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Human pentastomiasis discovered postmortem
Forensic Science International 137 (2003) 52–54
Human pentastomiasis discovered postmortem H. Yapo Ettea,*, L. Fantonb,1, K.D. Adou Brync, K. Bottia, K. Koffia, D. Malicierb a
Service d’Anatomie Pathologique et de Me´decine Le´gale, C.H.U. de Treichville, BP V 3, Abidjan, Ivory Coast De´partement de Me´decine Le´gale, Hoˆpital Edouard-Herriot, Place d’Arsonval, Lyon, Cedex 03 69437, France c Laboratoire de Parasitologie, U.F.R. des Sciences Me´dicales, Cocody BP V 166, Abidjan 01, Ivory Coast
b
Received 28 May 2003; accepted 2 July 2003
Abstract The autopsy of an 18-year-old girl who had died suddenly at home revealed generalised pentastomiasis. The location of this disease in the intestines was responsible for death by hemorrhagic enterocolitis. This discovery constituted an atypical case in our daily practice of forensic medicine. # 2003 Published by Elsevier Ireland Ltd. Keywords: Pentastomiasis; Postmortem; Armillifer grandis; Autopsy
1. Introduction Pentastomiasis or porocephalosis is a parasitic disorder due to infestation of man by a vermiform para-arthropod of the Armillifer genus [3]. Armillifer (A.) armillatus and Armillifer grandis have been observed in Africa. A third species, Armillifer monoliformis is rife in south-east Asia and Malaysia [1,10]. Adult A. armillatus and A. grandis parasites live in the pulmonary sacs of big snakes such as Pytho sebae (python), Bitis gabonica or Bitis nasicornis. The female lays eggs which are evacuated to the outside with the bronchial secretions of the snake [4]. The usual intermediate hosts are small rodents. Usually the eggs ingested by these rodents finish hatching to produce larvae which, after passing through their intestinal wall, are disseminated in the organs where they turn into nymphs. The nymph can only turn into an adult if it is ingested by the snake thus completing the cycle. Man becomes an accidental host by ingesting the eggs found on the ground, on food or the skin of snakes, or by consuming the undercooked or raw flesh of reptiles. Whatever the species,
pentastomiasis is almost always asymptomatic [9]. Most often the diagnosis occurs postmortem [7] or in the context of radiological examinations [6]. Sometimes, it can appear by chance during an examination of the fundus of the eye when the parasite migrates to the anterior chamber of the eye [2]. Pentastomiasis can also be revealed by an acute abdominal syndrome linked to intra-hepatic calcifications or visceral adhesions secondary to an inflammation around the parasite [6,8]. This observation constituted an unusual fatal form of disseminated pentastomiasis.
2. Observation During the year 2000, an 18-year-old woman, from the west of Ivory Coast (Man), a Yacuba, was found dead at her home in Abidjan. The family suspected an abortion because of some weeks of amenorrhea with abdominal pains and vomiting. A forensic autopsy was performed the following day at the forensic medicine unit in Abidjan. 2.1. External examination of the body
*
Corresponding author. E-mail addresses: [email protected] (H. Yapo Ette), [email protected] (L. Fanton). 1 Institute of Forensic Medicine of Lyon, Lyon Institute of Forensic Medicine, 12 Avenue Rockefeller, Lyon 69003, France.
The victim was a young black woman, of slim build (163 cm, 50 kg). The body showed dehydration and pallor of the skin and mucosa. There was no pelvic bulging or abnormal discharge from the vagina. The external genital
0379-0738/$ – see front matter # 2003 Published by Elsevier Ireland Ltd. doi:10.1016/S0379-0738(03)00281-0
H. Yapo Ette et al. / Forensic Science International 137 (2003) 52–54
53
Fig. 3. Massive presence of encysted larvae in the capsula hepatis. Fig. 1. Presence of encysted larvae on the surface and in the pulmonary parenchyma.
organs were normal. There was no suspicious lesion due to injury. 2.2. Autopsy In the thorax, the lungs contained inert, coiled, encysted larvae over all their surface and parenchyma (Fig. 1). The outer side of the pericardium also presented larvae. However, the pericardial cavity and heart had a normal appearance. There were also many coiled larvae on the parietal pleura. In the abdomen, the loops of the intestine had an abnormally dilated appearance and were dark red in color. Moving them produced a discharge of a blackish, foul-smelling liquid. Opening the intestine showed necrotic hemorrhagic mucosa, along with liquid, hemorrhagic stools. There was a massive invasion of the loops of the intestine by vermiform larvae (Fig. 2). All these lesions were more marked in the small intestine than in the colon. There were no fibrous adhesions of the intestine to the wall of the abdomen or false membranes. There were many larvae in the wall of the mesentery and some mesenteric adenopathies. There was no evidence of vascular thrombosis in the colic arterio-venous
Fig. 2. Extensive intestinal necrosis with infiltration of whitish larvae in the intestine wall.
pedicles and the vena cava. The stomach contained some larvae that had infiltrated the wall, but there were none in the gastric cavity. The liver was overrun with larvae both on its surface under the capsula hepatis which had thickened and in the hepatic parenchyma (Fig. 3). There were signs of compression of the bile ducts with considerable distension of the gall bladder (Fig. 4). The spleen, kidneys and pancreas were also infiltrated with larvae. The macroscopic appearance of the rest of the organs was normal. There was nothing to suggest a pregnancy or a recent abortion. 2.3. Parasitological examination During the autopsy, larvae were extracted from the intestinal wall and the liver and removed for parasitological examination. These were A. grandis nymphs (HETT, 1915) because of their smooth, whitish, vermiform appearance, their small size (10–15 mm long), with pronounced annulate relief, and a high number of rings. 2.4. Pathological examinations Samples were taken from the most infested organs for histological examination. The pulmonary parenchyma
Fig. 4. Armillifer grandis (larvae).
54
H. Yapo Ette et al. / Forensic Science International 137 (2003) 52–54
contained many parasites in cavities without peripheral fibrosis. The interalveolar septa were infiltrated with lympho-plasmocytes with vascular congestion. Examination of the small intestine showed extensive and almost total necrosis of the mucosa. The healthy areas had hemorrhagic suffusions combined with a diffuse infiltrate of lymphoplasmocytes and histiocytes surrounding the parasites. In the sub-mucosa, the blood vessels were dilated and very congested with the same inflammatory reaction. The colon’s appearance was the same as that of the small intestine with less necrosis of the mucosa. The architecture of the liver was preserved but there were many large parasites lodged in cavities surrounded by a fibrous shell infiltrated with lymphocytes. A thickening of the capsula hepatis which was infiltrated with parasites was also observed. 2.5. Toxicological analyses The search for toxic substances performed on samples of blood, bile, urine and stomach contents was negative. Blood alcohol was nil.
A. grandis was unusual in our region. In Ivory Coast it is A. armillatus pentastomiasis that is rife in its endemic form, whereas A. grandis is observed rather in central Africa [5,10,11]. This was therefore a rare fatal form of A. grandis pentastomiasis occurring in a normally non-endemic zone for this species. Paradoxically, we have no knowledge of any deaths in connection with this species in the zone where it is usually rife. It therefore seems possible that A. grandis might exist in certain species of reptiles that are consumed particularly in the west of Ivory Coast, notably in the Dixhuit Montagnes and Worodougou regions. Indeed, the first pediatric case reported and the victim of this observation were both originally from these regions where the eating habits and traditions are similar. This observation confirmed the seriousness of pentastomiasis for which there is no curative treatment at present. It suggests the development of prevention campaigns in the target populations, and studies of big snakes in order better to find out its geographical distribution.
References 3. Discussion The infestation of man by parasites of the Armillifer genus is fatal exceptionally. In Ivory Coast, the first case of death connected with this parasitosis was reported in 1979 [2]. The victim was a little girl of 5 years old, with the diagnosis of generalised pentastomiasis known before death. This was secondary to septicemia linked to the massive infestation of the lungs by A. grandis. In this observation the initial picture of sudden death constituted an unusual mode of revealing this parasitosis. The autopsy showed that the intestine was massively affected, reminiscent of amebic necrotic colitis [3]. The parasitological and pathological examinations confirmed the diagnosis of death by hemorrhagic enterocolitis of parasitic origin. This fatal complication has never been observed in A. armillatus pentastomiasis discovered postmortem. In these cases, the death was not connected directly with the parasitosis, but either with bacterial septicemia, with progressive ascites and pericarditis, or with digestive hemorrhage [11]. The macroscopic observations were similar to those reported in the 5-year-old girl [2]. However, no migration of the larvae to the eye or the brain was noted. The inflammatory reactions seemed also to be less invasive than those described for A. armillatus pentastomiasis where the inflammation provoked an acute surgical picture of the abdomen, and prevented exploration by laparoscopy [5,8]. As for the mode of contamination, questioning of the victim’s family provided confirmation that snake’s flesh was consumed habitually. However, human infestation by
[1] N.O. Azinge, E.G. Ogidi-Gbegbaje, J.A. Osunde, D. Oduah, Armillifer armillatus in Bendel State (Midwest) Nigeria (a village study in Ayogwiri Village, near Auchi, 120 km from Benin City) phase I, J. Trop. Med. Hygiene 81 (1978) 76–79. [2] V. Cagnard, J. Nicolas-Randegger, A. Dago Akribi, B. Rain, J.P. Nozais, P. Essoh Nomel, M. Ette, J. Doucet, G. Assale, G. N’Dri, Generalized and lethal pentastomiasis due to Armillifer grandis (Hett, 1915), Bull. Soc. Pathol. Exot. Filiales 72 (1979) 345–352. [3] D. Cutler, E. Avendano, P. Maldonado, M. Acosta, Necrotic amebic colitis, Am. J. Gastroenterol. 62 (1974) 345–349. [4] J.J. Drabick, Pentastomiasis, Rev. Infect. Dis. 9 (1987) 1087– 1094. [5] C. Faisy, B. Boye, A. Blatt, P. Boutes, J. Iloumbou, Porocephalosis, a little known parasitosis, literature review and a Congolese case report, Med. Trop. 55 (1995) 258–262. [6] A. Fisch, J. Leport, F. Bloch, A. Sebag, J. Frija, J.P. Petite, Human pentastomiasis: clinical and X-ray computed tomographic study of a case, Gastroenterol. Clin. Biol. 9 (1985) 263–265. [7] S.N. Guardia, H. Sepp, T. Scholten, I. Morava-Protzner, Pentastomiasis in Canada, Arch. Pathol. Lab. Med. 115 (1991) 515–517. [8] U. Herzog, P. Marty, F. Zak, Pentastomiasis: case report of an acute abdominal emergency, Acta Trop. 42 (1985) 261–271. [9] R. Pieron, Y. Mafart, B. Lesobre, D. Meyniel, Two cases of pentastomiasis observed in Paris, Sem. Hop. 58 (1982) 1047–1048. [10] J.T. Self, H.C. Hopps, A.O. Williams, Pentastomiasis in Africans, Trop. Geogr. Med. 27 (1975) 1–13. [11] H. Tiendrebeogo, D. Levy, D.D. Schmidt, Human pentastomiasis in Abidjan. A report on 29 cases, Rev. Fr. Mal. Respir. 10 (1982) 351–358.
Human pentastomiasis discovered postmortem H. Yapo Ettea,*, L. Fantonb,1, K.D. Adou Brync, K. Bottia, K. Koffia, D. Malicierb a
Service d’Anatomie Pathologique et de Me´decine Le´gale, C.H.U. de Treichville, BP V 3, Abidjan, Ivory Coast De´partement de Me´decine Le´gale, Hoˆpital Edouard-Herriot, Place d’Arsonval, Lyon, Cedex 03 69437, France c Laboratoire de Parasitologie, U.F.R. des Sciences Me´dicales, Cocody BP V 166, Abidjan 01, Ivory Coast
b
Received 28 May 2003; accepted 2 July 2003
Abstract The autopsy of an 18-year-old girl who had died suddenly at home revealed generalised pentastomiasis. The location of this disease in the intestines was responsible for death by hemorrhagic enterocolitis. This discovery constituted an atypical case in our daily practice of forensic medicine. # 2003 Published by Elsevier Ireland Ltd. Keywords: Pentastomiasis; Postmortem; Armillifer grandis; Autopsy
1. Introduction Pentastomiasis or porocephalosis is a parasitic disorder due to infestation of man by a vermiform para-arthropod of the Armillifer genus [3]. Armillifer (A.) armillatus and Armillifer grandis have been observed in Africa. A third species, Armillifer monoliformis is rife in south-east Asia and Malaysia [1,10]. Adult A. armillatus and A. grandis parasites live in the pulmonary sacs of big snakes such as Pytho sebae (python), Bitis gabonica or Bitis nasicornis. The female lays eggs which are evacuated to the outside with the bronchial secretions of the snake [4]. The usual intermediate hosts are small rodents. Usually the eggs ingested by these rodents finish hatching to produce larvae which, after passing through their intestinal wall, are disseminated in the organs where they turn into nymphs. The nymph can only turn into an adult if it is ingested by the snake thus completing the cycle. Man becomes an accidental host by ingesting the eggs found on the ground, on food or the skin of snakes, or by consuming the undercooked or raw flesh of reptiles. Whatever the species,
pentastomiasis is almost always asymptomatic [9]. Most often the diagnosis occurs postmortem [7] or in the context of radiological examinations [6]. Sometimes, it can appear by chance during an examination of the fundus of the eye when the parasite migrates to the anterior chamber of the eye [2]. Pentastomiasis can also be revealed by an acute abdominal syndrome linked to intra-hepatic calcifications or visceral adhesions secondary to an inflammation around the parasite [6,8]. This observation constituted an unusual fatal form of disseminated pentastomiasis.
2. Observation During the year 2000, an 18-year-old woman, from the west of Ivory Coast (Man), a Yacuba, was found dead at her home in Abidjan. The family suspected an abortion because of some weeks of amenorrhea with abdominal pains and vomiting. A forensic autopsy was performed the following day at the forensic medicine unit in Abidjan. 2.1. External examination of the body
*
Corresponding author. E-mail addresses: [email protected] (H. Yapo Ette), [email protected] (L. Fanton). 1 Institute of Forensic Medicine of Lyon, Lyon Institute of Forensic Medicine, 12 Avenue Rockefeller, Lyon 69003, France.
The victim was a young black woman, of slim build (163 cm, 50 kg). The body showed dehydration and pallor of the skin and mucosa. There was no pelvic bulging or abnormal discharge from the vagina. The external genital
0379-0738/$ – see front matter # 2003 Published by Elsevier Ireland Ltd. doi:10.1016/S0379-0738(03)00281-0
H. Yapo Ette et al. / Forensic Science International 137 (2003) 52–54
53
Fig. 3. Massive presence of encysted larvae in the capsula hepatis. Fig. 1. Presence of encysted larvae on the surface and in the pulmonary parenchyma.
organs were normal. There was no suspicious lesion due to injury. 2.2. Autopsy In the thorax, the lungs contained inert, coiled, encysted larvae over all their surface and parenchyma (Fig. 1). The outer side of the pericardium also presented larvae. However, the pericardial cavity and heart had a normal appearance. There were also many coiled larvae on the parietal pleura. In the abdomen, the loops of the intestine had an abnormally dilated appearance and were dark red in color. Moving them produced a discharge of a blackish, foul-smelling liquid. Opening the intestine showed necrotic hemorrhagic mucosa, along with liquid, hemorrhagic stools. There was a massive invasion of the loops of the intestine by vermiform larvae (Fig. 2). All these lesions were more marked in the small intestine than in the colon. There were no fibrous adhesions of the intestine to the wall of the abdomen or false membranes. There were many larvae in the wall of the mesentery and some mesenteric adenopathies. There was no evidence of vascular thrombosis in the colic arterio-venous
Fig. 2. Extensive intestinal necrosis with infiltration of whitish larvae in the intestine wall.
pedicles and the vena cava. The stomach contained some larvae that had infiltrated the wall, but there were none in the gastric cavity. The liver was overrun with larvae both on its surface under the capsula hepatis which had thickened and in the hepatic parenchyma (Fig. 3). There were signs of compression of the bile ducts with considerable distension of the gall bladder (Fig. 4). The spleen, kidneys and pancreas were also infiltrated with larvae. The macroscopic appearance of the rest of the organs was normal. There was nothing to suggest a pregnancy or a recent abortion. 2.3. Parasitological examination During the autopsy, larvae were extracted from the intestinal wall and the liver and removed for parasitological examination. These were A. grandis nymphs (HETT, 1915) because of their smooth, whitish, vermiform appearance, their small size (10–15 mm long), with pronounced annulate relief, and a high number of rings. 2.4. Pathological examinations Samples were taken from the most infested organs for histological examination. The pulmonary parenchyma
Fig. 4. Armillifer grandis (larvae).
54
H. Yapo Ette et al. / Forensic Science International 137 (2003) 52–54
contained many parasites in cavities without peripheral fibrosis. The interalveolar septa were infiltrated with lympho-plasmocytes with vascular congestion. Examination of the small intestine showed extensive and almost total necrosis of the mucosa. The healthy areas had hemorrhagic suffusions combined with a diffuse infiltrate of lymphoplasmocytes and histiocytes surrounding the parasites. In the sub-mucosa, the blood vessels were dilated and very congested with the same inflammatory reaction. The colon’s appearance was the same as that of the small intestine with less necrosis of the mucosa. The architecture of the liver was preserved but there were many large parasites lodged in cavities surrounded by a fibrous shell infiltrated with lymphocytes. A thickening of the capsula hepatis which was infiltrated with parasites was also observed. 2.5. Toxicological analyses The search for toxic substances performed on samples of blood, bile, urine and stomach contents was negative. Blood alcohol was nil.
A. grandis was unusual in our region. In Ivory Coast it is A. armillatus pentastomiasis that is rife in its endemic form, whereas A. grandis is observed rather in central Africa [5,10,11]. This was therefore a rare fatal form of A. grandis pentastomiasis occurring in a normally non-endemic zone for this species. Paradoxically, we have no knowledge of any deaths in connection with this species in the zone where it is usually rife. It therefore seems possible that A. grandis might exist in certain species of reptiles that are consumed particularly in the west of Ivory Coast, notably in the Dixhuit Montagnes and Worodougou regions. Indeed, the first pediatric case reported and the victim of this observation were both originally from these regions where the eating habits and traditions are similar. This observation confirmed the seriousness of pentastomiasis for which there is no curative treatment at present. It suggests the development of prevention campaigns in the target populations, and studies of big snakes in order better to find out its geographical distribution.
References 3. Discussion The infestation of man by parasites of the Armillifer genus is fatal exceptionally. In Ivory Coast, the first case of death connected with this parasitosis was reported in 1979 [2]. The victim was a little girl of 5 years old, with the diagnosis of generalised pentastomiasis known before death. This was secondary to septicemia linked to the massive infestation of the lungs by A. grandis. In this observation the initial picture of sudden death constituted an unusual mode of revealing this parasitosis. The autopsy showed that the intestine was massively affected, reminiscent of amebic necrotic colitis [3]. The parasitological and pathological examinations confirmed the diagnosis of death by hemorrhagic enterocolitis of parasitic origin. This fatal complication has never been observed in A. armillatus pentastomiasis discovered postmortem. In these cases, the death was not connected directly with the parasitosis, but either with bacterial septicemia, with progressive ascites and pericarditis, or with digestive hemorrhage [11]. The macroscopic observations were similar to those reported in the 5-year-old girl [2]. However, no migration of the larvae to the eye or the brain was noted. The inflammatory reactions seemed also to be less invasive than those described for A. armillatus pentastomiasis where the inflammation provoked an acute surgical picture of the abdomen, and prevented exploration by laparoscopy [5,8]. As for the mode of contamination, questioning of the victim’s family provided confirmation that snake’s flesh was consumed habitually. However, human infestation by
[1] N.O. Azinge, E.G. Ogidi-Gbegbaje, J.A. Osunde, D. Oduah, Armillifer armillatus in Bendel State (Midwest) Nigeria (a village study in Ayogwiri Village, near Auchi, 120 km from Benin City) phase I, J. Trop. Med. Hygiene 81 (1978) 76–79. [2] V. Cagnard, J. Nicolas-Randegger, A. Dago Akribi, B. Rain, J.P. Nozais, P. Essoh Nomel, M. Ette, J. Doucet, G. Assale, G. N’Dri, Generalized and lethal pentastomiasis due to Armillifer grandis (Hett, 1915), Bull. Soc. Pathol. Exot. Filiales 72 (1979) 345–352. [3] D. Cutler, E. Avendano, P. Maldonado, M. Acosta, Necrotic amebic colitis, Am. J. Gastroenterol. 62 (1974) 345–349. [4] J.J. Drabick, Pentastomiasis, Rev. Infect. Dis. 9 (1987) 1087– 1094. [5] C. Faisy, B. Boye, A. Blatt, P. Boutes, J. Iloumbou, Porocephalosis, a little known parasitosis, literature review and a Congolese case report, Med. Trop. 55 (1995) 258–262. [6] A. Fisch, J. Leport, F. Bloch, A. Sebag, J. Frija, J.P. Petite, Human pentastomiasis: clinical and X-ray computed tomographic study of a case, Gastroenterol. Clin. Biol. 9 (1985) 263–265. [7] S.N. Guardia, H. Sepp, T. Scholten, I. Morava-Protzner, Pentastomiasis in Canada, Arch. Pathol. Lab. Med. 115 (1991) 515–517. [8] U. Herzog, P. Marty, F. Zak, Pentastomiasis: case report of an acute abdominal emergency, Acta Trop. 42 (1985) 261–271. [9] R. Pieron, Y. Mafart, B. Lesobre, D. Meyniel, Two cases of pentastomiasis observed in Paris, Sem. Hop. 58 (1982) 1047–1048. [10] J.T. Self, H.C. Hopps, A.O. Williams, Pentastomiasis in Africans, Trop. Geogr. Med. 27 (1975) 1–13. [11] H. Tiendrebeogo, D. Levy, D.D. Schmidt, Human pentastomiasis in Abidjan. A report on 29 cases, Rev. Fr. Mal. Respir. 10 (1982) 351–358.