Hostname: page-component-5d84bcc8dc-pxjkr Total loading time: 0 Render date: 2026-09-16T08:18:59.923Z Has data issue: false hasContentIssue false
  • English
  • Français

Paragonimus and paragonimiasis in West and Central Africa: unresolved questions

Published online by Cambridge University Press:  13 September 2018

Neil Cumberlidge ,
David Rollinson ,
Jozef Vercruysse ,
Louis-Albert Tchuem Tchuenté Open the ORCID record for Louis-Albert Tchuem Tchuenté [Opens in a new window] ,
Bonnie Webster Open the ORCID record for Bonnie Webster [Opens in a new window]  and
Paul F. Clark Open the ORCID record for Paul F. Clark [Opens in a new window]
Neil Cumberlidge
Affiliation:
Department of Biology, Northern Michigan University, 1401 Presque Isle Avenue, Marquette, Michigan 49855, USA
David Rollinson
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
Jozef Vercruysse
Affiliation:
Faculty of Veterinary Medicine, Department of Virology, Parasitology, Immunology, Salisburylaan 133, B-9820 Merelbeke, Belgium
Louis-Albert Tchuem Tchuenté
Affiliation:
Centre for Schistosomiasis and Parasitology, University of Yaoundé I, Yaoundé,Cameroon
Bonnie Webster
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
Paul F. Clark*
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
Author for correspondence: Paul F. Clark, E-mail: p.clark@nhm.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Paragonimiasis, human lung fluke disease, is a foodborne anthropozoonosis caused by the trematodes assigned to Paragonimus and is regarded by the World Health Organization as a Neglected Tropical Disease (NTD). The life cycle of this medically important parasite centres on a complex freshwater biological community that includes two intermediate hosts: a mollusc and a decapod, usually a brachyuran. Although there is a perception that the biology, symptoms, diagnosis and treatment of Paragonimus is well understood, in reality, this is not the case, especially in Africa. Much remains unknown concerning the life-cycle of the parasite, its transmission, the current epidemiology of the disease, diagnosis and the effectiveness of treatment. Furthermore, cases of paragonimiasis may be misdiagnosed as resistant tuberculosis (TB) because of the similar pulmonary symptoms and no remission after anti TB therapy. The endemic foci of human paragonimiasis in Africa have been reported mainly in the forest zones of Upper Guinea (Liberia, Guinea and Ivory Coast) and Lower Guinea (Nigeria, Cameroon, Equatorial Guinea and Gabon). Despite the perceived medical importance of paragonimiasis, relatively little attention has been paid to this NTD since its discovery in Africa in the 1960s. This review focuses on the current understanding of the life cycle and transmission of Paragonimus in Africa, discusses its diagnosis and public health importance and highlights many outstanding gaps in the knowledge that still exist for this NTD.

Keywords

Host snailshuman lung fluke diseaselife cycleNeglected Tropical DiseaseparagonimiasisPotamonautinae crab hostsresistant tuberculosisWest and Central Africa

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Aka, K, Tchamra, M, Fadiga, D and Yapi, A (1995) Paragonimose pulmonaire: une cause d'hémoptysie. Afrique Biomédicale 1, 29–31.Google Scholar
Aka, NA, Adoubryn, K, Rondelaud, D and Dreyfuss, G (2008 a) Human paragonimiasis in Africa. Annals of African Medicine 7, 153–162.Google Scholar
Aka, NA, Assoumou, A, Adoubryn, KD, Djino, S, Domoua, K, Ouhon, J, Kouassi, EB, Rondelaud, D and Dreyfuss, G (2008 b) Persistance d'un foyer de paragonimose dans le département de Lakota, Côte d'Ivoire (Afrique de l'Ouest). Bulletin de la Société de Pathologie Exotique 101, 407–409.Google Scholar
Aka, NA, Assoumou, A, Adoubryn, KD, Djino, S, Domoua, K, Ouhon, J, Kouassi, EB, Rondelaud, D and Dreyfuss, G (2009) Un nouveau foyer de paragonimose humaine découvert en Côte d'Ivoire (Afrique de l'Ouest): le cas de l’ île de Lauzoua. Médecine tropicale 69, 263–266.Google Scholar
Arene, FO, Ibanga, E and Asor, JE (1998) Epidemiology of paragonimiasis in Cross River basin, Nigeria: prevalence and intensity of infection due to Paragonimus uterobilateralis in Yakurr local government area. Public Health 112, 119–122.Google Scholar
Bayssade-Dufour, C, Cabaret, J, Tami, G and Chippaux, JP (1994) Classification problems in Paragonimus spp., Trematoda. Specific identification by multivariate analysis of the eggs. International Congress of Parasitology, Izmir, Turkey. Abstracts 1, 100.Google Scholar
Bayssade-Dufour, C, Chermette, R, Šundić, D and Radujković, BM (2014) Paragonimus gondwanensis n. sp. (Digenea, Paragonimidae), parasite of mammals (humans and carnivores) in Cameroon. Ecologica Montenegrina 1, 256–267.Google Scholar
Bayssade-Dufour, C, Chermette, R, Šundić, D and Radujković, BM (2015) Paragonimus kerberti n.sp. (Digenea, Paragonimidae), parasite of carnivores in Cameroon. Ecologica Montenegrina 2, 271–277.Google Scholar
Blair, D, Agatsuma, T and Wang, W (2008) Paragonimiasis. In Murrell, KD and Fried, B (eds), Food-Borne Parasitic Zoonoses, Vol. 11. Fish and Plant-Borne Parasites. New York: Springer, pp. 117‒150.Google Scholar
Boguikouma, JB, Moussavou-Kombila, JB, Ondo-Ndong, F, M'Vou-Yaloula, R, Mabicka, B and Kombila, MJ (1997) Un cas gabonais de paragonimose pulmonaire. Médecine d'Afrique Noire 44, 1–2.Google Scholar
Brenes, R, Hangen, G and Duarte, G (1984) Revision de Paragonimus y paragonimiasis en Centroamerica y Panama. Revista Médica del Hospital Nacional de Niños, Costa Rica 19, 87–106.Google Scholar
Cabaret, J, Bayssade-Dufour, C, Tami, G and Albaret, JL (1999) Identification of African Paragonimidae by multivariate analysis of the eggs. Acta Tropica 72, 79–89.Google Scholar
Calvopiña, M, Romero, D, Casteñeda, B, Hashiguchi, Y and Sugiyama, H (2014) Current status of Paragonimus and paragonimiasis in Ecuador. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 109, 849–855.Google Scholar
Connolly, LE, Edelstein, PH and Ramakrishnan, L (2007) Why is long-term therapy required to cure tuberculosis? PLoS Medicine 4, e120.Google Scholar
Coulibaly, N, Cornet, L, Doucet, J and Loubiere, R (1975) Paragonimose pulmonaire associée à une bilharziose en Côte d'Ivoire. La Nouvelle presse médicale 4, 886.Google Scholar
Cumberlidge, N (1999) The Freshwater Crabs of West Africa, Family Potamonautidae. Paris: Faune et Flore Tropicales, IRD, vol. 35, 382 pp.Google Scholar
Daniels, SR and Bayliss, J (2012) Neglected refugia of biodiversity: mountainous regions in Mozambique and Malawi yield two novel freshwater crab species (Potamonautidae: Potamonautes). Zoological Journal of the Linnean Society 164, 498–509.Google Scholar
Despommier, DD, Gwadz, RW, Hotez, PJ and Knirsch, CA (2000) Parasitic Diseases, 4th Edn. New York: Apple Tree Productions, pp. xii, 345, ill.Google Scholar
Foster, J and Harper, D (2007) Status and ecosystem interactions of the invasive Louisianan red swamp crayfish Procambarus clarkii in East Africa. In Gherardi, F (ed.), Biological Invaders in Inland Waters: Profiles, Distribution, and Threats. Dordrecht: Springer, pp. 91–101.Google Scholar
Friant, S, Brown, K, Saari, MT, Segel, NH, Slezak, J and Goldberg, TL (2015) Lung fluke (Paragonimus africanus) infects Nigerian red-capped mangabeys and causes respiratory disease. International Journal for Parasitology: Parasites and Wildlife 4, 329–332.Google Scholar
Fürst, T, Duthaler, U, Sripa, B, Utzinger, J and Keiser, J (2012) Trematode infections liver and lung flukes. Infectious Disease Clinics of North America 26, 399–419.Google Scholar
Guillermai, DH (1981) Paragonimose en Afrique. A propos d'un cas Gabonais de paragonimose chez un enfant. Thèse de médecine faculté de médecine: Université de Clermont I.Google Scholar
Ibanga, ES and Eyo, VM (2001) Pulmonary paragonimiasis in Oban community in Akamkpa Local Government Area, Cross River State, Nigeria: prevalence and intensity of infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 159–160.Google Scholar
Keiser, J and Utzinger, J (2005) Emerging foodborne trematodiasis. Emerging Infectious Diseases 11, 1507–1514.Google Scholar
Keiser, J and Utzinger, J (2009) Food-Borne Trematodiases. Clinical Microbiology Reviews 22, 466–483.Google Scholar
Keiser, J, Engels, D, Büscher, G and Utzinger, J (2005) Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opinion on Investigational Drugs 14, 1513–1526.Google Scholar
Kum, PN and Nchinda, TC (1982) Pulmonary paragonimiasis in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 768–772.Google Scholar
Lane, MA, Barsanti, MC, Santos, CA, Yeun, M, Lubner, SJ and Weil, GJ (2009) Human paragonimiasis in North America following ingestion of raw crayfish. Clinical Infectious Diseases 49, e55–e61, https://doi.org/10.1086/605534Google Scholar
Luo, J, Wang, M-Y, Liu, D, Zhu, H, Yang, S, Liang, B-M and Liang, Z-A (2016) Pulmonary paragonimiasis mimicking Tuberculous pleuritis. Medicine 95, e3436.Google Scholar
Malek, EA, Brenes, R and Rojas, G (1975) Aroapyrgus costaricensis, hydrobiid snail host of paragonimiasis in Costa Rica. Journal Parasitology 61, 355–359.Google Scholar
Marty, AM and Neafie, RC (2000) Paragonimiasis. In Myers, WM, Neafie, RC, Marty, AM and Wear, DJ (eds), Pathology of Infectious Diseases, Vol. I. Helminthiases. Washington DC: Armed Forces Institute of Pathology, pp. 49‒67.Google Scholar
Mills, CD, Clark, PF and Morritt, D (2016) Flexible prey handling, preference and a novel capture technique in invasive, sub-adult Chinese mitten crabs. Hydrobiologia 773, 135–147.Google Scholar
Monson, MH, Koenig, JW and Sachs, A (1983) Successful treatment with praziquantel of six patients infected with the African lung fluke, Paragonimus uterobilateralis. The American Journal of Tropical Medicine and Hygiene 32, 371–375.Google Scholar
Morter, R, Adetifa, I, Antonio, M, Touray, F, De Jong, BC, Gower, CM and Gehre, F (2018) Examining human paragonimiasis as a differential diagnosis to tuberculosis in the Gambia. BMC Research Notes 11, 31.Google Scholar
Moyou-Somo, R and Guemgne-Simo, G (1995) Paragonimiasis in southwest Cameroon: isolation of microcercous cercariae from land snails caught in a Paragonimus africanus endemic zone. Wilderness and Environmental Medicine 6, 44–47.Google Scholar
Moyou-Somo, R, Enyong, PA, Kouamouo, J, Dinga, JS, Couprie, B and Ripert, C (1983) Etude de la paragonimose dans cinq départements de la Mémé (Sudouest du Cameroun). Résultats du traitement par le praziquantel. Scientific and Technical Review 6, 125–129.Google Scholar
Moyou-Somo, R, Enyong, PA and Kouamouo, J (1984) Isolation of Paragonimus africanus cercariae from a wild caught mollusc Potadoma freethi. XI Intentional Congress of Tropical Medicine and Malaria, Canada: Calgary, pp. 208.Google Scholar
Moyou-Somo, R, Kefie-Arreym, C, Dreyfuss, G and Dumas, M (2003) An epidemiological study of pleuropulmonary paragonimiasis among pupils in the peri-urban zone of Kumba town, Meme Division, Cameroon. BMC Public Health 3, 40.Google Scholar
Nkouawa, A, Okamoto, M, Mabou, AK, Eding, E, Yamasaki, H, Sako, Y, Nakao, M, Nakaya, K, Blair, D, Agatsuma, T, Enyong, P, Shibahara, T, Moyou-Somo, R and Ito, A (2009) Paragonimiasis in Cameroon: molecular identification, serodiagnosis and clinical manifestations. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 255–261.Google Scholar
Noble, ER, Noble, GA, Schad, GA and MacInnes, AJ (1989) Parasitology The Biology of Animal Parasites, 6th Edn. Philadelphia: Lea & Febiger, pp. 574.Google Scholar
Noeske, J, Nana Yakam, A and Abena Foe, JL (2016) Epidemiology of tuberculosis in Cameroon as mirrored in notification data, 2006‒2014. International Journal of Tuberculosis and Lung Disease 20, 1489–1494.Google Scholar
Nozais, JP, Doucet, J, Dunan, J and Assale N'dri, G (1980) Les paragonimoses en Afrique Noire. Apropos d'un foyer recent de Cote-d'Ivoire. Bulletin de la Société de pathologie exotique 73, 155–163.Google Scholar
Nwokolo, C (1974) Endemic paragonimiasis in Africa. Bulletin of the World Health Organization 50, 569‒571.Google Scholar
Ollivier, G, Boussinesq, M, Albare, JJ, Cumberlidge, N, Farhati, K, Chippaux, JP and Bayssade-Dufour, C (1995) Etude epidemlologique sur Paragonimus sp. dans le Sud-Cameroun. Bulletin de la Société de pathologie exotique 88, 164–169.Google Scholar
Ripert, C, Carrie, J, Ambroise-Thomas, P, Baecher, R, Kum, NP and Same-Ekobo, A (1981) Étude épidémiologique et clinique de la paragonimose au Cameroun. Résultats du traitement par le niclofolan. Bulletin de la Société de pathologie exotique 74, 319–331.Google Scholar
Sachs, R and Cumberlidge, N (1989) Isolation of microcercous cercariae from land snails caught in an endemic focus of P. uterobilateralis in Liberia, West Africa. Tropical Medicine and Parasitology 40, 69–72.Google Scholar
Sachs, R and Cumberlidge, N (1990 a) The dog as natural reservoir host for Paragonimus uterobilateralis in Liberia, West Africa. Annals of Tropical Medicine and Parasitology 84, 101–102.Google Scholar
Sachs, R and Cumberlidge, N (1990 b) Distribution of metacercariae in freshwater crabs in relation to Paragonimus infection of children in Liberia. Annals of Tropical Medicine and Parasitology 84, 277–280.Google Scholar
Sachs, R and Cumberlidge, N (1990 c) The dwarf river crab Liberonautes latidactylus nanoides Cumberlidge & Sachs 1989 – a new second intermediate host of Paragonimus uterobilateralis in Liberia. Tropical Medicine and Parasitology 41, 435–436.Google Scholar
Sachs, R and Cumberlidge, N (1991 a) Notes on the ecology of Homorus striatella (Rang, 1831), snail host of microcercous cercariae in Liberia, West Africa. Zeitschrift für Angewandte Zoologie 78, 45–53.Google Scholar
Sachs, R and Cumberlidge, N (1991 b) Metacercarial load of fresh-water crabs Liberonautes latidactylus in an endemic paragonimiasis focus in Liberia, West Africa. Zeitschrift für Angewandte Zoologie 78, 161–165.Google Scholar
Sachs, R and Voelker, J (1977) Affen als naturliche und experimentelle Endwirte afrikanischer Lungenegel (Paragonimus africanus, P. uterobilateralis). Tropical Medicine and Parasitology 28, 137–144.Google Scholar
Sachs, R and Voelker, J (1982) Human paragonimiasis caused by Paragonimus uterobilateralis in Liberia and Guinea. Tropical Medicine and Parasitology 30, 15–16.Google Scholar
Sachs, R, Kern, P and Voelker, J (1983) Paragonimus uterobilateralis as the cause of 3 cases of human paragonimiasis in Gabon. Tropical Medicine and Parasitology 34, 105–108.Google Scholar
Sachs, R, Albiez, EJ and Voelker, J (1986) Prevalence of Paragonimus uterobilateralis infection in children in a Liberian village. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 80–81.Google Scholar
Sanford, C, Jong, E and Pottinger, P (2016) The Travel and Tropical Medicine Manual, 5th Edn. New York: Elsevier, pp. 664.Google Scholar
Simarro, PP, Alamo, A, Sima, FO, Roche, J, Mir, M and Ndong, P (1991) Endemic human paragonimiasis in Equatorial Guinea. Detection of the existence of endemic human paragonimiasis in Equatorial Guinea as a result of an integrated sanitary programme. Tropical and Geographical Medicine 43, 326–328.Google Scholar
Traoré, SG, Koussemon, M, Odermatt, P, Aka, ND, Adoubryn, KD, Assoumou, A, Dreyfuss, G and Bonfoh, B (2001) Risque de contraction de trématodoses alimentaires avec la consommation des crustacés vendus sur les marchés d'Abidjan. Revue Africaine de Santé et de Productions Animales 120, 514–520.Google Scholar
Traoré, SG, Odermatt, P, Bonfoh, B, Utzinger, J, Aka, ND, Adoubryn, KD, Assoumou, A, Dreyfuss, G and Koussémon, M (2011) No Paragonimus in high-risk groups in Côte d'Ivoire, but considerable prevalence of helminths and intestinal protozoon infections. Parasites and Vectors 4, 96.Google Scholar
Udonsi, JK (1987) Endemic Paragonimus infection in the Upper Igwun Basin, Nigeria: a preliminary report on a renewed outbreak. Annals of Tropical Medicine and Parasitology 81, 57–62.Google Scholar
Voelker, J (1973) Morphologisch-taxionomische Untersuchungen uber Paragonimus uterobilateralis (Trematoda, Troglotrematidae) sowie Beobachtungcn uber den Lebenscylcus und die Verbreitung des Parasiten in Liberia. Zeitschrift für Tropenmedizin und Parasitologie 24, 4–20.Google Scholar
Voelker, J and Sachs, R (1974) Obeservations on the life cycle of Paragonimus uterobilateralis: the African Civet (Viverra civetta) as natural reservoir in Nigeria. Proc. 3rd International Congress of Parasitology, München 1, 529–530.Google Scholar
Voelker, J and Sachs, R (1977) On the distribution of the lung flukes, Paragonimus africanus and P. uterobilateralis, in the South West Province of Cameroon and in Eastern Nigeria as determined by examination of the intermediate crab hosts for infection with metacercariae. Zeitschrift für Tropenmedizin und Parasitologie 28, 120–133.Google Scholar
Voelker, J and Sachs, R (1985) Morphology of the lung fluke Paragonimus uterobilateralis occurring in Gabon, West Africa. Tropical Medicine and Parasitology 36, 210–212.Google Scholar
Voelker, J and Vogel, H (1965) Zwei neue Paragonimus-Arten aus West-Africa: Paragonimus africanus und Paragonimus uterobilateralis (Troglotrematidae, Trematoda). Zeitschrift für Tropenmedizin und Parasitologie 16, 125–147.Google Scholar
Voelker, J, Sachs, R, Volkmer, KJ and Braband, H (1975) Zur Epidemiologie der Paragonimiaais bei Mensch und Tier in Nigeria, Westafrika. Veterinär-medizinische Nachrichten 1/2, 158–172.Google Scholar
Vogel, H and Crewe, W (1965) Beobachtungen über die Lungenegel-Infektion in Kamerun (Westafrika). Zeitschrift für Tropenmedizin und Parasitologie 16, 109–125.Google Scholar
Volkmer, KJ and Braband, H (1975) Das Röntgenbild der afrikanischen Paragonimiasis. Röfo 122, 265–267.Google Scholar
Waikagul, J, Yaemput, S and Visiassuk, K (1986) The route of migration of Paragonimus siamensis Miyazaki & Wykoff, 1965 in the white rat. SE Asian Journal of Tropical Medicine and Public Health 17, 587–590.Google Scholar
WHO (1995) Control of foodborne trematode infections. Report of a WHO study group. World Health Organ. Technical Report Series 849, 1–157.Google Scholar
WHO (2010) Working to Overcome the Global Impact of Neglected Tropical Diseases: First WHO Report on Neglected Tropical Diseases. Geneva: World Health Organization, pp. ix+172.Google Scholar
Yeo, DCJ, Ng, PKL, Cumberlidge, N, Magalhaes, C, Daniels, SR and Campos, M (2008) A global assessment of freshwater crab diversity (Crustacea: Decapoda: Brachyura). In Balian, EV, Lévequè, C, Segers, H and Martens, M (eds), Freshwater Animal Diversity Assessment. Hydrobiologia 595, 275‒286.Google Scholar