 This difference is probably connected to the relevant clinical aspects of some tropical infections, such as malaria, often well known by these patients, with an inevitable hospitalization.
According to our experience, we can conclude that:
1. The range of health problems in immigrants often became broad after their arrival in Italy and included infectious diseases, such as HIV infection, tuberculosis, and viral hepatitis (the prevalent diseases in hospitalized immigrated patients), which reflect their poor conditions in life.
2. The international community should establish a set of priorities to reduce poverty and social inequalities that facilitate and maintain epidemic infections, such as malaria, in many areas of the world, and all these interventions should provide the involvement of local governments.19,20
The Italian Group for Immigrants Infectious Diseases Study includes:
L. Sacco Hospital Milano (T. Quirino, MD), San Salvatore Hospital Pesaro (M. Calducci, MD), Spedali Civili Hospital Brescia (G. Cadeo, MD), Universitari Clinic Brescia (I. El-Hamad, MD), Civile Hospital Ascoli Piceno (N. Vitucci, MD), Misericordia Hospital Grosseto (M.P. Allegri, MD), S. Carlo Hospital Potenza (B. Piretti, MD), Umberto I Policlinic II Hospital Division Roma (A. Paffetti, MD), Hospital Risceglie (R. Losappio, MD), Hospital Perugia (C. Sfara, MD), Universitari Clinic Foggia (G. Scotto, MD), S. Maria Goretti Hospital Latina (G. Salome, MD), Universitari Clinic Bari (P. Maggi, MD), C. Poma Hospital Mantova (S. Miccolis, MD), Umberto I Policlinic I Hospital Division Roma (A. Brogi, MD), Bambino Gesù Hospital Roma (L. Lancella, MD), S. Maria Annunziata Hospital Firenze (A. Gabbati, MD), Civile Hospital Legnano (M. Villa, MD), Hospital Biella (A. Salatino, MD), Universitari Clinic Ancona (D. Drenaggi, MD), II Universitari Clinic La Sapienza Roma (Prof. M. Ciardi), Umberto I Hospital Frosinone (M. Limodio, MD), Umberto I Policlinic III Hospital Division Roma (Prof. S. Delia), Universitari Clinic Catania (E. Caltabiano, MD; G. Cosentino, MD), Hospital Catania (M. Raspaglieli, MD), Hospital Avezzano (R. Mariani, MD), Universitary Clinic Bologna (S. Sabbatani, MD), Hospital Asti (A. Casabianca, MD), Hospital Cremona (D. Galloni, MD), S. Anna Hospital Ferrara (M. Pantaleoni, MD), Hospital Formia (F. Purificato, MD), S. Antonio Hospital Trapani (V. Portelli, MD), Hospitial Aosta (R. Chasseur, MD), Basilotta Hospital Nicosia (B. Benenat, MD), Hospital Campobasso (P. Sabatini, MD), Hospital Ravenna (G. Bellardini, MD), Hospital Trieste (A. Valencic, MD), Hospital Macerata (P. Milini, MD), Hospital Modica (F. Sebbia, MD), Universitari Clinic Chieti (Prof. E. Pizzigallo), Pugliese-Ciaccio Hospital Catanzaro (P. Scerbo, MD), Hospital Pescara (A. Consorte, MD), Hospital Varese (M. Gioia, MD), Hospital Caserta (G. Coviello, MD), Universitari Clinic Verona (A. Azzimi, MD), Papardo Hospital Messina (M. Allegra, MD), Gaslini Hospital Genova (G. Losurdo, MD), and Galliera Hospital Genova (P. Cristalli, MD).
1. Faura T, Garcia F, Isla P, et al. Health problems and social vulnerability in immigrants admitted for an infectious diseases: a case control study. Rev Clin Esp
2. Boggild AK, Yohanna S, Keystone JS, et al. Prospective analysis of parasitic infections in Canadian travellers and immigrants. J Travel Med
3. Caritas: Immigrazione dossier statistico 2002. Ed. Nuova Anterem, 2002.
4. Caritas: Immigrazione dossier statistico 2003. Ed. Nuova Anterem, 2003.
5. Ponticello A, Sturkenboom MC, Simonetti A, et al. Deprivation, immigration and tuberculosis incidence in Naples, 1996-2000. Eur J Epidemiol
6. Cacciani L, Baglio G, Rossi L, et al. Hospitalisation among immigrants in Italy. Emerg Themes Epidemiol
7. Marceca M, Geraci S, Tarsitani G. Il fenomeno immigratorio e il SSN, necessità di un riordinamento dei servizi. Milano: Argomenti di igiene pubblica ed ambientale, 1996, 12-20.
8. Spinelli A, Baglio G, Lispi L, et al. Health conditions of immigrant women in Italy. Ann Ig
. 2005;17:231-241 >[in Italian]>.
9. Sabbatani S, Baldi E, Mnfredi R, et al. Admission of foreign citizens to the general teaching hospital of Bologna, northeastern Italy: an epidemiological and clinical survey. Braz J Infect Dis
10. Lopez-Velez R, Huerga H, Turrientes MC. Infectious diseases in immigrants from the perspective of a tropical medicine referral unit. Am J Trop Med Hyg
11. Roberts A, Kemp C. Infectious diseases of refugees and immigrants: hookworm. J Am Acad Nurse Pract
12. Scotto G, Saracino A, Pempinello R, et al. SIMIT epidemiological multicentric study on hospitalized immigrants in Italy during 2002. J Immigr Health
13. Matteelli A, Volontario A, Gulletta M, et al. Malaria in illegal Chinese immigrants, Italy. Emerg Infect Dis
14. Santoro D, Visona R, Posterla L, et al. Migrants' admission to hospital: a retrospective study in Como from 1994 to 1998. J Travel Med
. 2000;7(6): 300-303.
15. Huerga H, Lopez-Velez R. Infectious diseases in sub-Saharan African immigrant children in Madrid, Spain. Pediatr Infect Dis
16. Jelinek T, Schulte K, Beherens R, et al. Imported Falciparum malaria
in Europe: sentinel surveillance data from European network on surveillance of imported infectious diseases. Clin Infect Dis
17. World Health Organization. Expert Committee on malaria. 20th Report. WHO Tech Rep Series
18. Romi R, Boccolini D, Majori G. Epidemiological trends of imported malaria in Italy 2000-2002. Giornale Italiano di Medicina Tropicale
19. Global Poverty Report 2002. Achieving the Millenium Development Goals in Africa. Progress, Prospects and Policy Implications. African Development Bank in collaboration with World Bank, June 2002.
20. Ramsay S. Global fund makes historic first round of payments. Lancet
© 2008 Lippincott Williams & Wilkins, Inc.