Spectrum of Helminth Infections in Migrants from Sub-Saharan Africa to Europe: A Literature Review

ABSTRACT.

Sub-Saharan Africa (SSA) is endemic to numerous neglected tropical diseases, including many helminth diseases. With the migration of people from this part of the world to Europe, as has been happening on a large scale since 2015, these diseases are becoming more relevant to European physicians. This work aims to summarize the recent literature on this topic and to raise awareness of helminth diseases afflicting SSA migrants. The databases PubMed, Embase, and MEDLINE were screened for literature published in English and German between January 1, 2015 and December 31, 2020. In total, 74 articles were included in this review. The spectrum of helminth infections in migrants from SSA found in the literature review is broad; current research, however, is particularly focused on infections with Schistosoma spp. and Strongyloides stercoralis. Both diseases are often characterized by a long course, with few or no symptoms, with the risk of long-term organ damage. Successful and reliable screening for schistosomiasis and strongyloidiasis is strongly recommended. However, the current diagnostic methods lack sensitivity and specificity, rendering the diagnosis challenging and reliable assessment of disease prevalence difficult. Novel diagnostic methods and a greater awareness of these diseases are urgently needed.

The year 2015 marked the beginning of the so-called “migrant crisis” in Europe. Conflicts in different countries of the world caused more than 1.3 million people to seek asylum in the European Union (EU). Although most of the migrants came from Syria, Afghanistan, and Iraq, there was also a significant proportion of people from Sub-Saharan Africa (SSA) (Figure 1). Migration from SSA hit its peak in 2016, with approximately 210,000 people seeking asylum in the 28 EU member states.¹

Figure 1.

Five SSA countries from which most asylum applicants came to Europe between 2015 and 2019. The pie charts show the five most frequent European countries where the asylum application was made. Data from 1.

The reasons for leaving one’s home country are diverse, and range from war and ethnic conflicts to climate change or the hope of improving one’s economic situation.^2,3 Severe circumstances in conflict regions; the long, dangerous journey to Europe; and stays in crowded and unsanitary refugee shelters make migration from SSA particularly dangerous. Many migrants suffer from diseases, and psychological and/or physical trauma.^4,5

Screening programs for migrants in European countries focus on communicable diseases—predominantly on tuberculosis.⁶ However, SSA is also endemic to many parasitic neglected tropical diseases (NTDs), including helminth infections.⁷ Thus, medical practitioners will be confronted with diseases that are not, or are no longer, common in Europe. This harbors the risk of delayed or incorrect diagnosis, which is especially problematic in the case of schistosomiasis and strongyloidiasis. Chronic urogenital schistosomiasis, caused by Schistosoma haematobium, can lead to long-term damage such as renal dysfunction and infertility, and is associated with squamous cell carcinoma of the bladder. Gastrointestinal schistosomiasis, caused by Schistosoma mansoni, can lead to liver fibrosis and portal hypertension.⁸ Patients with strongyloidiasis can develop hyperinfection syndrome when immunocompromised. The uncontrolled proliferation and dissemination of the pathogen can lead to paralytic ileus, respiratory distress, Gram-negative meningitis, and sepsis with high fatality rates.^9,10

In 2019, Asundi et al.¹¹ published a large systematic review and meta-analysis on the prevalence of schistosomiasis and strongyloidiasis in migrants to Europe and other high-income countries. The team found a seroprevalence of 24.1% for schistosomiasis and 14.6% for strongyloidiasis in migrants from SSA. This gives a good orientation of how widespread these diseases are in migrants. However, the authors of this meta-analysis also point out the high degree of heterogeneity of their data.

Our literature review—beginning with 2015, the year of the migrant crisis—aims to provide the most recent data on helminth disease in migrants from SSA and raise awareness of this topic. Although the focus lays on schistosomiasis and strongyloidiasis, the review also considers other helminth diseases that might be relevant in migrants from SSA.

METHODS

A review of the literature about helminth infections of migrants from SSA to Europe was performed. The databases PubMed, Embase, and MEDLINE were screened for literature published in English and German between January 1, 2015 and December 31, 2020. The search included the following terms and their combination: emigration and immigration/exp, refugees/exp, “asylum seeker*”, immigrants and emigrants/exp, migrants and transients/exp, “unaccompanied minor*”, migra*, emigra*, immigra*, refugee*, Europe/exp, helminthiasis/exp, “tropical disease*”, “neglected disease*”, helminth*, worm*, echinococcosis, “hydatid disease”, fasciol*, paragonim*, filariasis, onchocerciasis, “river blindness”, “Wuchereria bancrofti”, loiasis, “Loa loa”, hookworm*, “Necator americanus”, “Ancylostoma duodenale”, “Ascaris lumbricoides”, “Trichuris trichiura”, “soil-transmitted helminths”, geohelminths, schistosomiasis, bilharzia, taeniasis, cysticercosis, strongyloidiasis. The search was further limited to literature on human infections.

Original research and case reports that included data that could be assigned to migrants from SSA to Europe were considered suitable for this review. Data from people traveling to visit their friends and relatives were excluded, as well as data from tourists or internationally adopted children, because these groups have different risk profiles for helminth diseases than migrants (e.g., adopted children may have received treatment before adoption, visiting friends and relatives have often already lived for years in the host country and usually travel under safer circumstances). Cost-effectiveness analyses and studies that focused on treatment or explored the efficacy of diagnostic methods, reviews, meta-analyses, and conference abstracts were excluded. Unless otherwise stated, the prevalence rates mentioned in this review only come from studies in which more than 50 participants were screened.

In this review, the term “migrant” was used as an overarching term and included asylum seekers and refugees. However, it should be noted, that the terms are not interchangeable. “Refugee” is a well-defined term in international law that includes people who left their country because their life or freedom was in danger. The term migrant, on the other hand, is not precisely defined and is often used for people leaving their home country at their own choice.¹²

RESULTS

The search yielded 778 matches. After the removal of duplicates and application of the exclusion criteria, 74 articles were included in this review. The number of articles found for each helminth disease is shown in Supplemental Table 1. In the following, the spectrum of helminth disease and its prevalence (in studies with > 50 participants) are presented, as well as a selection of results from some of the reviewed papers.

Schistosomiasis.

Schistosomiasis was the disease described most frequently in patients from SSA. In most studies, microscopy and/or serology was used for diagnosis. The serological prevalence was between 5.8% and 50.5%. When microscopy only was used for diagnosis, prevalence was at 0% to 27%. Studies in which diagnostic methods were combined led to greater prevalence (17–58.9%). An overview of the schistosomiasis prevalence sorted by diagnostic method is shown in Table 1,^13–17 and Supplemental Table 2A and B.

Table 1.

Schistosomiasis prevalence based on a combination of diagnostic methods (studies with > 50 participants)

First author, year, country*	Characteristic of tested collective	Most frequent countries of origin of collective	No. of positive/no. of tested (% positive)	Diagnostic method
Chernet, 2018, Switzerland13	Asymptomatic, living in centers for asylum seekers Median age (IQR): 25 years (21–29 years) 88.8% male Months since arrival in Switzerland (IQR): 11 (8–22)	Eritrea	63/107 (58.9)	POC-CCA (Rapid Medical Diagnostics, Pretoria, South Africa), ELISA and immunofluorescent antibody tests for soluble egg-antigen and worm adult-antigen, microscopy of 2 stool samples (1 SAF fixed, one native)
Beltrame, 2017, Italy14	Referred to a Center for Tropical Diseases Characteristics not mentioned for patients from SSA	Nigeria, Mali, Ghana	101/300 (33.7)	CCA urine dipstick test (NADAL® CCA Bilharzia test, nal von minden, Moers, Germany), ELISA containing Schistosoma mansoni soluble antigens (Bordier Affinity Products SA, Crissier, Switzerland), microscopy of 3 concentrated (formol-ether) stool samples, urine microscopy after micropore filtration
Cuenca-Gomez, 2016, Spain15	Patients with chronic hepatitis B Mean age ± SD: 29.8 ± 7.18 years 94.7% male Mean length of residence in Spain ± SD: 50.42 ± 43.28 months	Senegal, Mali	170/507 (33.5)	Examination of 3 stool samples (Ritchie’s method), microscopy of concentrated urine sample and/or biopsy, qualitative determination of IgG antibodies against S. mansoni by means of an enzyme immunoassay (NovaLisaTM, NovaTec Immundiagnostica GmbH, Dietzenbach, Germany)
Buonfrate, 2018, Italy16	Living in refugee shelters, arrival in the past 6 months Median age (IQR): 23 years (20–27 years) 94.4% male	Mali, Nigeria	76/358 (21.2)	Examination of 3 concentrated stool samples (formol-ether), urine examination after micropore filtration, S. mansoni ELISA kit (Bordier Affinity Products SA, Crissier, Switzerland)
Boga, 2020, Spain17	Women attending a tropical medicine unit with or without symptoms Characteristics not mentioned for patients from SSA	Equatorial Guinea, Senegal, Nigeria	44/259† (17)	Microscopy of 3 concentrated stool samples (Copropack Extraction Kit C100; Cromakit, Granada, Spain), qualitative detection of IgG antibodies against Schistosoma spp. using ELISA (DRG Diagnostics®, Marburg, Germany)

CCA = circulating cathodic antigen; ELISA = enzyme-linked immunosorbent assay; Ig = immunoglobulin; IQR = interquartile range; POC = point of care; SAF = sodium acetate-acetic acid-formalin; SD = standard deviation; SSA = sub-Saharan Africa.

^*Articles sorted according to the prevalence found at screening.

^†Absolute number estimated, as it is not mentioned in the paper.

A study by Cobo et al.¹⁸ examined, among other variables, how long migrants attending a tropical diseases unit had lived in their host country before schistosomiasis was diagnosed. Their results were as follows: 42.3% of patients with schistosomiasis had lived in Spain for 3 years, 16.7% for more than 5 years, and 2.8% for more than 10 years before diagnosis. It is, however, not mentioned whether the patients had symptoms suggestive of schistosomiasis. In a study by Tilli et al.,¹⁹ symptomatic patients were diagnosed with urogenital schistosomiasis, on average, 5 months after symptom onset (mostly macroscopic hematuria and lower back pain) or after their arrival in Italy.

Several studies and case reports gave an account of complications and long-term effects of schistosomiasis, such as liver fibrosis, esophageal varices, splenomegaly, pulmonary hypertension, cardiomyopathy, portal hypertensive gastropathy or renal failure, squamous cell carcinoma of the bladder, and testicular ischemic necrosis resulting from vascular obstruction by schistosomes.^20–24 Some publications reported rarer manifestations of schistosomiasis, such as pulmonary nodules²⁵ and neurological manifestations.^26–28

Salas-Coronas et al.²³ found complications in 13 of 326 patients (4%) with parasitologically confirmed schistosomiasis; Roure et al.²² found complications in 22 of 61 migrants (36%) with Schistosoma spp. infection. In a study by Tilli et al.,¹⁹ 68% of 169 patients with urogenital schistosomiasis had at least one urinary tract alteration visible on ultrasound. Consecutive treatment with praziquantel reduced ultrasound abnormalities significantly.

Two studies with more than 500 and more than 200 participants, respectively, investigated co-infection of schistosomiasis (with an emphasis on S. mansoni infection) and chronic hepatitis B because previous studies from endemic countries—mainly Egypt and Brazil—had indicated that co-infection was associated with the risk of aggravated liver disease.^15,29–31 However, this could not be confirmed in the recent studies.^15,29

Strongyloidiasis.

The prevalence for strongyloidiasis in the reviewed articles ranged from 10.7% to 38.1% when several diagnostic methods were combined (Table 2^{16,18,23,32–35}). If serology only was used, prevalence ranged from 1.1% to 10.9%. In studies using stool microscopy or coproculture only, prevalence ranged from 0% to 3.6% (Supplemental Table 3A and B).

Table 2.

Strongyloidiasis prevalence based on a combination of diagnostic methods (studies with > 50 participants)

First author, year, country*	Characteristic of tested collective	Most frequent countries of origin of collective	No. of positive/no. of tested (% positive)	Diagnostic method
Cobo, 2015, Spain32	Patients diagnosed with filariasis Characteristics not mentioned for migrants from SSA	Guinea-Bissau, Senegal, Equatorial Guinea	37/97 (38.1)	Examination of stool (Ritchie’s method) Serology (not specified)
Salas-Coronas, 2015, Spain33	Adults with eosinophilia attending a tropical medicine unit Characteristics not mentioned for migrants from SSA	Senegal, Guinea Bissau, Mali	166/492 (33.7)	Examination of 3 (up to 9) concentrated stool samples (Richie’s method), charcoal culture, screening of serum IgG antibodies to Strongyloides stercoralis by means of ELISA (DRG® Strongyloides IgG, Marburg, Germany)
Buonfrate, 2018, Italy16	Living in refugee shelters, arrival in the past 6 months Median age (IQR): 23 years (20–27 years) 94.4% male	Mali, Nigeria	64/358 (17.9)	Examination of 3 concentrated stool samples (formol-ether), in-house immunofluorescence test
Salas-Coronas, 2018, Spain34	Attending a tropical medicine unit Mean age (range): 27.88 years (14–74 years) 83.8% male Mean time living in Spain (range): 6.06 months (1–12 months)	Senegal, Guinea Bissau, Mali	84/488 (17.2)	Examination of 3 concentrated stool samples (Ritchie’s method), ELISA (DRG® Strongyloides IgG, Marburg, Germany)
Cobo, 2016, Spain18	Attending a tropical medicine unit Characteristics not mentioned for migrants from SSA	Senegal, Mali, Guinea-Bissau	331/1,930 (17.2)	Examination of 3 stool samples (Ritchie’s method), culture, ELISA (DRG® Strongyloides IgG, Marburg, Germany)
Casado, 2019, Spain35	Adults attending a tropical medicine unit Characteristics not mentioned for migrants from SSA	Equatorial Guinea, Senegal	59/418 (14.1)	Examination of 3 formalin-ether concentrated stool samples, ELISA for anti-S. stercoralis antibodies (DRG Diagnostics®, Marburg, Germany)
Salas-Coronas, 2020, Spain23	Patients with schistosomiasis, with or without symptoms Mean age (range): 27.3 years (11–52 years) 93.9% male Mean time living in Spain (range): 39.6 months (1–288 months)	Mali, Senegal	35/326 (10.7)	Examination of 3 concentrated stool samples (Ritchie's method) Serology (not specified)

IQR = interquartile range; SSA = sub-Saharan Africa.

^*Articles sorted according to the prevalence found at screening.

Casado et al.,³⁵ who conducted a screening program for strongyloidiasis in migrants using serology, showed a high prevalence in migrants from eastern Africa (42.9% versus 16.3% in migrants from Central Africa and 10% in West African migrants). All patients testing positive in that study reported they walked barefoot in their home countries.

In a study by Martinez-Perez et al.,³⁶ on the management of hyperinfection syndrome and disseminated strongyloidiasis at reference centers in Spain, the authors described three cases in patients from SSA. All were male and originated from West Africa. One of them had lived in Spain for 31 years before strongyloidiasis was diagnosed by microscopy and serology.

Filariasis.

Concerning diseases caused by filaria in migrants from SSA, infections with Mansonella perstans and Loa loa were found predominantly. Prevalence of M. perstans based on direct filarial visualization ranged from 4.5% to 50.4%; prevalence of L. loa ranged from 0% to 12.7% (Supplemental Table 4).

Saito et al.³⁷ described that migrants from SSA with loiasis experienced fewer Calabar swellings and more eye worm compared with travelers (odds ratio, 0.12 and 3.4, respectively). Positive filarial serology was reported less frequently and microfilaremia more frequently in migrants than in travelers.

Onchocerciasis was hardly detected in screenings, although skin snips were performed in some studies.^33,38 High prevalence rates stand out in two studies by Puente et al.^39,40: 138 of 503 migrants with mansonelliasis (27.4%) and 22 of 131 migrants with loiasis (16.8%) were co-infected with Onchocerca volvulus (diagnosed by microscopy). In addition, two case reports noted infections with O. volvulus.^41,42

Infections with Wuchereria bancrofti were rarely described.^39,40,42

Geohelminths.

The prevalence of hookworm ova in stool examinations was between 0% and 41.2%; prevalence of Ascaris lumbricoides, between 0% and 17.9%; and Trichiuris trichiura, between 0% and 27.2%.^{13,16,18,23,33,34,38,40,43–45} It is noticeable that the prevalence of some geohelminths was particularly high in studies in which migrants with filariasis were examined.^32,39,40 Excluding these studies, the prevalence of hookworm infections reaches 25.6% (in a study with patients with eosinophilia), that of A. lumbricoides, 3.6%; and that of T. trichiura, 4.1%.^33,34,43

Taeniasis and neurocysticercosis.

Prevalence of infection with the adult worms of Taenia spp. (taeniasis) is diagnosed by microscopic stool examination. As in endemic countries, prevalence was low. In two studies by Salas-Coronas et al.,^33,34 prevalence was 0.2% in 492 migrants with eosinophilia and 1.2% in 488 newly arrived migrants to Spain. Ehlkes et al.⁴⁵ found Taenia spp. in 0.9% of the stool samples of 571 Eritrean migrants. Cobo et al.¹⁸ found a prevalence of 0.4% in 1930 migrants. Patamia et al.⁴⁶ found six cases of taeniasis in a group of more than 233 migrants; all patients came from Eritrea or Ethiopia. Zammarchi et al.⁴⁷ conducted a study with 164 migrants from SSA (mainly from western Africa), and no case of taeniasis could be confirmed by microscopy.

A few cases of neurocysticercosis (NCC), the infection with the cystic larvae of Taenia solium in the brain, meninges, and spinal cord, were described, but there was no systematic screening for the disease.^20,48,49

Echinococcosis.

Echinococcosis, or hydatid disease (caused by Echinococcus granulosus), was only reported very sporadically in migrants from SSA. Romero-Alegria et al.⁵⁰ found positive E. granulosus serology in 8 of 337 (2.4%) sub-Saharan African migrants from Equatorial Guinea, Mali, Senegal, and Gambia. Angheben et al.⁵¹ reported a case of a 26-year-old man from Niger with a hydatid liver cyst.

Other helminths.

Other helminths diagnosed in migrants from SSA were Fasciola hepatica,⁵² Hymenolepis nana,^{13,18,23,33,34,38,44,45,53,54} Enterobius vermicularis,^45,55 Toxocara spp.,^38,56 and Dicrocoelium dendriticum,^23,33,34,57 although the latter in some cases was considered false parasitism.

DISCUSSION

This literature review summarizes the wide range of helminth infections among migrants from SSA to Europe. Viewing the number of scientific publications, schistosomiasis and strongyloidiasis have received increased attention in recent years.

Although filarial infections were also often mentioned in the literature, there were hardly any cases of lymphatic filariasis or onchocerciasis, which could both indicate the success of eradication programs and be a result of the “healthy migrant effect,” which suggests that seriously ill people are less likely to be able to endure the challenges of migration.^42,58 Also, their diagnosis can be rather laborious, including skin snips (onchocerciasis) and nocturnal blood smears (lymphatic filariasis), and was not carried out in every study. All this could explain the small number of cases found.⁵⁹

Prevalence of infections with L. loa did not exceed 1% in most studies, in which unselected patients were screened. The prevalence of mansonelliasis, however, reached 9.1% in unselected patients and 13.6% in eosinophilic patients, reported primarily in studies from Spain.^33,34 The clinical picture of mansonelliasis is not very specific, but morbidity and mortality of this disease in migrants is clearly understudied and there is a lack of specific treatment options, which is why some authors consider it to be particularly neglected.⁶⁰

The two studies by Puente et al.^39,40 are an exception, in which the microscopically confirmed prevalence of (co-)infections with filariae (especially with O. volvulus) and geohelminths in patients originating mostly from Equatorial Guinea was much higher. It must be noted that in those studies, patients who already had a filarial co-infection were examined and thus probably came from highly affected areas. Also, the authors evaluated data from a period of around 20 years, and findings could reflect the time before the start of eradication programs.⁶¹

Other helminth diseases were far less common in migrants from SSA, such as infections with Taenia spp. or Echinococcus, although not many studies screened migrants systematically for the latter using ultrasound as an appropriate method.^33,34 Taeniasis is mostly caused either by T. solium, with pigs as intermediate hosts, or Taenia saginata, with cattle as intermediate hosts. An infection with T. solium has a greater impact on human health because it can affect the central nervous system and cause NCC—one of the leading causes of epilepsy in endemic countries. In studies^18,33,34 with a high proportion of migrants from predominantly Muslim countries, such as Senegal, Mali, or Somalia, the low prevalence of T. solium in stool samples can be related to religious dietary regulations. However, in countries with a religiously heterogeneous population, where pig rearing is more commonplace, Muslims may also become infected via the fecal–oral route and develop NCC.⁶² Unfortunately, in most of the studies, it was not clear whether the pathogen found in the stool was T. solium or T. saginata, because ova are indistinguishable in standard microscopy.^49,63,64

Hookworm, T. trichiura and A. lumbricoides, were found more commonly, but they often produce little morbidity. They also have a limited life span, so their prevalence decreases with the length of stay in the host country, and transmission is interrupted because of better hygienic conditions. However, they can play a role in groups at risk, such as children or pregnant women.^{18,34,45,52,65}

Among the helminthiases, schistosomiasis and strongyloidiasis in particular have been recognized as a major health risk for migrants from SSA because of their frequency, their chronic course, and the long-term consequences. Zammarchi et al.⁶⁶ describe an increase of strongyloidiasis and schistosomiasis cases in Italy from the 2011 to 2017, mainly in foreign-born subjects, which may reflect increased migratory movements during this period. Because the migration flow from SSA to Europe will likely continue in the coming decades, there are some issues with the management of schistosomiasis and strongyloidiasis that need to be addressed.⁶⁷

Diagnostic methods.

Diagnosis of schistosomiasis and strongyloidiasis has its difficulties. Direct parasitological diagnosis in stool, urine, or biopsy material lacks sensitivity, especially in patients with acute or low-burden infections.^8,10,45,68 Examination of multiple stool samples is a way to increase sensitivity further⁶⁹; however, obtaining one—let alone multiple samples—is not always feasible, as experience shows, because many patients consider this procedure unpleasant. It also implies that the patient has to return to the clinic several times, which may present difficulties for the patient.

In contrast, collecting blood samples for serological tests is generally more accepted, and serology is usually more sensitive than microscopy of stool or urine. A downside, however, is that serological tests cannot distinguish between an active, past, or treated infection. They can also show cross-reactivity with other helminth infections or be false negative.^10,70 In a study by Salas-Coronas et al.²³, 29.5% of patients with parasitologically confirmed schistosomiasis (mostly S. haematobium infection) had negative serology.

Therefore, screening for schistosomiasis in migrants based on serology alone is not sufficient and needs to be combined with other, ideally direct detection, methods. More recently developed tests include polymerase chain reaction or loop-mediated isothermal amplification, as well as the detection of circulating schistosome antigens such as the circulating cathodic antigen (CCA) and the circulating anodic antigen.^71–74 Such tests, however, were only used in very few of the reviewed articles because of the lack of widespread availability. Another option is the commercially available and easy-to-use point-of-care CCA test, which is more sensitive for S. mansoni than for S. haematobium. In endemic countries, this test performs satisfactorily, showing greater accuracy than microscopy-techniques.^74,75 However, the test is more reliable in patients with a high worm burden. This may explain why in migrant populations resident in nonendemic settings, the sensitivity of this tests was less than that of other parasitological and immunological tests, probably because of a low parasite burden.⁷¹

Heterogeneity in data.

The prevalence of helminth diseases varied greatly among studies reviewed. This may be explained in part by differences in sensitivity and specificity of diagnostic methods used. Microscopic examination is highly examiner dependent, and many diagnostic assays are not commercially available, so in-house tests are used. Both issues make interpretation of results and comparison among centers challenging. Also, study results vary depending on the degree of preselection of subjects. Greater prevalence is found in symptomatic patients and in patients with eosinophilia. Rates also tend to be higher when hospital inpatients are included, and lower when outpatients are examined or if study participants are recruited outside medical facilities.

Differences in prevalence may also be a result of the origin of the migrants studied. Some papers in this review, for example, indicate high prevalence of schistosomiasis among migrants from Mali, Senegal, Eritrea, and Ivory Coast.^13–15,76 Unfortunately, only a few studies mentioned the country of origin of the migrants, and even fewer studies differentiated between infected and uninfected depending upon origin. This is a missed opportunity to learn more about the epidemiology of the diseases using migrants as sentinels for disease prevalence in their home country, about which often no solid data exist. It is important, however, to interpret such data with caution because infection may have been acquired in a transit country. In addition, even within one endemic country, regions for schistosomiasis are commonly patchy in distribution; therefore, not only information regarding the country of origin, but more precisely about the region of origin, matters. Furthermore, migrants may not be representative for a country’s general population, because young men are overrepresented. Nevertheless, it would be interesting to investigate further the effect of the country of origin on the prevalence of a helminth disease.

Delay of diagnosis.

Helminth infections are often asymptomatic or have nonspecific symptoms, which increases the risk of being overlooked, especially by practitioners not familiar with the diseases.^{10,13,24,25,55,77} In this review, only few studies addressed this issue. Brindicci et al.⁷⁶ and Riccardi et al.⁷⁸ reported cases of migrants with hematuria who underwent antibiotic treatment, or excessive or unnecessary diagnostic measures before schistosomiasis was considered. Other studies^18,19,79 point to a delay of diagnosis, which could be a result of the difficult access to health care for migrants. In addition, asymptomatic migrants may simply not see the need to seek medical attention and may stay undiagnosed for a long period of time.

General screening with a focus on schistosomiasis and strongyloidiasis is recommended by the European Center for Disease Prevention and Control (ECDC),⁸⁰ but to our knowledge is not put into practice in a systematic way at the country level. Systematic screening could not only reduce morbidity and mortality in migrants, but also prevent the spread of schistosomiasis in Europe as it happened in France (Corsica) and Spain (Almería), where snail vectors for this pathogen exist.^81–83 Screening could also offer the opportunity to learn more about the epidemiology of the diseases in countries in SSA (with some limitations mentioned earlier). For that, however, standardized reporting also of noncommunicable diseases such as helminth infections in migrants at a European level would be required.

Serology is the recommended screening method for schistosomiasis and strongyloidiasis by the ECDC.^80,82 An additional diagnostic method for the diagnosis of schistosomiasis—for example, a point-of-care CCA test—could increase sensitivity further.⁸⁴ Nevertheless, it would be desirable if more specific and easy-to-use diagnostic tests were developed to obtain a precise picture of the prevalence. Presumptive treatment as recommended by the U.S. CDC could also be an option.⁸⁵ Both screening and presumptive treatment was shown to be more cost-effective than passive diagnosis, at least in the case of strongyloidiasis.⁸⁶

Limitations.

Although the literature included was limited to the most recent publications since the onset of the European “migrant crisis” in 2015, some of the period of data collection at times reaches back before 2015 and may not represent the most recent epidemiology. Also, only literature in English and German was reviewed. Publications from important immigration countries such as Spain, Italy, Greece, or France not published in English may be missing.

Interpretation of data may be hampered by the different study populations and diagnostic methods used in the publications or the fact that some studies did not mention the diagnostic methods exactly or the characteristics of the population screened.

Studies reviewed here used primarily laboratory methods for detection of helminth infections. This, however, may not be adequate to evaluate the importance of some NTDs such as hydatid disease or cysticercosis, for which imaging is required. Many studies were also carried out in specialized units with selected patients, which means that prevalence cannot simply be extrapolated to the general population.

Some helminthic diseases are also endemic to European countries (e.g., strongyloidiasis and taeniasis), so autochthonous infection cannot be ruled out completely.^87,88 Nevertheless, because of the lower prevalence in Europe, autochthonous infections should only account for a small proportion of infections among migrants.

Last, many studies do not mention why and under what circumstances people left their home country (e.g., seeking asylum, legal or illegal migration), making it difficult to judge how vulnerable the study population really is.

CONCLUSION

Our review shows a broad spectrum of helminth diseases in migrants from SSA, with a focus on schistosomiasis and strongyloidiasis. Prevalence of these diseases varies strongly from study to study, depending on the screened population and diagnostic tests used. As some studies show, diagnosis of helminth infections remains challenging for medical practitioners in Europe without experience in tropical medicine. Screening offers to migrants—with a focus on schistosomiasis and strongyloidiasis—could help to prevent long-term damage or fatal disease outcomes. Therefore, increasing awareness among physicians about the importance of helminth diseases in this group of patients is crucial. The implementation of standard screening measures at the country level as recommended by the ECDC is of great importance. Screening, however, should be combined with systematic data collection at the European level to inform clinical practice further.

Research in the field of many parasitic diseases is still hampered by a lack of both sensitive and specific diagnostic tests. Furthermore, novel diagnostic methods are needed urgently, as demanded clearly in the WHO 2030 road map of elimination of NTDs, to detect ongoing infection reliably, document cure, and guide safe and effective treatment.⁸⁹

Note: Supplemental tables appear at www.ajtmh.org.