561

Ann. Soc. belge Méd. trop. 1975, 55, 1, 59-64

THE PARASITIC IN MAN (*) by

A. FAIN

Summary - This paper is a review of human pentastomosis. So far five species belonging to three genera of Pentastomida have been found with centainty in man. The author discusses the pathogenic role of these species and the diagnosis of the nymphal pentastomosis in man.

KEYWORDS: Pentastomosis, human; Cancer; Review.

Introduction

The Pentastomida constitute a highly aberrant group of parasites. Ali the known species are parasitic in both adult and immature stages. Most of them are heteroxenous and have a complicated lite-cycle involving two successive hosts. In the most evolved genera, su ch as and , the definitive host is a carnivorous , either a large or a carnivore, and the intermediate host a mammal. In the more primitive genus Raillietiella, the adults live mainly in the lung of or lizards. The life cycle is not known with certainty but it seems that Raillietiella boulengeri a common lung parasite of African snakes utilizes sm ail lizards as intermediate hosts (Fain, 1961 addendum, and 1964). Recently Self (1969) has fed eggs of Raillietiella gehyrae to several species of /izards and recovered migrating primary larvae from the tissues. Some pentastomids are able to perform their entire development in the same host. So far a direct development has been observed for Sambonia lohrmanni Noc and Giglioli, a species /iving in the respiratory tract of the Komodo varanus (see Fain and Mortelmans, 1960) and for Reighardia sternae (Diesing, 1864), living in the lungs of Laridae (Haffner and Rack, 1965). In the pulmonary tissues of the varanus we found ail the intermediate forms between the embryo and the adults, including five successive larval stages. It is possible that some species of Raillietiella living in the lungs of lizards are also able to complete their life-cycle in these hosts.

(.) Paper presented at the Third International Congress of Parasitology, Munich 25-31 Aug ust 1974.

59 Lavoipierre, M.M. and Lavoipierre Michèle (1966) have reported the genus has not been observed v presence of larval pentastomids in the haemocoel of cockroaches in Africa by several authors as hun Singapore. They surmized that these are the intermediate by nymphs of Armillifer (see Fai hosts for a species of Raillietiella that infects the common house-gecko Recently Prathop et al. (196! in this area. Unfortunately they did not observe the preinfective larval stages aborigines by a species which th in the haemocoel of the cockroaches which could have proved that these this species belongs to the gent were true intermediate hosts and not sim ply «hôtes d'attente >, or paratenic hosts in which the larva had reencysted. Another point that 4. The genus Armillifer is re these authors have not investigated is the possible presence of preinfective which are able to produce nymp larval stages in the lung of the gecko. The discovery of such larvae would prove that the entire life cycle courd take place in the tissues of the gecko. a) The most corn mon specie Man is rarely infected by adult pentastomids. Nymphal on known only from Tropical Africa the contrary is not rare in this host. snakes such as the pythons an ln man the results generally from the consumption of water develop in various mammals incl or food infected by feces or lung mucus of snakes or carnivores, more A. armillatus has been reported rarely by eating infected snakes. A review of the species infecting man has this parasite was erroneously moniliformis or Armillifer monili been given by Fain in 1960. Since this date a number of new observations have been published and restatement of the question becomes necessary. encysted in a thin transparent, these nymphs may escape from tl ln man the nymphs are gene the thorax. Most of them are ene Pentastomids observed in man embedded in the superficial laye found in the omentum, the meSl Up to now five species of Pentastomida, belonging to three genera, abdominal organs. We found theE have been reported from man. close to the testicle in a native 01 for these nymphs in man are U 1. Leiperia cincinnalis Sambon. This species lives as an adult in the junctiva (De Coster and Rodhair lungs of African crocodiles. The nymphs have been found encysted in the Fain, 1960) and the eylid (Fain, connective tissue enveloping the intestine or in the muscles of various The presence of these nymph fishes. A nymph of this species was found once in the feces of a European tolerated and pathological com women in Lubumbashi, Zaïre (Fain, 1960 and 1961). This patient has however, they had produced imp probably become infected by eating fish harbouring this larva. This case death of the patients. In the fal of parasitism was considered, therefore to be purely accidentaI. nymphs were extremely nume. obstructed the large intestine. 2. The genus Linguatula is cosmopolitan and contains several species similar case in Zaïre in which th which live as adults in the nasal cavities of domestic and wild carnivores. angle of the large intestine and t Parasitism of man by the adults of this genus is very rare and has been site of the nymphal masses. observed only with , a species that lives in , Presently it is not known wh and foxes. Nymphal pentastomosis in man has been reported on several have been ingested by man are occasions and in various parts of the world. The nymphs were recovered reencyst in the peritoneal cavity­ from mesenteric Iymph nodes plus various viscera including the brain, passing of these re/atively large lungs, etc. Nymphs have also been found in the anterior chamber of the be more harmful than that of th_ eye of man at two occasions in North America (Hunter and Higgins, 1960; Rendtorff et al., 1962). In the Middle East nymphs of Linguatula serrata b) Armillifer moniliformis (DiE have been removed from the naso-pharynx of patients suffering of halzoun the lung of Asiatic pythons. Nym or marara syndrome (Schacher et al., 1969). So far the halzoun syndrome reported. Recently Prathap et ~ had been attributed to the presence in the naso-pharynx of flukes (Fasciola nymphs of Armillifer moniliformis hepatica) or leeches. formis) in 45,6 per cent of a serie: The liver and the lungs were the 3. The genus Porocephalus is represented only in Africa and in This species has been found America. Up to now human parasitism by either adults or nymphs of this Kinshasa, Zaïre, but so far nyml

60 chèle (1966) have reported the genus has not been observed with certainty. Ali the caseS reported from haemocoel of cockroaches in Africa by several authors as human porocephalosis were actually produced arthropods are the intermediate by nymphs of Armillifer (see Fain, 1960 and 1961). nfects the common house-gecko Recently Prathop et al. (1969) have reported in Malaysian erve the preinfective larval stages aborigines by a species which they cali Porocephalus moniliformis. Actually _ch could have proved that these this species belongs to the genus Armillifer. d not simply « hôtes d'attente» d reencysted. Another point that 4. The genus Armillifer is represented in man by three species ail of possible presence of preinfective which are able to produce nymphal pentastomosis. e discovery of such larvae would place in the tissues of the gecko. a) The most common species is (Wyman), and is 3.stomids. Nymphal parasitism on known only from Tropical Africa. The adults live in the lungs of the large snakes such as the pythons and vipers of the genus Bitis. The nymphs develop in various mammals including man and nymphal pentastomosis by y from the consumption of water A. armillatus has been reported frequently in man. In the earlier papers s of snakes or carnivores, more this parasite was erroneously reported under the names Porocephalus . of the species infecting man has moniliformis or Armillifer moniliformis. The nymphs are generally found Rte a number of new observations encysted in a thin transparent cystic membrane. In some circumstances the question becomes necessary. these nymphs may escape from their envelope and become free in the host. ln man the nymphs are generally located in the peritoneal cavity or in the thorax. Most of them are encysted beneath the capsule of the liver or -ved in man embedded in the superficial layers of this organ. They are also frequently found in the omentum, the mesenteries, the intestinal walls and in other llida, belonging to three genera, abdominal organs. We found these nymphs once along the spermatic canal close to the testicle in a native of Zaïre (Fain, unpublished). Other locations for these nymphs in man are the brain (Fornara, 1923), the ocular con­ species lives as an adult in the junctiva (De Coster and Rodhain, 1951, Gratama and Van Thiel, 1957 and have been found encysted in the Fain, 1960) and the eylid (Fain, 1960). ne or in the muscles of various The presence of these nymphs in the peritoneal cavity is generally weil j once in the feces of a European tolerated and pathological complications are very rare. In two cases, l60 and 1961). This patient has however, they had produced important lesions which were followed by the 1 harbouring this larva. This case death of the patients. In the fatal case described by Cannon (1942) the :0 be purely accidentaI. nymphs were extremely numerous and they had almost completely obstructed the large intestine. Bouckaert and Fain (1959) observed a itan and contains several species similar case in Zaïre in which the nymphs were located along the hepatic . of domestic and wild carnivores. angle of the large intestine and there was a distinct local peritonitis at the genus is very rare and has been site of the nymphal masses. species that lives in dogs, wolves Presently it is not known whether the nymphs of A. armillatus which an has been reported on several have been ingested by man are able to cross the intestinal wall and to orld. The nymphs were recovered reencyst in the peritoneal cavity. This question is important because the ious viscera incfuding the brain, passing of these relatively large nymphs through the intestinal wall could Id in the anterior chamber of the be more harmful than that of the microscopic embryos (Fain, 1960). merica (Hunter and Higgins, 1960; ast nymphs of Linguatula serrata b) Armillifer moniliformis (Diesing) : This species is very common in nx of patients suffering of halzoun the lung of Asiatic pythons. Nymphal parasitism in man has seldom been 169). So far the halzoun syndrome reported. Recently Prathap et al. (1969) have reported the presence of e naso-pharynx of flukes (Fascio/a nymphs of Armillifer moniliformis (erroneously named Porocephalus monili­ formis) in 45,6 per cent of a series of 30 autopsies on Malaysian aborigines. The liver and the lungs were the organs most frequently infected. resented only in Africa and in This species has been found once in the lung of an African python in IY either adults or nymphs of this Kinshasa, Zaïre, but so far nymphs have not been reported from Africa.

61 c) Armillifer grandis HeU. The adults of this species have frequently Zaïre, have found only three c been observed in the lungs of Bitis nasicornis. Nymphal infestations in man, from a total of 70.000 man have been reported in Zaïre. The nymphs are encysted in the omentum Recently immunological tect and the mesenteries in several natives living in a swampy forest area, ir, of nymphal pentastomosis. Th the Equatorial Province of Zaïre (Fain and Salvo, 1966). In this region diagnosis (Amy, 1973). Bitis nasicornis, the usual host of the adult parasite, is also very frequent. The nymphs of A. grandis are easily distinguished from those of A. armil­ Résumé - Les Pentastomldés parai latus by their smaller size and the greater number of circular cuticular Ce travail est une mise au point de thickenings. espèces. appartenant à trois genres de Recently we found a nymph of this species encysted in the eyelid of l'homme. Le rôle pathogène de ces c nymphale chez l'homme sont passés er a native from Kisangani, Zaïre (Fain, unpublished). Samenvatting - De Pentastomida Dit werk geeft een overzicht inzake Pentastomosis and cancer species. behorend tot drie soorten Pe, auteur bespreekt de pathogenische roi stomosis bij de mens. Galii-Valerio (1921) described a human case of fibrosarcoma of the A. 1 nasal cavities invaded by an adult of Linguatula serrata. Insl Ant Tobie et al. (1957) reported a worm (Linguatula serrata) Rec infestation in a patient with acute leukemia. We have observed a bronchial carcinoma in a Komodo varanus which was infected with Sambonia lohrmanni. This cancer had apparently originated from a villouspapilioma of the bronchial mucosa. Several young Amy. D. (1973) : La Pentastomose à Arr larvae of this pentastomid were found inside the villi. Other larvae or radiologique. Thèse, Faculté de Médl nymphs were embedded in the tracheal mucosa. This host was also Bouckaert. L. and Fain, A. (1959) : Een infected by the adult form of the same pentastomid (Fain and Mortelmans, loop. Ann. Soc. belge Méd. trop.• 39, Cannon. D. A. (1942) : linguatulid infest; 1960). Fain, A. (1960) : La pentastomose chez Although these three observations are not sufficient to prove the 516-532. carcinogenetic action of larval pentastomids, we think that they are Fain, A. (1961) :Les Pentastomidés de f interesting because they draw the attention to the possibility of this action Sei. Zool. 92, 1-115. Fain, A. (1964): Observations sur le in man. The high frequency of the primitive cancer of the liver, in the Acad. Roy. Belg. Bull. Classe de Scie Africans, could be in relation with the great prevalence of the nymphal Fain, A. (1966) : Pentastomida of Snake pentastomosis of the human liver in Central Africa. We think that Mem. Inst. Butantan, Simp. Internac.• Fain. A. (1973): ln Flynn. R. J. : Pan: experimental work should be performed in order to study the carcinogene­ mida, by Fain. Ames Iowa State Univ. tic actions of Armi/lifer armillatus in the liver. It should be necessary to Fain, A. (1974) : Human Infestation by select for that purpose animais that are especialiy susceptible to this kind Parasitology München. 25-31 August of cancer. Fain. A. and Mortelmans, J. (1960) : Obs chez le Varan. Preuve d'un dévelopç Belg. 5e Sér., 46 6.518,531. Fain, A. ~nd Salvo. G. (1966) : Pentast(J Diagnosis of nymphal pentastomosis in man grandis (Hell) en République Démoc 675-682. Faust, E. C., Russel, P. F. and Jung. F Nymphal pentastomosis in man by Armillifer armillatus is generaliy 8th Ed. Philadelphia. Lea and Febigel discovered during surgical intervention or at necropsies. Galli-Valerio. B. (1921) : Parasitologiscl! As long as the nymphs are alive they are not visible by X-rays. After Technik. Centralbl. BakI., 1Abl. 86, 3­ Gratama. S. and Van Thiel. P. H. (1957) : death they may calcify and become visible by X-rays. Their ring or horse­ Geogr. Trop. 9. 374. shoe form (10-14 mm in diameter) and their location in the abdominal Haffner. K. von and Rack, G. (1965) : Ne or thoracic cavity are characteristic. As a matter of fact the calcification dia sternae. Jahrb. Anal. 72, 419-444. Hunter, W. S. and Higgins. R. P. (1960) : of these nymphs is probably not a general phenomenon for in countries sitol. 46, 68. such as Zaïre where nymphal pentastomosis by Armillifer armillatus is very Khalil. G. M. and Schacher. J. F. (1965 common the discovery of calcificed nymphs, during routine X-rays examina­ Marrara syndrome. Amer. J. Trop. Me tions is exceptional. Van Wymeersch and Wanson (1954) working in Kinshasa, Lavoipierre, M. M. J. and Lavoipierre ~ Pentastomid. Nature 210 (5038), 845-8­ 62 of this species have frequently Zaïre, have found only three cases of calcified nymphal pentastomosis in :icornis. Nymphal infestations in man, from a total of 70.000 routine X-rays examinations. phs are encysted in the omentum Recently immunological techniques have been proposed for the detection 'ing in a swampy forest area, ir, of nymphal pentastomosis. They will probably provide a more accurate and Salvo, 1966). In this region diagnosis (Amy, 1973). It parasite, is also very frequent. ,guished from those of A. armi/­Résumé - Les Penta8tomldés parasitaire8 chez l'homme. ter number of circular cuticular Ce travail est une mise au point de nos connaissances sur la pentastomose humaine. Cinq espèces, appartenant à trois genres de Pentastomida ont été rencontrées avec certitude chez l'homme. Le rôle pathogène de ces diverses espèces et le diagnostic de la pentastomose Jecies encysted in the eyelid of nymphale chez l'homme sont passés en revue. Jublished). Samenvatting - De Pentastomida parasitair voor de mens. Dit werk geeft een overzicht inzake de menselijke pentastomosis. Tot heden werden vijf d cancer species, behorend tot drie soorten Pentastomida, met zekerheid bij de mens gevonden. De auteur bespreekt de pathogenische roi van deze soorten en de diagnose van nymfale penta­ stomosis bij de mens. 3.n case of fibrosarcoma of the A. Fain: Department of Medical Zoology, Prince Leopold Institute of Tropical Medicine, Nationalestraat 155, B-2000 !}uatula serrata. Antwerpen, Belgium. gue worm (Unguatula serrata) Received for publication on September 3, 1974. flia. :Jma in a Komodo varanus which REFERENCES i. This cancer had apparently bronchial mucosa. Several young Amy, D. (1973) : La Pentastomose à Armillifer armiflatus. Etude biologique, immunologique et inside the villi. Other larvae or radiologique. Thèse, Faculté de Médecine, Marseille. Bouckaert, L. and Fain, A. (1959) : Een geval van nymphale porocephalose met dodelijk ver­ II mucosa. This host was also loop. Ann. Soc. belge Méd. trop., 39, 793. •ntastomid (Fain and Mortelmans, Cannon, D. A. (1942) : Linguatulid infestation of man. Ann. TrOp. Med. Parasitol. 36, 160-166. Fain, A. (1960) : La pentastomose chez l'homme. Bull. Acad. Roy. Méd. Belg., Série Vie, 257, are not sufficient to prove the 516-532. Fain, A. (1961) :Les Pentastomidés de l'Afrique Centrale. Ann. Mus. Roy. Afr. Centr., Série 8 :>mids, we think that they are Sei. Zool. 92, 1-115. ln to the possibility of this action Fain, A. (1964): Observations sur le cycle évolutif du genre Raiffietiella (Pentastomida). itive cancer of the liver, in the Acad. Roy. Belg. Bull. Classe de Sciences, Série 5 L 9, 1036-1060. ~reat prevalence of the nymphal Fain, A. (1966) : Pentastomida of Snakes - Their Parasitological Role in Man and Animais. Mem. Inst. Butantan, Simp. Internac., 33 1, 167-174. Central Africa. We think that Fain, A. (1973): fn Flynn, R. J.: Parasites of Laboratory Animais: Chap. 16 - Pentasto­ 1 order to study the carcinogene­ mida, by Fain. Ames Iowa State University Press, p. 493-503. liver. It should be necessary to Fain, A. (1974): Human Infestation by Pentastomids. Proc. Third International Congress of •specially susceptible to this kind Parasitology München, 25-31 August, 1974 Vol. 2. Section c 14 (12) : 1028-1029. Fain, A. and Mortelmans, J. (1960) : Observations sur le cycle évolutif de Sambonia fohrmanni chez le Varan. Preuve d'un développement direct chez les Pentastomida. Bull. Acad. Sei. Belg. 5e Sér., 466,518-531. Fain, A. and Salvo, G. (1966) : Pentastomose humaine produite par des Nymphes d'Armiffifer lastomosis in man grandis (Hett) en République Démocratique du Congo. Ann. Soc. belge Méd. trop., 46, 6, 675-682. Faust, E. C., Russel, P. F. and Jung, R. C. (1970): Graig and Faust's Clinical Parasitology, .A.rmillifer armillatus is generally 8th Ed. Philadelphia, Lea and Febiger. Galli-Valerio, B. (1921) : Parasitologische Untersuchungen und Beitrâge zur parasitologische r at necropsies. Technik. Centralbl. Bakt., 1 Abt. 86, 349. { are not visible by X-rays. After Gratama, S. and Van Thiel, P. H. (1957) : Ocular localization of Armiffifer armiffatus. Doc. Med. le by X-rays. Their ring or horse­ Geogr. Trop. 9, 374. their location in the abdominal Haffner, K. von and Rack, G. (1965) : Neues ueber die entwicklung der Pentastomide Reighar­ dia sternae. Jahrb. Anat. 72, 419-444. a matter of fact the calcification Hunter, W. S. and Higgins, R. P. (1960) : An unusual case of human . J. Para­ rai phenomenon for in countries sitol. 46, 68. :sis by Armillifer armillatus is very Khalil, G. M. and Schacher, J. F. (1965): Linguatufa serrata in relation to Halzoun and the Marrara syndrome. Amer. J. Trop. Med. Hyg. 145,736-746. 1S, during routine X-rays examina­ Lavoipierre, M. M. J. and Lavoipierre, Michèle (1966) : An intermediate host of a Janson (1954) working in Kinshasa, Pentastomid. Nature 210 (5038), 845-846.

63 6 7

Prathap, K., Lau, K. S. and Bolton, J. M. (1969): Pentastomiasis: a Common finding at Ann. Soc. belge Méd. trop. Autopsy among Malaysian Aborigines. Amer. J. Trop. Med. Hyg. 18, 20-27. 1975, 55, 1, 59-64 Rendtorff, R. C. Deweese, M. W. and Murrah, W. (1962) : The occurrence of Linguatula serrata, a Pentastomid within the human eye. Amer. J. Trop. Med. Hyg., 11, 762-764. Schacher, J. F., Saab, S., Germanos, R. and Boustany, N. (1969) : The aetiology of halzoun in Lebanon : recovery of Linguatula serrata nymphs from two patients. Trans. Roy. Soc. Trop. Med. Hyg. 63, 854-58. Self, J. J. (1969) : Biological relationships of the Pentastomida : a bibliography on the Penta­ stomida. Exp. Parasitol. 24, 63-119. Sweatman, G. K. (1971): and Pentastomids. In Parasitic Diseases of Wild Mammals. John W. Davis and Roy C. Anderson, Ames, The Iowa State University Press, 1-64. THE PENTASTOM Tobie, J. E., Edgcomb, J. H. and Freireich, E. J. (1957): Tongue worm (Linguatula serrata) infestation in a patient with acute leukemia. Amer. J. Clin. Path. 28, 628-633. Van Wymeersch, H. and Wanson, M. (1954) : La porocéphalose nymphale et son image radiolo­ gique. Ann. Soc. belge Méd. trop., 34, 517.

1 1 Summary - This paper is a review of to three genera of Pentastomida have bee the pathogenic role of these species and

KEYWORDS : Pentastomosis, human; Can

I~

The Pentastomida constitute a known species are parasitic in t them are heteroxenous and hav successive hosts. In the most Linguatula, the definitive host is é or a carnivore, and the intermedi genus Raillietie/la, the adults live The Iife cycle is not known witt" boulengeri a common lung parasi as intermediate hosts (Fain, 1961 Recently Self (1969) has fed species of Iizards and recovered Some pentastomids are able te same host. So far a direct develc lohrmanni Noc and Giglioli, a s the Komodo varanus (see Fain al f sternae (Diesing, 1864), living in ! 1965). In the pulmonary tissues of forms between the embryo and th stages. It is possible that some s of lizards are also able to compl.

(*) Paper presented at the Third 25-31 August 1974.

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