• View in gallery

    Computed tomography scan of the chest (axial plane) showing a well-defined lung nodule in the right lung.

  • View in gallery

    Histological examination of a biopsy specimen from a lung lesion. (A) Schistosoma egg surrounded by granulomatous inflammation and eosinophilic reaction (hematoxylin and eosin stain, magnification ×100); (B) Schistosoma egg exhibiting a prominent terminal spine (hematoxylin and eosin stain, magnification ×400); (C) strongly positive acid-fast egg's shell (modified Ziehl–Neelsen stain, magnification ×400).

  • 1.

    World Health Organization, 2015. Schistosomiasis. Fact sheet N°115. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/. Accessed October 15, 2015.

    • Search Google Scholar
    • Export Citation
  • 2.

    Nicolls DJ, Weld LH, Schwartz E, Reed C, von Sonnenburg F, Freedman DO, Kozarsky PE, 2008. GeoSentinel Surveillance Network. Characteristics of schistosomiasis in travelers reported to the GeoSentinel Surveillance Network 1997–2008. Am J Trop Med Hyg 79: 729734.

    • Search Google Scholar
    • Export Citation
  • 3.

    Ross AG, Vickers D, Olds GR, Shah SM, McManus DP, 2007. Katayama syndrome. Lancet Infect Dis 7: 218224.

  • 4.

    Schwartz E, Rozenman J, Perelman M, 2000. Pulmonary manifestations of early schistosome infection among nonimmune travelers. Am J Med 109: 718722.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cooke GS, Lalvani A, Gleeson FV, Conlon CP, 1999. Acute pulmonary schistosomiasis in travelers returning from Lake Malawi, sub-Saharan Africa. Clin Infect Dis 29: 836839.

    • Search Google Scholar
    • Export Citation
  • 6.

    Colebunders R, Verstraeten T, Van Gompel A, Van den Ende J, De Roo A, Polderman A, Visser L, 1995. Acute schistosomiasis in travelers returning from Mali. J Travel Med 2: 235238.

    • Search Google Scholar
    • Export Citation
  • 7.

    Jauréguiberry S, Paris L, Caumes E, 2010. Acute schistosomiasis, a diagnostic and therapeutic challenge. Clin Microbiol Infect 16: 225231.

  • 8.

    Pavlin BI, Kozarsky P, Cetron MS, 2012. Acute pulmonary schistosomiasis in travelers: case report and review of the literature. Travel Med Infect Dis 10: 209219.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonçalves EC, Fonseca AP, Pittella JE, 1995. Frequency of schistosomiasis mansoni, of its clinicopathological forms and of the ectopic locations of the parasite in autopsies in Belo Horizonte, Brazil. J Trop Med Hyg 98: 289295.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gobbi F, Martelli G, Attard L, Buonfrate D, Angheben A, Marchese V, Bortesi L, Gobbo M, Vanino E, Viale P, Bisoffi Z, 2015. Schistosoma mansoni eggs in spleen and lungs, mimicking other diseases. PLoS Negl Trop Dis 9: e0003860.

    • Search Google Scholar
    • Export Citation
  • 11.

    Baharoon S, Al-Jahdali H, Bamefleh H, Elkeir A, Yamani N, 2011. Acute pulmonary schistosomiasis. J Glob Infect Dis 3: 293295.

  • 12.

    Kolosionek E, Graham BB, Tuder RM, Butrous G, 2011. Pulmonary vascular disease associated with parasitic infection—the role of schistosomiasis. Clin Microbiol Infect 17: 1524.

    • Search Google Scholar
    • Export Citation
  • 13.

    Smith JH, Christie JD, 1986. The pathobiology of Schistosoma haematobium infection in humans. Hum Pathol 17: 333345.

  • 14.

    Morris W, Knauer CM, 1997. Cardiopulmonary manifestations of schistosomiasis. Semin Respir Infect 12: 159170.

  • 15.

    Villar F, Goria O, Hervé S, Lestrat J, Perrot S, Scotté M, 2000. Shunt porto-cave intra-hépatique. Revue de la littérature, à propos d'un cas. Gastroenterol Clin Biol 24: 582584.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization, 1987. Atlas of the Global Distribution of Schistosomiasis. 16-Togo-Benin. Available at: http://www.who.int/schistosomiasis/epidemiology/en/togo_benin.pdf. Accessed August 30, 2015.

    • Search Google Scholar
    • Export Citation
  • 17.

    McMahon JE, 1969. Schistosoma bovis eggs in human faeces. Trans R Soc Trop Med Hyg 63: 545.

  • 18.

    Chunge R, Katsivo M, Kok P, Wamwea M, Kinoti S, 1986. Schistosoma bovis in human stools in Kenya. Trans R Soc Trop Med Hyg 80: 849.

  • 19.

    Mouchet F, Develoux M, Magasa MB, 1988. Schistosoma bovis in human stools in Republic of Niger. Trans R Soc Trop Med Hyg 82: 257.

  • 20.

    Muller RL, Taylor MG, 1972. The specific differentiation of schistosome eggs by the Ziehl-Neelsen technique. Trans R Soc Trop Med Hyg 66: 1819.

    • Search Google Scholar
    • Export Citation
  • 21.

    Thomas CO, Lawrence RA, 1996. Parasites in human tissues. Hum Pathol 27: 214.

  • 22.

    Bourée P, 1979. Schistosoma intercalatum: critères épidémiologiques de différenciation. Med Mal Infect 9: 397406.

  • 23.

    Southgate VR, van Wijk HB, Wright CA, 1976. Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S. intercalatum and their natural hybrid. Z Für Parasitenkd Berl Ger 49: 145159.

    • Search Google Scholar
    • Export Citation
  • 24.

    Ratard RC, Greer GJ, 1991. A new focus of Schistosoma haematobium/S. intercalatum hybrid in Cameroon. Am J Trop Med Hyg 45: 332338.

  • 25.

    Ripert C, 2003. Schistosomiasis due to Schistosoma intercalatum and urbanization in central Africa. Bull Société Pathol Exot 96: 183186.

    • Search Google Scholar
    • Export Citation
  • 26.

    Moné H, Minguez S, Ibikounlé M, Allienne J-F, Massougbodji A, Mouahid G, 2012. Natural Interactions between S. haematobium and S. guineensis in the Republic of Benin. Scientific World Journal 2012: 793420.

    • Search Google Scholar
    • Export Citation
  • 27.

    N'Dong FO, Mbamendame S, Assapi MN, Mbourou JB, Roy E, Kombila M, Diané C, 2005. Pulmonary bilharziosis due to Schistosoma haematobium: pitfalls of species diagnosis. A case report from Libreville, Gabon. Médecine Trop Rev Corps Santé Colon 65: 163166.

    • Search Google Scholar
    • Export Citation
  • 28.

    Mutani A, Christensen NO, Frandsen F, 1985. A study of the biological characteristics of a hybrid line between male Schistosoma haematobium (Dar es Salaam, Tanzania) and female S. intercalatum (Edea, Cameroun). Acta Trop 42: 319331.

    • Search Google Scholar
    • Export Citation
  • 29.

    Webster BL, Southgate VR, 2003. Compatibility of Schistosoma haematobium, S. intercalatum and their hybrids with Bulinus truncatus and B. forskalii. Parasitology 127: 231242.

    • Search Google Scholar
    • Export Citation
  • 30.

    Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, Rollinson D, 2009. Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 5: e1000571.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Early Detection of Schistosoma Egg–Induced Pulmonary Granulomas in a Returning Traveler

View More View Less
  • Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Institut de Biologie en Santé, Angers, France; Groupe d'Etude des Interactions Hôte-Pathogène, L'UNAM Université, Université d'Angers, Angers, France; Laboratoire d'Anatomo-Cytopathologie, Centre de Pathologie de l'Ouest, Angers, France; Maison Médicale des Spécialistes, Village Santé Angers Loire, Trélazé, France

We report the case of a French traveler who developed acute pulmonary schistosomiasis 2 months after visiting Benin. He presented with a 1-month history of fever, cough, and thoracic pain. Initial investigations revealed hypereosinophilia and multiple nodular lesions on chest computed tomography scan. Lung biopsies were performed 2 months later because of migrating chest infiltrates and increasing eosinophilia. Histological examination showed schistosomal egg–induced pulmonary granulomas with ova exhibiting a prominent terminal spine, resembling Schistosoma haematobium. However, egg shells were Ziehl–Neelsen positive, raising the possibility of a Schistosoma intercalatum or a Schistosoma guineensis infection. Moreover, involvement of highly infectious hybrid species cannot be excluded considering the atypical early pulmonary oviposition. This case is remarkable because of the rarity of pulmonary schistosomiasis, its peculiar clinical presentation and difficulties in making species identification. It also emphasizes the need to consider schistosomiasis diagnosis in all potentially exposed travelers with compatible symptoms.

Introduction

Schistosomiasis is one of the most common neglected tropical diseases. In 2013, an estimated 261 million people were infected worldwide.1 In endemic areas, the chronic phase of the disease causes significant morbi-mortality among local populations, while the acute phase is responsible for a non-negligible morbidity in travelers. According to the GeoSentinel Surveillance Network, 410 schistosomiasis cases were diagnosed among ill travelers between 1997 and 2008, mostly acquired in Africa.2 We present a rare case of pulmonary schistosomiasis in a traveler to Benin, who was diagnosed 4 months after suspected contamination.

Case Presentation

In April 2013, a 21-year-old French man presented to a private clinic for a 1-month chief complaint of cough and thoracic pain. He returned from a 3-week trip to Republic of Benin (February 2013) where he bathed several times into rivers nearby Natitingou and Djougou (Atakora and Donga departments, respectively). Six weeks after returning home, he reported a febrile episode with pulmonary symptoms including dry cough, chest pain, and a brief pruritic rash (< 24 hours).

The blood tests showed hypereosinophilia (1.3 G/L) and elevated C-reactive protein (55 mg/L). Chest radiography was unremarkable. Amoxicillin was empirically given, as well as a short course of corticosteroids, to treat a hypothetical community-acquired pneumonia. Thoracic computed tomography (CT) revealed multiple bilateral lung nodules with irregular shapes, without ground-glass halos, reticular opacities, or mediastinal lymphadenopathies (Figure 1).

Figure 1.
Figure 1.

Computed tomography scan of the chest (axial plane) showing a well-defined lung nodule in the right lung.

Citation: The American Society of Tropical Medicine and Hygiene 94, 3; 10.4269/ajtmh.15-0765

Considering both pulmonary abnormalities and increasing eosinophil count (1.8 G/L), a transbronchial biopsy was performed. Unfortunately, it led to nonrelevant results (nonspecific edematous and congestive changes without any malignant sign). Another chest CT scan was performed on May 2013 and showed a distinctly different distribution of pulmonary nodules. Suspecting an infectious/inflammatory etiology, a lung biopsy was carried out (June 2013). Histological examination revealed several epithelioid granulomas around Schistosoma eggs, associated with eosinophilic infiltrates (Figure 2A). Some eggs exhibited a prominent terminal spine, resembling Schistosoma haematobium (Figure 2B). Neither schistosomula nor adult worms were detected. No vascularitis or malignant criteria were noticed. Meanwhile, a modified Ziehl–Neelsen stain performed on tissue sections resulted positive (Figure 2C), raising the possibility of a Schistosoma intercalatum, Schistosoma guineensis, or hybrid species involvement.

Figure 2.
Figure 2.

Histological examination of a biopsy specimen from a lung lesion. (A) Schistosoma egg surrounded by granulomatous inflammation and eosinophilic reaction (hematoxylin and eosin stain, magnification ×100); (B) Schistosoma egg exhibiting a prominent terminal spine (hematoxylin and eosin stain, magnification ×400); (C) strongly positive acid-fast egg's shell (modified Ziehl–Neelsen stain, magnification ×400).

Citation: The American Society of Tropical Medicine and Hygiene 94, 3; 10.4269/ajtmh.15-0765

In July 2013, the patient was referred to hospital for complementary investigations. Schistosomiasis serology was positive using commercial indirect hemagglutination assay [IHA] (titer of 1:160, threshold = 1:160) (Fumouze Diagnostics, Levallois-Perret, France) and enzyme-linked immunosorbent assay [ELISA] (optical density = 1.65, threshold = 0.37) (Bordier Affinity Products, Crissier, Switzerland). Microscopic examination of stool and urine samples that were collected once following specialized consultation resulted negative for ova and parasites. Eosinophilia decreased gradually on complete blood count. The patient received praziquantel 40 mg/kg once daily.

After 3 months, no more symptoms were reported, physical examination was unremarkable, and lung opacities on chest CT scan disappeared. Eosinophil count was within normal limits (0.5 G/L) and serological markers (IHA and ELISA) remained stable.

Discussion

Acute schistosomiasis is a clinical picture occasionally observed during the early course of infection with Schistosoma sp.3 It may occur a few weeks after cutaneous penetration of cercariae and is characterized by nonspecific symptoms including fever, cough, headache, and urticaria, commonly associated with eosinophilia. Oviposition, which characterizes the chronic phase of the disease, classically occurs weeks later. The symptomatic acute phase, mostly limited to nonimmune subjects, may include pulmonary manifestations mimicking other helminthic diseases (e.g., Loeffler syndrome).47 Pavlin and others8 identified, over a retrospective chart review, 89 cases of acute pulmonary schistosomiasis (APS) in travelers. Patients reported dry cough with dyspnea, wheeze, or chest pain, occurring within 2–8 weeks after exposure and healing within a few weeks/months. Chest X-rays and CT -scan usually showed bilateral nodules with ground-glass halos, more or less diffuse and transient. Pulmonary involvement is more common with Schistosoma mansoni than S. haematobium infection, but it remains a major sign of S. haematobium infection, even more frequent than fever.8

Schistosome eggs are exceptionally found in the lungs during APS. Indeed, ectopic oviposition, corresponding to eggs trapped in tissues outside the perivesicular or mesenteric plexuses (i.e., excluding the urinary tract, liver, and intestine), is mainly reported after a postmortem examination, especially with S. mansoni. Interestingly, Gonçalves and others showed that among 313 autopsy-proven S. mansoni infections, the lungs were the most common ectopic site (29.7%), but almost all organs can be affected.9 A case of pulmonary mansonic schistosomiasis diagnosed in a migrant who underwent a lung biopsy because of multiple nodules in both lungs was recently published.10 However, schistosome eggs were also found in liver and stool samples together with periportal fibrosis, defining the chronic stage of schistosomiasis. By contrast, Baharoon and others reported a case of APS confirmed by a biopsy in a traveler showing similar imaging features, only 10 weeks after exposure: laboratory tests revealed hypereosinophilia and a positive schistosomiasis serology, while a Schistosoma ovum was detected in tissue sections.11 Similarly, in our case, the initial picture (symptoms, eosinophilia, and CT scan features) was consistent with APS. Moreover, anatomopathological study of persistent lung lesions, approximately 4 months after bathing, showed unexpected egg-induced granulomas.

Early pulmonary oviposition raises some questions. It could attest to a fast and massive egg laying into perivesical or mesenteric plexuses, with egg's migration from portal and caval veins to the lungs. Nonetheless, urine and stool analysis were both negative for ova and parasites, and no rectal biopsy was performed in the absence of urinary or digestive functional signs. Portal hypertension with intrahepatic portacaval shunts, allowing the embolization of ova from the portal system to the pulmonary arterial tree is a well-known mechanism.12 However, this theory should be discarded in our case because: 1) the patient did not suffer from any portal hypertension symptoms; 2) histopathology does not evoke S. mansoni (lateral-spined eggs), and unlike this species, other schistosomes (e.g., S. haematobium, S. intercalatum, or S. guineensis) are exceptionally involved in periportal or “Symmer's pipestem” fibrosis13,14; 3) hepatic fibrosis and portal venous system destruction generally settle down gradually, it is thus highly improbable that our patient would have developed a portosystemic shunt within 4 months; 4) congenital hepatic portal venous fistula or spontaneous aneurysmal portal-hepatic venous shunts do exist, but it remains extremely rare.15 Erratic adult worm migration into pulmonary circulation with straight egg laying could also be a valid possibility, but no adults were found in lungs.

Species-level identification was difficult. Morphological analysis on hematoxylin-eosin stain (terminally spined egg group) associated with epidemiological data suggested a S. haematobium. Indeed, this species is largely distributed through the country in many areas, with some of them located nearby our patient's bathing places.16 However, a real-time PCR targeting a S. haematobium-specific sequence resulted negative on biopsy containing schistosome eggs. A Schistosoma bovis infection could also be discussed. This terminally spined egg species is mainly responsible for cattle infections but can occasionally be found in humans.1719 Ziehl–Neelsen stain questions this possibility. Actually, positive acid-fast shell of terminally spined eggs theoretically rules out S. haematobium or S. bovis,20,21 whose differential diagnosis includes S. intercalatum and S. guineensis, two very close species. Their eggs' morphometry is characterized by a lozengic shape (instead of a round shape), a higher length (up to 250 μm), and a long slightly curved terminal spine.22 Transmission of these two anthropophilic species occurs almost exclusively in restricted areas of central Africa.2326 Sporadic cases among travelers have also been reported across west Africa (Burkina Faso, Tchad, Mali, and Nigeria), but no transmission focus was precisely identified. To our knowledge, S. intercalatum has never been reported in Benin, whereas S. guineensis was mentioned in only one publication.26 A similar case—of uncertain diagnosis—was described in Gabon in 2005 by N'Dong and others, but the authors concluded to a S. haematobium lung disease considering epidemiological, pathophysiological, and morphological criteria, in the absence of molecular study and despite the positive Ziehl–Neelsen stain.27 Ultimately, the possibility of a hybrid species involvement such as S. haematobium/S. bovis, S. haematobium/S. guineensis, or S. haematobium/S. intercalatum cannot be ruled out. In fact, some hybrids have shown, during experimental designs, greater cercarial productivity from intermediate hosts, as well as higher infectivity and longevity, compatible with rapid and atypical lung damages.28,29 In Cameroon, a S. haematobium/S. intercalatum hybrid was detected in human stool and urine specimens.23,24 More recently, Huyse and others have demonstrated by egg genotyping (collected from human stool and urine samples) that hybridization between schistosomes species is not a rare phenomenon.30 Furthermore, interestingly, the molecular evidence of hybridization between S. haematobium and S. guineensis was described for the first time in Benin in 2012.26

In conclusion, this case is remarkable for the rarity of pulmonary schistosomiasis, its peculiar clinical presentation, and the difficulty to identify the species. Because the exact genetic nature of the eggs was not determined, we cannot exclude the possibility of an infection with S. intercalatum (never reported in Benin) or with a hybrid species such as S. haematobium/S. guineensis (occasionally described in Benin), the atypical evolution preferentially supporting the latter. In both cases, it would be—to our knowledge—the first description of pulmonary schistosomiasis involving these aforementioned species. Such report also emphasizes the need for clinicians working in non-endemic areas to consider schistosomiasis diagnosis in all potentially exposed travelers presenting with compatible symptoms.

ACKNOWLEDGMENTS

We thank Jean-Louis Koeck and Philippe Leroy, Hôpital d'Instruction des Armées Robert Picqué, Bordeaux, France, for performing PCR assays.

  • 1.

    World Health Organization, 2015. Schistosomiasis. Fact sheet N°115. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/. Accessed October 15, 2015.

    • Search Google Scholar
    • Export Citation
  • 2.

    Nicolls DJ, Weld LH, Schwartz E, Reed C, von Sonnenburg F, Freedman DO, Kozarsky PE, 2008. GeoSentinel Surveillance Network. Characteristics of schistosomiasis in travelers reported to the GeoSentinel Surveillance Network 1997–2008. Am J Trop Med Hyg 79: 729734.

    • Search Google Scholar
    • Export Citation
  • 3.

    Ross AG, Vickers D, Olds GR, Shah SM, McManus DP, 2007. Katayama syndrome. Lancet Infect Dis 7: 218224.

  • 4.

    Schwartz E, Rozenman J, Perelman M, 2000. Pulmonary manifestations of early schistosome infection among nonimmune travelers. Am J Med 109: 718722.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cooke GS, Lalvani A, Gleeson FV, Conlon CP, 1999. Acute pulmonary schistosomiasis in travelers returning from Lake Malawi, sub-Saharan Africa. Clin Infect Dis 29: 836839.

    • Search Google Scholar
    • Export Citation
  • 6.

    Colebunders R, Verstraeten T, Van Gompel A, Van den Ende J, De Roo A, Polderman A, Visser L, 1995. Acute schistosomiasis in travelers returning from Mali. J Travel Med 2: 235238.

    • Search Google Scholar
    • Export Citation
  • 7.

    Jauréguiberry S, Paris L, Caumes E, 2010. Acute schistosomiasis, a diagnostic and therapeutic challenge. Clin Microbiol Infect 16: 225231.

  • 8.

    Pavlin BI, Kozarsky P, Cetron MS, 2012. Acute pulmonary schistosomiasis in travelers: case report and review of the literature. Travel Med Infect Dis 10: 209219.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonçalves EC, Fonseca AP, Pittella JE, 1995. Frequency of schistosomiasis mansoni, of its clinicopathological forms and of the ectopic locations of the parasite in autopsies in Belo Horizonte, Brazil. J Trop Med Hyg 98: 289295.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gobbi F, Martelli G, Attard L, Buonfrate D, Angheben A, Marchese V, Bortesi L, Gobbo M, Vanino E, Viale P, Bisoffi Z, 2015. Schistosoma mansoni eggs in spleen and lungs, mimicking other diseases. PLoS Negl Trop Dis 9: e0003860.

    • Search Google Scholar
    • Export Citation
  • 11.

    Baharoon S, Al-Jahdali H, Bamefleh H, Elkeir A, Yamani N, 2011. Acute pulmonary schistosomiasis. J Glob Infect Dis 3: 293295.

  • 12.

    Kolosionek E, Graham BB, Tuder RM, Butrous G, 2011. Pulmonary vascular disease associated with parasitic infection—the role of schistosomiasis. Clin Microbiol Infect 17: 1524.

    • Search Google Scholar
    • Export Citation
  • 13.

    Smith JH, Christie JD, 1986. The pathobiology of Schistosoma haematobium infection in humans. Hum Pathol 17: 333345.

  • 14.

    Morris W, Knauer CM, 1997. Cardiopulmonary manifestations of schistosomiasis. Semin Respir Infect 12: 159170.

  • 15.

    Villar F, Goria O, Hervé S, Lestrat J, Perrot S, Scotté M, 2000. Shunt porto-cave intra-hépatique. Revue de la littérature, à propos d'un cas. Gastroenterol Clin Biol 24: 582584.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization, 1987. Atlas of the Global Distribution of Schistosomiasis. 16-Togo-Benin. Available at: http://www.who.int/schistosomiasis/epidemiology/en/togo_benin.pdf. Accessed August 30, 2015.

    • Search Google Scholar
    • Export Citation
  • 17.

    McMahon JE, 1969. Schistosoma bovis eggs in human faeces. Trans R Soc Trop Med Hyg 63: 545.

  • 18.

    Chunge R, Katsivo M, Kok P, Wamwea M, Kinoti S, 1986. Schistosoma bovis in human stools in Kenya. Trans R Soc Trop Med Hyg 80: 849.

  • 19.

    Mouchet F, Develoux M, Magasa MB, 1988. Schistosoma bovis in human stools in Republic of Niger. Trans R Soc Trop Med Hyg 82: 257.

  • 20.

    Muller RL, Taylor MG, 1972. The specific differentiation of schistosome eggs by the Ziehl-Neelsen technique. Trans R Soc Trop Med Hyg 66: 1819.

    • Search Google Scholar
    • Export Citation
  • 21.

    Thomas CO, Lawrence RA, 1996. Parasites in human tissues. Hum Pathol 27: 214.

  • 22.

    Bourée P, 1979. Schistosoma intercalatum: critères épidémiologiques de différenciation. Med Mal Infect 9: 397406.

  • 23.

    Southgate VR, van Wijk HB, Wright CA, 1976. Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S. intercalatum and their natural hybrid. Z Für Parasitenkd Berl Ger 49: 145159.

    • Search Google Scholar
    • Export Citation
  • 24.

    Ratard RC, Greer GJ, 1991. A new focus of Schistosoma haematobium/S. intercalatum hybrid in Cameroon. Am J Trop Med Hyg 45: 332338.

  • 25.

    Ripert C, 2003. Schistosomiasis due to Schistosoma intercalatum and urbanization in central Africa. Bull Société Pathol Exot 96: 183186.

    • Search Google Scholar
    • Export Citation
  • 26.

    Moné H, Minguez S, Ibikounlé M, Allienne J-F, Massougbodji A, Mouahid G, 2012. Natural Interactions between S. haematobium and S. guineensis in the Republic of Benin. Scientific World Journal 2012: 793420.

    • Search Google Scholar
    • Export Citation
  • 27.

    N'Dong FO, Mbamendame S, Assapi MN, Mbourou JB, Roy E, Kombila M, Diané C, 2005. Pulmonary bilharziosis due to Schistosoma haematobium: pitfalls of species diagnosis. A case report from Libreville, Gabon. Médecine Trop Rev Corps Santé Colon 65: 163166.

    • Search Google Scholar
    • Export Citation
  • 28.

    Mutani A, Christensen NO, Frandsen F, 1985. A study of the biological characteristics of a hybrid line between male Schistosoma haematobium (Dar es Salaam, Tanzania) and female S. intercalatum (Edea, Cameroun). Acta Trop 42: 319331.

    • Search Google Scholar
    • Export Citation
  • 29.

    Webster BL, Southgate VR, 2003. Compatibility of Schistosoma haematobium, S. intercalatum and their hybrids with Bulinus truncatus and B. forskalii. Parasitology 127: 231242.

    • Search Google Scholar
    • Export Citation
  • 30.

    Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, Rollinson D, 2009. Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 5: e1000571.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Yohann Le Govic, Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Institut de Biologie en Santé, 4 rue Larrey, 49933 Angers Cedex 9, France. E-mail: yohann.legovic@chu-angers.fr† These authors contributed equally to this work.

Conflict of interest: Because this work did not include any primary research, no ethics committee approval was sought.

Authors' addresses: Noémie Coron and Ludovic de Gentile, Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Institut de Biologie en Santé, Angers, France, E-mails: coron.noemie@gmail.com and ludegentile@chu-angers.fr. Yohann Le Govic, Marc Pihet, and Dominique Chabasse, Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Institut de Biologie en Santé, Angers, France, and Groupe d'Etude des Interactions Hôte-Pathogène, L'UNAM Université, Université d'Angers, Angers, France, E-mails: yohann.legovic@chu-angers.fr, mapihet@chu-angers.fr, and dochabasse@chu-angers.fr. Sami Kettani, Laboratoire d'Anatomo-Cytopathologie, Centre de Pathologie de l'Ouest, Angers, France, E-mail: kettani.sami@gmail.com. Sandrine Hemery, Maison Médicale des Spécialistes, Village Santé Angers Loire, Trélazé, France, E-mail: sandrine.beneteau@gmail.com.

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