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Cholecystectomy for cholecystitis in patients with acquired immune deficiency syndrome
Cholecystectomy for Cholecystitis in Patients With Acquired lnmlune Deficiency Syndrome Philippe Wind, MD, Jean M. Chevallier, MD, David Jones, MD, Pascal Frileux, MD, Paul H. Cugnenc, MD, Paris, France
Acalculous cholecystitis, a recognized manifestation o f acquired immune deficiency s y n d r o m e (AIDS), causes abdondnal pain which can be relieved by cholecystectomy. T h e indications for cholecystectomy have remained undefined, however, because the chulecystitis is usually a c c o m pmfied by generalized cholangitis and it is difficult to distinguish the relative clinical i m p o r t a n c e o f the two problems. Since 1 9 8 5 , we have p e r f o r m e d c h o l e c y s t e c t o m y on 8 patients with AIDS who had clinical manifestations o f acute cholecystitis associated with a thickening o f the gallbladder wall by 5 nun to 12 ram. Two o f the 8 had gallstones and 4 had associated cholangitis. All had b e e n t r e a t e d with antibiotics for 2 0 to 1 8 0 days bef o r e surgery, but physical d e t e r i o r a t i o n had p r o g r e s s e d in e v e r y case. At the m o m e n t of surgical i n t e r v e n t i o n , 4 patients had multiple o r g a n failure. One patient died 3 days postoperatively, but the rest r e c o v e r e d rapidly with resolution o f the abdominal pain and sepsis. Two patients died 2 0 days after surgery due to complications of AIDS. T h e remaining 5 died due to AIDS at 6, 9, 10, 12, and 14 m o n t h s after surgery. Two of this g r o u p d e v e l o p e d progressive chulangitis with raised serum alkaline phosphatase. O u r exp e r i e n c e indicates that c h o l e c y s t e c t o m y should be c o n s i d e r e d for the t r e a t m e n t o f severe and persistent symptoms o f hepatobiliary manifestations o f AIDS notwithstanding the p r e s e n c e of cholangitis.
pain and fever.8.9 Ultrasound commonly reveals marked biliary tract abnormalities including thickening of the gallbladder wall? °.ll The difficulty of distinguishing the relative clinical importance of cholecystitis and cholangitis in these patients makes it hard to establish indications for surgery. Removal of the gallbladder may alleviate symptoms due to cholecystitis but is unlikely to help with those due to cholangitis. 4 We reviewed our experience of cholecystectomy in AIDS patients to determine the indications and value of surgery.
syndrome (AIDS)) It causes abdominal pain which can be relieved by cholecystectomy.2s Approximately 80% of AIDS patients with cholecystitis also present a diffuse cholangitis affecting both the intra- and extrahepatic bile d u c t s . 6'7 These patients show biochemical evidence of cholestasis without increased serum bilirubin levels, but the cholangitis can be a significant cause of abdominal
P A T I E N T S AND M E T H O D S In June 1991, H6pital La~nnec was providing inpatient or outpatient care to 1,100 HIV-seropositive individuals. Twenty-one of these patients were admitted with clinical signs of cholecystitis and or cholangitis. All had right hypochondrial or epigastric pain, fever, abnormal liver function tests, and ultrasonic evidence of gallbladder wall thickening of more than 3 mm. After diagnosis with cholecystitis, they received regular outpatient care with repeated liver function tests and ultrasound examinations. Ultrasound and/or CT scan evidence of intra- or extrahepatic bile duct dilatation, duct wall thickening, or bile duct stenosis was considered suggestive of cholangitis) °.~1 Bile duct opacification confirmed the diagnosis of cholangitis, showing these same abnormalities, especially the intrahepatic and papillary stenosis. Each patient's HIV seropositivity was confirmed by HIV EIA enzyme-linked immunosorbent assay (ELISA) and a Western blot antibody test. All 21 patients were treated medically with antibiotics. Thirteen recovered from their symptoms or did not reach a stage where surgery was considered necessary. Unfortunately, they have all since died of other complications of AIDS. The remaining 8 patients underwent cholecystectomy for acute cholecystitis. Cholangiograms were performed via the accessory bile duct in 6, 1 of whom also underwent preoperative endoscopic retrograde cholangiopancreatography (ERCP). One patient had ERCP alone, and technical difficulties thwarted bile duct opacification in 1 patient. In addition to the gallbladder, a liver biopsy was examined histologically. Samples of bile were sent for bacteriological, virological, and parasitological examinations.
From the General and Digestive Surgical Service, Hrpital La~nnec, Paris, France. Requests for reprints should be addressed to Philippe Wind, MD, Hrpital La~nnec, 42 rue de S~vres, Paris 75007, France. Manuscript submitted July 23, 1992, and accepted in revised form May 19, 1993.
RESULTS Eight patients, with a mean age of 43.7 :t: 10.3 years (range 32 to 58), underwent cholecystectomy for acute cholecystiffs. Seven were homosexual men and 1 was a woman who had been infected during a blood transfusion. AIDS had been diagnosed an average of 10.6 +_2 months (range 0 to 24) before the appearance of biliary symptoms. Every pa-
holecystitis, usually of an acalculous variety, most often due to cytomegalovirus or cryptosporidia, is a recC ognized manifestation of acquired immune deficiency
244
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168 SEPTEMBER 1994
CHOLECYSTECTOMY IN AIDS PATIENTS/WIND ET AL
tient was classified Center for Diseases Control (CDC) Group IV at the time of his or her operation. ~2All had right hypochondrial or epigastric pain, fever of over 38.5°C, and weight loss surpassing 10% of body weight. None had a prior history of hepatobilary disease. Four suffered from diarrhea. All 8 patients had normal serum bilirubin levels (mean + SD 12.2 + 3.4 pmol/L [range 7 to 16]), and other biochemical liver-function measurements were also normal in 4. Four had elevated gamma-glutamyl transpeptidase levels between 2N and 5N (N = upper level of normal range). Among these patients, there were 3 instances of high serum alkaline phosphatase I levels, ranging from 5N to 8N, and 3 instances of abnormal levels of serum glutamic oxaloacetic transaminase, between 1.5N and 2N. All 8 patients had reduced total white cell counts, the number ranging from 450/mm 3 to 1,887/mm 3 (average 1,154 + 501/mm3). In addition, all patients had reduced Thelper (CD4) lymphocytes, the levels ranging from 2/mm 3 to 500/mm 3 (average 238 + 131/ram3). The ratio of Thelpers versus T-suppressors (CD4/CD8) was also reduced (mean + SD 0.36 + 0.19 [range 0.09 to 0.59]). In 5 patients, serology was positive for cytomegalovirus. Cryptosporidia were isolated from stool samples in 4 of the 8 patients, 1 of whom also had amoebae. Ultrasound revealed thickening of the gallbladder wall varying from 5 mm to 12 mm in all patients and gallstones in 2. In 1 case ultrasound demonstrated abnormalities of the intrahepatic bile ducts suggestive of cholangitis. CT scan was performed in 2 patients and demonstrated abnormalities suggestive of cholangitis in both cases. The decision to operate was made on the basis of the persistence of fever and other symptoms despite 20- to 180day antibiotic treatment, the aggravation of the patient's poor general state, and (in 7 patients) the onset of abdominal rigidity. Four patients had multiple organ failure with respiratory distress, hypotension, and renal insufficiency at the moment of surgical intervention. Laparotomy confirmed gallbladder disease in all cases, but the operative findings were less remarkable than anticipated from the patients' clinical pictures. Macroscopically, the gallbladder appeared neither distended nor gangrenous. The wall was moderately inflamed with significant subserosal edema, the inflammation predominantly affecting the neck of the gallbladder and the accessory bile duct. No additional patients had gallstones beyond the 2 who were identified by ultrasound. Intraoperative bile duct opacification yielded normal results in 3 patients and revealed evidence of cholangitis involving intrahepatic bile ducts in 4. One patient with cholangitis had cholangiographic evidence of progressive stenosis of the papilla. Histological examination of the gallbladders confirmed acute cholecystitis in every case, with most patients having inflammation of the mucosa and evidence of ulceration. Two patients had cytomegalovirus inclusions, 1 had cryptosporidial infection, and I had both pathogens. All bile cultures were negative. Hepatic biopsy disclosed portal fibrosis in 4 cases and lymphomatous cells in 1 patient who, nevertheless, had no gross lymphoma. One patient died 3 days after surgery due to progressive septic shock. The rest recovered rapidly with total resolu-
tion of their abdominal pain and sepsis. Two patients, 1 of whom had been diagnosed as having cholangitis, died 20 days after surgery due to complications of AIDS. One developed tetraplegia and staphylococcal pneumonia, the other pancytopenia. The 5 patients who survived past 3 weeks died due to AIDS 6, 9, 10, 12, and 14 months after surgery. Two of these patients diagnosed by bile duct opacification as having cholangitis, developed elevated serum alkaline phosphatase levels, but retained normal serum bilirubin levels. Both suffered from mild, recurrent, intermittent abdominal pain which was different from their preoperative pain. The 3 remaining patients, I of whom had been diagnosed during operation as having cholangitis, remained asymptomatic until death. COMMENTS The decision to perform cholecystectomy in 8 patients with AIDS and cholecystitis was made on clinical grounds. Neither their abnormal liver function tests nor ultrasound abnormalities contributed to the decision. The rapid postoperative improvement in general condition and the resolution of the sepsis and multiple organ failure suggest that the cholecystitis was indeed causative of the patients' clinical conditions. There was a marked contrast between the severity of the clinical features and the relative paucity of macroscopic and histological findings. Although gangrene is found in the gallbladders of 30% of patients with acalculous cholecystitis who do not have AIDS, ~3 none of these patients with AIDS had gangrene. Two had gallstones. Associated cholangitis and evidence of cytomegalovirus inclusions in the gallbladder wall suggested that the stones were not solely responsible for the clinical condition of 1 of these 2. Cholecystitis in AIDS patients is usually associated with diffuse cholangitis affecting both the intra- and extrahepatic biliary tracts. The agents most commonly incriminated in cholecystitis and cholangitis in AIDS patients are cytomegalovirus and cryptosporidia. It has also been suggested that biliary infection could be a direct manifestation of HIV infection or of immunosuppression. 9 AIDS patients with cholangitis may develop papillary stenosis which eventually requires treatment by endoscopic sphincterotomy. 68 In the case of coexistent intrahepatic biliary stenosis, cholestasis may persist following cholecystectomy or sphincterotomy4.6.7 and may explain the recurring symptoms in 2 patients in this study. Biochemical and ultrasonic abnormalities in AIDS patients with cholangitis were of little help in the decision to operate. They remained unchanged from the onset of the symptoms, despite the progressive deterioration of the patient's general condition and the worsening of abdominal signs. Thus, cholecystectomy should be considered for treatment of hepatobilary manifestations of AIDS when symptoms are severe and persisting, the presence of cholangitis notwithstanding. REFERENCES 1. Pitlik SD, Fainstein V, Rios A, et al. Cryptosporidial cholecystitis. NEJM. 1983;308:977.
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168
SEPTEMBER 1994
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CHOLECYSTECTOMY IN AIDS PATIENTS/WIND ET AL
2. Aaron JS, Wynter CD, Kirton OC, Simko V. Cytomegalovirus associated with acalculous cholecystis in a patient with acquired immune deficiency syndrome. Am J GastroenteroL 1988;83: 879-881. 3. Cosserat J, Carlier AM, Bloch F, et al. Cholangites et chol6cystites alithiasiques chez deux malades atteints de SIDA. Presse Med. 1991 ;20:25-27. 4. Iannuzzi C, Belghiti J, Menu Y, et al. La chol6cystite alithiasique chez les patients porteurs du SIDA est le t6moin d'une cholangite diffuse. Gastroenterol Clin Biol. 1989;13:A244. 5. Kavin H, Jonas RB, Chowdhury L, Kabins S. Alcaculous cholecystitis and cytomegalovirus infection in the acquired immunodeficiency syndrome. Ann Intern Med. 1986;104:53-54. 6. Cello JP. Acquired immunodeficiency syndrome cholangiopathy: spectrum of disease. Am J Med. 1989;86:539-546. 7. Dolmatch BL, Laing FC, Federle MP, et al. AIDS-related cholangitis: radiographic findings in nine patients. Radiology. 1987;163: 313-316.
246
8. Roulot D, Valla D, Brun-Vezinet F, et al. Cholangitis in the acquired irnrnunodeficiency syndrome: report of two cases and review of the literature. Gut. 1987;28:1653-1660. 9. Viteri AL, Greene JF, Jr. Bile duct abnormalities in the acquired immune deficiency syndrome. Gastroenterology. 1987;92:2014-2018. 10. McCarty M, Choudhiri AH, Helbert M, Crofton ME. Radiological features of AIDS related cholangitis. Clin Radiol. 1989;40:582-585.
I 1. Yana C, Frija J, Cyna-Gorse F, et al. Aspects radiologiques des inflammations non calculeuses des voies biliaires au cours du SIDA. J RadioL 1989;70:411-414. 12. Centers for Disease Control. Classification system for human T lymphotropic virus Ill/lymphadenopathy associated virus infection. Ann Intern Med. 1986;105:234-237. 13. Savoca PE, Longo WE, Zucker KA, et al. The increasing prevalence of acalculous cholecystitis in outpatients. Ann Surg. 1990;21 1:433--437.
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168 SEPTEMBER 1994
Acalculous cholecystitis, a recognized manifestation o f acquired immune deficiency s y n d r o m e (AIDS), causes abdondnal pain which can be relieved by cholecystectomy. T h e indications for cholecystectomy have remained undefined, however, because the chulecystitis is usually a c c o m pmfied by generalized cholangitis and it is difficult to distinguish the relative clinical i m p o r t a n c e o f the two problems. Since 1 9 8 5 , we have p e r f o r m e d c h o l e c y s t e c t o m y on 8 patients with AIDS who had clinical manifestations o f acute cholecystitis associated with a thickening o f the gallbladder wall by 5 nun to 12 ram. Two o f the 8 had gallstones and 4 had associated cholangitis. All had b e e n t r e a t e d with antibiotics for 2 0 to 1 8 0 days bef o r e surgery, but physical d e t e r i o r a t i o n had p r o g r e s s e d in e v e r y case. At the m o m e n t of surgical i n t e r v e n t i o n , 4 patients had multiple o r g a n failure. One patient died 3 days postoperatively, but the rest r e c o v e r e d rapidly with resolution o f the abdominal pain and sepsis. Two patients died 2 0 days after surgery due to complications of AIDS. T h e remaining 5 died due to AIDS at 6, 9, 10, 12, and 14 m o n t h s after surgery. Two of this g r o u p d e v e l o p e d progressive chulangitis with raised serum alkaline phosphatase. O u r exp e r i e n c e indicates that c h o l e c y s t e c t o m y should be c o n s i d e r e d for the t r e a t m e n t o f severe and persistent symptoms o f hepatobiliary manifestations o f AIDS notwithstanding the p r e s e n c e of cholangitis.
pain and fever.8.9 Ultrasound commonly reveals marked biliary tract abnormalities including thickening of the gallbladder wall? °.ll The difficulty of distinguishing the relative clinical importance of cholecystitis and cholangitis in these patients makes it hard to establish indications for surgery. Removal of the gallbladder may alleviate symptoms due to cholecystitis but is unlikely to help with those due to cholangitis. 4 We reviewed our experience of cholecystectomy in AIDS patients to determine the indications and value of surgery.
syndrome (AIDS)) It causes abdominal pain which can be relieved by cholecystectomy.2s Approximately 80% of AIDS patients with cholecystitis also present a diffuse cholangitis affecting both the intra- and extrahepatic bile d u c t s . 6'7 These patients show biochemical evidence of cholestasis without increased serum bilirubin levels, but the cholangitis can be a significant cause of abdominal
P A T I E N T S AND M E T H O D S In June 1991, H6pital La~nnec was providing inpatient or outpatient care to 1,100 HIV-seropositive individuals. Twenty-one of these patients were admitted with clinical signs of cholecystitis and or cholangitis. All had right hypochondrial or epigastric pain, fever, abnormal liver function tests, and ultrasonic evidence of gallbladder wall thickening of more than 3 mm. After diagnosis with cholecystitis, they received regular outpatient care with repeated liver function tests and ultrasound examinations. Ultrasound and/or CT scan evidence of intra- or extrahepatic bile duct dilatation, duct wall thickening, or bile duct stenosis was considered suggestive of cholangitis) °.~1 Bile duct opacification confirmed the diagnosis of cholangitis, showing these same abnormalities, especially the intrahepatic and papillary stenosis. Each patient's HIV seropositivity was confirmed by HIV EIA enzyme-linked immunosorbent assay (ELISA) and a Western blot antibody test. All 21 patients were treated medically with antibiotics. Thirteen recovered from their symptoms or did not reach a stage where surgery was considered necessary. Unfortunately, they have all since died of other complications of AIDS. The remaining 8 patients underwent cholecystectomy for acute cholecystitis. Cholangiograms were performed via the accessory bile duct in 6, 1 of whom also underwent preoperative endoscopic retrograde cholangiopancreatography (ERCP). One patient had ERCP alone, and technical difficulties thwarted bile duct opacification in 1 patient. In addition to the gallbladder, a liver biopsy was examined histologically. Samples of bile were sent for bacteriological, virological, and parasitological examinations.
From the General and Digestive Surgical Service, Hrpital La~nnec, Paris, France. Requests for reprints should be addressed to Philippe Wind, MD, Hrpital La~nnec, 42 rue de S~vres, Paris 75007, France. Manuscript submitted July 23, 1992, and accepted in revised form May 19, 1993.
RESULTS Eight patients, with a mean age of 43.7 :t: 10.3 years (range 32 to 58), underwent cholecystectomy for acute cholecystiffs. Seven were homosexual men and 1 was a woman who had been infected during a blood transfusion. AIDS had been diagnosed an average of 10.6 +_2 months (range 0 to 24) before the appearance of biliary symptoms. Every pa-
holecystitis, usually of an acalculous variety, most often due to cytomegalovirus or cryptosporidia, is a recC ognized manifestation of acquired immune deficiency
244
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168 SEPTEMBER 1994
CHOLECYSTECTOMY IN AIDS PATIENTS/WIND ET AL
tient was classified Center for Diseases Control (CDC) Group IV at the time of his or her operation. ~2All had right hypochondrial or epigastric pain, fever of over 38.5°C, and weight loss surpassing 10% of body weight. None had a prior history of hepatobilary disease. Four suffered from diarrhea. All 8 patients had normal serum bilirubin levels (mean + SD 12.2 + 3.4 pmol/L [range 7 to 16]), and other biochemical liver-function measurements were also normal in 4. Four had elevated gamma-glutamyl transpeptidase levels between 2N and 5N (N = upper level of normal range). Among these patients, there were 3 instances of high serum alkaline phosphatase I levels, ranging from 5N to 8N, and 3 instances of abnormal levels of serum glutamic oxaloacetic transaminase, between 1.5N and 2N. All 8 patients had reduced total white cell counts, the number ranging from 450/mm 3 to 1,887/mm 3 (average 1,154 + 501/mm3). In addition, all patients had reduced Thelper (CD4) lymphocytes, the levels ranging from 2/mm 3 to 500/mm 3 (average 238 + 131/ram3). The ratio of Thelpers versus T-suppressors (CD4/CD8) was also reduced (mean + SD 0.36 + 0.19 [range 0.09 to 0.59]). In 5 patients, serology was positive for cytomegalovirus. Cryptosporidia were isolated from stool samples in 4 of the 8 patients, 1 of whom also had amoebae. Ultrasound revealed thickening of the gallbladder wall varying from 5 mm to 12 mm in all patients and gallstones in 2. In 1 case ultrasound demonstrated abnormalities of the intrahepatic bile ducts suggestive of cholangitis. CT scan was performed in 2 patients and demonstrated abnormalities suggestive of cholangitis in both cases. The decision to operate was made on the basis of the persistence of fever and other symptoms despite 20- to 180day antibiotic treatment, the aggravation of the patient's poor general state, and (in 7 patients) the onset of abdominal rigidity. Four patients had multiple organ failure with respiratory distress, hypotension, and renal insufficiency at the moment of surgical intervention. Laparotomy confirmed gallbladder disease in all cases, but the operative findings were less remarkable than anticipated from the patients' clinical pictures. Macroscopically, the gallbladder appeared neither distended nor gangrenous. The wall was moderately inflamed with significant subserosal edema, the inflammation predominantly affecting the neck of the gallbladder and the accessory bile duct. No additional patients had gallstones beyond the 2 who were identified by ultrasound. Intraoperative bile duct opacification yielded normal results in 3 patients and revealed evidence of cholangitis involving intrahepatic bile ducts in 4. One patient with cholangitis had cholangiographic evidence of progressive stenosis of the papilla. Histological examination of the gallbladders confirmed acute cholecystitis in every case, with most patients having inflammation of the mucosa and evidence of ulceration. Two patients had cytomegalovirus inclusions, 1 had cryptosporidial infection, and I had both pathogens. All bile cultures were negative. Hepatic biopsy disclosed portal fibrosis in 4 cases and lymphomatous cells in 1 patient who, nevertheless, had no gross lymphoma. One patient died 3 days after surgery due to progressive septic shock. The rest recovered rapidly with total resolu-
tion of their abdominal pain and sepsis. Two patients, 1 of whom had been diagnosed as having cholangitis, died 20 days after surgery due to complications of AIDS. One developed tetraplegia and staphylococcal pneumonia, the other pancytopenia. The 5 patients who survived past 3 weeks died due to AIDS 6, 9, 10, 12, and 14 months after surgery. Two of these patients diagnosed by bile duct opacification as having cholangitis, developed elevated serum alkaline phosphatase levels, but retained normal serum bilirubin levels. Both suffered from mild, recurrent, intermittent abdominal pain which was different from their preoperative pain. The 3 remaining patients, I of whom had been diagnosed during operation as having cholangitis, remained asymptomatic until death. COMMENTS The decision to perform cholecystectomy in 8 patients with AIDS and cholecystitis was made on clinical grounds. Neither their abnormal liver function tests nor ultrasound abnormalities contributed to the decision. The rapid postoperative improvement in general condition and the resolution of the sepsis and multiple organ failure suggest that the cholecystitis was indeed causative of the patients' clinical conditions. There was a marked contrast between the severity of the clinical features and the relative paucity of macroscopic and histological findings. Although gangrene is found in the gallbladders of 30% of patients with acalculous cholecystitis who do not have AIDS, ~3 none of these patients with AIDS had gangrene. Two had gallstones. Associated cholangitis and evidence of cytomegalovirus inclusions in the gallbladder wall suggested that the stones were not solely responsible for the clinical condition of 1 of these 2. Cholecystitis in AIDS patients is usually associated with diffuse cholangitis affecting both the intra- and extrahepatic biliary tracts. The agents most commonly incriminated in cholecystitis and cholangitis in AIDS patients are cytomegalovirus and cryptosporidia. It has also been suggested that biliary infection could be a direct manifestation of HIV infection or of immunosuppression. 9 AIDS patients with cholangitis may develop papillary stenosis which eventually requires treatment by endoscopic sphincterotomy. 68 In the case of coexistent intrahepatic biliary stenosis, cholestasis may persist following cholecystectomy or sphincterotomy4.6.7 and may explain the recurring symptoms in 2 patients in this study. Biochemical and ultrasonic abnormalities in AIDS patients with cholangitis were of little help in the decision to operate. They remained unchanged from the onset of the symptoms, despite the progressive deterioration of the patient's general condition and the worsening of abdominal signs. Thus, cholecystectomy should be considered for treatment of hepatobilary manifestations of AIDS when symptoms are severe and persisting, the presence of cholangitis notwithstanding. REFERENCES 1. Pitlik SD, Fainstein V, Rios A, et al. Cryptosporidial cholecystitis. NEJM. 1983;308:977.
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168
SEPTEMBER 1994
,945
CHOLECYSTECTOMY IN AIDS PATIENTS/WIND ET AL
2. Aaron JS, Wynter CD, Kirton OC, Simko V. Cytomegalovirus associated with acalculous cholecystis in a patient with acquired immune deficiency syndrome. Am J GastroenteroL 1988;83: 879-881. 3. Cosserat J, Carlier AM, Bloch F, et al. Cholangites et chol6cystites alithiasiques chez deux malades atteints de SIDA. Presse Med. 1991 ;20:25-27. 4. Iannuzzi C, Belghiti J, Menu Y, et al. La chol6cystite alithiasique chez les patients porteurs du SIDA est le t6moin d'une cholangite diffuse. Gastroenterol Clin Biol. 1989;13:A244. 5. Kavin H, Jonas RB, Chowdhury L, Kabins S. Alcaculous cholecystitis and cytomegalovirus infection in the acquired immunodeficiency syndrome. Ann Intern Med. 1986;104:53-54. 6. Cello JP. Acquired immunodeficiency syndrome cholangiopathy: spectrum of disease. Am J Med. 1989;86:539-546. 7. Dolmatch BL, Laing FC, Federle MP, et al. AIDS-related cholangitis: radiographic findings in nine patients. Radiology. 1987;163: 313-316.
246
8. Roulot D, Valla D, Brun-Vezinet F, et al. Cholangitis in the acquired irnrnunodeficiency syndrome: report of two cases and review of the literature. Gut. 1987;28:1653-1660. 9. Viteri AL, Greene JF, Jr. Bile duct abnormalities in the acquired immune deficiency syndrome. Gastroenterology. 1987;92:2014-2018. 10. McCarty M, Choudhiri AH, Helbert M, Crofton ME. Radiological features of AIDS related cholangitis. Clin Radiol. 1989;40:582-585.
I 1. Yana C, Frija J, Cyna-Gorse F, et al. Aspects radiologiques des inflammations non calculeuses des voies biliaires au cours du SIDA. J RadioL 1989;70:411-414. 12. Centers for Disease Control. Classification system for human T lymphotropic virus Ill/lymphadenopathy associated virus infection. Ann Intern Med. 1986;105:234-237. 13. Savoca PE, Longo WE, Zucker KA, et al. The increasing prevalence of acalculous cholecystitis in outpatients. Ann Surg. 1990;21 1:433--437.
THE AMERICAN JOURNAL OF SURGERY ® VOLUME 168 SEPTEMBER 1994