# Multidisciplinary challenges by ‘pure’ and hybrid Schistosoma species introduced into southwestern Europe

Alejandra de Elías-Escribano, Patricio Artigas, Joaquín Salas-Coronas, María Pilar Luzon-Garcia, Manuel Jesús Soriano-Pérez, Nerea Castillo-Fernández, María Cecilia Fantozzi, Alberto Martínez-Ortí, Jerome Boissier, Santiago Mas-Coma, et al.

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Alejandra de Elías-Escribano, Patricio Artigas, Joaquín Salas-Coronas, María Pilar Luzon-Garcia, Manuel Jesús Soriano-Pérez, et al. Multidisciplinary challenges by ‘pure’ and hybrid Schistosoma species introduced into southwestern Europe. Philosophical Transactions of the Royal Society B: Biological Sciences, 2026, 381 (1941), pp.20250087. 10.1098/rstb.2025.0087. hal-05468968

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**Cite this article:** De Elías-Escribano *A et al.* 2026
Multidisciplinary challenges by 'pure' and hybrid *Schistosoma* species introduced into southwestern Europe. *Phil. Trans. R. Soc. B* **381**: 20250087.
https://doi.org/10.1098/rstb.2025.0087

Received: 2 April 2025

Accepted: 27 June 2025

One contribution of 14 to the Royal Society
Science+ meeting issue 'Parasite evolution and
impact in action: exploring the importance and
control of hybrid schistosomes in Africa and
beyond'.

**Subject Areas:**

health and disease and epidemiology, molecular
biology

**Keywords:**

imported schistosomiasis, 'pure' and hybrid
infections, morphogenetic analysis of *Schistosoma*
eggs, potential risk of emergence of hybrid
*Schistosoma*, Spain, Europe

**Author for correspondence:**

María Dolores Bargues
e-mail: m.d.bargues@uv.es

Multidisciplinary challenges by 'pure' and
hybrid *Schistosoma* species introduced
into southwestern Europe

Alejandra De Elías-Escribano<sup>1,2</sup>, Patricio Artigas<sup>1,2</sup>, Joaquín Salas-Coronas<sup>2,3,4</sup>,
María Pilar Luzon-García<sup>2,3,4</sup>, Manuel Jesús Soriano-Pérez<sup>2,3,4</sup>, Nerea Castillo-
Fernández<sup>2,3,4</sup>, María Cecilia Fantozzi<sup>1,2</sup>, Alberto Martínez-Orti<sup>1,2</sup>, Jerome
Boissier<sup>5</sup>, Santiago Mas-Coma<sup>1,2</sup>, María Adela Valero<sup>1,2</sup> and María Dolores
Bargues<sup>1,2</sup>

<figure><img src="image_5.png" /></figure>

In Europe, imported schistosomiasis affects a diverse range of patients,
including migrants, travellers, visiting friends and relatives, and expatriates
who have lived in endemic areas. The variety of regions linked to these
patients' origins or destinations increases the likelihood of infections from
different *Schistosoma* species and hybrids. This work aims to address the
multidisciplinary challenges posed by 'pure' and hybrid *Schistosoma* species
in southwestern Europe. It explores (i) the role of molecular analysis
in identifying species and hybrids, (ii) the importance of morphogenetic
studies of *Schistosoma* eggs, (iii) the potential risk of hybrid *Schistosoma*
infections emerging in Europe and (iv) the clinical management, diagnosis
and treatment of schistosomiasis in non-endemic European countries.
The study includes examples of 'pure' and hybrid species detected in a
tropical medicine unit in Almería, Spain. In this context, the complexity
of managing not only the clinical aspects, diagnosis and treatment of this
disease, but also the need and readiness to quantify the risks and prevent
future outbreaks of schistosomiasis in Europe are evident. *Schistosoma*
hybrids potentially able to adapt to new European habitats are a challenge,
which highlights the need for appropriate surveillance and preventive
measures to avoid the introduction of schistosomiasis into Europe.

This article is part of the Royal Society Science+ meeting issue 'Parasite evolution and impact in action: exploring the importance and control of hybrid schistosomes in Africa and beyond'.

**1. Introduction**

Schistosomiasis is the second most prevalent parasitic disease globally, with
over 150 million people infected annually, most commonly in sub-Saharan
Africa [1]. In Europe, infections are primarily associated with travelling to
endemic regions or with migrants from endemic countries for schistosomia-
sis [2] arriving in Europe via legal migration or through irregular border

© 2026 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.

<footnote n="1"><sup>1</sup>Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain</footnote>

<footnote n="2"><sup>2</sup>Centro de Investigación Biomédica en Red de Enfermedades Infecciosas (CIBERINFEC), Instituto de Salud Carlos III, Madrid, Spain</footnote>

<footnote n="3"><sup>3</sup>Grupo de Investigación en Salud Internacional de Almería (GISIA), Faculad de Ciencias de la Salud, Universidad de Almería, La Cañada de San Urbano, Almería, Spain</footnote>

<footnote n="4"><sup>4</sup>Unidad de Medicina Tropical, Hospital Universitario Poniente, El Ejido, Almería, Spain</footnote>

<footnote n="5"><sup>5</sup>University of Perpignan Via Domitia, Perpignan, France</footnote>

<footnote>ADE-E, 0000-0002-6147-0300; PA, 0000-0002-2815-1324; JS-C, 0000-0002-4302-7022;
MPL-G, 0000-0001-5260-7072; MJS-P, 0000-0002-0003-8207; NC-F, 0000-0002-7197-5652;
MCF, 0000-0002-4552-3177; AM-O, 0000-0001-6816-1140; JB, 0000-0002-0793-3108;
SM-C, 0000-0002-1685-7004; MAV, 0000-0003-1584-8330; MDB, 0000-0003-2347-7269</footnote>
crossings, including both land border and sea crossings [3]. Over the past two decades, schistosomiasis has appeared as the second most prevalent neglected tropical disease in migrants across European nations [4].

In recent years, Southern European countries have suffered a considerable increase in irregular migratory flow, mainly from sub-Saharan countries. Cases of imported schistosomiasis have become increasingly prevalent, mainly in the context of global migration. Among the European countries that have reported cases of imported schistosomiasis are Italy, Switzerland, Belgium, Ireland, Germany, England, Portugal, France, The Netherlands and Spain [2,4–9]. Schistosomiasis poses a significant public health challenge in Europe due to its potential to cause severe long-term clinical complications [8,10], including chronic urogenital and hepato-intestinal disorders [11].

Although human schistosomiasis is not endemic in Europe, autochthonous transmission of *Schistosoma haematobium* has been confirmed in three European countries: Portugal (reported in 1920 and considered extinct by 1966) [12], France (first detected in 2011 and with ongoing transmission) [13–17] and Spain (occurred in 2003 and retrospectively reported in 2019) [18].

A growing concern is the emergence of hybridization events in endemic regions of Africa [19–25], with West African countries being the most involved in migration to Europe. Natural hybridizations are known (i) between human-infecting schistosome species such as *S. haematobium* × *Schistosoma guineensis* (*Sh* × *Sg*) [26] or *Schistosoma mansoni* × *S. haematobium* (*Sm* × *Sh*) [27]; (ii) between animal-infecting schistosome species like *Schistosoma bovis* × *Schistosoma curassoni* (*Sb* × *Sc*) [20]; (iii) and between schistosome species that typically infect humans and schistosome species that typically infect animals such as *S. mansoni* × *Schistosoma rodhaini* (*Sm* × *Sr*) [28], *S. mansoni* × *Schistosoma mattheei* (*Sm* × *Smat*) [25], *S. haematobium* × *S. bovis* (*Sh* × *Sb*) [20] or *S. haematobium* × *S. mattheei* (*Sh* × *Smat*) [25]. Today, these *Schistosoma* hybrids are no longer restricted to schistosomiasis-endemic countries. Notably, the schistosomiasis outbreak in Corsica involved a hybrid species in autochthonous transmission [29]. Furthermore, studies have identified the presence of *Schistosoma* hybrids in both migrants and travellers diagnosed in Europe [30–34]. This highlights the importance of vigilance of imported cases and the need for species identification in non-endemic settings.

In Europe, the patient profile with imported schistosomiasis is very heterogeneous, including migrants, travellers, visiting friends and relatives, or expatriates, living in an endemic area for a long period and then returning to Europe. Furthermore, the schistosomiasis-endemic regions associated with these patients' countries of origin, travel destinations or workplaces are numerous and highly diverse. All of these increase the possibilities of detecting infections caused by both different *Schistosoma* species and hybrids, which complicates the diagnosis and treatment. Given this complexity, the aim of this work concerns the multidisciplinary challenges involved in the classification of 'pure' *Schistosoma* strains and hybrids introduced into southwestern Europe. The term 'pure' is used here according to the results obtained from the traditionally employed nuclear ribosomal DNA (rDNA) and mitochondrial DNA (mtDNA) markers. Conversely, the term hybrid is applied when there is a discrepancy in species assignment between these markers or when two alleles from different species (either human or animal) are detected in the same individual. We have therefore considered: (i) the identification of 'pure' species and hybrids by molecular analysis of *Schistosoma* eggs; (ii) the importance of morphogenetic studies in *Schistosoma* eggs; (iii) the potential risk of emergence of hybrid *Schistosoma* infections in Europe; and (iv) the clinical management, diagnostic procedures and treatment of schistosomiasis patients in non-endemic countries in Europe. Finally, 'pure' and hybrid schistosomes detected in a tropical medicine unit (TMU) of a non-endemic country (Almería, Spain) are included as an example.

The complexity of managing not only the clinical aspects, diagnosis and treatment of this disease, but also the need to be prepared to quantify the risks and prevent future outbreaks of schistosomiasis in Europe is evident. Recent outbreaks including autochthonous transmission in regions such as Corsica (France) [15] and Almería (Spain) [18] highlight this complexity. In addition, the detection of hybrid *Schistosoma* species adapting to new European habitats is a challenge. Appropriate surveillance and preventive measures are needed to face this evolving landscape of schistosomiasis in Europe.

## 2. Molecular analyses of *Schistosoma* eggs for hybrid detection

Egg morphology differs among *Schistosoma* species. It should be considered that the egg morphology *a priori* corresponds to the genotype of the female schistosome, which is responsible for producing the egg shell. However, egg morphology does not always correspond to the genetic identity of the respective *Schistosoma* species. Indeed, the specific profile may correspond to a hybrid between two *Schistosoma* species. Moreover, atypical morphologies of *Schistosoma* eggs may reflect phenotypic intraspecific variability within a single *Schistosoma* species or indicate potential hybridization events [26,29,30,35].

Molecular analyses of eggs shed by patients diagnosed with schistosomiasis have provided a better understanding of the genetic variability of both 'pure' and hybrid strains of schistosomes reaching Europe. Increasing molecular studies are essential to assess the prevalence and potential impact of infections by hybrid schistosomes in non-endemic settings. Findings of hybrid schistosomes reported in migrants and/or travellers returning from an endemic country are listed in table 1.

### (a) Hybrids of the *haematobium* group

The most common hybrids reported in West and Central African countries concern the *haematobium* group, mainly those involving *S. haematobium* and the livestock parasites *S. bovis* or *S. curassoni* [20,23,39,40]. In endemic regions, these hybrids are usually identified by genetic characterization of miracidia collected from patients' urine [20,40–42].

Given that schistosomiasis cases in Europe are predominantly imported from Africa, which bears the highest global burden of this disease [43], the detection of hybrid infections in patients diagnosed in Europe is, *a priori*, not unexpected. Nevertheless, studies focusing on the genetic identification of *Schistosoma* eggs from infected patients still remain sporadic in Europe. Despite
<table><caption>**Table 1.** Genetic hybrid combinations of *Schistosoma* spp. reported in Europe and confirmed by molecular analyses of eggs shed by infected people. EU, European; *Sh*, *Schistosoma haematobium*; *Sb*, *S. bovis*; *Sc*, *S. curassoni*; *Sm*, *S. mansoni*; *Sg*, *S. guineensis*; *Smat*, *Schistosoma mattheei*; *Sh* × *Sb*, *S. haematobium* × *S. bovis*; *Sh* × *Sc*, *S. haematobium* × *S. curassoni*; *Sh* × *Sb* × *Sc*, *S. haematobium* × *S. bovis* or *S. curassoni*; *Sh* × *Sb* × *Sc*, *S. haematobium* × *S. bovis* × *S. curassoni*.</caption><thead><tr><th>hybrid combinations</th><th>people infected</th><th>geographical locality of infection (country)</th><th>diagnosed in (country)</th><th>references</th></tr></thead><tbody><tr><td>Sh × Sb</td><td>EU-tourist and local people</td><td>Corsica, France</td><td>France</td><td>[14,15,17,29,36]</td></tr><tr><td>Sh × Sb</td><td>Belgian travellers</td><td>Mali</td><td>Belgium</td><td>[30]</td></tr><tr><td>Sh × Sb</td><td>non-EU immigrants</td><td>Mali, Mauritania, Senegal</td><td>Spain</td><td>[33,37]</td></tr><tr><td>Sh × Sc</td><td>non-EU immigrants</td><td>Côte d'Ivoire, Mali, Mauritania, Senegal</td><td>Spain</td><td>[33,37]</td></tr><tr><td>Sh × Sm</td><td>non-EU immigrants</td><td>Côte d'Ivoire</td><td>France</td><td>[31,32]</td></tr><tr><td>Sh × Sm</td><td>non-EU immigrants</td><td>Guinea-Bissau, Senegal</td><td>Spain</td><td>[37]</td></tr><tr><td>Sm × Sh</td><td>non-EU immigrants</td><td>Côte d'Ivoire, Mali</td><td>Spain</td><td>[34]</td></tr><tr><td>Sm × Sh + Sh × Sb/Sc</td><td>non-EU immigrants</td><td>Guinea-Bissau</td><td>Spain</td><td>[34]</td></tr><tr><td>Sm × Sh + Sh × Sc</td><td>non-EU immigrants</td><td>Côte d'Ivoire</td><td>Spain</td><td>[34]</td></tr><tr><td>Sh × Sb × Sc</td><td>non-EU immigrants</td><td>Mali</td><td>Spain</td><td>[33]</td></tr><tr><td>Smat × Sh<sup>a</sup></td><td>EU travellers</td><td>South Africa</td><td>Belgium</td><td>[38]</td></tr></tbody></table>

this, recent research has provided evidence of hybrid infections. An example is a study conducted in Belgium, where DNA sequencing confirmed that eggs found in the urine of travellers returning from Mali belonged to a *S. haematobium* × *S. bovis* hybrid infection [30].

Further evidence has been provided by a study on 54 migrants diagnosed with urogenital schistosomiasis in Spain. Among a total of 642 eggs with *S. haematobium*-like morphology shed in the urine, the genetic analysis revealed that 83.33% were *S. haematobium* and 16.67% were hybrids. The most frequent hybrid combinations were *S. haematobium* × *S. bovis* (68.18%) and *S. haematobium* × *S. curassoni* (31.82%) [33]. This study identified a patient from Mali with hybrid eggs resulting from the crossbreeding of three species: *S. haematobium* × *S. bovis* × *S. curassoni*. Although human cases of such a three-species hybrid have been reported in endemic regions, they remain sporadic. To date, *S. haematobium* × *S. bovis* × *S. curassoni* hybrids have only been identified in Niger [22] and Mali [39]. The genetic profile of these three-species hybrid eggs supports the hypothesis that they are not first-generation hybrids, but rather the result of parental backcrosses and/or relatively recent hybrid lineages [22,39].

Moreover, a patient from Senegal was found to harbour eggs of two different hybrid types: *S. haematobium* × *S. bovis* and *S. haematobium* × *S. curassoni* [33]. The presence of multiple hybrid types within a single patient was also reported in another study of sub-Saharan migrants [34]. In this case, two individuals from Côte d'Ivoire and Guinea-Bissau shed hybrid eggs of *S. mansoni* × *S. haematobium* and *S. haematobium* × *S. bovis*/*S. curassoni* in their urine. This phenomenon has also been observed in endemic regions such as Senegal [20], where the transmission of several *Schistosoma* species overlaps in certain areas.

It is worth noting that a high number of sub-Saharan migrant patients from Mali, Mauritania, Senegal and Côte d'Ivoire, specifically 22/54 (40.74%), and diagnosed in Spain, simultaneously carried 'pure' and hybrid eggs in their urine [34]. This is consistent with previous studies, where molecular analyses showed that 38.7% of migrant patients with schistosomiasis were carriers of mixed infections and shed both 'pure' and hybrid eggs, with up to 50% of patients carrying hybrids in the case of Senegal [37]. These data are similar to the number of patients who were carriers of *Schistosoma* hybrids found in the Corsican outbreak, which revealed that 7/12 (58%) patients examined shed *S. haematobium* × *S. bovis* hybrid eggs [15].

Furthermore, hybrid infections have been reported even in patients who do not shed eggs or in whom eggs are not detected. An interesting example comes from a study in which sequencing of *Schistosoma* mitochondrial and nuclear DNA extracted from serum samples revealed the presence of an *S. mattheei* × *S. haematobium* hybrid in a cohort of travellers infected in South Africa [38].

It is important to note that both urine and stool samples must be examined for *Schistosoma* eggs, as egg excretion patterns may vary depending on the species and hybrid forms. Recent findings from Malawi have demonstrated that the *S. haematobium* × *S. mattheei* hybrid is much more commonly detected in stool than in urine [25].

## (b) Hybrids between two human *Schistosoma* species

Prior to the detection of hybrids by molecular methods, the presence of lateral-spined eggs in urine was thought to be ectopically excreted *S. mansoni* eggs due to a 'spill-over' caused by high parasite loads [44,45]. This phenomenon of detecting *S. mansoni*-like eggs in urine has been widely reported in endemic countries. For example, in Cameroon, *S. mansoni*-like eggs were found in 14.5% of urine samples and *S. haematobium* eggs in 3% of stool samples [45]. In two northern Senegalese communities, 53% of infected subjects had mixed *S. mansoni* and *S. haematobium* infections, of which 15% showed ectopic egg elimination [46]. In two communities in Nigeria, the prevalence of ectopic *S. mansoni*-like eggs in urine was 4.7% [47].

However, recent studies suggest that ectopic eggs are more likely to be potential hybrids. This is exemplified by eggs with an *S. mansoni*-like morphology, ectopically shed in the urine of migrants from Côte d'Ivoire and diagnosed in France, which were found to be *S. mansoni* × *S. haematobium* hybrids [31,32].

<footnote><sup>a</sup>DNA extracted from serum samples.</footnote>
Ectopic *S. mansoni*-like eggs in urine have also been detected in patients diagnosed in Spain. In this study, 46 ectopic *S. mansoni*-like eggs from six sub-Saharan migrant patients (from Senegal, Guinea-Bissau, Côte d'Ivoire and Mali) were genotyped individually. These eggs, containing a fully developed miracidium inside, were genetically confirmed as hybrids between *S. mansoni* and *S. haematobium* using rapid diagnostics by polymerase chain reaction (RD-PCR), sequencing and cloning [34]. Mito-nuclear signatures and nuclear and mitochondrial haplotypes obtained from these eggs showed a mitochondrial profile (*cox1*) of *S. mansoni* and a ribosomal hybrid profile (internal transcribed spacers, ITSs) (*S. mansoni* × *S. haematobium*), due to the presence of alleles from both species, with a double chromatogram showing peaks of equal height at the positions that differentiate *S. mansoni* from *S. haematobium* [34]. Additionally, this type of hybrid was also obtained from two eggs excreted in this case in the faeces of one migrant patient from Senegal, with an *S. mansoni*-like morphology. Although it could be a case of contamination during sample collection, this type of hybrid has also been previously reported in faeces [27,31].

The fact that most studies in endemic countries have not used molecular tools may explain why, despite the number of studies reporting the presence of ectopic *S. mansoni*-like eggs in urine [27,31,46], *S. mansoni* × *S. haematobium* hybrids have rarely been detected in studies conducted in endemic countries. Only one study conducted in children in Senegal [12] has reported these unexpected hybrids in their urine. The detection of *S. mansoni* × *S. haematobium* hybrids in patients diagnosed in Europe from different endemic countries suggests that these hybrids may be more common than previously thought in West Africa, occurring not only in Senegal but probably also in Guinea-Bissau, Côte d'Ivoire and Mali, as molecularly confirmed at geographical distance [31,32,34].

### 3. Importance of morphogenetic studies in *Schistosoma* eggs

The morphology of *Schistosoma* eggs has been fundamental for species identification, thanks to features such as size, shape and position of the spine [48]. In early traditional studies, the unique morphology of *Schistosoma* eggs was defined primarily by their length, width and length/width ratio. It is important to highlight that investigations on *S. intercalatum* eggs demonstrated significant variability in the length-to-width ratio [49]. Additionally, traditional morphometric assessments do not adequately capture the 'spindle' shape exhibited by certain morphological phenotypes [50].

Furthermore, some of the earliest traditional phenotypic observations on schistosomes suggested the possible existence of hybrids between human and animal species, mainly based on morphological analysis of eggs [22]. Indeed, early hybridization experiments, such as those performed by Taylor [51] with *S. mansoni*, *S. rodhaini*, *S. mattheei*, *S. haematobium* and *S. bovis*, showed that the hybrid eggs had a morphology intermediate between the parental species, indicating the potential of their analysis to detect hybridization events.

The incorporation of molecular techniques has provided new perspectives on the *Schistosoma* genus [33,34,40,52,53]. Many early phenotypic observations have been questioned or dismissed as identification errors, highlighting the need for a characterization approach that integrates precise genetic and phenotypic analyses in the study of *Schistosoma* eggs. However, morphogenetic studies in *Schistosoma* eggs are still scarce [35,50,54,55].

*Schistosoma* eggs exhibit distinct morphological characteristics that are crucial for disease diagnosis. As previously proposed, the egg morphology of *Schistosoma* spp. could be more accurately assessed by including additional measurements and applying geometric morphometric methods [35]. The variability in size and shape of *Schistosoma* eggs highlights the necessity to have standardized measurements available enabling detailed morphological analyses. In this regard, a standardized approach for the quantitative comparison of morphological characteristics of 'pure' eggs (according to RD-PCR of *cox1* and ITSs sequencing) from *S. haematobium*, *S. mansoni* and *S. bovis* was proposed [54]. This approach includes 17 measurements involving size, shape and spine features and two ratios such as the egg shape ratio and the elongation ratio. Previous studies with simpler measurements allowed for the description of two morphotypes of the terminal-spined eggs collected from infected patients in Corsica [29]. Round-to-oval-shaped eggs of the typical *S. haematobium* morphotype were shared by 26.7% of the eggs, whereas the more elongate and lozenge-shaped non-typical *S. haematobium* egg morphotype was found in the majority of the eggs (73.3%). Unfortunately, morphological and genetic characterizations were not performed on the same eggs, and the morphotype and genotype of hybrid eggs have so far not been correlated. Difficulties in the procedures evidently underlie this problem.

It should be noted that schistosome species exhibit intraspecific morphometric variation, with egg size differing both within the same host species and between different host species [50,56,57]. Nevertheless, due to the considerable complexity of the morphology of *Schistosoma* species eggs, there is insufficient research focusing on the intraspecific variability of their shape and size. For species that produce eggs with lateral spines, morphometric analyses of *S. mansoni* eggs from the island of Guadeloupe indicated intrapopulation variability [58]. In the category of schistosomes with terminal spines, both interspecific and intraspecific variability have been explored in several studies [54,59–63]. A recent study highlighted the impact of geographic factors on the morphometric variability of genetically 'pure' *S. haematobium* eggs from sub-Saharan migrants diagnosed in Spain [50], emphasizing the importance of accounting for the geographic origin of the patient when conducting egg morphometric analyses. In this study, genetically 'pure' *S. haematobium* eggs of migrant patients from Mali, Mauritania and Senegal were classified into three morphotypes (round, elongated and spindle) when comparing between countries. The results suggest that *S. haematobium* eggs show great shape variability within the three populations and, unexpectedly, round or elongated shapes are not always the most common phenotypes of genetically 'pure' *S. haematobium* eggs, as previously believed.

In Senegal, there is an overlap zone of *S. haematobium* and *S. bovis*, in which the terminal-spined eggs from infected subjects do not show distinct morphotypes and were considered as typical *S. haematobium* eggs by traditional measurements. However, molecular analyses of these eggs revealed two distinct mitochondrial *cox1* profiles (*S. bovis* and *S. haematobium*) and a single nuclear rDNA ITS profile (*S. haematobium*). Accordingly, it was suggested that egg morphology using traditional measurements is not a reliable indicator of hybrid ancestry [35].
S. haematobium is characterized by low genetic diversity, with only two main clades identified based on mitochondrial haplotypes across its distribution in Africa [20,64], and microsatellites do not appear to be useful in distinguishing structured populations [53]. Therefore, the observed differences in S. haematobium morphotypes between countries [50] are surprising. Unfortunately, genetic data from valuable analyses of egg morphotypes are too limited. Moreover, additional studies on the intraspecific variability of the egg phenotype are needed.

These studies highlight the importance of conducting studies on the morphogenetic characteristics of eggs of *Schistosoma* species, both 'pure' and hybrids, in the way to allow for a correlation between phenotype and genotype.

# 4. Emergence risk of hybrid schistosome infections in Europe

## (a) *Schistosoma haematobium* and its hybrids

The unexpected autochthonous outbreak of urogenital schistosomiasis in Corsica, France, represented a turning point for all countries in the circum-Mediterranean region [13,65,66]. The disease, caused by a S. haematobium × S. bovis hybrid strain imported from Senegal [15,29], has become established on this Mediterranean island, as additional cases have recently been identified in the Solenzara River, located in the island's southeastern region [17,36]. The persistence of this infection appears to be linked to the ability of *Bulinus truncatus*, the intermediate snail host, to survive through the winter while maintaining the infection and subsequently releasing viable cercariae once optimal temperatures are again reached [67]. One of the B. truncatus strains examined in the aforementioned study was sourced from Almería, Spain, a region where recent autochthonous cases of human urogenital schistosomiasis have also been reported [18]. Molecular evidence has confirmed the presence of migrant patients in the area carrying both 'pure' and hybrid schistosome species [37]. Therefore, although health authorities are implementing the necessary measures, the potential transmission of both S. haematobium and its hybrids by B. truncatus in the area still remains evident. This B. truncatus population has been molecularly studied by sequencing *cox1* (GenBank acc. no. KR108924), confirming a 100% homology with other isolates of B. truncatus from Portugal and Senegal [68] (which was also the area of origin of the schistosome strains introduced into the French island of Corsica).

*Bulinus* snails are known to act as intermediate hosts for both S. haematobium and S. bovis [15,40,52,69–74]. *Schistosoma haematobium* and hybrids of the S. haematobium group appeared to be more specific and were transmitted exclusively by B. truncatus [75], while S. bovis can also infect *Planorbarius* snails (widely present in the Iberian Peninsula and Portugal), together with *Bulinus* species. Furthermore, in Spain and Portugal, the snail *Planorbarius metidjensis* is a known transmitter of S. bovis [72] and has been found in wild populations naturally infected with S. haematobium during the schistosomiasis outbreak of the 1920s [76–79]. These countries are experiencing significant migratory flows from African regions today. Moreover, climate change may contribute to the expansion of snail habitats by enabling their adaptation to new environmental conditions. The spread of these snails may also be facilitated by the trade of aquatic plants or bird migrations [68,80].

The increased movement of people, including migration, combined with the widespread presence of planorbid snail species that are susceptible to S. haematobium and their hybrids in Mediterranean countries, emphasizes the risk of urogenital schistosomiasis spreading further in Europe. Moreover, hybridization in schistosomes is associated with heterosis (hybrid vigour), including the ability of hybrid schistosomes to expand their range thanks to the snail intermediate hosts [70,81–83]. In non-endemic areas, schistosomiasis introduction may occur when a competent intermediate host snail is locally available [79,84], although some examples of snail host shifts can occur when parasites disperse to new environments in which their natural primary hosts are absent [85]. Notably, *Bulinus* species have been documented in Cyprus, Greece and Crete, Italy (Sardinia and Sicily), Malta, Spain and Portugal [15,86–89], while *P. metidjensis*, a typical species of North Africa (Morocco and Algeria) [90,91], is commonly found in Spain and Portugal [78,92–94]. So far, it has been experimentally demonstrated that *P. metidjensis* is immune to experimental infection with hybrid S. haematobium × S. bovis parasites collected in Corsica that contain 23% genetic material from S. bovis [71]. This is consistent with the predominance of S. haematobium within the genome of this hybrid, although further experimental studies with other strains of *P. metidjensis* from Europe or Africa are necessary to verify whether they could be compatible and serve as a host.

The snail in which the parasite develops influences the production rhythm of cercariae. For example, in S. bovis, cercarial production during the patent period followed one big peak only when the cercariae developed in *Bulinus*, but followed a sinuous rhythm when larval development occurred in *P. metidjensis*, alternating periods of high and low production [73].

Climate change is predicted to have different effects on B. truncatus habitat suitability in different regions. Recent studies utilizing both correlative and mechanistic models have indicated a net increase of up to 17% in the total area of suitable habitat, mainly in Central Africa and Southern Europe. In these regions, urogenital schistosomiasis has a low prevalence or is currently absent, respectively. Thus, the spread of B. truncatus has the potential to put new populations at risk for urogenital schistosomiasis transmission [95]. In Europe, the establishment of widespread autochthonous schistosomiasis transmission is improbable, despite the presence of the intermediate snail host [3,96]. A risk map of the distribution of B. truncatus snails in Spain and Portugal [86] has been developed in order to better delineate the potential areas of transmission.

## (b) *Schistosoma mansoni* × S. haematobium hybrids

The potential viability of S. mansoni and S. haematobium hybrid eggs and their ability to infect *Bulinus* or *Biomphalaria* snails has not yet been demonstrated. Although preliminary experimental studies on the mating of S. mansoni and S. haematobium have been conducted [97], they did not include a genetic analysis of the eggs produced after crossbreeding between parents of
both species, as has been performed in other experimental studies, such as those involving *S. mansoni* × *S. bovis* [98]. Moreover, further experimental research is required to assess the viability and transmission potential of offspring resulting from *S. mansoni* × *S. haematobium* crosses, which would provide valuable insights into their possible impact on disease epidemiology. However, this is far from simple, as it should be considered that many different hybrids may be originated, several unviable and others viable, and without forgetting that in nature, backcrosses with genetically 'pure' species may increase hybrid vigour. Summing up, assessing the viability of such hybrids will unavoidably be a long process needing efforts in many overlapping endemic areas.

Transmission of *S. mansoni* has never been reported in Europe. However, *Biomphalaria tenophila*, a snail involved in the transmission of *S. mansoni* in Brazil, has been found in Romania [99], where this susceptible snail species has not only been introduced but has also successfully established itself [100]. Careful consideration should be given to the potential for host switching and the expansion into new areas. Given the relatively low specificity with which schistosomatids select their intermediate hosts [101,102] and their capacity to infect other mollusc groups, such as lymnaeids [103], it is crucial to monitor such a possibility of transmission, even though it has not yet been confirmed. Some snails that are susceptible to this infection, including *B. glabrata*, *B. straminea*, *B. tenophila* and *B. pfeifferi*, intermediate hosts of *S. mansoni* in South America, have already demonstrated the ability to spread schistosomiasis into new continents [3].

# 5. Clinical and diagnostic aspects of schistosomiasis in non-endemic European countries

## (a) Clinical management of schistosomiasis in migrant populations

Despite the public health importance of schistosomiasis, it is often underdiagnosed in non-endemic regions, and there are significant delays in its detection outside specialized centres [104–106]. Migrants from endemic areas, a particularly vulnerable group, face long delays in diagnosis, as highlighted by a multicentre cohort study in Italy, which reported a mean delay of 31 months from arrival, reaching 110 months for asymptomatic patients [107]. This delay can lead to significant associated morbidity, including long-term complications associated with chronic infection [8,10,107,108].

The lack of standardized diagnostic protocols and treatment strategies at international and often national level exacerbates the problem in Europe [105]. Variability in diagnostic methods has resulted in reported detection rates ranging from 7.5% to 43% among migrants from endemic areas [109]. In addition, the diverse clinical manifestations of schistosomiasis, combined with limited familiarity among healthcare providers with tropical diseases, often result in missed or delayed diagnoses of patients [110]. Migrant populations also face significant barriers to accessing healthcare, including language barriers, cultural differences, legal restrictions and financial limitations [4].

After recognizing the public health impact of schistosomiasis, European health authorities now recommend systematic serological screening for the disease in migrant populations from high-endemic countries (sub-Saharan Africa and focal areas in Asia and South America) who have arrived in the last 5 years [111]. Such an approach not only significantly prevents chronicity and associated sequelae but also provides direct clinical benefits to patients and reduces healthcare costs associated with managing complications [4,112], as well as avoiding potential autochthonous transmission. Harmonization of case definitions, as recently proposed by experts from institutions affiliated with GeoSentinel and TropNet [105,106], along with standardization of diagnostic and treatment protocols, is another critical factor in improving the detection and clinical management of imported schistosomiasis in non-endemic areas.

In this context, surveillance networks and medical societies play a key role in developing consensus on the management of imported diseases, acting as platforms for collaboration between experts and facilitating the harmonization of clinical and diagnostic criteria [105,106,109,113–115]. Such a consensus not only improves the quality of care but also contributes to the training of professionals and the development of more effective health policies.

In Spain, a consensus document has recently been developed to guide the screening, diagnosis and treatment of imported schistosomiasis [109]. This document emphasizes that serological screening should be carried out in at-risk populations from endemic areas, regardless of symptoms or laboratory abnormalities. To confirm the infection, a combination of serological and direct diagnostic methods is recommended. Regarding treatment, praziquantel (single 40 mg kg⁻¹ dose) remains the primary option, though follow-up is underlined to detect potential complications or recurrences due to treatment failures.

Clinical and analytical follow-up of patients infected with hybrid species in non-endemic areas is an ideal situation to understand their response to praziquantel treatment without the risk of reinfection from endemic zones. However, the main limitation is the availability of techniques that can confirm the patient's true cure [11]. Microscopy has low sensitivity, and antibodies remain positive for a long time after treatment, making it difficult to distinguish between active and past infections. On the other hand, molecular techniques such as PCR and loop-mediated isothermal amplification (LAMP) also have the disadvantage of detecting DNA for extended periods after parasite clearance. Antigen tests, especially the CAA test [116], are the most promising methods to confirm the patient's real cure and, therefore, the treatment response. However, this technique is still not widely used and is currently only available as an external service at Leiden University Medical Centre in the Netherlands.

## (b) Diagnosis of imported schistosomiasis: a challenge for hybrid detection

In routine clinical practice, schistosomiasis is mainly diagnosed by the detection of *Schistosoma* eggs in urine, faeces or biopsies, which remains the gold standard, or by serological techniques. These techniques, which are routinely used to diagnose imported schistosomiasis in Europe [109,117–119], are unable to differentiate between 'pure' or hybrid schistosomes.
The detection of hybrid eggs/miracidia is only possible through molecular techniques. Most studies focusing on the detection of hybrids within the genus *Schistosoma* have been performed using a multi-locus approach combining mtDNA and rDNA markers, as single-locus approaches are often insufficient to detect hybridization and/or introgression [22].

Molecular techniques combining the mitochondrial *cox1* gene and nuclear ITS regions have been widely used to distinguish *Schistosoma* species and identify hybrids in patients from endemic areas [20,39,41,42]. Although sequencing the entire *cox1* gene and the complete intergenic nuclear ribosomal DNA would allow for a more accurate species identification, these methods remain time-consuming and costly. Therefore, these approaches typically integrate ITS-2 sequencing with a rapid one-step PCR (RD-PCR) assay that targets the *cox1* gene and allows discrimination between three *Schistosoma* species (*S. haematobium*, *S. mansoni* and *S. bovis/S. curassoni*) by amplicon size.

This approach has limitations. One is that ITS-2 sequencing cannot distinguish between *S. bovis* and *S. curassoni*, so in this particular case, an additional marker, most commonly 18S, must be used. To overcome this limitation, researchers have developed the duplex tetra-primer ARMS-PCR assay as an improved alternative [120]. This technique incorporates both ITS and 18S markers into a single reaction, eliminating the need to sequence both markers. As a result, ARMS-PCR significantly reduces the processing time and cost for differentiating *S. haematobium*, *S. bovis*, *S. curassoni* and their hybrids.

Interestingly, a novel real-time PCR assay has been developed to enable the rapid screening and identification of *Schistosoma* hybrids [121]. This technique, which is being used in endemic areas, combines two separate real-time PCR reactions: one targeting mtDNA and the other nuclear DNA. Both assays discriminate between *Schistosoma* species by analysing high-resolution melting peaks. Specifically, the mtDNA real-time PCR is a species-specific multiplex assay that targets the tRNA-Lys gene markers for *S. curassoni*, *S. bovis*, *S. haematobium* and *S. mansoni*, and the ND6 and ND4 genes for *S. mattheei* and *S. margrebowiei*, respectively, thereby expanding the range of species detectable compared to RD-PCR.

LAMP technology presents a higher sensitivity than microscopy for the diagnosis of imported urinary schistosomiasis [122]. LAMP has also been evaluated to detect DNA from *S. haematobium*--*S. bovis* hybrids [123], but to date has not yet been used with clinical samples.

Despite significant advances in *Schistosoma* hybrid detection techniques, their use remains limited for research in settings and is not yet standardized for clinical practice. In addition, the use of next-generation sequencing methods has clearly shown that the frequency of hybrids is largely underestimated [124]. Further progress is needed to develop rapid and accessible methods to enable routine hybrid detection in diagnostic settings.

# 6. 'Pure' and hybrid *Schistosoma* species detected in a tropical medicine unit in a non-endemic region: Almería, Spain

In recent years, Spain has seen an increase in the number of irregular migrants, including subjects from sub-Saharan Africa, driven by armed conflict, political instability and climate change [125]. The main migratory routes to reach Spain, and consequently Europe, are across the Canary Islands (Atlantic route) or through the Spanish cities Ceuta and Melilla, sited in North Africa; in addition, across the Mediterranean Sea, either coming from Libya to Italy or from Morocco, crossing the Strait of Gibraltar in small boats.

The Poniente area is an administrative and health region located in the province of Almería, in southeast Spain (figure 1). It holds a population close to 300,000 inhabitants, with a migrant share of 21%, many of them coming from sub-Saharan countries to work in horticultural greenhouses. This region is known for its extensive greenhouse agriculture, which covers 31,614 hectares, often referred to as the 'vegetable garden of Europe' (figure 1). It was precisely in this locality where local transmission affected four farmers who became infected after swimming in a pool used for irrigating nearby crops [18], and where competent *B. truncatus* snails were present [68,86,126].

Schistosomiasis is one of the most prevalent diseases diagnosed by the TMU of the Poniente University Hospital (Almería, Spain) among the sub-Saharan migrant population living in the region [7,8]. This TMU, in a study to assess the burden of disease in newly arrived African patients, found that 32.2% tested seropositive for *Schistosoma* [7]. In addition, a retrospective observational study of 3090 screened individuals identified 326 confirmed cases (10.5%), with severe complications occurring in 4% of patients (5% with hepatointestinal and 3.5% with urogenital schistosomiasis) [8]. Following a standardized protocol, patients found positive for schistosomiasis were offered free treatment (single 40 mg kg⁻¹ dose of praziquantel) with clinical, radiological and analytical follow-up after three months. Patients with schistosomiasis-related ultrasound abnormalities undergo further imaging three to six months after treatment.

Given the potential clinical implications of *Schistosoma* hybrids, molecular analyses have been performed with patients from this TMU who were diagnosed with schistosomiasis. Only urine or faecal samples with positive confirmation by egg findings were included for genetic identification [33,34].

During the period from October 2016 to February 2025, a total of 1065 eggs found in urine and faeces from 80 patients from nine African countries were individually processed to describe their mito-nuclear signature by *cox1* RD-PCR and ITS-2/18S sequencing and cloning, and haplotype identification by means of the complete ITS1-5.8S-ITS2 rDNA and *cox1* sequencing. A total of 35% (28/80) of the patients were simultaneously carrying 'pure' and hybrid eggs in their urine. Among the 'pure' species, *S. haematobium*, *S. mansoni* and *S. guineensis* (Sg) have been genetically identified. Among the hybrid combinations, those resulting from the interaction of two species (*S. haematobium* × *S. bovis*, *S. haematobium* × *S. curassoni* and *S. mansoni* × *S. haematobium*) and three species (*S. haematobium* × *S. bovis* × *S. curassoni*) were detected. Migrant patients studied were carriers of (i) only one *Schistosoma* species, 63.75% (51/80); (ii) two *Schistosoma* species in co-infection, 1.25% (1/80); 'pure'+hybrid *Schistosoma* species, 35% (28/80). Worth mentioning are the high frequency of different hybrid types and the presence of up to
<figure><img src="image_6.png" /></figure>

**Figure 1.** (A,B) Satellite images of southern Spain showing densely packed greenhouses (in white) in the province of Almería (photo credit: NASA/GSFC/METI/ERSDAC/JAROS, and U.S./Japan ASTER Science Team). (C) Irrigation pool inside greenhouses (photo credit: S. Mas-Coma). (D) Aerial view of greenhouses in Almerimar, Spain (https://www.istockphoto.com/es/foto/invernaderos-de-panorama-a%C3%A9reo-en-el-almerimar-espa%C3%B1a-qm1141933789-306131733) (photo credit: amoklv, ID: 1141933789). (E) Graphical summary of 'pure' and hybrid *Schistosoma* species according to country of origin of migrant patients in whom they were detected. Administrative areas were obtained from the Database of Global Administrative Areas (GADM) Base 4.1 v dataset, and additional spatial data were acquired from the Food and Agriculture Organization of the United Nations statistical data (FAOSTAT). These datasets were integrated into a project using QGIS version 3.40.4. *Sh*, *Schistosoma haematobium*; *Sb*, *S. bovis*; *Sc*, *S. curassoni*; *Sm*, *S. mansoni*; *Sg*, *S. guineensis*; *Sh* × *Sb*, *S. haematobium* × *S. bovis*; *Sh* × *Sc*, *S. haematobium* × *S. curassoni*; *Sh* × *Sb/Sc*, *S. haematobium* × *S. bovis* or *S. curassoni*; *Sh* × *Sb* × *Sc*, *S. haematobium* × *S. bovis* × *S. curassoni*.

three species involved in such hybrids (S. *haematobium* × S. *bovis* + S. *haematobium* × S. *curassoni*; S. *mansoni* × S. *haematobium* + S. *haematobium* × S. *bovis*/*S. curassoni*) in the urine of the same patient [33,34]. Concerning the countries of origin, the patients from Mali (13 out of 17 patients, 76.47%) are those presenting the most hybrids, followed by patients from Senegal (9/18, 50%), Mauritania (4/9, 44.44%) and Guinea-Bissau (1/3, 33.33 %) (figure 2).

Up to the present, little is known about hybrid species regarding clinical picture, diagnostic challenges and potential treatment problems [37,127]. The study conducted in Spain with sub-Saharan migrant patients [37] concluded that although *Schistosoma* hybrids are associated with increased morbidity, they do not affect the efficacy of diagnostic tests or response to treatment. Importantly, all patients in the study were also carriers of 'pure' *Schistosoma* eggs, which could influence the results in terms of the effectiveness of diagnostic tests. This study highlights the importance of identifying hybrids for more accurate clinical management. Collaboration between researchers and physicians is essential to understand the impact of these hybrids on morbidity and treatment response.

## 7. Conclusions

Hybrid *Schistosoma* lineages pose a significant challenge to schistosomiasis control and elimination, with their full impact still under discussion. Molecular, phenotypic and phylogenetic analyses of eggs excreted by migrants and travellers in Europe reveal infections caused by both 'pure' *Schistosoma* species (*Sh*, *Sm*, *Sg*) and hybrids (*Sm* × *Sh*, *Sh* × *Sb*, *Sh* × *Sc*, *Sh* × *Smat*). Hybrid eggs (*Sm* × *Sh*) have been predominantly detected in ectopic eliminations, while hybrids between species of the *haematobium* group have been consistently found in urine.

Molecular studies confirm the presence of hybrid eggs involving three-species interactions (*Sh* × *Sb* × *Sc*) in patients from Mali and two types of hybrids in the same patient involving three species (*Sh* × *Sb* + *Sh* × *Sc*; *Sm* × *Sh* + *Sh* × *Sb/Sc*) from Senegal, Côte d'Ivoire and Guinea-Bissau.

Notably, 35% of schistosomiasis cases (28/80) in a Spanish TMU involve hybrid infections. Based on the current data, key endemic countries contributing hybrid lineages to Europe include Mali, Senegal, Côte d'Ivoire, Mauritania, Guinea-Bissau and South Africa.

The presence of snails as potential vectors of urinary schistosomiasis in southwestern Europe, coupled with increasing migration from endemic regions, climate change and global warming, unrestricted access of carriers (infected people) to open freshwater sources (natural and artificial snail-vector-inhabited water collections), and the introduction of diverse *Schistosoma* species and hybrids underlie pressing challenges on non-endemic countries, particularly in Europe, about the need to be prepared. These challenges highlight the importance of identifying hybrids for more accurate clinical management, diagnosis and treatment for a better understanding of their impact on morbidity and treatment response. The potential adaptation of *Schistosoma* hybrids in Europe highlights the need for enhanced surveillance and prevention.
<figure><img src="image_7.png" /><figcaption>**Figure 2.** Graphical representation of the number of migrant patients (inside the bars) carrying: 'pure' *Schistosoma* eggs in urine (dark blue); 'pure' and hybrid *Schistosoma* eggs in urine (midea blue); coinfections *Schistosoma haematobium* and *S. mansoni* (green); 'pure' and hybrid *Schistosoma* eggs with ectopic shedding of *Sm*-like eggs in urine (light blue); and 'pure' *Schistosoma* eggs in stools (magenta), by country of origin.</figcaption></figure>

**Ethics.** This work did not require ethical approval from a human subject or animal welfare committee.

**Data accessibility.** This article has no additional data.

**Declaration of AI use.** We have not used AI-assisted technologies in creating this article.

**Authors' contributions.** A.D.E.-E.: data curation, formal analysis, investigation, methodology, validation, visualization, writing—original draft, writing—review and editing; P.A.: data curation, formal analysis, investigation, methodology, visualization; J.S.-C.: funding acquisition, investigation, resources, validation, visualization, writing—review and editing; M.P.L.-G.: investigation, methodology, resources; M.J.S.-P.: investigation, methodology, resources; N.C.-F.: investigation, methodology, resources; M.C.F.: investigation, methodology; A.M.-O.: investigation, methodology, resources; J.B.: supervision, validation, visualization, writing—review and editing; S.M.-C.: conceptualization, supervision, validation, visualization, writing—review and editing; M.A.V.: formal analysis, investigation, methodology, supervision, validation, visualization, writing—original draft, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

**Conflict of interest declaration.** We declare we have no competing interests.

**Funding.** M.D.B. was funded by CIBER de Enfermedades Infecciosas (CB21/13/00056), Instituto de Salud Carlos III (ISCIII), Ministry of Science and Innovation, and the European Union – NextGenerationEU, Madrid, Spain and PROMETEO Program, Programa de Ayudas para Grupos de Investigación de Excelencia (2021/004), Generalitat Valenciana (GVA) Valencia, Spain; J.S.C. was funded by Consejería de Salud y Familias de la Junta de Andalucía (PI-001-2019), co-financed with FEDER funds (European Regional Development Fund), Sevilla, Spain; S.M.-C. and J.S.-C. were funded by Red de Investigación de Centros de Enfermedades Tropicales – RICET (RD16/0027/0023 and RD16/0027/0013), Instituto de Salud Carlos III-Subdirección General de Redes y Centros de Investigación Cooperativa RETICS, Ministry of Health and Consumption, Madrid, Spain; A.D.E.-E. was supported by a Fellowship of the Programa de Ayudas de la Generalitat Valenciana y Fondo Social Europeo, 2019 (ACIF/2019/182).

**Acknowledgements.** The authors would like to thank M.V.M. G. Colangelli, a member of the Sanitary Parasitology Unit, Department of Parasitology of the University of Valencia, Spain, for her collaboration in receiving and processing samples. Technical support was provided by the Servicio Central de Secuenciación para la Investigación Experimental (SCSIE) of the Universidad de Valencia (Unit of Genomics for DNA sequencing, Dr A. Martínez; and Unit of Microscopy, Dr M.P. Gómez).

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