Br. J. Surg. 1992, Vol. 79, December, 1335-1 338

M. S. Khuroo, S. A. Zargar, G. N. Yattoo, P. Koul, B. A. Khan, M. Y. Dar and M. S. Alai Department of Gastroenterology, institute of Medical Sciences, Srinagar 190 01 1, Kashmir, India Correspondence to: Professor M. S. Khuroo

Ascaris-induced acute pancreatitis The incidence, clinical disease and outcome of acute pancreatitis caused by ascariasis in an endemic area of Kashmir, India, was studied prospectively. Ascariasis was an aetiological factor in 59 of 256 patients (23.0 per cent) with acute pancreatitis. Worms had invaded the bile duct in 51 patients, the pancreatic duct in four and both ducts in four. Pancreatitis was mild in 46 patients and severe in 13. Associated pyogenic cholangitis was present in eight. Acute complications occurred in I 1 patients. Endoscopic retrograde cholangiopancreatography ( E R C P ) was performed in all cases within 72 h of admission and delineated ascarides in the duodenum invading the ampullary orijice ( 4 4 patients), in the bile duct (5.5) and in the pancreatic duct (eight). A t ERCP, worms were extracted f r o m the ampullary orijice and removed via the mouth of 33 patients with intractable epigastric pain, leading to rapid relief of symptoms. The eight patients with pyogenic cholangitis underwent endoscopic nasobiliary drainage to decompress the bile ducts; worms were extracted f r o m the bile duct of three of these patients using a Dormia basket. A total of 56 patients recovered f r o m acute illness with a combination of conservative and endoscopic treatment; the other three required emergency surgery. A t a mean(s.d.) follow-up of 19( 7 ) months, ten patients showed symptomatic worm reinvasion of the biliary tree. The overall mortality rate was 3 per cent.

Ascaris lurnbricoides is the most common helminth worldwide, and ascariasis is recognized as one of the less common causes of acute pancreatitis. Such pancreatitis occurs by direct worm invasion of the pancreatic duct (pancreatic ascariasis), by worm invasion of the ampullary orifice, entering the bile duct and blocking the pancreatic duct orifice (biliary ascariasis), and by worm invasion of both the bile duct and pancreatic duct (biliary and pancreatic ascariasis). Although biliary ascariasis is a known cause of pancreatiti~l-~, the fact that the literature contains only a few isolated reports of pancreatic ascariasis demonstrates its r a r i t ~ ~ Moreover, -~. the present knowledge of Ascaris-induced acute pancreatitis is scanty and an adequate description of the clinical disease and outcome is lacking. Kashmir in India is an area in which ascariasis is endemic: in a recent survey the prevalence was 30 per cent of adults and 60 per cent of children7. Ascariasis here is as frequent a cause of symptomatic adult biliary disease as gallstones'. In this paper 59 patients with Ascaris-induced acute pancreatitis are reported, including eight with pancreatic invasion, who were prospectively studied for clinical disease and outcome. Endoscopic extraction of worms from the duodenum and across the ampullary orifice as a part of the overall management is highlighted.

tomography on admission and at intervals thereafter. Severity of pancreatitis was predicted according to the criteria of Imrie er the attack was predicted to be mild if the prognostic score was 0-2 and severe if 3-8. Acute pancreatitis was considered to be caused by A . lurnbricoides infection when adult worms were detected in the biliary tree and/or pancreatic duct at ultrasonography and/or ERCP. The aetiology of acute pancreatitis was as follows: gallstones, 112 (43.8 per cent): ascarides, 59 (23.0 per cent); other, ten (3.9 per cent); and undefined, 75 (29.3 per cent). A passing reference to some of these patients has been made in an earlier reportlo.

Results The study group comprised six children and 53 adults (34 women, 19 men) of mean(s.d.) age 34( 10) (range 8-61) years. Of these, 51 had biliary ascariasis, four had pancreatic involvement, and four had invasion of both biliary and pancreatic systems. The biliary tree contained a single worm in 18 patients, two worms in 24 and three or more in 13. The pancreatic duct was invaded by a single worm in seven patients and by four worms in one. Upper abdominal pain referred to the back of duration 1-6 days and vomiting were typical presenting symptoms (Table I ). Cholangitis, defined as a symptom complex of high fever with rigors, jaundice and upper

Patients and methods From June 1986 to December 1991, 256 patients were admitted with a diagnosis of acute pancreatitis based on a serum amylase level >800 units11 and a compatible clinical picture. Patients with acute exacerbation of chronic pancreatitis were not included in this study. Ultrasonography of the liver, biliary tree and pancreas was carried out using a real-time scanner (Aloka SSD256; Aloka, Tokyo, Japan) within 24 h of admission and thereafter every 24-48 h to detect complications. The sonographic diagnosis of biliary or pancreatic ascariasis was made when non-shadowing long echogenic structures with a central sonolucent tube were visualized in the biliary tree or pancreatic duct. Endoscopic retrograde cholangiopancreatography ( E R C P ) using a side-viewing duodenoxope (JFB3 or JFIT-10; Olympus Optical, Tokyo, Japan) was carried out within 72 h of admission in patients with suspected biliary or pancreatic ascariasis on the basis of the clinical or ultrasonographic criteria previously described8. From April 1989, all patients with severe pancreatitis underwent enhanced computed

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0007 1323/Y2/.1?1335 04

~. . . ..

1992 Ruttcrworlh Hcincmnnn Lld

Table 1 Clinical ,/>uturi~so f Ascaris-rihtid acute pancreatitis in 59 pat ilW/.S

No. of patients ~

~~

~~~~

~~~

~~~

Abdominal pain Back pain Nausea and vomiting Roundworms in vomitus Fever Jaundice Tender hepatomegaly Gallbladder lump Decreased bowel sounds

- ~~~

~

59 ( l o o ) 44 (75) 52 (88) 50 (85) 17 (29) 15 (25) 23 (39) 8 (14) 8 (14)

Values in parentheses are percentages

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Ascaris-induced acute pancreatitis: M. S. Khuroo et al

Table 2 Morbidity and mortu1it.v in 59 paiients with Ascaris-related acute panereatitis with respect to the site of worm invasion into ihe bile duct andlor pancreatic duci Site of invasion

Duodenal ascarides invading ampullary orifice Severity of pancreatitis Mild Severe Complications* Pseudocyst Renal failure Respiratory failure Shock Disseminated intravascular coagulation Death

Biliary tree alone ( n = 51)

Pancreatic duct alone (n=4)

Both ducts (n=4)

40

0

4

41 10 8 3

2 3

5

2 0

1

1

0

1

*Four patients had two or more complications

Figure 1 Ultrasonogruphj reuea/ing U ihick h g non-shadowing echogenic strip (arrow)containing a centralsonoluceni iube, represeniing the digestice tract of the roundworm, within the diluted common bile duci

(CBD)

Radioqraphic findinqs Ultrasonography delineated worms in four of the eight patients with pancreatic ascariasis and in SO (91 per cent) of the SS with biliary invasion (Figure I ) ; 36 had an enlarged poorly echogenic pancreas and three had a pseudocyst. All patients underwent ERCP between 24 and 72 h after admission. Ascarides were seen to be moving actively in the duodenal lumen and invading the ampullary orifice in 44 patients. All those with severe pancreatitis had worms in the duodenum and blocking the ampullary orifice, but none of the four with pancreatic ascariasis alone had worms in the duodenum or invading the ampullary orifice. The bile duct was cannulated in all cases, and the pancreatic duct in 39. An attempt was made to fill the main pancreatic duct only. The pancreatic duct was dilated slightly (4-5 mm in the head) in patients with single-worm invasion of the pancreatic duct (Figures 2 and 3 ) but was found to be 9 mm in one patient with four-worm invasion. The pancreatic duct diameter ranged from 3 to 6 (mean 4.2) mm in the head region in patients with biliary tree invasion. I

_

I

Treatment and follow-up Initial treatment consisted of restricting oral intake and administration of intravenous fluids, antibiotics and analgesics. EEeclive anthelminthic therapy (mebendazole 100 mg orally twice daily for 3 days) was administered once the acute symptoms had subsided. In 33 patients with intractable pain not responding to analgesics, the worms from the duodenum and/or across the ampullary orifice were trapped during duodenoscopy with a polypectomy snare or a punch biopsy forceps and extracted via the mouth by withdrawing the endoscope along with the instrument holding the worms. Each of these patients had two to six worms extracted in one session and so sometimes needed repeated insertion of the endoscope; five with unremitting pain underwent two sessions of extraction. Endoscopic worm removal led to rapid relief of symptoms. Eight patients with associated pyogenic cholangitis had a nasobiliary catheter (7-Fr ENBD catheter; William Cook, Bjmerskov, Denmark) placed in the bile duct at ERCP for biliary decompression and drainage. Worms were extracted from the bile duct in three of these eight patients by introducing a basket into the bile duct through the ampullary orifice at ERCp; the were then engaged and extracted from the bile duct. The endoscope was removed along with the basket

abdominal pain or tenderness, was present in eight patients. Peritoneal aspirate produced haemorrhagic fluid in two. Acute pancreatitis was predicted to be mild in 46 patients (78 per cent) and severe in 13 (22 per cent) (Table 2 ) . All four patients with pancreatic ascariasis had a mild attack, whereas three of the four with biliary and pancreatic invasion had severe pancreatitis. The prevalence of severe pancreatitis in patients with biliary ascariasis was 20 per cent. Nine of the 13 patients with a severe attack had three or more worms in the biliary tree. The complication rate among those whose pancreatitis was predicted to be mild was 15 per cent compared with 39 per cent of patients predicted to have a severe attack. Laboratory findings Stool examination revealed ova of A . lurnbricoides in all patients. The mean(s.d.) serum bilirubin level was 29( 14) (range 17-53) pmol/l. The serum bilirubin level was < 17 pmol/l in 26 patients, 18-34 pmol/l in 18 and > 34 pmol/l in 15. Serum alkaline phosphatase was raised to a mean(s.d.) concentration of 820(210) (range 580-1140) units/] in 45 patients, all of whom had worm invasion of the biliary tree. Serum amylase levels ranged from 900 to 4160 (mean(s.d.) 1600(272 units/'. Blood cultures were taken from 25 patients, eight yielding micro-organisms: Escherichia coli in six and Klebsiella uerogenes in two.

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Figure 2 ~ndo.vcopic,rctrogrucfe c.h(J/Ungi(JpUnc.retIfUgTUph?,in u putimt witji mi/cipuncrcwti/is rerculiny u long /inrur filling defecr a/onq rhe enrirc punc,rcatii, duct (urrows)

Br. J. Surg., Vol. 79, No. 12, December 1992

Ascaris-induced acute pancreatitis: M. S. Khuroo et al.

Figure 3 Endoscopic retrograde cholangiopancveatoyraph~in a patient with stwere puncreutitis. The pancreutic duct contains u lineur jilliny defect in its distal half (arrows). The common bile duct is packed with multiple roundl.cwnis

holding the worms. Endoscopic sphincterotomy was not performed in any of the present patients to facilitate extraction of worms. A total of 56 patients (45 with mild pancreatitis and 11 of 13 with severe pancreatitis, including all eight with pyogenic cholangitis) recovered completely with a combination of conservative and endoscopic treatment and were discharged within 7-29 (mean(s.d.) 16(6)) days. The remaining three patients with intractable pain underwent surgery: one with haemorrhagic pancreatitis died following extraction of 15 worms from the biliary tree and four from the pancreatic duct; ten worms were extracted from the bile duct of the second through a choledochotomy; and surgery for an enlarging pseudocyst was performed in the third. The last two patients recovered, In 53 patients, exit of worms from the ductal system was assessed by ERCP 6-8 weeks after the initial attack. Worms had moved out of the ducts in 47 and persisted in the biliary tree in six, in whom endoscopic extraction from the bile ducts was attempted. Endoscopic sphincterotomy was not performed to extract worms, which were successfully removed from the bile duct with the help of a Dormia basket in five cases. The single patient in whom endoscopic extraction failed has since undergone surgery, at which three dead worms were recovered from the bile duct. Patients were advised to take anthelminthic therapy every 2 months. Of the 58 survivors, 36 had a mean(s.d.) follow-up of 19(7) (range 2-29) months. Thirteen episodes of severe abdominal pain requiring hospitalization occurred in ten patients, all of which (biliary colic in five cases, cholangitis in three, acalculous cholecystitis in two, pancreatitis in three) were caused by worm reinvasion of the biliary tree. N o reinvasion of the pancreatic duct was noted. One patient with severe pancreatitis died on the seventh day in hospital during a second admission. All the others recovered rapidly with conservative treatment or extraction of worms from the papillary orifice (five cases). Five patients underwent ERCP during a symptom-free period to assess 'silent' worm reinvasion; none was present. None of the patients developed symptoms of pancreatic insufficiency or calcification.

Discussion The aetiology of acute pancreatitis varies geographically. The present study shows ascariasis as an aetiological cause of this

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No. 12, December 1992

condition in 23 per cent of patients. Ascariasis has a worldwide distribution affecting one-quarter of the total population, mostly in developing countries in the tropics and subtropics' Although ascariasis is rare in the developed world, clinicians should be aware of abdominal complications related to it because of the increased movement of tourists, immigrants and refugeesI2-' '. Adult roundworms cause acute pancreatitis under the following circumstances: invasion into the bile duct through the papilla of Vater causing its blockage or spasm (biliary ascariasis); invasion into the pancreatic duct (pancreatic ascariasis ); or both (biliary and pancreatic ascariasis). Invasion of the pancreatic duct is rare owing to its narrowness: in a series of 500 patients with hepatobiliary and pancreatic ascariasis, only seven (1.4 per cent) showed worms invading the pancreatic duct l o . In the present study pancreatic ascariasis alone produced mild pancreatitis; partial blockage of the duct of Wirsung and a patent Santorini's duct may have protected these patients from developing a severe attack. Also, blockage of ampullary orifices may be critical in causing hypertension in the pancreatic duct and inducing severe pancreatitis. The ampullary orifice was not blocked by worms in any of the four patients with pancreatic ascariasis. In contrast, invasion of the biliary tract produced a more severe form of pancreatitis, with high morbidity. Because the adult worm has invaded the ampullary orifice, biliary obstruction usually presents with concurrent pancreatic obstruction. Simultaneous invasion of both the bile and pancreatic ducts led to severe pancreatitis in a high percentage of the patients studied. Both these situations probably caused pancreatic duct obstruction with bile regurgitation and entry of micro-organisms. These mechanisms both result in activation of pancreatic enzymes, with the development of pancreatitis. Ultrasonography is a safe and reliable tool for delineating worms in the biliary tree and also for monitoring their ex;t8.15.16 . H~wever, its sensitivity for the detection of a single worm in the bile duct is only 50 per cent'. Ultrasonography also has only a limited role in the diagnosis of pancreatic ascariasis, due to its high false-negative rate4. ERCP is not only an excellent tool for detecting worms but it can also play a major therapeutic role in the management of ascariasis-related p a n ~ r e a t i t i s ~ . ' ~No . complications were attributable to ERCP in the present series. Endoscopic extraction of worms from the duodenum and across the ampullary orifice led to rapid relief of symptoms. Removal of worms invading the ampulla of Vater facilitated drainage of the pancreatic duct and so favourably influenced the outcome. The actively moving ascarides in the duodenal lumen may invade the ampullary orifice to exacerbate pancreatitis, and their extraction via the mouth may also have contributed to the rapid recovery. Although only a randomized controlled trial can demonstrate the effect of this therapeutic procedure on morbidity, length of hospital stay and mortality rate, the rapid relief of symptoms in the present patients is impressive. Pancreatic pain not amenable to analgesics has become a major indication for urgent ERCP at this centre. Biliary or pancreatic symptoms recurred in many patients due to worm reinvasion. Regular anthelminthic therapy every 2 months is necessary to ensure a worm-free intestinal tract in an endemic area whereminfection rates are so high. Worms were not seen inside the pancreatobiliary tree during the symptom-free period, an observation confirmed in a sonographic study of the prevalence of biliary tract worms in the general population7. In summary, this study has shown that ERCP and the endoscopic extraction of worms are safe procedures in patients with Ascaris-induced acute pancreatitis; a skilled endoscopist is required. Endoscopic removal of worms from the duodenum and ampulla of Vater favourably affect the outcome and serve as an effective alternative to surgery. This therapeutic procedure should be considered an important part of the overall management of such patients".

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M.S. Khuroo et al.

References 1. 2. 3. 4. 5.

6. 7. 8. 9.

Khuroo MS, Zargar SA. Biliary ascariasis: a common cause of biliary and pancreatic disease in an endemic area. Gastroenterology 1985; 88: 418-23. Choi TK, Wong J. Severe pancreatitis caused by parasites in the common bile duct. J Trop Med Hyg 1984; 87: 211-14. Chen YS, Den BX, Huang BI, Xu LZ. Endoscopic diagnosis and management of Ascaris induced acute pancreatitis. Endoscopy 1986; 18: 127-8. Leung JWC, Mok SD, Metroweli C. Ascaris induced pancreatitis. AJR Am J Roentgenol 1987; 149: 511-12. Rigby HM. Acute haemorrhagic pancreatitis. Roundworm in the pancreatic duct. Br J Surg 1923; 10: 419-20. Novis IMS. Partial obstruction of the pancreatic duct by roundworm. Br J Surg 1923; 10: 421. Khuroo MS, Mahajan R, Zargar SA, Javid G, Sapru S. Prevalence of biliary tract disease in India: a sonographic study in adult population in Kashmir. Gut 1989; 30: 201-5. Khuroo MS, Zargar SA, Mahajan R, Bhat RL, Javid G. Sonographic appearances in biliary ascariasis. Gastroenterology 1987; 93: 267-72. Imrie CW, Benjamin IS, Ferguson JC et al. A single-centre

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10. 11. 12. 13. 14.

15. 16. 17.

double-blind trial of Trasylol therapy in primary acute pancreatitis. Br J Surg 1978; 65: 337-41. Khuroo MS, Zargar SA, Mahajan R. Hepatobiliary and pancreatic ascariasis in India. Lancet 1990; 335: 1503-6. Gabaldon A, Mofid C, Morishta K, Moskovski S, Sankale M, Standen DD. Control of ascariasis (report of WHO committee). World Health Organ Tech Rep Ser 1967; 379: 6-7. Raney R, Lilly J, McHardy G . Biliary calculus of round-worm origin. Ann Intern Med 1970; 12: 405-7. Schulman A. Biliary ascariasis presenting in the United States. Am J Gastroenterol 1977; 68: 167-70. Manialawi MS, Khattar NY, Helmy MM, Burcharth F. Endoscopic diagnosis and extraction of biliary ascariasis. Endoscopy 1986; 18: 204-5. Schulman A, Loxton AJ, Heydenrych JJ, Abdurahman KE. Sonographic diagnosis of biliary ascariasis. AJR Am J Roentgenol 1982; 139: 485-9. Cerri CG, Leite GJ, Correia DJ et al. Sonographic evaluation of Ascaris in the biliary tract. Radiology 1983; 146: 753-4. Zargar SA, Khuroo MS. Therapy of biliary ascariasis and its rationale. Gastroenterology 1987; 93: 668-9 (Letter).

Paper accepted 8 May 1992

Br. J. Surg.. Vol. 79, No. 12, December 1992

Ascaris-induced acute pancreatitis.

The incidence, clinical disease and outcome of acute pancreatitis caused by ascariasis in an endemic area of Kashmir, India, was studied prospectively...
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