Introduction

Human schistosomiasis, namely bilharzia, is an infectious disease caused by trematodes belonging to the genus Schistosoma. The number of people infected by this parasite is estimated to be at least 230 million worldwide and >80 % cases are in Africa [1]. Currently, six species have been described in human pathology: S.mansoni, S. hematobium, S. intercalatum, S. guineensis, S. japonicum and S. mekongi. Basically, excluding last two species, which are located to Asia electively, all the others can be found in Africa; only S. Mansoni is present in the Americas. The geographic distribution of Schistosoma species is related to the presence of the suitable snail hosts in the natural habitat. Briefly, the lifecycle of Schistosoma includes a mammalian definitive host (human beings is thought to be the predominant reservoir), which eliminates parasite eggs through urine (S. hematobium) or stool (all other species). In the unsalted and fresh water, eggs become ciliated miracidia, which penetrate into the intermediate host, namely snails: here, thousands of cercariae are generated asexually and released again in the water. After cercariae have gone beyond the skin of the mammalian host, these penetrate into the bloodstream and colonize the venules, generating eggs by sexual reproduction [2]. Except for the dermatitis related to cercariae skin penetration, most morbidity caused by this infection is due to eggs deposition in the gastrointestinal system and in the urinary/genitourinary tract and/or to the associated chronic immune response [3]. Therefore, the clinical spectrum includes both acute illnesses, characterized with symptoms like fever, malaise, headache, abdominal pain (known as Katayama syndrome), and chronic diseases due to granulomatous immune response to eggs, leading to several clinical manifestations depending on the organ involvement (mainly urinary, genital and gastro-intestinal tract). However, ectopic eggs deposition can cause unusual and severe diseases (e.g. cerebral schistosomiasis). Finally, chronic infection, which is facilitated by malnutrition, can lead to impaired growth and intellectual development in children [2, 4, 5].

Patient’s Medical Report

On May 26th, a 16-year old refugee from Gambia (hosted in a community of southern Milan area since March 2015) has been brought to the Pediatric Emergency Department of Melegnano Hospital, because of gross hematuria persisting for 2 days. The patient reported that he had been in Italy since December 2014.

The boy was asymptomatic and complained of gross hematuria without any other urinary discomfort or pain. However, despite the language difficulties, we knew that he had presented the same clinical problem around 4–6 weeks ago, but that time hematuria had a spontaneous resolution. An accurate personal history could not be recorded. The physical exam resulted to be completely normal; blood count and biochemistry had no significant abnormalities, except for very mild eosinophilia (500 cells/mm3). Because of the clinical and the social setting, the patient was admitted to our pediatric ward, in order to perform further diagnostic investigations. The initial diagnostic work-up started with phase contrast microscopic examination of urinary erythrocytes (in order to localize the source of urinary bleeding), microbiological culture of urine and of pharyngeal swab, abdomen ultrasound and specific blood tests (infectious serology, measurement of C3 and C4 complement factor, plasma protein electrophoresis, serum immunoglobulin levels).

These blood tests and the ultrasonography showed no pathological findings; moreover, urine culture and the research of group A Streptococcus pyogenes in the pharyngeal swab resulted to be negative. However, the phase contrast urine analysis showed many (>80 %) dismorphic erythrocytes, suggesting a glomerular source of gross hematuria.

This finding prompted to re-consider carefully this clinical case; the origin and social setting made us think of some unusual etiologies of hematuria in European countries. Among diagnostic hypothesis, urinary schistosomiasis resulted to be the most consistent with the clinical picture and we planned a urine collection in such a way to increase the likelihood to reveal the presence of parasite eggs. Therefore, urine of a mid-morning sample was collected from the patient in a series of sterile containers, after doing knee-bends: those were well-labeled in order to know the temporal sequence of urine emission, as eggs are supposed to be found more easily in the terminal part of urine stream. Of course, the sample was immediately brought to the laboratory and was centrifuged at 3000 rpm for 10 min. The supernatant was discarded and about 0.5 ml of residual urine was retained to dissolve the pellet. Then, the urinary solution was placed on a slide and examined under the microscope at 100× magnification. The presence of Schistosoma eggs was detected (Fig. 1) and the morphologic features displaying a delicate terminal spine (Fig. 2) confirmed the species as being S. haematobium. Moreover, stool examination resulted to be negative for Schistosoma eggs. As the diagnosis of urinary schistosomiasis caused by S. haematobium was made through the findings of eggs in urine, no serologic testing was requested in this case, which can be useful because shedding of eggs can be intermittent, making difficult the direct microbiological diagnosis sometimes.

Fig. 1
figure 1

Presence of Schistosoma egg in patient’s urine sample

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Fig. 2
figure 2

Morphologic features of parasite egg, displaying a delicate terminal spine, which confirms the species as being S. haematobium

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After the diagnosis of urinary schistosomiasis caused by S. haematobium was achieved, the specific treatment with praziquantel has been administered. The patient received a unique dose of praziquantel equals to 60 mg/kg, according to the most recent guidelines. No adverse reactions (e.g. vomiting, dizziness) have been recorded and the gross hematuria started improving gradually. The patient has been discharged on May 30th and a follow-up program, including a re-evaluation of urine parasite eggs at 1 month, has been established.

Discussion

Schistosomiasis is endemic in many countries of sub-Saharan Africa and Middle East, which account for majority of affected people worldwide. Other endemic areas are in the Americas, especially some regions of Brazil, and in Asia, primarily China, Philippines and Mekong River basin. In these regions, the most common form of Schistosoma-related disease is represented by chronic schistosomiasis, as a result of repeated exposure to the parasite and, probably, of in utero priming of the adaptive immune system, because of mother’s infection. For this reason, acute schistosomiasis, also known as Katayama syndrome, is more often observed in people travelling to endemic regions [2].

Schistosomiasis in industrialized countries is almost always an imported disease and, in past decades, most cases diagnosed in Europe were travellers [6].

Currently, the major source of imported schistosomiasis could be related to the massive migration of people to Europe from the aforementioned endemic areas of Africa [7]. However, most cases of imported schistosomiasis by immigrants and refugees are supposed to be lost for several reasons. As explained above, many people affected with chronic/endemic schistosomiasis can be asymptomatic or complain of mild symptoms, which are often overlooked, also because most immigrants are undocumented and have a reduced access to health system. Moreover, medical services for tropical diseases are located primarily at specialized centers; unfortunately, some imported diseases are under-recognized by general physicians and a trained personnel is often required in order to reach a correct diagnosis.

These observations suggest that the burden of schistosomiasis in Europe is under-estimated and it might be disclosed in future through the emergence of chronic diseases (such as hepatic and pulmonary fibrosis, neuroschistosomiasis, carcinoma of the bladder, etc.) with high costs for health systems [8].

Moreover, further concerns derive from the fact that S. haematobium can survive 3–10 years on average in their human host [2], meaning that the spreading in the environment from affected people could continue for many years after their arrival in Europe. Therefore, considering this aspect, in future schistosomiasis might become more than an imported disease. Indeed, some cases of autochthonous bilharzia (by S. haematobium) have been reported in France recently, while the previous cases originating in Europe dated back 1960s or before. One of these reports regards a pediatric infection acquired in Corsica in 2013, which gained medical attention because of gross hematuria [9].

Gross hematuria is a common presenting symptom of genito-urinary schistosomiasis, which is actually an uncommon cause of urinary bleeding in the industrialized countries. Interestingly, persistent or intermittent hematuria, which often occurs several months or even years after immigrants' arrival in Europe, resulted to be the main symptom leading to the diagnosis of schistosomiasis, especially in adolescents [10].

Thus, a particular attention should be paid in countries of south boundaries of Europe, where the number of immigrants is increasing and most of them are undocumented. For instance, in a single center of identification and assistance for asylum seekers in Italy, between 2009 and 2010, seven young people were diagnosed as having urinary schistosomiasis, because of the presence of gross hematuria in their personal history [8]. Considering the exponential arrival of immigrant people to Italy in last few years, the potential number of people carrying the parasite in Italy (and eventually in Europe) is very likely to be dangerously increased. Similarly to Corsica, there are some Italian areas where the parasite can find its intermediate host, namely Bulinus truncatus [8, 9]. Moreover, in the perspective of public health system, an early diagnosis followed by the appropriate treatment with praziquantel is less expensive than diagnosing and treating the late complications of parasite infection.

Conclusion

Gross hematuria or a personal history of persistent/recurrent hematuria in people coming from endemic areas of Africa requires that urinary schistosomiasis must be actively sought by physicians, also outside referral centers for imported and/or tropical diseases. Indeed, the high number and the undocumented form of the ongoing migration from Africa, which is being in last few years in Italy, impairs health controls other than those related to acute and/or severe clinical conditions. Therefore, general physicians and the medical personnel working in the emergency departments should consider urinary schistosomiasis in immigrants and refugees whenever they complain of hematuria without other evident cause. An appropriate and careful collection and microscopic analysis of urine samples can lead to a correct diagnosis, which can be reached also in undedicated laboratories. Moreover, a costless campaign of detection of urine blood by dipstick at least in immigrants hosted in reception centers might help to reach an early diagnosis of urinary schistosomiasis in a greater number of cases and, thus, might limit the costs for the public health system and the potential spreading of the parasite in the environment.