Our study analyzes two schistosomiasis screening strategies used in the clinical practice of an International Health Institution in Barcelona, Spain, from 2014 to 2017. All diagnosed cases correspond to immigrants, mostly from Equatorial Guinea. This country is probably over-represented due to historical and cultural ties with Spain and the high degree of awareness of the importance of screening in this group. Similar demographic characteristics have been reported in cohorts within the Spanish territory (17,18).
The rationale for screening schistosomiasis in a population from endemic areas is that the disease is highly prevalent, and that treatment with praziquantel is safe and effective18,19. In studies in endemic populations, the rate of schistosomiasis varies between 20-40% (19,20). In migrants, the prevalence varied between 1% and 18% depending on the screening technique (parasitological vs serological study), according to a recent meta-analysis (21–23). In our study the overall prevalence, including both screening strategies, was 11.5%.
It should be noted that the effectiveness of the parasitological study depends largely on the experience of the observer, and therefore may vary significantly between laboratories; moreover, in contexts with a low egg burden, egg excretion may vary at different times of the day; even in the same sample the eggs may be unevenly distributed (24,25). The use of more objective techniques would allow screening to be expanded and performed in primary care units, and not necessarily in specialized centers.
In this situation, the sensitivity of the technique should be prioritized over specificity, although performing two tests in parallel could be used to increase the accuracy of detection and inform schistosome specy (8). In our study, the percentage of diagnosed cases in our cohort resulted similar in both described strategies. A possible explanation could be the high specialization of the reference laboratory, which optimizes the sensitivity of direct observation techniques. This condition might not be generalized to other contexts with less specialized laboratory personnel.
In this study, the serology used was an ELISA based on crude antigens of S. mansoni. Several studies show that this technique is more sensitive than direct visualization of eggs, mainly in adults in non-endemic areas with light infections (26,27). Nevertheless, the sensitivity of commercial tests for other Schistosoma species could be compromised. Thus, sensitivity varies between 50 and 90% for S. mansoni and 20 and 70% for S. haematobium (28).
Prevalence of imported eosinophilia among travelers and immigrants is reported between 8% and 28.5%, that is consistent with the reported prevalence of 16.8% in our cohort. Etiological diagnosis is often troublesome and, depending on the depth of the study and on the population analyzed, a parasitic cause is identified in 17–75.9% of the individuals. Among the difficulties encountered to compare studies are the heterogeneity of the studied populations, the study designs and the different diagnostic protocols (15). In schistosomiasis, eosinophilia is not a consistent finding (29,30), mainly in adult migrant patients, with initial infection probably in childhood, and low parasite load. In our study, 50% had eosinophilia. However, this finding could be influenced by the usual presence of coinfections in these patients, such as strongyloidiasis, filariasis and soil-transmitted infections. Consistently with other studies (18,31), IgE elevation was higher (68%); however, one third of the patients diagnosed had no abnormality. Therefore, screening for the disease should be based primarily on origin in the case of migrants, and on risk activities in the case of travelers, rather than on the presence of these parameters (21).
Once screening has been performed, the question of what the exact procedure is to follow once individuals are considered positive is not clear. There are few guidelines on the management of these patients, either symptomatic or asymptomatic. Some guidelines recommend performing a parasitological examination in the case of a positive serology, and performing an ultrasound only if eggs are found (32). Although this is essential to differentiate the species, the low sensitivity of the parasitological test and the presence of lesions in patients without egg detection suggest that an ultrasound should be performed in all patients, regardless of the parasitological result and the presence of symptoms (33,34). In our study, in all patients diagnosed, either by parasitological study or by serology, treatment was considered. However, the percentage of ultrasounds performed was very low, reflecting the difficulties on an appropriate follow-up in many contexts. One third of the performed ultrasound showed pathological findings in relation to the infection.
One limitation of schistosomiasis serology is that its use to differentiate between current and past infection is very limited, since antibody titers vary significantly after adequate treatment (35). In our study, only 2.5% of patients underwent control serology, of which 73% were positive. In general, the follow-up of migrant patients is difficult, especially in the screening of asymptomatic population, due to socioeconomic and idiomatic limitations, high mobility and lack of disease perception (36). Mechanisms need to be in place to ensure non-discrimination in health care access, such as access to cultural mediators, improvement of health literacy through targeted health promotion interventions, supranational communication system and effective asylum policies, among others (37,38).
Due to the limitations of both techniques currently used, new tests with higher sensitivity, higher specificity, and capable of differentiating current from past infections, should be developed. Meanwhile, the combination of several serological techniques, the western blot technique, or the immuno-chromatographic test (ICT) have shown a higher sensitivity (28).
A recent evaluation of several diagnostic tools found that a rapid commercial serological ICT test with 96% sensitivity would have the potential for being used as a single screening test for migrants from Sub-Saharan Africa (39). Molecular techniques (serum or excreta PCR) also have a high performance, improving the sensitivity of serology and allowing confirmation of the Schistosoma species involved. Furthermore, they can be useful for monitoring outcome (40). More efforts should be made to make these tests widely available for their use in daily practice.
Regarding general screening, an important proportion of the cohort was diagnosed with some infectious diseases, which encourages the maintenance of screening programs with the active participation of actors such as NGOs, community organizations and other health care departments. The lower rate of infections in our study compared to similar publications could be probably explained due to the exclusion of individuals with symptoms or known eosinophilia/elevated IgE (17,18). Concerning general migrant health status, it is worthy reported the high prevalence of cardiovascular conditions, even among such a young population as the included in this cohort (41). Specific, culturally oriented strategies and resources should be available to ensure also detection and management of non-communicable diseases in these vulnerable populations (42).
This study presents important limitations mainly due to its retrospective design. Information bias due to incomplete data in medical records could have influenced the results concerning serological interpretation. As foresaid, selection bias might not be completely avoided despite tight inclusion criteria. Also, the sample size of both strategies considerably differs, making difficult a significant comparison between groups. In the same line, the sample of schistosomiasis cases is too limited to draw robust conclusions. The high rate of loss to follow-up, related to the precarious life conditions, is the cause of a substantial amount of data losses, especially concerning follow-up information. Finally, it is worthy remarking that inclusion was limited to asymptomatic subjects coming from SSA and thus, results might not be generalized to other populations. Despite these remarkable limitations, we believe that this study provides valuable data on the screening of Sub-Saharan migrants in the clinical practice.