Results From Screening Immigrants of Low-Income Countries: Data From a Public Primary Health Care
- Poster presentation of “Screening of tuberculosis in Barcelona's immigrant population (Catalonia, Spain)” by Olga Hladun, Albert Grau, M. Esther Esteban, Maria Villanueva, and Vanessa Alvarez at the 6th European Congress on Tropical Medicine and International Health 2009, Verona, Italy, 6–10 September, 2009.
- Poster presentation of “Gender differences among the immigrant population attended in Primary Care in downtown Barcelona” by M. Esther Esteban, Olga Hladun, Robert Carreras-Torres, and Albert Grau at the European Population Conference 2012, Stockholm, 13–16 June, 2012.
A total of 3,132 immigrants from low- and middle-income countries were involved in a cross-sectional observational study to screen for infectious diseases among immigrants attending public primary health care (PHC) centers. The study was conducted to clarify the degree of demographic differences and risk predictors of these diseases.
Demographic and clinical variables, screening for infectious diseases [hepatitis B and C, human immunodeficiency virus infection, syphilis, and tuberculosis (TB)], and analytical data (anemia, hematuria, and liver function) were recorded from immigrants attending a public PHC unit in Barcelona.
Global hepatitis B, including chronic and previous, reached 18.1%; Morocco as the country of origin [odds ratio (OR) 2.1, 95% confidence interval (CI) 1.07–4.14] and gastrointestinal symptoms (OR 1.9, CI 1.18–3.02) were risk factors. Hepatitis C prevalence was 3.3% with elevated hepatic transaminase levels as a risk factor (OR 26.1, CI 8.68–78.37). Positive syphilis was 3.1%; latent and active TB rates were 28.1 and 5.8%, respectively. Concerning TB, we found remarkable differences both among WHO regions of origin (the Eastern Mediterranean region showed the highest rate of active TB, 8%) and the three categories of years of residence in Spain (6.5% for <1 year, 12.8% for 1–5 years, and 10% for >5 years).
The data allowed recommendation of a minimal screening of TB in immigrants from low-income countries regardless of the years of residence in Spain, hepatitis C in patients with altered transaminase levels, and hepatitis B in patients with gastrointestinal symptoms and/or from Morocco.
For some of the years during the last two decades, Spain has been among the top 10 countries with the highest number of immigrants: 4,607,936 immigrants in 2005 to 6,377,524 in 2010. Most of these citizens (85%–90%) are from low- and middle-income countries. In Catalonia, a heavily industrialized region in Spain, the immigrant population has increased 12-fold since 1999, with a 48.5% increase in 2001 (257,320 immigrants). Nevertheless, because of the economic crisis that has been specially affecting Southern Europe since 2009 a downward trend with a 3.8% of year-to-year decrease has been identified. However, immigration still remains a relevant phenomenon in Catalonia.
Although immigrants usually have good health and socioeconomic status within their original countries, they come from geographical regions or transit countries where transmissible infections (cosmopolitan diseases) and tropical diseases are more prevalent than in the host country. Furthermore, both the migratory journey and the resettlement environment are important factors in the final health status of immigrants. In Spain, currently there are numerous articles and guidelines[2-5] all authored by referral centers of Tropical and International Health Departments or by Infectious Disease Departments. However, there is an almost complete lack of studies in international medical databases reporting the current health status of the immigrants attended to in the public primary health care (PHC) centers.
The fact that PHC network is the basis of the Spanish public health system, and one of the first contact points for migrants seeking health care (as well as emergency services), highlights its usefulness in screening for infectious diseases. In Spain, until September 2012, immigrants had free access to PHC irrespective of the time of residence in the country. PHC network provides longitudinal health monitoring to all population (migrant and autochthonous). Most of the publications related to PHC only focus on guidelines for migrants' health[6, 7] or deal with the access and utilization of health resources.[8, 9] Data from PHC centers, such as the one described here, complement the studies from tropical medicine and infectious disease departments.
The aim of this study has been to screen for five infectious diseases in migrants attending a public PHC unit in Barcelona (capital of Catalonia) in an area of high concentration of migrants from low- and middle-income countries. The diseases are tuberculosis (TB); hepatitis B virus (HBV), hepatitis C virus (HCV), human immunodeficiency virus (HIV) infections; and syphilis. These diseases have been selected because of their high prevalence in the countries of origin, the availability of effective treatments, and the remarkable proportions that they have reached among communicable diseases in Barcelona. As an example, 47.7% of the TB cases detected in 2009 in Barcelona (24 of 10,000) involved patients from Pakistan, Bolivia, Peru, and Romania.
Here, we describe the prevalence of these diseases and a set of relevant clinical signs to clarify the degree of demographic differences and the existence of risk predictors in order to: (1) improve guidelines including clear referral mechanisms to specialized units, (2) optimize resources, and (3) reinforce the importance of public PHC centers for this task.
This was a cross-sectional observational study focused on immigrants from low- and middle-income countries who attended the public PHC center “Ambulatori Doctor Lluís Sayé-CAP Raval Nord” for the first time, between February 2001 and February 2005. This center is located in “El Raval,” one of the two neighborhoods of the historical center of Barcelona. In this neighborhood, immigrants comprise 48.6% of the total resident population.
The PHC center enrolled all patients who accomplished the following inclusion criteria: immigrants from low- and middle-income countries older than 15 years. At the time of their first visit, we recorded for each patient the written informed consent, demographic data (age, sex, country, WHO region of origin, and years of residence in Spain), and clinical variables (respiratory: cough and dyspnea; gastrointestinal: dyspepsia, epigastralgia, abdominal pain, or gastrointestinal reflux; urinary: dysuria, polaquiuria, gross hematuria; skin symptoms: itching or any injuries; systemic symptoms: asthenia and/or malaise). The PHC center elaborated an internal guideline (not published) to screen for infectious diseases in immigrants following the guidelines of the Unit of Tropical Medicine and International Health “Drassanes” of Barcelona, placed in the same district. For each patient, the decision about the infectious diseases to screen for (TB, syphilis, HBV and HCV infections, and HIV status) was done taking into account these guidelines and the medical judgment. With the same criteria, detection of anemia, hematuria, abnormal urinalysis, and liver function was also explored. Hence, in spite of having reviewed 3,132 immigrants, some clinical tests were conducted only in some of the participants. In the intermediate and final visits (at 16 months from the first visit) we recorded the screening results of infectious diseases and analytical data. Clinical tests and definitions are shown in Table 1.
Table 1. Clinical tests of infectious disease/analytical data and definitions
|Hepatitis B, N = 1,094||Hepatitis B surface antigen (HBsAg) and anticore to HB (anti-HBc). Previous: HBsAg negative and anti-HBc positive; chronic: HBsAg positive and anti-HBc positive; global hepatitis B: previous and chronic hepatitis B|
|Hepatitis C, N = 1,248||Antibodies to HC (AcHC)|
|Human immunodeficiency virus, N = 1,164||ELISA screening, confirmed with Western blot test|
|Syphilis, N = 1,190||Rapid plasma reaginic (RPR) test, confirmed by Treponema pallidum hemagglutination (TPHA) test.Previous: only TPHA was reactive; positive: both RPR and TPHA were reactive: global: previous and positive syphilis|
|Tuberculosis, N = 309||Tuberculin test positive with >10 mm induration in patients <35 years, patients younger than 35 years with positive Mantoux were also screened through Thorax X-ray. Thorax X-ray performed for all patients >35 years. Latent: only tuberculin test positive; active: radiological signs of active tuberculosis|
|Anemia, N = 1,562||Complete blood count, hemoglobin levels: male <13 mg/L; female <12 mg/L|
|Hematuria, N = 1,085||Basic urinalysis detecting more than five red blood cells per high-power field (HPF)|
|Liver function, N = 1,585||Elevation of liver transaminase levels: alanine aminotransferase level (ALT) ≥ 120 U/L; aspartate aminotransferase level (AST) ≥ 120 U/L; gamma-glutamyltransferase level (GGT) ≥ 105 U/L|
|Abnormal urinalysis, N = 1,085||Presence of hematuria, leukocyturia (≥5 leukocytes per HPF), or urinary tract infection (presence of leukocyturia and positive nitrites)|
Nonrandom associations among categorical variables were ascertained through Fisher's exact test, chi-square test, and likelihood chi-square ratio test depending on the number of categorical variables and the sample sizes. Multivariate statistical analyses were performed with a logistic forward Wald stepwise regression test. For each infectious disease and clinical sign, the predictor variables included were sex, age (categorized into five groups: <25, 25–29, 30–34, 35–39, and >40 years), WHO region of origin, country of origin, years of residence in Spain (categorized into three groups: <1, 1–5, and >5 years), and clinical variables. The final results were presented as odds ratios (ORs) with 95% confidence intervals (CIs). Statistical analyses were carried out using spss 15.0 for Windows (SPSS Inc., Chicago, IL, USA).
The main characteristics of the 3,132 patients analyzed are summarized in Table 2. Pakistan (23.3%) and Ecuador (20.7%) were the countries of origin with the highest frequencies. Although the gender proportion in our sample was quite similar (58.2% of men and 41.8% of women) there were statistically significant differences for the distribution of patients by age groups (p < 0.001). The majority of men were aged 25 to 34 years, whereas women were found predominantly in the ranges of <25 and ≥40 years. WHO regions of origin also showed significant gender differences (p < 0.001): 45.3% of men were from the Eastern Mediterranean region in contrast with the 62% of women who came from the Americas. The distribution of infectious diseases and other relevant clinical signs and test results are presented in Table 3.
Table 2. Age, years of residence in Spain, and WHO region of origin of patients
|Age groups (years)||N = 1,310||N = 1,822||N = 3,132|| |
|15–24||308 (23.5%)||296 (16.2%)||604 (19.3%)||<0.001|
|25–29||279 (21.3%)||439 (24.2%)||718 (22.9%)|| |
|30–34||245 (18.7%)||429 (23.5%)||674 (21.5%)|| |
|35–39||182 (13.9%)||264 (14.5%)||446 (14.2%)|| |
|40–44||129 (9.8%)||176 (9.6%)||305 (9.7%)|| |
|45–49||75 (5.7%)||138 (7.6%)||213 (6.8%)|| |
|>50||92 (7.1%)||80 (4.4%)||172 (5.5%)|| |
|Years of residence in Spain||N = 1,113||N = 1,277||N = 2,390|| |
|<1||505 (45.4%)||501 (39.2%)||1,006 (42.1%)||0.401|
|1–5||347 (31.2%)||521 (40.8%)||686 (36.3%)|| |
|>5||261 (23.4%)||255 (19%)||516 (21.6%)|| |
|WHO region of origin||N = 1,310||N = 1,822||N = 3,132|| |
|Africa||15 (1.1%)||46 (2.5%)||61 (1.9%)||<0.001|
|The Americas||812 (62%)||580 (32%)||1,392 (44.4%)|| |
|Southeast Asia||18 (1.4%)||148 (8.1%)||166 (5.3%)|| |
|Europe||69 (5.3%)||39 (2.1%)||108 (3.4%)|| |
|Eastern Mediterranean||121 (9.2%)||826 (45.3%)||947 (30.2%)|| |
|Western Pacific||275 (21%)||183 (10.1%)||458 (14.6%)|| |
Table 3. Distribution of screened diseases and other relevant clinical signs and analytical data in the total sample, and in the WHO regions
|HBV infection||Chronic HBV||29/1,094||1/18||2/575||2/57||3/20||13/273||8/151||<0.001|
|HCV infection|| ||41/1,248||1/20||11/655||0/65||1/23||27/328||1/157||<0.001|
|HIV infection|| ||14/1,164||0/17||11/622||1/61||0/23||1/320||1/139||0.432b|
HBV and HCV Infections
Global (previous and chronic) and chronic HBV infections were detected in 18.1 and 2.6% of cases, respectively. Statistically significant differences between sexes were found for global (p = 0.001) and chronic HBV infection (p = 0.002), with men showing the highest rates. Age ranges showed statistically significant differences only for global HBV infection (p = 0.014) owing to the high frequency of positive HBV patients older than 40 years (26%). Hepatitis B by WHO regions showed significant differences for both global and chronic cases (Table 3). For global HBV infection, patients from Europe (35%), Africa (33.3%), and Western Pacific (32.4%) showed the highest frequencies, whereas patients from the Americas showed the lowest values (8.9%).
Frequency of hepatitis C in the total sample was 3.3%. Statistically significant differences were identified for age groups (p = 0.003) owing to the high frequency of HCV in patients aged 35 to 39 and ≥40 years, and for WHO regions (Table 3). The Eastern Mediterranean region showed the highest incidence (8.2%).
HIV infection, Syphilis, and TB
For HIV infection, 1.2% of the serological tests were positive. We failed to detect any statistically significant difference for demographic variables. Global (previous and positive) syphilis was detected in 4.5% of patients and positive syphilis in 3.1%. Statistically significant differences were detected only among WHO regions owing to the lower values of global syphilis in patients from the Western Pacific and Eastern Mediterranean regions compared with the remaining ones.
Latent and active TB were detected in 28.1 and 5.8% of patients, respectively. No statistically significant differences were found for any of the demographic variables (age, sex, country, WHO region of origin, and years of residence in Spain) recorded. A total of 6.5% of patients <35 years of age with a positive Mantoux test had active pulmonary TB.
Analytical Data: Anemia, Hematuria, and Abnormal Urinalysis
There were significant gender-specific differences in clinical signs in women versus men: anemia (12.5% vs 2.9%, p < 0.001), hematuria (9.9% vs 2.5%, p < 0.001), and abnormal urinalysis (29.1% vs 6.4%, p < 0.001). On reviewing cases of anemia we found that 50.4% corresponded to microcytic anemias, 12.8% to beta-thalassemia minor, 11.1% to unspecified anemias, 8% to normocytic anemia, 1.7% were due to chronic kidney disease, and 0.8% to celiac disease and hemolytic anemia. When stratified by age the samples showed slightly higher frequencies of anemia in women older than 50 years (14.2%) than in women from 15 to 50 years (12.2%). We failed to detect any case of Schistosoma haematobium in the analyses of hematuria.
Associations between clinical symptoms and diseases or analytical results are reported in Table 4. The presence of gastrointestinal symptoms was significantly associated with all types of hepatitis. However, only the HCV infection showed a significant association with elevated liver transaminase levels: 43.3% of the patients with HCV infection showed this hepatic alteration in comparison with the 4% reported in non-HCV patients. Respiratory symptoms were associated with active TB, with 44% of patients showing both the disease and the symptom. We detected an association between urinary symptoms and anemia, hematuria, and pathological urinalysis. Systemic symptoms were associated with both anemia and hematuria.
Table 4. Significant associations between clinical and analytical variables, and diseases or analytical results
|Chronic HBV infection||27.6%, p = 0.042||Active tuberculosis||44%, p = 0.026||Anemia||26.5%, p = 0.002||19.7%, p = 0.011||HCV infection||43.3%, p = 0.028|
|Global HBV infection||20.2%, p = 0.002|| || ||Hematuria||39.4%, p < 0.001||21.2%, p = 0.006|| || |
|HCV infection||26.8%, p < 0.001|| || || || || || || |
Predictors of Infectious Diseases and Analytical Data
The main results obtained from the logistic, forward stepwise-multivariate regression tests are summarized in Table 5. Only those variables showing significant associations are reported. In each case, the Omnibus and Homer–Lemeshov tests revealed goodness-of-fit to the model.
Table 5. Multivariate predictors of infectious diseases and analytical data
|Global HBV infection||Country: Morocco||2.102 (1.067–4.140)||0.032|
|Age group: <25 years||0.338 (0.192–0.595)||0.000|
|Age group: 25–29 years||0.535 (0.318–0.900)||0.018|
|Gastrointestinal symptoms||1.886 (1.179–3.017)||0.008|
|HCV infection||Elevation of liver transaminase levels||26.081 (8.679–78.372)||<0.0001|
|HIV infection||Sex: Female||0.103 (0.018–0.588)||0.011|
|Lack of urinary symptoms||0.061 (0.011–0.330)||0.005|
|Syphilis||Age group: <25 years||0.381 (0.150–0.967)||0.042|
|Age group: 30–34 years||0.319 (0.116–0.875)||0.027|
|Active tuberculosis||1–5 years of residence in Spain||0.680 (0.005–0.890)||0.040|
|Anemia||Sex: Female||6.7 (3.689–12.283)||<0.0001|
|Systemic symptoms||1.9 (1.109–3.190)||0.019|
|Hematuria||Sex: Female||4.01 (1.896–8.495)||<0.0001|
|Nonspecific symptoms||2.7 (1.356–5.412)||0.005|
|Abnormal urinalysis||Sex: Female||4.657 (2.869–7.561)||<0.0001|
|Age group: <25 years||0.573 (0.332–0.988)||0.045|
|Age group: 30–34 years||0.507 (0.284–0.906)||0.022|
|Nonspecific symptoms||1.881 (1.087–3.257)||0.024|
The significant predictors of global HBV infection were country of origin, gastrointestinal symptoms, and age group. Morocco as the country of origin (OR 2.1, CI 1.07–4.14) and the presence of gastrointestinal symptoms (OR 1.89, CI 1.18–3.02) appeared to be risk factors for this disease, whereas the age group of less than 25 years and those of 25 to 29 years had lower odds (OR 0.34, CI 0.19–0.59; OR 0.53, CI 0.32–0.90, respectively). Presence of elevated liver transaminase levels appeared as the only, but extremely relevant, predictor associated with hepatitis C (OR 26.08, CI 8.68–78.37).
Female gender (OR 0.10, CI 0.02–0.59) and lacking urinary symptoms (OR 0.06, CI 0.01–0.33) showed lower odds for HIV infection. Age groups younger than 25 years (OR 0.38, CI 0.15–0.97) and 30 to 34 years (OR 0.32, CI 0.12–0.87) had lower odds for syphilis. Active TB only showed a significant association with the number of years of residence in Spain. The interval of 1 to 5 years of residence showed the lowest odds (OR 0.68, CI 0.005–0.890).
With regard to clinical signs, female gender appeared as a risk predictor of anemia (OR 6.7, CI 3.69–12.28), hematuria (OR 4.01, CI 1.90–8.49), and abnormal urinalysis (OR 4.66, CI 2.87–7.56). Systemic symptoms were also risk predictors of anemia (OR 1.9, CI 1.11–3.19), hematuria (OR 2.7, CI 1.36–5.41), and abnormal urinalysis (OR 1.88, CI 1.08–3.25).
This study analyzes one of the largest numbers of immigrant patients screened in a public PHC unit in Spain. The US health care services have a long tradition of studies dealing with immigrants' health and primary care. The recent works by Barnett and colleagues and McCarthy and colleagues underline the need to screen migrants for diseases such as TB to develop guidelines to optimize the health of immigrants. In Spain similar studies have been conducted only in referral centers.[2, 16] However, the increasing number of migrants necessitates the involvement of public PHC centers in order to optimize resources and provide a timely response to the health needs of the immigrant population. Our sample is representative of the immigrant population from low-income countries living in a disadvantaged neighborhood of Barcelona that could be extended to districts of urban cities with similar characteristics. However, the main limitation of our sample is the low representation of sub-Saharan African patients. Historically, these patients have been attended to in the Unit of Tropical Medicine and International Health “Drassanes” located in the same district of the city.
Global HBV infection in our sample reaches a value similar (18.11%) to that described in comparable patients in Sweden but considerably lower than that reported in referral units of Spain[16, 18] (44.8%–63.1%), Greece (53.1%), and Italy (38.9%). The underrepresentation of sub-Saharan African patients in this study may account for such differences. Global and chronic HBV infection rates show significant differences for gender, age group, WHO regions, and clinical gastrointestinal symptoms. Morocco as the country of origin (OR 2.1) and the presence of gastrointestinal symptoms (OR 1.9) are risk factors for global HBV infection.
We found a hepatitis C prevalence of 3.3%, within the ranges described in Spanish referral centers[16, 21] (3.1%–6.1%) and North Italy (3.2%–4.8%) but remarkably higher than that described in Central Europe[23-26] (0.6% in Germany and 1% in France). WHO regions of origin showed statistically significant differences: Eastern Mediterranean (8.2%) is the region with the highest values. Multivariate analysis revealed elevated liver transaminase levels as a risk factor (OR 26.1). This association could seem platitudinous, but in our sample 1,530 patients were not checked for transaminase levels. If we consider that there was 5.1% of altered transaminase levels in the global sample, and 16% of these patients with altered transaminase levels were HCV positive, there could be up to 12 nondetected cases of HCV infection in 1,530 patients, an inferred number that is in accordance with that described in the clinical experience recorded in the literature.
The data for HIV infection are insufficient to draw any conclusion because we found only 14 positive results from 1,164 patients tested (1.2%). The low representation of sub-Saharan African patients as stated above, and the possibility that many patients from other WHO regions with suspected HIV infection are referred to tertiary centers could be the reason for this low prevalence.
Global (4.5%) and positive syphilis (3.1%) show lower values when compared with data from referral units (10.2% for global and 6.4% for positive syphilis) in Spain. We found significant differences according to the WHO regions of origin. The highest rates correspond to the African region (global syphilis 11.7%) and the lowest to the Western Pacific (1.4%). We note that this qualitative serologic test is a treponemal test (it detects all subspecies of Treponema pallidum, not only Treponema pallidum pallidum) and this could lead to an overestimation of the rate of syphilis.
The latent TB rate (28.1%) is higher than that published for Southern Europe (15%, Spain, Greece, and Portugal) and intermediate between the incidence (46.5% vs 20.8%) reported by two Spanish studies.[16, 21] Had the screening been performed only in 309 patients, a latent TB rate of 28.1% is certainly a serious matter, reinforced by the 6.5% of active TB detected in our patients younger than 35 years with positive Mantoux test. In our sample there were 2,051 patients younger than 35 years to be screened through a skin tuberculin test. However, only 15% of them were finally screened. The test was not requested in 1,251 cases, accounting for 61% of the whole population of the study and adding a bias to our results. A plausible explanation for this low request could be that latent TB is an entity often unnoticed by the medical stratum. The lack of fulfillment with the tuberculin test could be another reason to explain the low percentage of patients screened (15%), but in our sample only 21% of the requested patients failed to comply with the tuberculin test. Concerning active TB, our rate (5.8%) is lower than the 8.7% reported in a previous study in Spain.
We found different active TB rates among the three categories of years of residence in Spain, with lower values for the range of 1 to 5 years (2.8%) when compared with the remaining ones (6.5% for <1 year and 10% for <5 years). Latent TB showed similar rates in the three age ranges (26.6% for <1 year, 30% for 1–5 years, and 37.5% for >5 years). These data fail to support the idea of higher TB rates among the first year of residence in the host country. Active and latent TB rates in our study reached the highest values when immigrants reported more than 5 years of residence in Spain. This finding, together with both the lower prevalence of TB in the host country compared to the countries of origin and the additional risk of infection, reinforces the need for a complete screening of TB.
In this study, hemoglobin levels and abnormal urinalysis have been found to be useful to detect anemia and urinary pathologies but not to screen for tropical diseases.
It has to be emphasized that cost-cutting exercises such as the exclusion of nonregular immigrants from public PHC services could result in negative health effects for immigrants, increasing health needs in the medium and long term.
This screening allows for suggestion of the following minimal testing: (1) TB screening, particularly in patients from Southeast Asia, the Western Pacific, and Eastern Mediterranean regions; (2) liver transaminase levels and subsequent HCV screening in patients with altered levels, paying special attention to those from Eastern Mediterranean, Africa, and Europe; (3) HBV screening in patients with gastrointestinal symptoms and/or from Morocco; (4) syphilis detection in patients from Africa, Europe, and America; (5) HIV detection depending on patients' risk factors; and (6) anemia and hematuria determination in women.
We thank M. Villanueva for her assistance in the data collection, and I. Molina, A. Batista, and M. Via for their insightful comments. This work has been supported by the Institut Català de Salut, Generalitat de Catalunya. We thank the anonymous reviewers who helped us to improve this work.
Declaration of Interests
The authors state that they have no conflicts of interest.