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Ann Thorac Surg 2007;83:1096-1101
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Acute Cholecystitis Complicating Cardiac Surgery: Case Series Involving More Than 16,000 Patients

Jurgen Passage, MBBSa,*, Pragnesh Joshi, MS, MCha, Daniel V. Mullany, FJFICMb

a Department of Cardiac Surgery, Prince Charles Hospital, Chermside, Queensland, Australia
b Department of Intensive Care, Prince Charles Hospital, Chermside, Queensland, Australia

Accepted for publication September 14, 2006.

* Address correspondence to Dr Passage, 17/7 Nurmi Ave, Newington, NSW 2127, Australia (Email: jpassage53{at}hotmail.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Acute cholecystitis after cardiac surgery is rare but carries a high mortality. Its management remains controversial.

Methods: We reviewed all cases of calculous cholecystitis (CC) and acalculous cholecystitis (ACC) encountered at our institution over the past 11 years. Data collection included preoperative variables, details of performed procedures, postoperative course, and outcome.

Results: The overall incidence was 0.03% for CC and 0.08% for ACC (5 and 13 of 16,576 patients, respectively). Patients in the ACC group appeared to be sicker patients whereas most patients in the CC group had an uncomplicated recovery from cardiac surgery. The diagnosis was straightforward with typical presentation and ultrasonographic findings in the CC group. In the ACC group, the presentation was less specific, and although useful as diagnostic tool, ultrasonography findings were not as consistent as in the CC group. In the CC group, 3 patients underwent surgery, and 2 patients were treated conservatively. One patient died of cardiac causes after uncomplicated cholecystectomy. In the ACC group, 7 patients were treated medically and 6 patients underwent surgery. The overall mortality was 23% (3 patients). All deaths occurred in patients treated surgically.

Conclusions: Given the low incidence of CC, we do not recommend preoperative screening or intervention for cholelithiasis. Treatment should be according to established guidelines. Patients with ACC, without overt peritonitis, should initially be treated conservatively with appropriate antibiotics. However, failure of significant improvement within 48 hours or a worsening clinical picture should lead to surgical intervention.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Gastrointestinal complications after open heart surgery are rare but confer a high risk of mortality. Reported incidence ranges from 0.5% to 2.1%, and mortality is between 15% and 42% [1–8]. Acute cholecystitis comprises 6% to 18% of these complications [1, 2, 4, 6]. Acute acalculous cholecystitis (ACC) has largely been reported in series of critically ill patients, and its management is controversial [9–13]. The recent occurrence of an unexpectedly high number of patients with acute cholecystitis after open heart surgery in our institution led us to systematically review all cases over the past 11 years. We sought to identify the presence of previously reported risk factors, method of diagnosis, and management instituted, as well as the outcome in this patient cohort.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
The charts of all patients with an International Classification of Diseases code involving any disease of the gallbladder or unspecified gastrointestinal complication during an admission for open heart surgery between 1995 and 2005 were reviewed. A total of 78 patients were identified, and after review of these, 18 patients with a diagnosis of acute cholecystitis were selected for this study. Data collection included preoperative, operative, and postoperative data, diagnostic investigations, treatment instituted for cholecystitis, and outcomes, including complications. Given the different etiology, the data for calculous cholecystitis (CC) and ACC were separately reviewed. The Ethics Committee of our institution approved the study, and individual patient consent was waived.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
From January 1995 and December 2005, a total of 16,576 open heart operations were performed at our institution, with an overall in-hospital mortality of 1.67%.

Calculous Cholecystitis Group
Acute CC developed in 5 patients (CC group) during their recovery from open heart surgery (incidence 0.03%). Four patients were male, and the median age was 68 years. Only 1 patient had a remote history of cholecystitis. Preoperative variables are listed in Table 1.


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  		Table 1 Preoperative Risk Profile
 
One patient underwent isolated coronary artery bypass graft surgery (CABG), 2 patients isolated valve surgery, and 2 patients had a combined procedure. All but 1 patient had the procedure done electively, and there were 2 redo operations. The median cardiopulmonary bypass (CPB) time was 87 minutes (range, 79 to 148), and no patient required placement of an intra-aortic balloon pump. Postoperatively, 1 patient was diagnosed with low cardiac output state and 4 patients had atrial fibrillation. One patient had a deep sternal wound infection. The causative organism was methicillin-resistant Staphylococcus Aureus. Debridement was performed 4 days before he had symptoms and signs of cholecystitis. No other significant cardiovascular complication was encountered in this group. All patients were extubated on the first postoperative day, and the median intensive care unit (ICU) stay was 1 day (range, 1 to 3).

The median time to symptoms of cholecystitis after open heart surgery was 9 days (range, 6 to 15). Right upper quadrant pain and tenderness, nausea, and vomiting were present in all patients. One patient had significant fevers and rigors due to Klebsiella bacteremia. No patient was clinically jaundiced.

Abdominal ultrasonography was performed in all patients within 24 hours of onset of symptoms. Findings are listed in Table 2.


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  		Table 2 Ultrasonographic Findings
 
Laboratory investigations revealed a raised white cell count in 4 patients (white cell count was normal in all 5 patients before open heart surgery). Mixed patterns of mildly raised liver function tests were present in all 5 patients.

Treatment was instituted in all 5 patients after ultrasonography scan confirmed the diagnosis. Laparoscopic cholecystectomy was performed in 3 patients. One of these required conversion to an open procedure owing to technical difficulties. The gallbladder was obviously inflamed in all 3 cases. Histopathologic examination confirmed acute CC in all specimens. In the remaining 2 patients, conservative treatment with antibiotics was commenced.

There was 1 death. This patient underwent redo CABG after presenting with an out-of-hospital cardiac arrest. After uneventful early recovery, he had right upper quadrant pain and tenderness 1 week after surgery. He underwent uncomplicated laparoscopic cholecystectomy 9 days after open heart surgery. Despite an uncomplicated recovery, sudden cardiac death occurred 6 days after the cholecystectomy. A postmortem examination was not performed.

The patient who underwent open cholecystectomy had ongoing problems with abdominal sepsis, related to a Tenckhoff catheter for long-term peritoneal dialysis. He was discharged 1 month after his initial open heart surgery. The remaining 3 patients recovered without any further complications and were discharged 13 to 24 days after surgery.

Acalculous Cholecystitis Group
Thirteen patients were diagnosed with acute ACC (ACC group) after open heart surgery (incidence 0.08%). Nine patients were male, and the median age was 64 years (range, 13 to 76). Preoperative details are listed in Table 1. The details of the performed procedures are listed in Table 3. Four procedures were emergent, and there were 2 redo operations. Median CPB time was 113 minutes (range, 51 to 280). Four patients required placement of an intra-aortic balloon pump, and median duration of support was 5 days (range, 3 to 6). Median ICU stay was 9 days (range, 1 to 54), and median duration of mechanical ventilation was 6 days (range, 1 to 33), with 10 patients ventilated for more than 48 hours after open heart surgery. Postoperative complications are listed in Table 4.


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  		Table 3 Performed Procedures in Acalculous Cholecystitis Group
 

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  		Table 4 Postoperative Complications in Acalculous Cholecystitis Group
 
Median period from open heart surgery to onset of abdominal symptoms and signs was 5 days (range, 1 to 17). Nine patients were in ICU at the time of diagnosis, with 7 patients still on ventilatory support. The most common symptoms were localized right upper quadrant pain and abdominal distension (Table 5).


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  		Table 5 Symptoms and Signs of Acalculous Cholecystitis
 
Abdominal ultrasonography was performed in 12 of the 13 patients within 24 hours of onset of symptoms or signs. Gallbladder distension and thickening of the gallbladder wall were the most common findings (Table 2). At least one abnormal finding was present in all 12 patients, and 2 or more in 8 patients. Three patients also underwent computed tomography (CT) of the abdomen 0 to 3 days after ultrasonography because of suboptimal ultrasonography images in 2 patients, whereas in 1 patient, CT was the first investigation. That showed gallbladder distension in all and wall thickening in 2. In 1 patient, pericholecystic inflammatory stranding was recognized by CT. One patient was diagnosed during emergency laparotomy for ischemic bowel 5 days after open heart surgery without prior imaging.

The median white cell count for the ACC group was 12.3 x 109/L (range, 6.7 to 22.7 x 109/L) and was normal in 6 of 13 patients, whereas in all but 1 patient (with active endocarditis) the white cell count was normal before open heart surgery. Liver function testing revealed a mixed pattern of mildly raised values.

Treatment with antibiotics was commenced within 24 hours of ultrasonography in 10 patients. In 1 patient, antibiotics were commenced 5 days after ultrasonography. Six patients underwent surgery 0 to 11 days after ultrasonography. One patient underwent laparoscopic cholecystectomy immediately after ultrasonography. In the patient who was diagnosed during laparotomy for ischemic bowel, cholecystectomy was performed concomitantly 5 days after open heart surgery. In a further 2 patients, laparoscopic cholecystectomy was carried out 2 days after commencement of antibiotics without improvement.

One patient had laparoscopic cholecystectomy 11 days after diagnosis of acute ACC. In this patient endoscopic retrograde cholangiopancreaticography and bilary duct stent placement was initially performed on 2 separate occasions, without improvement. Findings at surgery included extensive gallbladder necrosis with perforation and generalized peritonitis.

One patient had laparoscopic surgery 7 days after ultrasonography and failure to respond to antibiotic treatment. Tube cholecystostomy only was performed due to hemodynamic instability intraoperatively. Symptoms improved, and the tube was removed uneventfully 4 weeks after surgery. One patient underwent diagnostic laparoscopy and peritoneal lavage alone, as mild edema of the gallbladder was the only finding at surgery. This patient recovered without complications.

There were 3 deaths (23% mortality). All deaths occurred in patients who underwent surgical intervention. The first fatal outcome occurred in the patient who had ischemic bowel on the fifth postoperative day despite uncomplicated early recovery from elective CABG. Multiple further surgical interventions were performed owing to complications arising from bowel surgery. Intractable gastrointestinal bleeding developed, and the patient died 40 days after his initial open heart surgery.

The second death was of the patient who had delayed cholecystectomy after bilary duct stent placement. This patient underwent bilateral sequential lung transplantation for end-stage chronic obstructive lung disease. Onset of jaundice, diffuse abdominal pain, and tenderness was noted 5 days after surgery. Ultrasonography scan revealed a distended gallbladder with normal wall thickness and no evidence of pericholecystic fluid. Abdominal CT confirmed these findings. Obstructive jaundice was diagnosed and endoscopic retrograde cholangiopancreaticography with bilary duct stent placement was performed on days 7 and 8 after onset of symptoms. The patient’s clinical condition worsened, and repeat ultrasonography revealed a markedly thickened gallbladder wall and free fluid. During laparoscopic cholecystectomy, gangrenous cholecystitis with extensive perforation was noted. The postoperative period was complicated by septic shock and respiratory failure due to aspiration pneumonia. The patient died of multiorgan failure 10 weeks after open heart surgery.

The third death was a patient who underwent emergency CABG and mitral valve repair after a large myocardial infarction complicated by acute mitral insufficiency. The patient required inotropic support, intra-aortic balloon pump placement, and mechanical ventilation preoperatively. The postoperative period was complicated by prolonged low cardiac output state, acute renal failure, atrial dysrhythmias, and peripheral arterial embolization. The patient had right upper quadrant pain and abdominal distension on the second postoperative day. Ultrasonography scan showed a small gallbladder with a thickened wall. Antibiotic therapy was commenced without clinical benefit, and the patient underwent laparoscopic cholecystectomy 6 days after open heart surgery. At surgery, a gangrenous gallbladder was noted. The postoperative period was complicated by persistent low cardiac output and subsequent multiorgan failure. The patient died 9 days after open heart surgery.

The remaining 3 surgically treated patients suffered no further gall bladder–related complications. They were discharged from ICU at 13, 21, and 62 days after open heart surgery, respectively. Cardiac failure requiring inotropic support was the main cause of prolonged ICU stay in 2 of these patients, whereas 1 patient had suffered a stroke after open heart surgery and required ventilation for a prolonged period.

In the patients treated with antibiotics alone, the abdominal symptoms and signs resolved. The ICU stay ranged from 1 to 33 days (median, 8) after open heart surgery, with cardiac failure being the main contributing factor to longer ICU admissions.

There appeared to be no difference in clinical presentation or results of imaging performed in the surgically treated group compared with the conservatively treated group. The occurrence of complications after open heart surgery was comparable in both groups.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Calculous Cholecystitis Group
The incidence of acute CC complicating open heart surgery in our study was exceedingly low. Patients suffering this complication generally had an uncomplicated course after open heart surgery, and their preoperative cardiovascular risk profile appeared to be better than that in patients in the ACC group. The presenting symptoms and signs were consistent with acute CC in all patients, and the diagnosis was confirmed by ultrasonography scan. The only death occurred in a patient with a likely cardiac substrate for fatal dysrhythmia. The outcome for the 4 survivors was similar in the surgically and medically managed patients. Which treatment strategy was chosen was totally at the discretion of the consulted general surgeon. No differences in the clinical status or investigation results were apparent between surgically and medically managed patients.

Previous publications have recommended the simultaneous surgical treatment of cholelithiasis and cardiac conditions or cholecystectomy before elective cardiac surgery [14, 15]. There are also reports demonstrating a higher prevalence of cholelithiasis in patients after open heart surgery [16]. However, the prevalence of cholelithiasis in the general population is reported to be between 9% and 15% [17–19] and only 1.5% to 2% of patients a year become symptomatic [20]. Assuming a prevalence of 10% in our study population, 1,660 patients would require additional cholecystectomy either before or combined with open heart surgery.

Although cholelithiasis is common in the general population, our results suggest that it rarely leads to complications in the postoperative period after open heart surgery. We therefore do not recommend preoperative screening or preemptive cholecystectomy. In the rare event of CC complicating open heart surgery, we recommend treatment according to guidelines for this condition.

Acalculous Cholecystitis Group
Acalculous cholecystitis is largely a disease of critically ill patients. Reported risk factors include major surgery, trauma, and thermal injuries [9, 10, 13]. A recent trend to an increase in incidence has been reported by several authors [9, 21]. This trend is also apparent in our series, with 8 of the 13 cases occurring within the last 2 years.

The pathogenesis of acute ACC is not clearly delineated but is likely to be multifactorial. Bile stasis due to increased viscosity of bile and ampullary constriction due to narcotic analgesia can lead to distension of the gallbladder, with increased wall pressure. Positive pressure ventilation has been shown in experimental studies to increase intraluminal pressure in the common bile duct and contributes to increased pressure of the gallbladder wall [22]. Visceral hypoperfusion in the postoperative period due to low cardiac output syndrome has been documented as a risk factor for the development of ACC [13, 23]. The combination of increased wall tension of the gallbladder wall and hypoperfusion potentially leads to ischemia of the gallbladder mucosa, a likely central part of the pathogenesis of ACC. This is supported by a series of angiographic studies of ACC gallbladder specimens, showing multiple arterial occlusions and absent or minimal venous filling [24]. The release of cytokines such as factor XII and platelet-activating factor due to surgical trauma have also been implicated in the development of ACC [25, 26].

Similarly to previous reports, we found that ACC occurred most frequently in critically ill patients. In our opinion, it represents a consequence of the critical condition of the affected patients. Nine of the 13 patients with ACC were diagnosed with low cardiac output state after their open heart surgery and required prolonged use of inotropes and vasopressors (>48 hours). Ten patients were on prolonged positive pressure ventilatory support (>48 hours). We also noted that a disproportionally high number of patients (4 of 13 patients) required intra-aortic balloon pump support after open heart surgery. Prolonged CPB time has been suggested to increase the incidence of major gastrointestinal complications after open heart surgery [2, 7, 27–29]. However, other studies found no significant differences in the frequency of gastrointestinal complications in patients undergoing open heart surgery with and without CPB [30]. In our cohort, the median CPB time in patients with ACC was longer than in patients with CC (113 minutes [range, 51 to 280] versus 87 minutes [range, 79 to 148]).

The diagnosis of ACC in the critically ill patient is challenging. Clinical evaluation is hampered by alterations in mental status due to sedation, analgesia, and communication problems because of mechanical ventilation. Classical signs and symptoms of acute cholecystitis such as right upper quadrant pain with tenderness, nausea, and vomiting were not found to be reliably present in previous series [10, 13, 27]. We describe similar findings (Table 5).

Laboratory findings were similarly nondiagnostic. A mild leukocytosis was present in most but appeared to be temporary, unrelated to the development of ACC in the absence of perforation. Mixed abnormalities of liver function tests were found in the majority of cases, but were again nonspecific. These findings are in keeping with previous publications [10, 13, 27].

No consensus exists in the imaging modality of choice. Suggested radiologic investigations include ultrasonography, CT, and radionuclide studies [9, 13, 27]. Sensitivity of ultrasonography in the diagnosis of ACC has been reported between 30% and 100%, with specificity ranging from 80% to 94% [9, 31, 32]. Positive findings include gallbladder distension, wall thickening, and sludge formation. In our patient cohort, ultrasonography was performed in 12 of the 13 cases (Table 2). In 11 of 12 patients, treatment for ACC was commenced after the first ultrasonography study. Computed tomography scanning was performed in 3 patients in addition to ultrasonography. That was helpful in cases with limited ultrasonography. No patient underwent radionuclide studies.

We believe that ultrasonography should be the first imaging investigation as it easily performed at the bed side and in our experience was diagnostic in 10 of 12 patients. Computed tomography is helpful in patients with poor images. However, negative imaging should not be used to exclude ACC if clinical findings are suggestive, as false negative studies are possible and delay in treatment may have dire consequences. Laparoscopy should be performed if possible in any case with a doubtful diagnosis and no response to antibiotics, allowing treatment in the form of cholecystectomy.

The overall mortality in our study was 23% (3 of 13 patients), which compares favorably with other reports [10, 13, 27, 33]. All deaths occurred in patients treated with cholecystectomy. However, in none of these patients do we consider the surgical intervention for ACC per se as the primary cause of death. Surgical intervention was delayed in 2 of the 3 patients who died, and in both, the gallbladder was found to be gangrenous, with peritonitis due to perforation in 1 patient. Earlier surgical treatment may have prevented this deterioration. It also has to be recognized that our cohort, as those in other reports of this condition, represents a group of patients with a high mortality rate even in the absence of cholecystitis.

Given the favorable outcome of patients treated conservatively, we believe that antibiotic treatment should be commenced in all patients with a suspected diagnosis of ACC. This should be directed against the most common bacteria isolated from bile in acute cholecystitis (Escherichia coli, Klebsiella species, and Enterococcus faecalis) and also cover anaerobes such as Clostridia and Bacteroides species [9]. However, in light of the complications seen in patients with delayed surgical intervention, we strongly recommend early surgery if no significant improvement is seen within 1 to 2 days of antibiotic treatment.

As in many published reports, laparoscopic cholecystectomy was the procedure of choice in our series [9, 13, 21, 27]. Percutaneous transhepatic cholecystostomy has been utilized with good results in 2 series and offers a valid alternative, particularly in patients deemed to unstable to undergo laparoscopic intervention. It is less invasive and has the advantage of being able to be performed at the patient’s bedside in the ICU [12, 34]. Yang and colleagues [11] used laparoscopic cholecystostomy in 6 patients with ACC without morbidity or mortality. In our opinion, that offers no advantage as laparoscopy is still required, and the procedure is contraindicated in patients with a gangrenous gallbladder, encountered in 4 of 13 patients with ACC in our series.

We recognize the limitations of retrospective analysis of a small number of cases, a problem common to most other studies of this condition owing to its rarity. This also precluded statistical analysis comparing the frequency of risk factors, operative variables, occurrence of postoperative complications, and mortality between our patient cohort and the entire group of patients undergoing open heart surgery during the study period. We believe, however, that this review is useful for establishing a more standardized approach to treating this entity.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
The authors would like to thank Dr Kylie Passage for her help in editing the manuscript, as well as the following surgeons, whose patients were included in this study: Drs John Dunning, Peter Tesar, Peter Pohlner, Homayoun Jalali, Trevor Fayers, Robert Tam, Alan Gale, Graeme Hart, and Andrew Clarke.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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