Schistosomiasis in children: review of 51 imported cases in Spain

Schistosomiasis is caused by Schistosoma spp. and affects more than 230 million people worldwide according to the WHO.1 In endemic areas, up to 60–80% of school-aged children and 20–40% of adults are actively infected.2 Chronic infection during childhood contributes to growth impairment and learning disability.3 In non-endemic countries, schistosomiasis may be detected in immigrants or travellers to endemic regions. As clinical suspicion is low in untrained healthcare professionals and screening programs are lacking, data on the epidemiology of the disease in non-endemic areas are scarce.4,5 The rationale for schistosomiasis screening in non-endemic countries is a high estimated prevalence of the infection in people coming from endemic areas, the availability of sensitive detection methods, and the potential to prevent serious complications.7 Regarding the diagnosis of schistosomiasis, direct visualization of the ova in urine, stool, or tissue biopsies (according to the species) is the gold-standard technique. However, its sensitivity depends on the quantity of ova in the sample and the observer’s experience.2 Serology has better sensitivity but low specificity because of the inability to distinguish recent from past infection and due to cross-reactions with other helminths. Therefore, a positive result must be confirmed by a direct method in patients who have lived in endemic areas and may have received antiparasitic therapy.8,9 The aim of this study was to describe the epidemiologic, clinical, and diagnostic characteristics of paediatric schistosomiasis in a non-endemic area. Demographic, clinical and microbiological data were retrospectively collected from all consecutive cases of paediatric (≤18 years) schistosomiasis diagnosed between January 2010 and December 2017 at Vall d’Hebron-Drassanes International Health Unit (Barcelona, Spain). For analysis purposes, patients were classified as immigrants, visiting friends and relatives (VFR), or tourists. Immigrants were children born in endemic countries and now living in Spain. VFR children were those born in Spain of immigrant parents who travelled to foreign countries to visit their family or relatives. Case definition was based on detection of Schistosoma spp. ova in stool, urine, or tissues (confirmed cases). Positive serology for Schistosoma spp. was also considered diagnostic in symptomatic patients and in asymptomatic VFR or tourist patients who had recently travelled to an endemic area (probable cases). Detection of Schistosoma ova was performed by microscopy examination using concentration techniques, in urine and/or faeces samples. An enzyme immunoassay (Novalisa Schistosoma mansoni IgG. NovaTec Immunodiagnostica GmbH, Germany) was used to detect specific IgG antibodies against S. mansoni. The choice of diagnostic technique and requests for ultrasonography were made by the treating physician. The study was approved by the local Ethics Committee for Clinical Investigation. Demographic, clinical and microbiological features by patient population groups IQR, interquartilic range; NA, not apply; VFR, visiting friends and relatives; *Pulmonary hypertension and myocardiopathy were attributed to chronic schistosomiasis as all other causes were ruled out, and the relationship is plausible **4 patients were co-infected with S. mansoni, S. haematobium and/or S. intercalatum Demographic, clinical and microbiological features by patient population groups IQR, interquartilic range; NA, not apply; VFR, visiting friends and relatives; *Pulmonary hypertension and myocardiopathy were attributed to chronic schistosomiasis as all other causes were ruled out, and the relationship is plausible **4 patients were co-infected with S. mansoni, S. haematobium and/or S. intercalatum Fifty-one patients were included (median 6 patients/year [IQR 3–8]), 41 (78%) male. Median age was 14.0 [IQR 11–16.5] years. Forty-three were immigrants, 4 VFR, and 4 tourists. All patients were from or had travelled to African countries. After the clinical interview, 19 patients (38%) reported symptoms consistent with schistosomiasis, mainly haematuria (12 patients). Diagnosis was made by direct visualization of Schistosoma spp. ova in samples from 41 patients (80%): 21 in urine, 23 in stool and 1 in bladder biopsy. Serology was carried out among 17 patients from whom diagnosis was confirmed by microscopic identification of ova in 7 patients, all immigrants. In the remaining 10 patients, stool and urine examination yielded negative results, but serology was considered diagnostic for the following reasons: 6 patients were immigrants from endemic areas with symptoms and/or eosinophilia, 2 were symptomatic tourists, and 2 were asymptomatic tourists, tested because of a diagnosis of acute schistosomiasis in their travel group. Demographic, clinical and microbiological features of the cases are shown in Table 1. Regarding the 22 patients with urinary schistosomiasis, 8 had eosinophilia and haematuria, 4 only haematuria, 6 only eosinophilia, and 4 showed no abnormalities. Bladder and renal ultrasonography were performed in 13 patients and detected abnormalities in 6 cases: bladder wall thickening (3), bladder tumours (2), and ureter, bladder, and prostate calcifications (1). All patients were treated with a single dose of praziquantel (40 mg/kg/day). Serial ultrasonography performed in 3/6 patients with urogenital abnormalities (2 with bladder tumours and 1 with wall thickening) showed complete resolution of the lesions. The 3 other patients were lost to follow-up. The paucisymptomatic presentation of the disease in our cohort matches with findings from previous reports. In one study including 11 international travellers who became infected in Corsica (6 adults and 5 children), all were asymptomatic at the time of the diagnosis and only one had microscopic haematuria.7 In a systematic screening of children from sub-Saharan Africa, only 11/42 (26%) patients diagnosed with schistosomiasis showed haematuria.6 Regarding the distribution of the clinical forms, intestinal schistosomiasis was predominant in our cohort (33/51 patients), followed by urinary schistosomiasis (22/51). There were 4 co-infections, S. haematobium was the most common species detected (43%), and S. mansoni and S. intercalatum were equally present (24%). This distribution of species differed from previous findings in Europe,4 as there was a higher incidence of S. intercalatum in our study (26% of all Schistosoma spp. identified). This may be because most of our patients were from Equatorial Guinea, a former Spanish colony where this specie is endemic. With regard to the diagnostic methods, 80% of patients, mainly immigrants and VFR, were diagnosed by microscopic detection. Serology allowed additional diagnosis of probable cases in 10 patients with negative microbiological studies, increasing the screening performance by 24%; and was the method most likely to diagnose tourists (4/4 patients). It is important to highlight that more than half the patients (mainly immigrants) had co-infection with other pathogens. This is a common scenario in patients coming from endemic areas, as was seen in another Spanish study, in which 56% of immigrant children had some type of co-infection.10 The main limitations of the study are its retrospective nature and the lack of standardization of the diagnostic methods. In conclusion, schistosomiasis must be ruled out in all patients visiting or traveling from endemic areas, even in absence of symptoms or eosinophilia. A dual approach including serology and direct methods is recommended. We thank Celine Cavallo for English language support. They authors didn’t received any financial support for this work. The authors declare that they have no conflicts of interest for this work. ASA, ES, NMP and PSP conceived and developed the aim of the study. NMP, IPG, ES, ME and FZ collected and validated the data. IPG, ASA and NMP performed the statistical analysis. AMN, PSP, NMP, ME developed the conclusions and wrote the article. All the authors have reviewed and approved the final version of the manuscript.