Journal of Infection (I992) 24, 87-9o
CASE REPORT Ectopic enterobiasis:
a case report and review
N a d i a G. T o r n i e p o r t h , * II R. D i s k o , t A. Brandish: and D. Barutzkig
* Second Department of Internal Medicine, t Institute of Hygiene and Medical Microbiology, Technical University of Munich, ~ Pathological Institute, Nordstadt Hospital, Hannover and ~Institute for Comparative Tropical Medicine and Parasitology, University of Munich, Germany Accepted for publication 2I August I99I Summary Enterobius vermicularis (' p i n w o r m ') is rarely f o u n d o u t s i d e the g a s t r o - i n t e s t i n a l tract. W e d e s c r i b e a case of e x t r a - i n t e s t i n a l p i n w o r m abscess associated with a n i n g u i n a l h e r n i a in a n adult. A b r i e f review of the l i t e r a t u r e is g i v e n a n d possible m e c h a n i s m s of tissue i n v a s i o n are discussed.
Introduction P i n w o r m disease, caused by the n e m a t o d e Enterobius vermicularis, is the most c o m m o n h e l m i n t h infection worldwide. 1 M a n is the principal natural host of the parasite. Adult pinworms live on the mucosa of the caecum, appendix and adjacent colon, where they rarely cause any significant pathology. Gravid females w a n d e r to the perianal and perineal regions, mainly at night, where they usually die after oviposition. T h e most c o m m o n clinical complaints are local itching and restless sleep due to nocturnal anal pruritus; m a n y infections, however, remain asymptomatic. Ectopic enterobiasis is rare. Most cases have been d o c u m e n t e d in women, describing inflammatory or granulomatous lesions in the genital tract or the abdominal cavity. 2-6 Some unusual sites include the lungs, breast, spleen, ureter and kidney, 6 the prostate, 7 and liver. 8-n T o our knowledge this is the first report o f a p i n w o r m abscess associated with an inguinal hernia in a male patient.
Case report A 79-year-old m a n was admitted for surgery of a p r e s u m e d incarcerated left inguinal hernia. T h e hernia had been present for the past 5 years, but had never troubled the patient. F o u r t e e n days before admission, he had noticed a painful swelling in the area. O n examination, an inflamed, indurated markedly tender mass (approximately 8 cm in diameter) was palpable. A n incarcerated indirect inguinal hernia was suspected. Routine diagnostic investigations were normal. T h e r e was no increase of eosinophilic granulocytes in the peripheral blood. Jj Address correspondence to: Dr N. G. Tornieporth, D.T.M.&H. (Lond), Second Department of Internal Medicine, Technical University of Munich, Ismaninger Strasse 22, 8000 Munich 80, Germany. oi63-4453/92/OlOO87+o4 $03.o0/0
© I992 The British Society for the Study of Infection
88
N.G. TORNIEPORTH ET AL.
Surgical exploration of the region revealed a purulent abscess in the subcutaneous fat. Following resection of the abscess, the hernia was treated according to standard surgical procedures. Macroscopically, the intestine appeared intact. Recovery of the patient was uneventful. T h e pathological specimen (8"5 x 3"o cm) weighed 27"7 g and consisted of subcutaneous fat with inflammatory changes, haemorrhages and minor areas of necrosis on its surface. Histologically, multiple abscesses were found within the fatty t i s s u e - s o m e recent and some older and surrounded by a layer of granulomatous tissue. T h e r e was a diffuse infiltration of the fatty tissue by granulocytes and monocytes. Eosinophilic granulocytes were abundant in the exudate and in the surrounding infiltrate (Plate I). Charcot-Leyden crystals were not seen. T h e abscesses contained oval bodies with a subcapsular hyaline zone and granular structures in the centre (Plate I), which could be identified as ova of E. vermicularis. Many of these ova were already disintegrating. Parts of a worm or a connection to the intestinal wall could not be demonstrated. A tissue specimen of 3 g of formalised material was homogenised and incubated in a 1% trypsin solution for 9o min. After sedimentation, a large number of liberated, slightly asymmetric eggs (55 x 25 # m ; Plate 2), typical of E. vermicularis, were found. Repeated attempts to detect ova by applying adhesive tape swabs to the perianal region and by stool examinations (merthiolate-iodine-formaldehyde-concentrationmethod) were unsuccessful. Bacteriological cultures of the abscess material grew Escherichia coll. Discussion
Extra-intestinal enterobiasis is rare. A comprehensive review of the cases reported before I95o is given by Symmers. 6 T h e most frequent ectopic site is the female genital tract. Lesions may be found in the vagina, cervix, uterus, the ovaries and frequently the fallopian tubes2 Granulomas of the pelvic peritoneum have been observed, mostly in proximity to the uterus and its adnexa. 6 It is now generally accepted that the gravid female worms can migrate up the female reproductive tract and thus gain access to the abdominal cavity, a'4'6 Parasites of either sex may also migrate through pre-existing lesions of the intestinal wall such as ulcers, diverticula, abscesses, fistulae or operation wounds.a. 3.6.12 Chandrasoma and Mendis, a however, describe a case in a male patient, where no breach in the intestinal wall was apparent. T h e y propose two possible explanations for their findings. T h e r e may have been a defect in the intestinal wall which had healed after allowing the passage of the worm(s), or alternatively there might be active penetration of the intact intestinal wall by the parasites. Our patient presented with a pre-existing left inguinal hernia. Macroscopically, the bowel seemed intact though it was thought possible that the intestinal wall had been damaged mechanically by a gliding hernia, thus allowing one or more worms to escape. In addition a senile atrophy of the bowel in this 79-year-old patient may have facilitated the penetration by the parasite(s). Chandrasoma and Mendis a report an incidental finding in a 46-year-old
yournal of Infection
Plates I and 2
Plate ~. Histological section of the abscess: oval bodies with a subcapsular hyaline zone and granular structures in the centre identified as ova of Enterobius vermicularis (arrowed), s u r r o u n d e d by multiple eosinophilic granulocytes (e.). PAS. × 28o.
Plate 2. Egg of Enterobius vermicularis (55 × 25 #m) liberated after trypsination of abscess material, x 28o. l'~. G. TORNIEPORTH ET AL.
(Facing p. 88)
Ectopic enterobiasis : case report
89
w o m a n presenting with bilateral indirect inguinal hernias. D u r i n g routine h e r n i o r r h a p h y a granulomatous mass attached to the p e r i t o n e u m of the right hernial sac was f o u n d which contained ova of E. vermicularis. T h e authors explain the presence of ova on the p e r i t o n e u m of this patient by the c o m m o n l y reported migration up the female reproductive tract of a gravid worm, which p r o b a b l y perished in the vicinity of the lesion. In comparison, tissue invasion in our patient m u s t have been via the bowel wall. T h e possible penetrative force of E. vermicularis is also a subject of discussion concerning the route of infection in the rare cases of hepatic granuloma. T M H a e m a t o g e n o u s spread following migration of the parasite(s) through the diseased colon wall seems probable when considering the case described b y Slais and colleagues, n who found the parasite within the portal vein. Other authors do not exclude the possibility of active penetration of the liver capsule b y the parasite(s), s-l° In the majority of cases, the pathological changes due to parasites or ova outside the gastro-intestinal tract are slight, and many lesions are incidental findings at surgery or at necropsy. GClinical findings are often unrelated to the parasitic lesion and peripheral eosinophilia is only occasionally observed. 2'1~ W h e n pathological changes are observed they are predominantly due to the release of toxic products b y degenerated and necrotic worms and their ova, which provoke a granulomatous response. 6 T h e greyish-white granulomas attain a diameter of up to I cm, are s u r r o u n d e d b y a fibrous capsule and m a y contain the remains of the often degenerated worm, as well as its more resistant ova, within a zone of necrosis. 6 Fibrotic material, a varying n u m b e r of eosinophils, neutrophil granulocytes, foreign b o d y giant cells, lymphocytes and sometimes C h a r c o t - L e y d e n crystals m a y be observed in the lesions. T h e macroscopic appearance and the histopathology correlate with the age of the lesion. 6 T h e massive presence of eosinophils in our tissue specimen strongly suggests that the worm(s) and the ova caused the tumour. Bacteria adhering to the w o r m surface (E. coli) led to secondary infection and abscess formation. Williams and D i x o n 14 underline the importance of the ova in eliciting an inflammatory response of the host. T h e y examined 182 appendices containing ova of E. vermicularis and f o u n d a significant correlation b e t w e e n inflammatory and obstructive changes and the presence of ova in the organs. T h e migration of w o r m s outside the gastro-intestinal tract may lead to severe complications, such as salpingitis, 4,G abscess of the uterus 2'6 and peritonitis, 3'n'13 or may mimic other serious diseases: carcinoma of the colon, 13 Crohn's disease 18 or even metastatic carcinoma, which may lead to unnecessary radical surgery. 5 T h u s , although ectopic lesions due to E. vermicularis are rare, they should be considered not only in the differential diagnosis of other ' h e l m i n t h o m a s ,15 b u t also of several important abdominal conditions, 12'13 especially if the histopathological findings include an unusually high n u m b e r of eosinophils within a granulomatous lesion. 6 5
J I N 24
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N. G. T O R N I E P O R T H
ET AL.
References i. Benenson AS. Enterobiasis. In: Benenson AS, Ed. Control of communicable diseases in man. I4th ed. Washington, D.C. : American Public Health Association, I985: IO9-I i I. 2. Beddoe H L . Peritoneal granuloma due to Enterobius vermicularis. Am J Dis Child I956; 9I : 577-580. 3. Chandrasoma PT, Mendis KN. Enterobius vermicularis in ectopic sites. Am J Trop Med Hyg I977; z6 : 644-649. 4. Croce EJ, MacGillivray W F , Murphy CJ. Salpingitis due to Enterobius vermicularis. N EnglJ Med I956; z54: 67-69. 5. Fitzgerald TB, Mainwaring AR, Ahmed A. Pelvic peritoneal oxyuriasis simulating metastatic carcinoma. A case report. J Obstet Gynaecol Br Commonwealth I974; 8I: 248-250. 6. Symmers WSC. Pathology of oxyuriasis. Arch Path I95o; 5o: 475-516. 7. Symmers WSC. Two cases of eosinophilic prostatitis due to metazoan infestation (with Oxyuris vermicularis, and with a larva of Linguatula serrata). ,7 Pathol Bacteriol I957; 73: 549-555. 8. Daly J J, Baker GF. Pinworm granuloma of the liver. Am J Trop Med Hyg 1984; 33 : 62-64. 9. Little M D , Cuello CJ, D'Alessandro A. Granuloma of the liver due to Enterobius vermicularis. Report of a case. Am `7 Trop Mecl Hyg I973 ; zz: 567-569. Io. Mondou EN, Gnepp DR. Hepatic granuloma resulting from Enterobius vermicularis. Am `7 Clin Pathol I989; 9 I : 97-Ioo. I I . Slais J. A threadworm granuloma in the human liver. Helminthologia I963; 4: 479-483. I2. Marteau P, Flourie B, Lavergne A, Garin F, Bertin P, Rambaud JC. Granulome ~ oxyures du m6sent6re. Gastroenterol Clin Biol I989; I3: 738-74o. i3. McDonald GSA, Hourihane DO'B. Ectopic Enterobius vermicularis. Gut I972; I3: 621-626. I4. Williams DJ, Dixon M F . Sex, Enterobius vermicularis and the appendix. Br,7 Surg I988; 75: I225--I226" I5. Anthony PP, McAdam I W j . Helminthic pseudotumours of the bowel: thirty-four cases of helminthoma. Gut I972; I3: 8-i6.
CASE REPORT Ectopic enterobiasis:
a case report and review
N a d i a G. T o r n i e p o r t h , * II R. D i s k o , t A. Brandish: and D. Barutzkig
* Second Department of Internal Medicine, t Institute of Hygiene and Medical Microbiology, Technical University of Munich, ~ Pathological Institute, Nordstadt Hospital, Hannover and ~Institute for Comparative Tropical Medicine and Parasitology, University of Munich, Germany Accepted for publication 2I August I99I Summary Enterobius vermicularis (' p i n w o r m ') is rarely f o u n d o u t s i d e the g a s t r o - i n t e s t i n a l tract. W e d e s c r i b e a case of e x t r a - i n t e s t i n a l p i n w o r m abscess associated with a n i n g u i n a l h e r n i a in a n adult. A b r i e f review of the l i t e r a t u r e is g i v e n a n d possible m e c h a n i s m s of tissue i n v a s i o n are discussed.
Introduction P i n w o r m disease, caused by the n e m a t o d e Enterobius vermicularis, is the most c o m m o n h e l m i n t h infection worldwide. 1 M a n is the principal natural host of the parasite. Adult pinworms live on the mucosa of the caecum, appendix and adjacent colon, where they rarely cause any significant pathology. Gravid females w a n d e r to the perianal and perineal regions, mainly at night, where they usually die after oviposition. T h e most c o m m o n clinical complaints are local itching and restless sleep due to nocturnal anal pruritus; m a n y infections, however, remain asymptomatic. Ectopic enterobiasis is rare. Most cases have been d o c u m e n t e d in women, describing inflammatory or granulomatous lesions in the genital tract or the abdominal cavity. 2-6 Some unusual sites include the lungs, breast, spleen, ureter and kidney, 6 the prostate, 7 and liver. 8-n T o our knowledge this is the first report o f a p i n w o r m abscess associated with an inguinal hernia in a male patient.
Case report A 79-year-old m a n was admitted for surgery of a p r e s u m e d incarcerated left inguinal hernia. T h e hernia had been present for the past 5 years, but had never troubled the patient. F o u r t e e n days before admission, he had noticed a painful swelling in the area. O n examination, an inflamed, indurated markedly tender mass (approximately 8 cm in diameter) was palpable. A n incarcerated indirect inguinal hernia was suspected. Routine diagnostic investigations were normal. T h e r e was no increase of eosinophilic granulocytes in the peripheral blood. Jj Address correspondence to: Dr N. G. Tornieporth, D.T.M.&H. (Lond), Second Department of Internal Medicine, Technical University of Munich, Ismaninger Strasse 22, 8000 Munich 80, Germany. oi63-4453/92/OlOO87+o4 $03.o0/0
© I992 The British Society for the Study of Infection
88
N.G. TORNIEPORTH ET AL.
Surgical exploration of the region revealed a purulent abscess in the subcutaneous fat. Following resection of the abscess, the hernia was treated according to standard surgical procedures. Macroscopically, the intestine appeared intact. Recovery of the patient was uneventful. T h e pathological specimen (8"5 x 3"o cm) weighed 27"7 g and consisted of subcutaneous fat with inflammatory changes, haemorrhages and minor areas of necrosis on its surface. Histologically, multiple abscesses were found within the fatty t i s s u e - s o m e recent and some older and surrounded by a layer of granulomatous tissue. T h e r e was a diffuse infiltration of the fatty tissue by granulocytes and monocytes. Eosinophilic granulocytes were abundant in the exudate and in the surrounding infiltrate (Plate I). Charcot-Leyden crystals were not seen. T h e abscesses contained oval bodies with a subcapsular hyaline zone and granular structures in the centre (Plate I), which could be identified as ova of E. vermicularis. Many of these ova were already disintegrating. Parts of a worm or a connection to the intestinal wall could not be demonstrated. A tissue specimen of 3 g of formalised material was homogenised and incubated in a 1% trypsin solution for 9o min. After sedimentation, a large number of liberated, slightly asymmetric eggs (55 x 25 # m ; Plate 2), typical of E. vermicularis, were found. Repeated attempts to detect ova by applying adhesive tape swabs to the perianal region and by stool examinations (merthiolate-iodine-formaldehyde-concentrationmethod) were unsuccessful. Bacteriological cultures of the abscess material grew Escherichia coll. Discussion
Extra-intestinal enterobiasis is rare. A comprehensive review of the cases reported before I95o is given by Symmers. 6 T h e most frequent ectopic site is the female genital tract. Lesions may be found in the vagina, cervix, uterus, the ovaries and frequently the fallopian tubes2 Granulomas of the pelvic peritoneum have been observed, mostly in proximity to the uterus and its adnexa. 6 It is now generally accepted that the gravid female worms can migrate up the female reproductive tract and thus gain access to the abdominal cavity, a'4'6 Parasites of either sex may also migrate through pre-existing lesions of the intestinal wall such as ulcers, diverticula, abscesses, fistulae or operation wounds.a. 3.6.12 Chandrasoma and Mendis, a however, describe a case in a male patient, where no breach in the intestinal wall was apparent. T h e y propose two possible explanations for their findings. T h e r e may have been a defect in the intestinal wall which had healed after allowing the passage of the worm(s), or alternatively there might be active penetration of the intact intestinal wall by the parasites. Our patient presented with a pre-existing left inguinal hernia. Macroscopically, the bowel seemed intact though it was thought possible that the intestinal wall had been damaged mechanically by a gliding hernia, thus allowing one or more worms to escape. In addition a senile atrophy of the bowel in this 79-year-old patient may have facilitated the penetration by the parasite(s). Chandrasoma and Mendis a report an incidental finding in a 46-year-old
yournal of Infection
Plates I and 2
Plate ~. Histological section of the abscess: oval bodies with a subcapsular hyaline zone and granular structures in the centre identified as ova of Enterobius vermicularis (arrowed), s u r r o u n d e d by multiple eosinophilic granulocytes (e.). PAS. × 28o.
Plate 2. Egg of Enterobius vermicularis (55 × 25 #m) liberated after trypsination of abscess material, x 28o. l'~. G. TORNIEPORTH ET AL.
(Facing p. 88)
Ectopic enterobiasis : case report
89
w o m a n presenting with bilateral indirect inguinal hernias. D u r i n g routine h e r n i o r r h a p h y a granulomatous mass attached to the p e r i t o n e u m of the right hernial sac was f o u n d which contained ova of E. vermicularis. T h e authors explain the presence of ova on the p e r i t o n e u m of this patient by the c o m m o n l y reported migration up the female reproductive tract of a gravid worm, which p r o b a b l y perished in the vicinity of the lesion. In comparison, tissue invasion in our patient m u s t have been via the bowel wall. T h e possible penetrative force of E. vermicularis is also a subject of discussion concerning the route of infection in the rare cases of hepatic granuloma. T M H a e m a t o g e n o u s spread following migration of the parasite(s) through the diseased colon wall seems probable when considering the case described b y Slais and colleagues, n who found the parasite within the portal vein. Other authors do not exclude the possibility of active penetration of the liver capsule b y the parasite(s), s-l° In the majority of cases, the pathological changes due to parasites or ova outside the gastro-intestinal tract are slight, and many lesions are incidental findings at surgery or at necropsy. GClinical findings are often unrelated to the parasitic lesion and peripheral eosinophilia is only occasionally observed. 2'1~ W h e n pathological changes are observed they are predominantly due to the release of toxic products b y degenerated and necrotic worms and their ova, which provoke a granulomatous response. 6 T h e greyish-white granulomas attain a diameter of up to I cm, are s u r r o u n d e d b y a fibrous capsule and m a y contain the remains of the often degenerated worm, as well as its more resistant ova, within a zone of necrosis. 6 Fibrotic material, a varying n u m b e r of eosinophils, neutrophil granulocytes, foreign b o d y giant cells, lymphocytes and sometimes C h a r c o t - L e y d e n crystals m a y be observed in the lesions. T h e macroscopic appearance and the histopathology correlate with the age of the lesion. 6 T h e massive presence of eosinophils in our tissue specimen strongly suggests that the worm(s) and the ova caused the tumour. Bacteria adhering to the w o r m surface (E. coli) led to secondary infection and abscess formation. Williams and D i x o n 14 underline the importance of the ova in eliciting an inflammatory response of the host. T h e y examined 182 appendices containing ova of E. vermicularis and f o u n d a significant correlation b e t w e e n inflammatory and obstructive changes and the presence of ova in the organs. T h e migration of w o r m s outside the gastro-intestinal tract may lead to severe complications, such as salpingitis, 4,G abscess of the uterus 2'6 and peritonitis, 3'n'13 or may mimic other serious diseases: carcinoma of the colon, 13 Crohn's disease 18 or even metastatic carcinoma, which may lead to unnecessary radical surgery. 5 T h u s , although ectopic lesions due to E. vermicularis are rare, they should be considered not only in the differential diagnosis of other ' h e l m i n t h o m a s ,15 b u t also of several important abdominal conditions, 12'13 especially if the histopathological findings include an unusually high n u m b e r of eosinophils within a granulomatous lesion. 6 5
J I N 24
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N. G. T O R N I E P O R T H
ET AL.
References i. Benenson AS. Enterobiasis. In: Benenson AS, Ed. Control of communicable diseases in man. I4th ed. Washington, D.C. : American Public Health Association, I985: IO9-I i I. 2. Beddoe H L . Peritoneal granuloma due to Enterobius vermicularis. Am J Dis Child I956; 9I : 577-580. 3. Chandrasoma PT, Mendis KN. Enterobius vermicularis in ectopic sites. Am J Trop Med Hyg I977; z6 : 644-649. 4. Croce EJ, MacGillivray W F , Murphy CJ. Salpingitis due to Enterobius vermicularis. N EnglJ Med I956; z54: 67-69. 5. Fitzgerald TB, Mainwaring AR, Ahmed A. Pelvic peritoneal oxyuriasis simulating metastatic carcinoma. A case report. J Obstet Gynaecol Br Commonwealth I974; 8I: 248-250. 6. Symmers WSC. Pathology of oxyuriasis. Arch Path I95o; 5o: 475-516. 7. Symmers WSC. Two cases of eosinophilic prostatitis due to metazoan infestation (with Oxyuris vermicularis, and with a larva of Linguatula serrata). ,7 Pathol Bacteriol I957; 73: 549-555. 8. Daly J J, Baker GF. Pinworm granuloma of the liver. Am J Trop Med Hyg 1984; 33 : 62-64. 9. Little M D , Cuello CJ, D'Alessandro A. Granuloma of the liver due to Enterobius vermicularis. Report of a case. Am `7 Trop Mecl Hyg I973 ; zz: 567-569. Io. Mondou EN, Gnepp DR. Hepatic granuloma resulting from Enterobius vermicularis. Am `7 Clin Pathol I989; 9 I : 97-Ioo. I I . Slais J. A threadworm granuloma in the human liver. Helminthologia I963; 4: 479-483. I2. Marteau P, Flourie B, Lavergne A, Garin F, Bertin P, Rambaud JC. Granulome ~ oxyures du m6sent6re. Gastroenterol Clin Biol I989; I3: 738-74o. i3. McDonald GSA, Hourihane DO'B. Ectopic Enterobius vermicularis. Gut I972; I3: 621-626. I4. Williams DJ, Dixon M F . Sex, Enterobius vermicularis and the appendix. Br,7 Surg I988; 75: I225--I226" I5. Anthony PP, McAdam I W j . Helminthic pseudotumours of the bowel: thirty-four cases of helminthoma. Gut I972; I3: 8-i6.
