Intraoperative Cholangiography

A Review of Indications and Analysis of Age-Sex Groups

STEVEN B. LEVINE, M.D.,* HARVEY J. LERNER, M.D., F.A.C.S.,* ELIZABETH D. LEIFER, M.A.,t STEVEN R. LINDHEIM, B.S.

A retrospective review was performed of patients who had biliary tract stone formation as the primary diagnosis for hospitalization and indication for surgery. Five hundred and eighty-nine consecutive charts were reviewed of patients admitted between 1975 and 1979. Intraoperative cholangiography was performed in 166 patients of whom 22 had common duct exploration. Choledochotomy in this series was performed in 63 cases without utilizing pre-exploratory cholangiography. A normal intraoperative cholangiogram was found to be 100% accurate; however, an abnormal cholangiogram was associated with a 16% false positive rate of exploration of the common duct. The incidence of unsuspected common duct stones detected only by intraoperative cholangiography was 2.3%. Age-sex analysis confirms a 10-year mean age difference between men and women within the population of this study (p < 0.001). This age-sex difference is maintained in patients without common duct pathology as well as in patients with sterile bile. However, the mean age difference between male and female patients with either demonstrable common duct obstruction by stones or infected bile as determined by routine intraoperative culture is not statistically significant. A review of the role of intraoperative cholangiography, and the experience at Northeastern Hospital is discussed.

From the Departments of Surgery of Northeastern Hospital and Pennsylvania Hospital, and the Department of Hospital and Management Information Services, Pennsylvania Hospital, Philadelphia, Pennsylvania

Methods

O VER THE COURSE OF the last 50 years, the practicality and utility of intraoperative cholangiography as a diagnostic tool has been a source of controversy in the literature. More recently, its routine use to screen patients for asymptomatic common duct pathology has been adamantly advocated. The purpose of this study is to review the literature on intraoperative cholangiography along with the experience at Northeastern Hospital. The effectiveness and accuracy, as well as the consequences of a normal or abnormal cholangiogram, is addressed.

Department of Surgery.

t Department of Hospital and Management Information. Reprint requests: Harvey J. Lerner, M.D., Chairman, Department of Surgery, Northeastern Hospital, 2301 E. Allegheny Avenue, Philadelphia,
Pennsylvania 19134. Submitted for publication: May 18, 1983.

The medical records of patients undergoing biliary tract surgery at Northeastern Hospital from 1975 to 1979 were reviewed. All patients had cholecystitis as the primary diagnosis for hospitalization and indication for surgery, thereby excluding all incidental cholecystectomies performed concomitant with other major procedures. Cases were identified by name and unit history number; and variables studied included age, sex, surgeon, referring physician, and other secondary diagnoses. Patients were classified by procedure and admission status, i.e., elective vs. emergency. Indications for common duct exploration were carefully noted according to previously described criteria in the literature (Table 1).1-8 The findings at choledochotomy were likewise recorded, wherein the description of sludge was equivalent to a common duct harboring stones. All intraoperative biliary cultures were reviewed and the results of these studies were also recorded. The intraoperative cholangiogram was performed by inserting a TAUT operative cholangiogram polyethylene catheter into the cystic duct and injecting 20 cc of 25% Hypaque solution. Two films were taken in addition to a preoperative scout film. The films were immediately interpreted by a radiologist and returned to the operating suite for the surgeon's review. The final formal reading was made later in the day by the radiologist. In this review, an abnormal cholangiogram was defined as any of the following: (1) a diameter ofthe common bile duct greater than 12 mm; (2) filling defect(s) in the common bile duct; (3) inadequate visualization of the lower end of the com-

692

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INTRAOPERATIVE CHOLANGIOGRAPHY TABLE 1. Incidence of Clinical Evidence

No. Patients No. who Harbored Stones in CD
19
4

693

Percentage*
61% 22%

Minor Preoperative Data History of jaundice History of pancreatitis X-ray evidence of stone in common bile duct Alk phosphatase > 100 Bilirubin 1.0 and <7.0 Major Preoperative Data Evidence of cholangitis** Bilirubin ;7.0 Recurrent signs and symptoms after cholecystectomy Diagnosis of biliary fistula Minor Intraoperative Data Small stones in gallbladder History of biliary colic with no stones in gallbladder Sediment of bile aspirated from common bile duct Major Intraoperative Data Palpable stone in common bile duct Dilated or thickened cystic duct Thickened common bile duct

31 18 3 167 111
17 14 4 1 57 12 4

1 34 31

20% 28% 71% 50%

12 7 4 I
14 0 2

25% 0%

22 38 55

21 16 25

95% 42% 45%

* Percentages do not add as patients may have one or more of the clinical symptoms. ** Cholangitis was defined by right-upper quadrant abdominal pain, a body temperature greater than 101 F, jaundice, and a white blood cell count that was either greater than 12,000/mm3 or demonstrated a left shift.

mon bile duct; and/or (4) no contrast seen in the duodenum.9-"

Intraoperative Cholangiography
One hundred and sixty-six intraoperative cholangiograms were performed. Common duct exploration (CDE) was performed in 22 patients, and 144 patients had no further biliary manipulation.
FLOWCHART OF PROCEDURES

Results

Five hundred and eighty-nine consecutive patients presented with cholelithiasis and/or choledocholithiasis. These patients were divided into five major categories according to their operative report (Fig. 1): (1) cholecystectomy without further biliary manipulation; (2) cholecystectomy with intraoperative cholangiogram; (3) cholecystectomy with intraoperative cholangiography and choledochotomy; (4) cholecystectomy and common duct exploration without a diagnostic intraoperative radiographic study; and (5) choledochotomy. There were four patients in this last category who presented with recurrent symptoms indicative of biliary tract obstruction and a history of cholecystectomy at a different institution. Comparison between surgeons affirmed no significant difference in length of hospital stay or postoperative morbidity. Morbidity in the series was defined as any identifiable cause for lengthening hospital stay beyond the median and mode of 8 days. Mean length of stay for elective admissions was 9.4 days, whereas those patients with acute cholecystitis admitted via the Emergency Room had an average length of stay of 10.6 days (p < 0.005). Morbidity among patients with acute biliary disease was 26.4%, and 11.6% in patients admitted electively (p < 0.001). Incidence of wound infection in this series was only 2.2%. Mortality incidence was 0.34%.

E Pats

CDE

FIG. 1. Flowchart of procedures.

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TABLE 2. Intraoperative Cholangiograms
All Patients No. Normal

LEVINE AND OTHERS

Ann. Surg. * December 1983

Patients with Indications for CDE

16 6 0 6

Patients without Indications for CDE

130 0 0 0 7 5 4 1

of this patient's chart demonstrated no preoperative clinical data suggestive of obstruction, and the only intraoperative clinical indication for choledochotomy was the presence of small stones in the gallbladder. The radiology report noted a filling defect in only one of two operative

cholangiograms
No. CDEs pos. stones neg. stones No. Abnormal

146 6 0 6

cholangiograms. Six patients had indications for common duct exploration despite normal cholangiography. None of these six
common ducts were found to contain stones. Four patients had preoperative and intraoperative indications for choledochotomy. The other two patients had thickened cystic ducts as their only indication. In this series, a negative cholangiogram was 100% accurate. To date, there have been no falsely normal cholangiograms reported. True positive cholangiography was defined as the number of patients with abnormal cholangiography whose choledochotomies yielded stones or whose postoperative history was suspect for biliary obstruction, divided by the total number of abnormal cholangiograms. In this series, the incidence of true positive studies was 84%, and false negative studies incidence was 16%. Among those patients with an abnormal cholangiogram and stones found in the common duct, only three were unsuspected, i.e., they had no significant preoperative clinical information to create suspicion of common duct obstruction, and they had no findings at surgery to indicate likewise. An additional three patients were slightly suspicious for common duct pathology having only two or three minor indications for exploration. The incidence of unsuspected stones is that absolute number divided by the number ofpatients who had normal intraoperative cholangiography with no clinical indications for choledochotomy; this calculates to 2.3%. The yield of common duct stones for those who had cholecystectomy, intraoperative cholangiography, and common duct exploration (Procedure 3) was 15/22 or 68.3%. If normal cholangiography had been on an absolute contraindication to choledochotomy, our yield would have been 93.8%. The yield of stones of those patients who had cholecystectomy and choledochotomy was 38/63 or 60.3%.

cholangiograms
No. CDEs pos. stones neg. stones

20 16 15 1

13*
11 11 0

* Only one known case of a patient who did not have CDE, but developed signs and symptoms of residual stone obstruction in follow-

up.

Among those patients who had cholecystectomy and operative cholangiography, 140 cholangiograms were interpreted as normal; four cholangiograms were abnormal. Two of these patients had no clinical indications for CDE and cholangiography showed filling defects without ductal dilatation. Intraoperatively, no stones were palpable and the operating surgeons elected not to perform choledochotomy; long-term follow-up of 5 and 7 years in these two patients proved no evidence for residual stones. The third patient had multiple indications of choledochotomy, and cholangiography demonstrated a dilated common bile duct. Stones were neither visualized nor palpated. Three years after his surgery, the patient was treated conservatively for cholangitis, abdominal pain, and hyperbilirubinemia. The fourth patient had mildly elevated liver enzymes and a dilated common bile duct by intraoperative cholangiography, but unfortunately was lost to follow-up. Twenty-two patients had common duct explorations following operative cholangiography. Sixteen of these patients had abnormal cholangiograms. Only one of these 16 patients did not yield a common duct stone. Review

Age-Sex Analysis
The population studied matched previous descriptive epidemiologic data.212"13" '9 The man to woman ratio was 1:3. The mean age for men was 59 years, and 48 years for women (p < 0.001). The ratio of women to men for each age group is best appreciated in figure 2. Similar analysis of the population by procedure maintains a 1:3 man to woman ratio; however, mean age differences do
vary.

AGE

FIG. 2. Age distribution of patients by

sex.

Mean ages are listed in table 3. Patients who had cholecystectomy with or without an intraoperative cholangiogram but without common duct exploration, i.e., Pro-

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INTRAOPERATIVE CHOLANGIOGRAPHY TABLE 3. Mean Age by Procedure and Culture. Mean Age St. Dev. (N) Men Women 48 47 47 55 44 63 17 16 19 19 16 15

695
p <0.001 <0.001 <0.05 no difference <0.0001 no difference

All patients Procedure one + two Procedure three + four, CDE negative Procedure three + four, CDE positive Patients with negative culture Patients with positive culture

58 57 58 62 55 64

14 (152) 14 (131) 7 (8) 19 (12) 15 (96) 12 (36)

(437) (369) (24) (41) (346) (57)

cedure 1 plus 2, had a 10-year age difference between men and women (p < 0.001). This same age difference is seen in patients who had choledochotomy that did not yield stones (p < 0.05). Examination of the population harboring stones in their common ducts reveals no significant differences in the mean ages between men and women. Furthermore, women with stones in their common ducts are older than women without stones in their common ducts, with a probability that this difference is due to chance of less than 0.06-a relationship not apparent in men. Interestingly, all six patients who had clinical data directing the surgeon to perform choledochotomy despite a normal cholangiogram were women. Four of these patients were under 39 years of age. Five hundred and thirty-five patients had their bile cultured during surgery. Age-sex analysis demonstrated a 10-year age difference between men and women if the bile was sterile. However, the mean age of patients with infected bile proven by culture was not significantly different between men and women. Within each sex group, patients with positive cultures were significantly older than those with negative cultures (men p < 0.01, and women p < 0.001).

Discussion
Intraoperative Cholangiography
Ever since its introduction in 1932 by Mirizzi, operative cholangiography has remained a controversial topic in the literature.'2 Its popularity as a technique to demonstrate the site of obstructive pathology blossomed in the United States in the early 1960s. By the 1970s, cholangiography was being advocated for all biliary surgery. The arguments in favor of routine operative cholangiography are many.2'3'7'9'1322 The most important application remains its use for selection of patients who have clinical indications for choledochotomy, yet may not be harboring stones at the time of surgery. Intraoperative cholangiography, or preoperative cholangiography via transhepatic or retrograde endoscopic approaches, is suggested by some to be a prerequisite to exploring the common duct. Intraoperative cholangiography which demonstrates a stone is usually helpful to

confirm clinical impressions; whereas a normal cholangiogram in this series was always accurate. Unsuspected stones lying in the choledochus that later in the hospital stay may necessitate common duct exploration remain the nemesis of the biliary tract surgeon. Studies of patients undergoing cholecystectomies demonstrate an incidence of choledolithiasis at the operating table of 7-18%.8,8,23-29 Review of the intraoperative cholangiography literature reveals that the yield of unsuspected stones ranges from 0.9% to 10% with most authors reporting yields of 3 to 7%.1-5,7,9,13,19,21,22,30-36 The ability to identify these stones, or the lack of them, remains the strongest issue in favor of routine operative cholangiography. Other arguments in favor of intraoperative cholangiography include several important issues. The number and location of common duct stones are easily identified, as are any other pathologic entities that may compromise the choledochal lumen. Intrahepatic lithiasis is most accurately diagnosed by this technique,'5 and although relatively rare in clinical circumstances, has been reported in 8.4% of patients with choledocholithiasis and jaundice at autopsy.37 Even cost-benefit analysis has been applied to advocate routine operative cholangiography.'4 The arguments against the routine use of operative cholangiography are fewer in number, but no less significant. l30'38'39-4 The issue of cost-effectiveness is not clear, since the value of unnecessary choledochotomies performed as a result of routine operative cholangiography in relation to cost-benefit is not well estimated. The issue of the unsuspected stone is even more complex. Assuming the incidence ofunsuspected stones was truly 3 to 7%, an interesting comparison can be made. Only 0.03 to 0.5% of patients without clinical indications for CDE will develop retained stones after cholecystectomy.3' Among those patients who had cholecystectomy and had indications for choledochotomy, but did not have the common duct explored, only 4 to 12% were symptomatic for retained stones.'8'35'42'43 In the study by Jolly and coworkers who were able to get good follow-up data, this figure was only 3.4%.'9 Crump's autopsy series presented common duct stones in 7 to 8% of 1000 necropsies reviewed, specifically seeking stones." Based upon the past 30 years of research and experience in gallbladder disease, and using the above figures, we can estimate that perhaps

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No. of Cholangiograms

LEVINE AND OTHERS

TABLE 4. Review of Literature

Ann.

Surg. * December 1983

True Pos.

False Pos.

True Neg. 97-100% 99% 100% 99% 99% 100% 100% 100% 100%

False Neg. 0-2.6% 0.75% 0%

1% 1.4% 0% 0% 0% 0%

Misleading Index*
0.38 0.28 0.19 0.50 0.19 0.73 0.20

Unsuspected Stones
0.9% 6.0% 6.0% 3% 6.3% 1.8% 3.7% 0.93% 2.3%

Yield of Stones 69.8% 84.6% 65.5% 63.8% 66.9% 60.0% 81.2% 63.8% 68.3%

Skillings et al.' Farha et al.7 Farris et al.9 Pagara et al.'3 Jolly et al.'9 Saltzstein et al.2' Wayne et al.22 Starke et al.30 Present study
*

377 500 400 289 671 423 354

440

166

70% 84% 68% 92% 78-79% 59% 81% 63-69% 84%

30% 16% 23% 8% 21-22% 41% 19% 31-38% 16%

"Misleading" index = Number of patients without clinical indications, with abnormal cholangiography, and a negative CDE/number
no more than one out of ten unsuspected common duct stones will ever be symptomatic. Using data presented by others as well as our own series, we calculated a "misleading" index (Table 4). This value equals the number of patients who had no clinical indications for CDE, had an abnormal cholangiogram, and did not yield stones during choledochotomy divided by the number of patients who had no clinical indications for CDE, had an abnormal cholangiogram, and had choledochotomy performed. This index indicated that 20% of attempts to find unsuspected common duct stones resulted in a negative choledochotomy, and 80% resulted in CDE that yielded stones. If indeed only 10% of these remaining positive choledochotomies would ever be symptomatic if left to their natural course of events, then only 8 out of 100 choledochotomies performed for unsuspected stones benefited the patient-the other 92 patients were exposed to the risk of choledochotomy. The consequences of common duct exploration must be re-emphasized. Multiple studies have demonstrated that choledochotomy increases the mortality of cholecystectomy up to six fold and that morbidity is twice as great.18,26,42,45"7 Furthermore, once the common duct has been manipulated, the incidence of recurrent stones is greatly increased, and any benefit age may have had to protect against obstruction is lost.'9'42'48 This last fact should help to prevent the surgeon from exploring the common ducts of younger patients unless the need is clearly indicated. Age-Sex Analysis Most ofthe age-sex data in the literature was published in the 1940s and 1950s. Recent analysis in light of cholangiography has looked at age, commenting that patients who harbor stones in their common ducts are older than those who have cholelithiasis only.6'9 This information is consistent with our own data. Autopsy studies offered the most information, reviewing large numbers of patients. Crump's review was performed in 1927 at the City Hospital in Vienna, wherein

of patients without clinical indications, with abnormal cholangiography, and a common duct that was explored.

he found that 25% of all patients with cholelithiasis will also have choledocholithiasis and that sex and age did not affect the probability for biliary tract obstruction.44 Kozoll's review from the Cook County Hospital identified the seventh decade as having the predominant incidence of common duct stone, but could not demonstrate a trend based on age.37 It must be considered that autopsy studies of conditions that are not uniformly lethal are biased in age distribution. It has been generally assumed since early studies that the duration of cholelithiasis is directly proportional to the probability of passing a stone into the common duct.28 However, there is recent evidence to question this maxim.6 Applemen and associates extensively reviewed 1127 choledochotomies and among this population noted that the incidence of common duct stones was greater in women than men until the fifth decade.24 In older patients, the incidence was closely equal between the sexes. The tendency for younger populations to pass common duct stones spontaneously has been noted.49 In adolescents, the yield of stones at common duct exploration is frustratingly low.50 This data supports the concept that women tend to develop stones at a younger age than men. Yet, common duct obstruction by these stones does not seem to be temporarized in men, whereas women do have a gap between the mean age for cholelithiasis vs. choledocholithiasis. Interestingly, if obstruction is necessary to cause biliary infection, then the culture results further support these differences. Although statistically insignificant, and for reasons as yet not clarified, premenopausal women may be somewhat protected against common duct obstruction and may be able to pass common duct stones more easily than similarly aged men or other age-sex groups.

Conclusions A review of 589 patients with nonmalignant biliary tract disease is presented. From this data and support from the literature one may conclude that: (1) intra-

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INTRAOPERATIVE CHOLANGIOGRAPHY

697

operative cholangiography can be safely performed; (2) this series does not support routine intraoperative cholangiography as a method to identify unsuspected stones in light of the high number of unnecessary choledochotomies needed to yield significant stones; (3) cholangiography is suggested as a prerequisite to common duct exploration, whether it be in the form of transhepatic, endoscopic retrograde, or intraoperative methods; (4) a normal intraoperative cholangiogram appears to be 100% accurate, and unless clinical indications are truly overwhelming, a normal cholangiogram should sway the surgeon away from performing choledochotomy; and (5) a palpable common duct stone is the best indication for exploring the common duct.

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