Acute cholecystitis in the sick patient.

Current Problems in Surgery 51 (2014) 441–466

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Current Problems in Surgery journal homepage: www.elsevier.com/locate/cpsurg

Acute cholecystitis in the sick patient Introduction The management strategies for patients with acute cholecystitis (AC) have evolved over time. Before the 1970s, management of AC involved initial treatment of the inflammation with antibiotics and then elective removal of the gall bladder 4-6 weeks after the emergent episode. In the 1970s and 1980s, this paradigm began to change and earlier open cholecystectomy became the treatment of choice. This more expedient approach allowed early cessation of the patient's pain, a decreased hospital length of stay, and a minimization of the complications associated with failed nonoperative management. Currently, studies demonstrated no difference in the amount of hemorrhage or the length of surgery of earlier vs delayed open cholecystectomy.1-7 After 1990, laparoscopic cholecystectomy (LC) became the preferred method for removal of the gall bladder. Initially, AC was considered a contraindication to LC because of higher conversion rates and an increased risk of complications.8 However, as laparoscopic expertise accrued, the equipment improved and the conversion rates and complications for earlier LC in the setting of AC decreased. A further advance assisting the safety of early LC was the concept of visualizing a “critical view of safety” as advocated by Strasberg and colleagues.9 Currently, LC has become the treatment of choice for AC,2,10 as it allows a shorter hospital stay, quicker recovery, and a reduction in overall medical costs.11-14 In relatively unusual circumstances, such as intraabdominal adhesions or inability to tolerate pneumoperitoneum, patients receive open cholecystectomy instead of LC. The magnitude of biliary disease has become enormous in recent years as LC has become a common major abdominal operation in the Western Hemisphere.15 In the United States alone, gallstone disease affects more than 20 million people and is associated with $6.3 billion in direct costs annually.16 One factor that may contribute to these costs is the high rate of recurrence after initial presentation of biliary symptoms, as they are 6%-50% for AC,17,18 5.3%-50% for common bile duct stones,19-21 and 16%-76% for gallstone pancreatitis.22-27 To prevent recurrent symptoms, patients are now treated with cholecystectomy within 48 hours of presentation for AC and evidence of mild gallstone pancreatitis.28,29 Despite the apparent benefit of early surgery in AC, only 40%-75% of patients with AC, gallstone pancreatitis, and common bile duct stones undergo cholecystectomy on initial hospitalization.30,31 The predominant reason is not entirely clear. In any surgically treated disease, the operation may be deferred owing to patient refusal, surgeon refusal, or anesthesiologist refusal. Personal reasons by any of the mentioned parties aside, the most

http://dx.doi.org/10.1067/j.cpsurg.2014.10.003 0011-3840/& 2014 Elsevier Inc. All rights reserved.

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S.R. Eachempati et al. / Current Problems in Surgery 51 (2014) 441–466

likely reason LC is not routinely performed at the initial indication is a perception that the patient is too “sick” or has too many medical conditions to undergo that operation at that particular time. These conditions can be short-term or long-term medical illnesses and may be either reversible or irreversible. An example of a short-term medical illness might be a pneumonia, which is often a reversible process, whereas CHF is an example of a chronic medical condition. The former process can be treated completely before an elective operation, whereas the latter one can never be fully treated and must be managed during an elective operation. Surgery is not benign for the “sick” patient. Although operation may be a better option for removing pathology and restoring the patient to a disease-free state, the actual act of operation confers a physiological insult owing to the tissue injury required by the operation or from the vasodilatory effects of general anesthesia. Importantly, the detrimental effects of both the operation and the anesthesia can occur after the actual operation has finished, as patients may have fatigability, pain, atelectasis, hypovolemia, or complications that may further delay the recovery. Anticipating the postoperative course of the patient is as important as assessing the intraoperative ability for a patient to tolerate the dissection and anesthesia of a procedure. This issue is magnified in the “sick” patient.

Who is the “sick patient” with AC? Defining who is “too sick” for any given operation potentially teems with subjectivity. All operations including LC may be associated with notable morbidity and mortality in certain highrisk patients. Some of the risk factors for these patients are short term in nature and sometimes the risks are more long term. The acute illnesses that complicate the decision for LC include those that are being actively treated in the hospital and those that can be managed outside the hospital. The former category would include relatively low mortality conditions that are being actively treated in the hospital, such as pneumonia in a younger patient, or a condition not requiring hospitalization, such as a case of outpatient influenza. In this instance, AC is potentially severe but has a high chance of resolution with treatment and that after successful treatment and time, the patient would reach a state where elective operation could proceed with no anticipated complications. In the case of the patient with pneumonia, the patient could be treated with antibiotics initially and if the gall bladder symptoms improved, the patient could be treated with elective LC as an outpatient. If the AC does not improve, the gall bladder could be removed after improvement in the pneumonia without a prolonged interval. Rarely, in this example, the patient would need a drainage procedure such as a percutaneous placed catheter (drainage) as the patient would most likely be able to tolerate operation in the near term with no contraindications. However, in some cases, the patient has a life-threatening disease that is being actively managed and LC is not safe in the near term. The spectrum of these diseases is enormous and includes myocardial infarction (MI) or active treatment for cancer. An example of the latter situation includes a patient with a lethal condition such as leukemia that requires chemotherapy when the patient presents with AC. This therapy could even be giving the patient a relative contraindication to any operation because of neutropenia or thrombocytopenia. Initially, this patient would receive medical therapy such as antibiotics and pain control, but if this approach were to fail, the patient might have no definitive option for treatment of the AC in the near term and would likely be a candidate for nonsurgical invasive treatment. Many of these cases are determined on an individual basis, but the underlying strategy involves decompressing the gall bladder and treating any concomitant infection. In addition to severe acute conditions, many chronic conditions that are not being optimally controlled could complicate the approach to AC. Many of these conditions are age related and manifest in various degrees of morbidity. The age-related changes can include pathologic alterations to the cardiovascular, cerebrovascular, pulmonary, immunologic, and renal systems of the patient.32,33 The resulting debilities yield potential increases in perioperative complications, such as MI, congestive cardiac failure, stroke, pneumonia, or atelectasis.34,35


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Different organizations have tried to define the risk stratification of a patient who is undergoing a given operation such as LC. The stratifications can be by a general assessment, the age of the patient, or the influence of a particular severe organ-specific disease. A discussion of some of the stratification systems and individual processes is warranted to understand who is the “sick” patient with AC. American Society of Anesthesiologists class One of the most widely used systems of assigning surgical risk is the American Society of Anesthesiologists (ASA) class (Table 1). This method describes a patient in 1 of 6 categories of physical status ranging from “status 1”,or a healthy patient, to “status 6”, a brain-dead patient undergoing organ donation (Table 1). The original classification system was created in 194136 and has subsequently undergone modifications.37 Retrospective analysis of 108,878 operations revealed that ASA class 4 was associated with a mortality rate that ranged from 10%-30%.38 Another retrospective study of 5878 surgical patients revealed ASA to be correlated with postoperative outcomes.39 The simplicity of the ASA system explains its widespread use, but this same simplicity creates some limitations. The ASA classification system does not take into account operative factors such as the nature of the operation, the experience of the anesthesiologist or the operation, or the type of facility in which the operation is being performed.40 Another limitation of the ASA system is that it does not specifically account for patient factors such as age, sex, body mass index, or pregnancy. In addition, individualized physiological criteria, such as preoperative blood pressure or heart rate, are not weighted. Finally, the classifications allows for perhaps too much subjectivity as multiple practitioners may give different ASA levels to the same patient for the same operation. The ASA class has been studied with respect to biliary disease. A study of the National Surgical Quality Improvement Program (NSQIP) database from 2005-2008 revealed that, of the 65,511 cholecystectomies performed, 58.2% were on patients classified as ASA 2, whereas 2.6% were performed on patients classified as ASA 4.41 This discrepancy in the number of patients belonging to each group may result from some clinician bias in management of sicker patients, as some high-risk patients with AC who are described as ASA 4 may preferentially undergo percutaneous cholecystostomy (PC) instead of operative cholecystectomy. In a retrospective study of 61 high-risk patients treated for AC from 2005-2010, 80% of those who were ASA 4 received PC, as compared with just 4% among those who were ASA 3.42 In addition, this study showed no difference in age, Acute Physiologic Assessment and Chronic Health Evaluation II (APACHE II) score, Physiological and Operative Severity Score for the enumeration of Mortality and Morbidity, or severity of cholecystitis between the percutaneous group and the cholecystectomy group. The authors also noted a 17.2% mortality rate in the percutaneous intervention–treated group compared with no deaths in the cholecystectomytreated group. As no prospective randomized studies evaluating outcome after cholecystectomy in patients who are ASA class 4 are available, this classification alone should not be used to determine operative risk in patients with AC. Therefore, other factors must be examined to create a more accurate risk stratification system. Table 1 American Society of Anesthesiologists (ASA) classification system ASA ASA ASA ASA ASA ASA

physical physical physical physical physical physical

status status status status status status

1 2 3 4 5 6

A A A A A A

normal healthy patient patient with mild systemic disease patient with severe systemic disease patient with severe systemic disease, which is a constant threat to life moribund patient who is not expected to survive without the operation declared brain-dead patient whose organs are being removed for donor purposes

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Age A patient's age is also often used both formally and informally to gauge operative risk. The data suggesting age alone is a major risk factor for morbidity with AC have been mixed. In a series, an elderly patient undergoing either a semielective cholecystectomy or an outpatient elective cholecystectomy could maintain similar outcomes to younger patients.43 Again, however, the nature of this study and its mostly elective population is flawed by the potential of investigator bias. For other patients with AC, some studies reinforce that early cholecystectomy can be performed safely in the elderly population with some selection.44-46 Nonetheless, this practice still has been shown to be accompanied by more risk than seen in younger patients, as the elderly patients in some studies were documented to possess more comorbidities and decreased physiological reserve.47,48 Although most cholecystectomies can be completed laparoscopically in the elderly, a minority will require conversion to an open approach, which dramatically increases the risk of cardiopulmonary complications. According to a retrospective study of 411 patients treated for AC, 17% were 80 years or older.49 These elderly patients were more likely to present with gangrenous cholecystitis. They also experienced more complications and had increased mortality. After adjusting for comorbidities, age was still found to be independently associated with poor outcomes after cholecystectomy. A recent review noted that the elderly patient with acute AC may have a high morbidity rate of up to 51% and mortality rate as high as 34%. Consequently, these authors recommended that early cholecystectomy be performed in elderly patients as soon as they are found to have symptomatic gallstones, if no contraindications exist, to prevent the increased complications seen after the development of AC.43 Other studies revealed slightly more contrasting results in different population groups of highrisk patients with biliary disease. A large NSQIP study on 15,248 patients aged 65 years or older who underwent elective cholecystectomy revealed that the overall mortality rate was 0.9%.50 In this study, elective ambulatory cholecystectomy was associated with decreased mortality and decreased complications. A study of 29,818 Medicare patients admitted for AC revealed that 25% of patients did not undergo cholecystectomy at their first admission and that this was associated with a 38% gallstone-related readmission rate compared with a 4% readmission rate, in those who received cholecystectomy.51 Failure to perform cholecystectomy was associated with an increased 2-year mortality of approximately 20%. These data implied that LC should be performed in the elderly early in the disease process and that delaying definitive operation was associated with increased morbidity and mortality. However, attributable mortality was not studied and operations may have been purposely avoided in sicker patients. Other data have demonstrated that patients older than 70 years who require emergent abdominal operation with ASA scores of 3 or 4 have reported mortalities of 31% and 57%, respectively. Morbidity rates for ASA 3 or 4 patients have been reported as 63% and 100% respectively.52 Overall, these studies and others in different populations and surgical groups have tried to determine the perioperative relative risk. The timing of death in patients with terminal cancer, Gold stage IV chronic obstructive pulmonary disease (COPD), New York Heart Association class IV heart failure, or end-stage hepatic failure is impossible to predict. The risk and benefits of operation must be weighed against the risk of recurrent biliary tract disease. Although LC appears to be better tolerated, there is always the risk that safe gall bladder removal would require conversion to an open procedure. The risks of operation in patients with multiple comorbidities are difficult to quantify. The American College of Surgeons has published an online calculator for operative risk (http:// riskcalculator.facs.org/) to give the physician more accurate information regarding risk of potential adverse events and allow frank conversations between physicians and patients. Although this risk calculator may be a valuable tool when discussing treatment options with patients, it is only an estimate. The only justifiable conclusion is that whenever possible, if operation is being considered for high-risk patients, medical optimization is recommended to lower the risk of operation, unless the surgery is absolutely immediately necessary.


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Coronary artery disease Although the presence of severe cardiovascular disease was considered a relative contraindication to performing cholecystectomy in the past, the data have been mixed.53,54 According to a NSQIP study, of 65,511 cholecystectomies performed between 2005 and 2008, 0.71% of patients had congestive heart failure. In the same study, patients with ischemic heart disease after emergency operation experienced a 14% mortality rate.53 Given this high mortality rate, patients with AC and ischemic heart disease would apparently be better served by PC tube than more invasive surgery. However, a retrospective study of patients who underwent LC comparing patients with and without severe coronary artery disease (CAD) revealed no significant difference in mortality rates between the 2 groups. The patients with severe cardiovascular disease did experience a longer hospital stay, but there was no significant difference in the morbidity rate.54 Recently, other studies have shown that LC may be performed in patients with severe CAD and even left ventricular assist devices.55-58 A case review of 15 patients who underwent placement of an intra-aortic balloon pump to augment their cardiac function before cholecystectomy revealed a reasonable mortality rate of 13%.59 A study of cholecystectomy in patients who received heart transplants showed that 72.2% were operated on for AC, with an overall mortality rate of 2.2%. Interestingly, the mortality rate was higher for open cholecystectomy than for and was also significantly higher in emergent cases compared with elective cases.60 Given the high mortality rate associated with emergent operations in this group of patients, these data suggest that elective cholecystectomy before the development of AC should be considered. Optimizing and assessing the patient with CAD who is a potential candidate for cholecystectomy has been studied.61-67 The American College of Cardiology and the American Heart Association 2007 Guidelines recommend waiting 4-6 weeks for elective operation in patients with severe CAD.66 Livhits and colleagues retrospectively analyzed the California Patient Discharge Database for patients undergoing common elective procedures with and without MI and found that, for patients undergoing cholecystectomy, the rate and relative risk of another postoperative MI did not decrease significantly until 60 days after MI. The 30-day mortality risk was greatest when cholecystectomy was performed within 30 days of MI, and this risk did not wane until after 60 days (Table 2). Consequently, these authors recommended delaying any elective operation for at least 8 weeks and considering medical optimization during this interval.67 As mentioned several risk calculators have been developed to estimate the risk of perioperative MI or cardiac arrest.61-65 The American College of Surgeons recently developed a risk calculator risk index that showed ASA class, dependent functional status, age, abnormal creatinine (4 1.5mg/dL), and type of surgery were associated with cardiac risk after surgery.41 Although these risk calculators yield potentially important information for patient counseling, they offer no guide about how to improve the patient's likelihood of undergoing operation successfully.

Table 2 Post-myocardial infarction (MI) results from time of MI until cholecystectomy

0-30 d 31-60 d 61-90 d 91-180 d 181-365 d No recent MI

30-d MI (%)

30-d Mortality (%)

1-y Mortality (%)

28.8 17.8 6.5 5.7 3.9 0.9

10.5 6.9 5.9 4.8 5.9 2.3

28.0 26.4 19.9 18.7 19.2 8.0

Reproduced with permission from Livhits et al.67

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Chronic obstructive pulmonary disease Several features of COPD render it a major risk factor for patients undergoing LC. Insufflation during laparoscopic surgery is associated with adverse effects on pulmonary function and these effects are more pronounced in patients with COPD. Additionally, the patients may be more likely to be less mobile and be more likely to have thromboembolic complications after operation. The patients may wait longer to undergo elective operation and be more likely to have longer operative times or more chance of conversion than an open operation. Data have shown patients with COPD to be at potentially higher risk for LC. According to the NSQIP database, among cholecystectomy procedures performed between 2005 and 2008, 2.6% were in patients with COPD. In a retrospective review of patients who underwent emergency operation, the mortality rate among patients with COPD was 12%.53 A case-control study was performed to evaluate outcomes after LC in patients with COPD.68 There were no deaths in either group and the length of surgery and length of hospital stay were not significantly different. The end-tidal CO2 was higher in the COPD group, but this feature did not appear to affect morbidity or length of stay. These data suggest that in patients with COPD, LC in an elective setting should be given consideration for appropriately selected patients.

Cirrhosis The influence of cirrhosis on biliary disease has been studied extensively.69-72 Owing to the past associations with higher mortality, cirrhosis has been considered a relative contraindication to cholecystectomy. Interestingly, the prevalence of gallstones in patients with cirrhosis is 3 times higher than in noncirrhotic patients, but the pathophysiology of this association has never been elucidated.69,70 However, recent experience has changed the opinion that surgery should be absolutely avoided in cirrhotic patients. The major reason for this change has most likely been the extensive experience clinicians have garnered in treating critically ill patients during hepatic transplantation and using those principles of perioperative care in patients with biliary disease. A meta-analysis of 3 randomized controlled trials comparing laparoscopic and open cholecystectomy in patients with cirrhosis revealed decreased complications and shorter length of stay in the laparoscopic group.71 In this study, there was no significant difference in ChildTurcotte-Pugh (CTP) class between laparoscopic and open groups. Clearly, certain factors influence the likelihood of poor outcomes for biliary surgery in patients with cirrhosis. The rate of postoperative hepatic insufficiency was higher in the open cholecystectomy group, but this was not statistically significant. A retrospective review of 94 cirrhotic patients who underwent LC showed that operation could be performed but the conversion rate was 11% and that 4 of the 94 patients died. The mortality rate in patients who were CTP class C was 100%. After analysis, factors associated with increased morbidity are low serum albumin level, elevated international normalized ratio, CTP, and number of red blood cell transfusions.72 The Model for End-Stage Liver Disease score was not associated with mortality, but was associated with morbidity. Another retrospective review of 220 cirrhotic patients who received LC revealed that preoperative Model for End-Stage Liver Disease score greater than 13 was a predictor of complications whereas CTP class was not.73 Given these data in aggregate, one concludes that LC may be performed safely in cirrhotic patients, but these patients should be highly selected and optimized for operation. Additionally, we would recommend that cirrhotic patients who receive elective operation should receive their care in centers experienced in hepatic transplantation.

End-stage renal disease End-stage renal disease (ESRD) combined with biliary disease has been studied. ESRD affects approximately 900,000 people in the United States and patients requiring hemodialysis have a


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higher prevalence of gallstones than the general population.74 According to the NSQIP database, of the 65,511 cholecystectomy procedures performed from 2005-2008, 1% were in patients with ESRD.41 The adverse effects of ESRD on the treatment of AC have been difficult to quantify because the studied populations have been so heterogeneous. ESRD has been shown to have a negative influence on the morbidity associated with AC, as shown by a retrospective study of patients on hemodialysis who received abdominal surgery showed a 70% mortality rate for those who received emergency surgery compared with a 10% mortality rate for those who underwent elective operation.75 Outcomes after LC for gall bladder lesions, not necessarily with AC, have been studied in patients with and without ESRD. In 1 study, the results revealed no significant difference in morbidity, mortality, or length of stay between groups.76 These data would indicate that ESRD alone is not a contraindication to LC in selected patients. Although patients with ESRD can be routinely prepared for an elective procedure, performing any emergency or even urgent operation, including LC, in patients with ESRD may be logistically difficult. The patients may need hemodialysis before general anesthesia owing to electrolyte abnormalities or severe acidosis. The decreased platelet function in patients with ESRD may complicate hemostasis efforts during any operation. In an operation for AC in which a severe inflammatory response may dominate the view of the entire operative field, a lack of hemostasis may be particularly profound. Inability to visualize the essential field can lead to increased blood loss, length of surgery, conversion to open surgery owing to poor visualization, and perioperative complications. Given these potential difficulties with emergency operation in patients with ESRD, some clinicians have preferred PC in high-risk patients with AC. Independent of the method of treatment, the morbidity and mortality of patients with AC and ESRD can be prominent. In a study of ASA class 4 patients with ESRD and AC, all the patients underwent PC as first-line therapy, with a 21% mortality rate.77 Another study compared outcomes after PC and cholecystectomy and showed no significant difference in overall morbidity or mortality in patients on chronic hemodialysis who presented with AC. The authors also showed that the outcomes were not influenced by severity of illness as they found no significant difference in ASA class, APACHE II score, or comorbidities between groups.78 Although not statistically significant, AC-attributable mortality was higher in the PC group than in the cholecystectomy group. The length of stay was also higher in the PC group. Further conclusions were difficult to draw as the populations were not randomized and the clinicians may have opted for the PC in certain patients for reasons not captured by the study.

Cerebrovascular disease The concept of cerebral autoregulation maintains that intrinsic factors in the brain allow cerebral blood flow to be relatively constant over a wide range of systemic blood pressures. Following a stroke, this cerebral autoregulation is demonstrably impaired over an indeterminate time course.79 Aries and colleagues80 examined the extent of autoregulation impairment after stroke and its course over time by reviewing transcranial Doppler studies of cerebral autoregulation in the setting of documented ischemic stroke. These authors concluded that there was a progressive deterioration of cerebral autoregulation in the first 5 days after stroke, and full recovery back to baseline of cerebral autoregulation required at least 3 months. To understand the risks of stroke on planned elective operations such as LC, one must understand some other intricacies of cerebral physiology. After a stroke, the brain must recover sufficiently from its past cellular ischemia and inflammation before further encountering any metabolic stressors such as the hemodynamic alterations associated with surgery and anesthesia. Unfortunately, concrete recommendations regarding the safety of an elective procedure following stroke are largely nonspecific and based on minimally stratified observations. Although no relevant studies specifically examined the safety of LC after stroke, a recent investigation of the association between prior stroke and the risk of major adverse

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cardiovascular events was performed in a large and unselected cohort of patients undergoing noncardiac elective operation.81 These authors found that prior ischemic stroke was associated with an adjusted 1.8- and 4.8-fold increased relative risk of 30-day mortality and 30-day major adverse cardiovascular events, respectively, compared with patients without prior stroke. These findings mirrored the observations studying the normalcy of cerebral autoregulation impairment after stroke, as patients in this study with strokes were at particularly high risk for morbidity for the first 3 months after the stroke and the risks did not fully decrease until approximately 9 months after stroke. Interestingly, the increased relative risk associated with a prior stroke did not seem to differ between low or intermediate-risk operations and high-risk operations. Consequently, the recommendation can be made that patients who have had a prior stroke remain at substantially higher risk for an adverse outcome following surgery and that whenever possible, elective surgery should be delayed to least 3 months and preferably 9 months following the stroke.

Critical illness Although any patient can theoretically be at risk for acute calculous cholecystitis, critically ill patients have been shown to be at risk for potentially lethal acalculous cholecystitis.82,83 A retrospective review of critically ill patients with acalculous cholecystitis who underwent cholecystectomy (all were performed open) revealed a mortality rate of 44%.84 These patients had a mean APACHE II score of 25 and 64% had multi-organ failure on the day of cholecystectomy. The most common organ systems to be affected were respiratory and cardiovascular systems. Although the APACHE II and the Simplified Acute Physiology Score II scores were not significantly different between survivors and nonsurvivors, the Sequential Organ Failure Assessment score was. These data indicate that the “sickest of the sick” critically ill patients appear to be at the highest risk for some form of AC in intensive care units.

Acalculous cholecystitis Acalculous cholecystitis possesses a pathophysiology, a set of risk factors, disease course, prognosis, and treatment that differ from that of acute calculous cholecystitis. Gallstones are the most common cause of AC, but acute acalculous cholecystitis (AAC) most often occurs in sicker patients, including the elderly, those in intensive care units, or those with multiple comorbidities.85 Frequent populations cited at risk for AAC include patients with trauma, burns, recent surgery, abdominal infection, diabetes mellitus, abdominal vasculitis,86 ESRD,87 congestive heart failure, and recent resuscitation from cardiac or hemorrhagic shock.85,88 Other groups for this disease include patients with cancer either from metastases to the porta hepatis 89 or acute myelogenous leukemia90 and bone marrow transplant patients who have been reported to have as high as a 4% rate of acalculous cholecystitis.91 Certain risks and causes of AAC have been described.85 Bile stasis and gall bladder ischemia have been implicated in the pathogenesis of AAC. Volume depletion, use of opioid analgesics, total parenteral nutrition, and even mechanical ventilation with positive end-expiratory pressure may result in bile stasis and increase in intraluminal bile duct pressure. Perfusion may be further decreased by hypotension or the administration of vasoactive drugs. Reperfusion injury has been suggested as another factor in the development of AAC.85 Regardless of the inciting cause, AAC appears to be because of failure of the gall bladder microcirculation with cellular hypoxia.92 This observation is supported by the pathologic observation of high rates of gall bladder necrosis and perforation in patients with AAC compared with those with calculous cholecystitis.93,94 Further supporting the finding that AAC results from ischemia are the differences in gall bladder arteriography between acute calculous cholecystitis and AAC.83 Interestingly, gall bladders with gallstone disease have been shown to have arterial dilatation and extensive venous filling consistent with acute inflammation, whereas AAC gall bladders


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have multiple arterial occlusions and minimal-to-absent venous filling consistent with ischemia. With the high mortality rate associated with cholecystectomy in patients with AAC, PC with delayed cholecystectomy has been historically performed for this disease process.95 The diagnosis can be made with ultrasound (Fig 1) but is often made with computed tomography scanning as the clinicians are trying to detect any abdominal pathology in a critically ill patient (Fig 2). A review of 55 patients treated in this fashion revealed a mortality rate of 5.4%.96 Within 72 hours, 95.7% of patients showed resolution of their symptoms. The complications associated with PC included a hepatic laceration requiring operation (n ¼ 1) and a catheter dislodgment requiring reinsertion (n ¼ 2). Another study of 42 patients with sepsis and either calculous or acalculous cholecystitis compared emergent cholecystectomy with PC.97 The mortality rates were not significantly different between the PC and emergent cholecystectomy groups, but PC was associated with significantly fewer complications. Furthermore, 2 patients who did not respond to PC required emergent cholecystectomy owing to gangrenous cholecystitis. The incidence of gangrenous cholecystitis is reported to be higher (40%-80%) in patients with acalculous cholecystitis compared with those with calculous cholecystitis (2%-31%).98-102 Given these data, emergency cholecystectomy in patients with acalculous cholecystitis is associated with a mortality rate ranging from 16%-44%. PC in this patient population with a planned cholecystectomy at a later interval may be the safest option.103

Defining the sick patient for AC Examining these individual organ systems, we start to understand that the sick patient is one who has a major deterioration in at least 1 organ system or is a patient with impaired function in multiple systems. Patient who had recent MI or stroke optimally require an interval before elective operation to minimize the complications of that surgery of at least 8 weeks for MI and 9 months for stroke. Naturally, this scenario can only be followed if the reason for the elective procedure is not immediately threatening to the patient's viability. No particular age presents an absolute contraindication to LC. However, if the patient's life expectancy without AC would be less than 6 months, initial nonsurgical management would be recommended.

Fig. 1. This image is from an abdominal ultrasound of a critically ill patient with acute acalculous cholecystitis. The gall bladder is thickened and markedly dilated without the presence of gallstones. (Color version of figure is available online.)

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Fig. 2. This CT scan image reveals severe acute acalculous cholecystitis. The gall bladder is extremely dilated. The circumferential enhancement of the thickened wall reveals the intense inflammatory process of the disease. CT, computed tomography.

Our practice would be to wait at least 3 months to perform cholecystectomy after uncomplicated MI or 6 months after uncomplicated stroke, unless the patient is having severe symptoms attributable to the gall bladder. In certain complicated cases, other factors abound, such as the necessity for blood thinners after a coronary stenting procedure, which may exceed 6 months. Withholding these vital medications to allow the performance of surgery at a time when they are most indicated sometimes creates unwarranted risks in many patients. Having an armamentarium of available options in these difficult cases allows the clinician to make the appropriate choice in both acute calculous and acalculous cholecystitis. Alternatives to surgery in AC Percutaneous transhepatic gall bladder drainage (PTGBD) (also known as a PC tube placement) is considered a safe alternative to early cholecystectomy in high-risk patients with AC (Fig 3).103 Although PTGBD was first performed in the 1970s5 and remains the most widely established technique, several alternatives have become popularized in the past 2 decades. Percutaneous transhepatic gall bladder aspiration (PTGBA) is an alternative method where the gall bladder contents are puncture aspirated without placing a drainage catheter. Next, endoscopic transpapillary gall bladder drainage (ENGBD) and endoscopic transpapillary gall bladder stenting (ENGBS) are endoscopic alternatives via the traditional transpapillary route. Finally, with recent improvements in endoscopic ultrasound (EUS), EUS-guided gall bladder drainage has been described via the antrum of the stomach or the bulb of the duodenum.104 Advantages and disadvantages of each technique are listed in Table 3. Percutaneous transhepatic gall bladder drainage If the patient is deemed a nonsurgical candidate for LC owing to a severely acute or poorly controlled chronic condition, the patient can receive either noninvasive medical therapy such as antibiotics and pain control. If this strategy fails, the patient would next be a candidate for an invasive nonsurgical treatment that would decompress the inflamed gall bladder. PTGBD is the


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Fig. 3. This is a CT scan image of a patient who has received a percutaneous transhepatic stent. The pigtail is coiled in the lumen of the gall bladder. CT, computed tomography. (Color version of figure is available online.)

most common method for nonoperative gall bladder drainage in patients who are not candidates for surgery. PTGBD is an interventional radiologic procedure designed to decompress the severely inflamed gall bladder, and its use has been described in high-risk surgical patients unresponsive to medical therapy and as first-line treatment to delay

Table 3 Advantages and disadvantages of nonsurgical drainage techniques for acute cholecystitis

percutaneous transhepatic gall bladder drainage (PTGBD)

Percutaneous gall bladder aspiration (PTGBA)

Endoscopic nasogallbladder drainage (ENGBD)

Advantages

Disadvantages

High success rate

Patient discomfort due to external tube Potential for dislodgment

Extensive clinical experience bile peritonitis unlikely Can be long-term solution Can irrigate tube Can perform cholecystography No external tube so more comfortable for patient Low risk No transhepatic puncture Can irrigate if clogged Allows enteral bile flow

Endoscopic transpapillary gall bladder stenting Endoscopic ultrasound (EUS)–guided transmural nasogallbladder drainage

Allows enteral bile flow No external tubes so more comfortable for patient Can irrigate tube

Can perform cholecystography No hepatic bleeding risk Endoscopic ultrasound (EUS)-guided transmural gall bladder stenting

Patient comfort as no external tube Can be a long-term solution No hepatic bleeding risk

Transhepatic nature can lead to bleeding Possibility of bile peritonitis No ability for cholecystography May lead to recurrent symptoms Requires endoscopy Patient discomfort due to nasal tube Sinusitis risk Operator dependent No option for irrigation Postprocedure pancreatitis Operator dependent Requires endoscopy Patient discomfort due to nasal tube Possible dislodgment by patient Drainage suboptimal Duodenal perforation is risk Operator dependent Requires endoscopy Duodenal perforation is a risk Bile peritonitis Irrigation requires endoscopy

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cholecystectomy (Fig 4).105-107 We have observed that some interventional radiologists prefer a hydroxy iminodiacetic acid scan before nonsurgical gall bladder decompression to document nonfilling of the gall bladder and confirm the diagnosis of AC. This test is certainly justifiable before to an invasive procedure in some patients who are severely ill and in whom the diagnosis of AC is unclear. To decompress the gall bladder, various methods have been described, but the most common is ultrasound-guided transhepatic gall bladder puncture. This drainage can be performed with minimal anesthesia and an 18-gauge needle. Gall bladder puncture is performed under direct ultrasound guidance to avoid injury to adjacent structures. A 6- to 10-F pigtail catheter is then placed in the gall bladder, using a guidewire under fluoroscopy with Seldinger technique.108 Technical and clinical response rates to PTGBD have been reported between 56% and 94%, with consistently higher success being documented in more recent studies.109-113 The primary advantage of PTGBD in high-risk surgical patients is the avoidance of general anesthesia and its associated cardiovascular risks.108,109 Despite these benefits, up to 16% of patients with PTGBD experience complications, including bile peritonitis, bleeding, catheter dislodgement, and pneumothorax. PTGBD may also be inappropriate for patients with massive ascites or coagulopathy owing to risks of bile peritonitis and bleeding, respectively. Additionally, discomfort from the catheter can prominently decrease the patient's quality of life because of impaired mobility and potential for sleep deprivation.111-113 Although the literature recognizes a high rate of morbidity and conversion to open cholecystectomy rate among high-risk surgical patients undergoing LC,114 there are no randomized controlled trials that directly compare the outcomes of PTGBD to LC.110 Therefore, the outcomes of PTGBD are difficult to quantify compared with those of early LC for high-risk surgical patients with AC. Based on the limited retrospective data in the literature, the success rates for PTGBD are fairly high, mortality related to the procedure (0.36%) is low, but the overall mortality rate following PTGBD (15.4%) appears to be equal to or higher than that for emergency LC (4.5%).110 This mortality rate may be attributed to selection bias, as patients treated with PTGBD are frequently more ill than patients treated with LC. There are 2 randomized controlled trials comparing PTGBD with conservative management in patients with AC. In 2002, Hatzidakis and colleagues. found no difference in the resolution of symptoms or overall mortality when comparing PTGBD to nonoperative management in highrisk surgical patients. The authors concluded that nonoperative treatment should be attempted first, and PTGBD be reserved for those unresponsive to initial medical management.108 Subsequently, Akyürek and colleagues107 compared PTGBD with early LC and medical management with delayed LC in high-risk surgical patients. Although the conversion to open

Fig. 4. This patient is receiving a percutaneous transhepatic gall bladder stent. (A) The catheter is passing through the abdominal wall. The liver is the lighter structure to the left where the inflamed gall bladder is the darker structure to the right. (B) The stent is seen in the lumen of the gall bladder abutting the posterior wall of the gall bladder adjacent to the liver. It should be noted that the patient also has a transpapillary stent decompressing the common bile duct. (Color version of figure is available online.)


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cholecystectomy and complication rates were similar in both groups, the study did show a shorter hospital stay and lower overall cost in the group treated with PTGBD and early LC. These authors advocated for percutaneous drainage in high-risk surgical patients over medical management. There is no randomized controlled trial comparing PTGBD with emergency LC in high-risk patients. With the advances in surgical laparoscopic training, intensive care management and perioperative anesthesia, the outcomes of PTGBD and LC may be more equivalent than the literature suggests. To fully determine the actual outcomes in these groups, the percutaneous cholecystostomy versus laparoscopic cholecystectomy for acute acalculous cholecystitis (CHOCOLATE) trial is an ongoing randomized controlled trial comparing morbidity and mortality between LC and PTGBD in high-risk surgical patients.114

Percutaneous transhepatic gall bladder aspiration PTGBA is a method to aspirate the gall bladder with a small-gauge needle under ultrasonographic guidance.106 It is an easy, low-cost, bedside-applicable procedure, without the patient discomfort encountered with an indwelling catheter (PTGBD). Fundamentally, PTGBA should not work in the setting of infection by the principle of all infections needing continuous drainage. However, infection is not the inciting factor in AC, as its primary mode of tissue damage is obstruction of the cystic duct causing increased intraluminal pressure, venous congestion, and impaired lymphatic drainage. With these effects, the gall bladder mucosa becomes ischemic and releases inflammatory mediators causing trauma, edema, ulcers, and possible wall necrosis. Secondary bacterial infection can then occur from the initial obstruction and activation of the inflammatory cascade. Secondary infections complicate up to 50% of clinical courses, as 40%-50% of cases have been shown to have positive bile cultures.115 Infection may not always be present, making continuous drainage excessive in some patients. One-time aspiration of bile from the obstructed gall bladder removes the irritant luminal contents and reduces the intraluminal pressure, thereby providing relief before the onset of infection. Further studies have concomitantly used antibiotic irrigation during aspiration to counteract any infection that may be present; however, the effectiveness of this technique is unclear owing to limited data. When comparing PTGBA and PTGBD, Chopra and colleagues argued that PTGBA should be the procedure of initial choice as the technical (97%-100%) and clinical (71%-77%) response rates are remarkably high. PTGBD should be saved as a salvage procedure for those failing to respond to a single PTGBA.116 Using this method, 77% of patients in this study avoided PTGBD. Tsutsui and colleagues117 advocated for repetitive PTGBA in patients who fail to show improvement initially, arguing that the most patients respond within 2 PTGBAs, thereby avoiding the placement of an indwelling catheter. The incidence of adverse events for PTGBA is lower (0%-4%) than that for PTGBD, and no serious adverse events have been reported.118 If one favors PTGBA, instances do exist when PTGBD is preferable to gall bladder aspiration. Gall bladder aspiration may not be technically feasible in patients with viscous, sludge-laden bile. In such patients, PTGBD has a greater chance of success because of the larger caliber of the catheter and the potential for repeated irrigation.119 In addition, because it does not provide continuous drainage, PTGBA is inappropriate in patients in whom the indication for gall bladder drainage is to provide relief from a distal biliary obstruction, such as in biliary malignancies. Despite its potential advantages, PTGBA has not been widely adopted as a standard treatment modality because AC is commonly thought to require continuous drainage while the data supportive of PTGBA is limited to case series and retrospective reviews. Additionally, as the patient is generally going to the interventional radiology suite for aspiration, the managing team may feel that the additional morbidity of placing a drainage catheter may be minimal in feasibility, cost, and effort, while the potential benefit of further drainage and prevention of recurrent cholecystitis may prove valuable.

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Endoscopic transpapillary gallbladder drainage and stenting ENGBD involves placement of a nasobiliary drainage tube and generally does not require biliary sphincterotomy. After successful bile duct cannulation, a guidewire is advanced into the cystic duct and subsequently into the gall bladder. A 5- to 8.5-F pigtail nasobiliary drainage tube catheter is then placed into the gall bladder.106 The procedure has been reported in patients with specific comorbidities, including end-stage liver disease or coagulopathy, where transhepatic techniques are contraindicated. In ENGBS, the procedure is identical to ENGBD, but a 6 to 10-F-diameter double pigtail stent (Fig 5) is placed instead of a nasobiliary drainage tube. The completed procedure can then be visualized on a plain film radiograph to ensure the pigtail is in the lumen of the gall bladder (Fig 6).106 When larger diameter stents are placed (ie, 10 F), a sphincterotomy is performed to prevent postendoscopic retrograde cholangiopancreatography (ERCP) pancreatitis.118 Also, unlike ENGBD, stents cannot be irrigated to prevent occlusion by blood or debris, which is a potential cause for concern over time.118 Although supportive data are limited, a meta-analysis of ENGBD and ENGBS by Itoi and colleagues118 demonstrated a technical success rate of 81% and 96% and a clinical response rate of 75% and 88%, respectively. These early results are comparable to the success rates of the more established approaches of PTGBD and PTGBA, but longer-term results have not been established. This study also found the incidence of adverse events to be similar to that of PTGBD (0%-16%). Notably, LC can be performed on these patients with PTGBD, following resolution of the acute inflammation and sepsis. The tube or stent can then be removed preoperatively or intraoperatively when the time comes.118 Both ENGBD and ENGBS require difficult endoscopic techniques and only case series have been conducted at a limited number of institutions.119 Both methods have not yet been established as a standard of care. Therefore, although the results are promising, these are newer

Fig. 5. This picture is captured endoscopically during placement of a transcystic gall bladder stenting procedure. The blue stent is being advanced into the common bile duct over a guidewire and into the gall bladder. (Courtesy: Drs Michel Kahaleh and Monica Rajaram Gaidhane.) (Color version of figure is available online.)


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Fig. 6. This patient has received an endoscopically placed transcystic gall bladder stent. The pigtail in the right upper quadrant is in the gall bladder. The patient has also received a pancreatic stent.

options for a specific patient population and should currently only be performed in high-volume centers by skilled endoscopists with sufficient training. More data evaluating the success of these procedures as well as detailing their potential complications including postprocedure pancreatitis and duodenal perforation need to be tabulated to define their exact role in the treatment of AC in high-risk patients. Endoscopic ultrasound-guided transmural gall bladder drainage Although EUS-guided drainage procedures have been safely used with peripancreatic fluids, including those from pancreatic pseudocysts and pancreatic, subphrenic, and splenic abscess, little is known regarding EUS-guided transmural gall bladder drainage (EUS-GBD) for high-risk patients with AC.104 The endoscopic approach describes the initial puncture being made at the prepyloric antrum of the stomach or the bulb of the duodenum with a 19-gauge needle to access the gall bladder body or neck while avoiding visible vessels. From there, bile is aspirated and sent for culture. A guidewire is passed through the needle and coiled into the gall bladder. After removal of the needle, the tract is dilated using a 6-7 F bougie. A 5-F nasobiliary drainage tube or stent is subsequently placed.120 EUS-GBD is particularly useful in patients with large amounts of perihepatic ascites who, therefore, cannot undergo PTGBD. In addition, EUS-GBD is useful and safe for patients with coagulopathy and for those taking antiplatelet or antithrombotic medication. The EUS-GBD puncture site is at the prepyloric antrum or duodenal bulb, both of which are less vascularized than direct puncture through the liver when compared with PTGBD. Furthermore, there is less discomfort with EUS-GBD than with PTGBD, primarily because the PTGBD puncture site is in the subcostal area of the right flank, an area very sensitive to pain.34 The development of the linear echoendoscope has led to transmural entry and drainage of pancreatic fluid, and this is now regarded as the method of choice. More recently, the transmural approach has been reported to be successful in internal bile drainage of the gall bladder.34 The EUS-guided transmural approach to the gall bladder for bile aspiration raises concerns regarding the development of bile peritonitis. Theoretically, the gall bladder does not have adhesions to the gastrointestinal tract, raising the possibility of bile leakage during the procedure causing bile peritonitis. However, this complication has rarely been reported, suggesting that the inflamed gall bladder wall has adhered to adjacent structures sufficiently to prevent leakage through the puncture site.121

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The transmural approach has several potential advantages in comparison with the transpapillary approach. One advantage includes the avoidance of cannulation-related pancreatitis. Additionally, the procedure is not limited in its success by the configuration of the cystic duct, which may be difficult to cannulate in certain instances. The transmural approach also has several potential advantages compared with the percutaneous approach, including the avoidance of complications such as hematoma and pneumothorax. The transmural approach can also be employed in patients with perihepatic ascites with less concern for bile peritonitis than the percutaneous approach.104 Nonetheless, the procedure does have potential disadvantages and described complications, including bile peritonitis, pneumoperitoneum,, puncture-induced hemorrhage, stent occlusion, inadvertent tube dislodgment, and stent migration into the gall bladder or peritoneal cavity.104,122 Enhanced clinical experience may prove to mitigate some of these potential complications. Jang and colleagues addressed the issue of bile peritonitis by discussing the higher likelihood of bile peritonitis with a plastic stent than a metal stent. The authors argued that the insertion of a plastic stent requires a fistula tract of diameter larger than, or at least equal to, the diameter of the inserted stent. Because of its expandability, a metal stent can seal the gap between the stent and fistula of the gall bladder wall more securely than a plastic stent and prevent bile leakage.122 Although a report of bile peritonitis with a plastic stent has been described,121 the small sample sizes examining the safety of each procedure have proved insufficient in showing that metal stents are overall safer in preventing bile leakage than plastic stents during this procedure.121-123 The pneumoperitoneum reported in these studies appears to be self-limiting and resolves almost immediately following the procedure.34 The pneumoperitoneum typically occurs during dilation; the use of carbon dioxide for insufflation during the procedure may lead to the rapid resolution of the pneumoperitoneum and relief of pain. Nonetheless, EUS-GBD is not a commonly utilized technique. Therefore, like the endoscopic gall bladder drainage techniques, it should be performed only in high-volume centers by skilled endoscopists and further prospective evaluations are needed to gauge its safety and success profile.

Risks of delaying gall bladder removal Currently, when a patient presents with AC, the clinicians have the option to perform either early or delayed gall bladder removal or a nonoperative treatment strategy. “Early cholecystectomy” is generally defined as removal of the gall bladder within 72 hours from the onset of symptoms, although other authors have more liberally defined early cholecystectomy as less than 7 days from the onset of symptoms.15 “Delayed cholecystectomy” has been variably defined as greater than 96 hours after the onset of symptoms to 6 or more weeks after symptom onset. More commonly, delayed cholecystectomy refers to the longer time period of 6 or more weeks. Delaying gall bladder removal after development of gall bladder disease symptoms may pose risks to the patient. For patients presenting with biliary colic, a study found that 22.5% developed gallstone-related complications in patients monitored an average of 4.2 months prior to cholecystectomy.16 These complications included pancreatitis, gall bladder empyema, gall bladder perforation, interval AC, cholangitis, and obstructive jaundice. For patients presenting with AC, 18%-50% developed similar gallstone-related complications while waiting for cholecystectomy.124-129 Investigators have studied the natural history of AC from a different perspective. On examining a database of nearly 30,000 Medicare patients, Riall and colleagues51 found that 25% of patients did not undergo cholecystectomy on their index admission. Of these patients, 27% went on to have a cholecystectomy. Of the remaining patients who did not undergo cholecystectomy within 2 years, 38% had a gallstone-related readmission costing Medicare an additional $7000 for each readmission. The patients who did not undergo cholecystectomy had a worse 2-year survival rate. Importantly, this study did not ascertain whether these patients who did not undergo surgery had more comorbidities and risks for mortality than the other patients


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who underwent earlier cholecystectomy and also did not study the factors influencing the decision to choose nonoperative management. Some current international guidelines recommend that patients presenting with biliary pancreatitis undergo early cholecystectomy after resolution of pancreatitis and before hospital discharge to prevent similar recurrent biliary symptoms.130-134 However, practice varies by region as some centers may preferentially delay cholecystectomy after acute pancreatitis. In a meta-analysis of 998 patients, 48% underwent cholecystectomy during the index admission.135 Additionally, 52% underwent a delayed cholecystectomy that ranged from 19-58 days after the initial onset of symptoms, with the median being 40 days. During that time, 18% were readmitted: 3% with AC, 8% with biliary pancreatitis, and 7% with biliary colic. To further analyze this question, the Dutch pancreatitis study group is currently enrolling subjects with gallstone pancreatitis in a study called the Pancreatitis of Biliary Origin, Optimal Timing of Cholecystectomy trial comparing early LC (within 72 hours of symptom onset) with late LC (25-30 days) after randomization. The primary end points of the Pancreatitis of Biliary Origin, Optimal Timing of Cholecystectomy trial are mortality and sudden readmission for biliary events.134 Some centers have felt that endoscopic sphincterotomy after biliary pancreatitis may suffice for early treatment in lieu of cholecystectomy to prevent recurrent symptoms before delayed cholecystectomy. In a study, patients who underwent ERCP with sphincterotomy decreased their risk of readmission from 24% to 10% and their risk of developing recurrent biliary pancreatitis from 9% to 1%. Notably in this Dutch series, the risk of developing AC or biliary colic was unchanged after ERCP.135

Delayed cholecystectomy after percutaneous drainage Several studies have reported that critically ill patients treated with percutaneous drainage had an overall complication rate significantly lower than critically ill patients treated with emergency cholecystectomy.136,137 In a series, LC was often attempted in even the most critically ill patient, but there was a high open cholecystectomy rate.136 Even in those that were started laparoscopically, the conversion rate was high, most often because of inflammation that made structures in the hilum difficult to identify. The major complications following emergency cholecystectomy were bleeding or biliary leak requiring repeat operation. Mortality, which was not different between both the groups, was attributed to the patient's underlying disease. Both Winbladh and colleagues110 and Anderson and colleagues137 found that patients who underwent cholecystostomy were associated with higher mortality rates, increased total charges, and longer lengths of stay. Notably, in observational series, those patients treated with cholecystostomy were more likely to be older and have more comorbidities than those treated with cholecystectomy.137 In a population-based cohort of 10,304 patients with AC managed by percutaneous drainage, at 1 year, 40% had undergone cholecystectomy, 18% had died, and 49% had another gallstonerelated emergency department visit or admission.126 When comparing patients who underwent percutaneous drainage with those who underwent cholecystectomy, those who died and those who survived without cholecystectomy were older and had more comorbidities. This result suggests that clinicians were perhaps more reluctant to perform cholecystectomy on certain patients for reasons not discernible from the data. Whether the risk of recurrent AC in itself mandates that cholecystectomy be performed after percutaneous drainage for acute calculous cholecystitis remains controversial.47 In the study by Melloul and colleagues, the authors found a 17% recurrence rate of AC in patients with gallstones that underwent percutaneous drainage.136 These authors and others have therefore recommended that cholecystectomy should be mandatory in patients with calculous cholecystitis, whether performed early or in a delayed fashion.85,136 However, other clinicians have observed that as postoperative morbidity can be significant, cholecystectomy should only be considered in patients with recurrent AC.47,138

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Because of the ongoing debate, the currently enrolling CHOCOLATE trial is designed to provide the surgical community with an evidence-based guideline in the treatment of acute calculous cholecystitis in high-risk patients. High-risk patients, defined as APACHE-II score 7-14, with acute calculous cholecystitis are randomized to either percutaneous drainage or LC.114 The aim of the study is to prove superiority for the LC group. Questions that surround the practice of percutaneous drainage for both acute acalculous and calculous cholecystitis involve the duration of time the drain is left in the gall bladder and whether a study is needed before the drain removal. Practice patterns have generally demonstrated that the drain is generally left until interval cholecystectomy or an arbitrary time of several weeks to several months. Some authors have recommended that if a cholangiogram through the percutaneous drain shows that the duct is open and free of stones, then the drain may be removed.85 Others have recommended that the drain should remain in place indefinitely until the gall bladder is removed. Many physicians feel that for acalculous cholecystitis, an interval cholecystectomy is not necessarily required.85 The aforementioned CHOCOLATE trial will specifically investigate the latter question. Clearly, the main controversies surround the patient with multiple comorbidities who is at higher risk for perioperative complications for cholecystectomy. These complications may include a longer length of stay, cardiopulmonary complications, or a higher conversion rate to open cholecystectomy. One recommended strategy is clamping the tube in patients with acalculous cholecystitis for 1 week after a 4-week period of drainage. If clamping the tube is tolerated by the patient, we remove the tube. We maintain the same practice in patients with calculous cholecystitis who are nonoperative candidates.

Intraoperative damage control In some cases during attempted LC, the surgeon encounters a severely inflamed gall bladder that may preclude standard LC. These circumstances can include a situation in which a patient is severely ill and is thought to be a poor candidate for the physiological stress for a prolonged laparoscopic operation, an open surgical procedure, or an operation where potential exists for significant bleeding or even biliary ductal injury. Which of these options is undertaken depends on multiple factors, including feasibility, technical safety and ability to avoid complications, patient tolerance for increased operative time and postoperative morbidity, and the local resources necessary to support postoperative interventions (Table 4). If the surgeon deems intraoperatively that LC cannot be performed, several intraoperative damage control techniques should be considered. If the patient can tolerate an open procedure and the decision is reached expediently, sometimes conversion to an open cholecystectomy is a useful strategy. Another option includes intraoperative cholecystic drainage where a laparoscopic cholecystostomy tube in placed. Here, a laparoscopic purse-string suture is placed on the dome of the gall bladder and a Malekot tube (14-16 F) is placed in the gall bladder for drainage after intraoperatively suctioning out as much bile and stones as possible. In some cases, the difficulty is because of a thick rind around the gall bladder. Occasionally, incising the rind and dissecting it away from the gall bladder will leave a soft gall bladder for which the cholecystectomy can proceed in a standard fashion. Table 4 Techniques of laparoscopic intraoperative damage control for severe acute cholecystitis 1. Cholecystostomy tube 2. Cholecystotomy with stone(s) removal 3. Extensive dissection of medial and lateral peritoneal attachments 4. Dissection from the “top” or “middle” down to the neck of the gall bladder 5. Gall bladder division at or above the infundibulum-cystic duct junction with Endo GIA stapler, ENDOLOOP, or suture 6. Laparoscopic partial or subtotal cholecystectomy


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In these cases, the surgeon can perform some maneuvers to provide treatment to the gall bladder pathology in a less invasive fashion. The actual maneuver can depend on the actual situation that is making the operation difficult. Sometimes the gall bladder can be too thickwalled to grasp and simple aspiration does little to improve the retraction. In this case, creating a hole, at least 1- to 2-cm high on the gall bladder away from the primary structures can allow decompression. Additionally, the hole may be used to remove a large stone from the gall bladder and facilitate retraction. In other cases, the gall bladder cannot be grasped because the entire gall bladder lumen has been replaced with stones. In this instance, a hole in the gall bladder can be made and the stones retrieved with a large stone grasper through the subxiphoid 10-mm port. In the authors' experience, sometimes up to 200 stones of varying sizes can be present in the gall bladder and require innumerable passes with the large stone grasper (Fig 7). Remarkably, after removal of a large stone or multiple smaller stones, the dissection in the Calot triangle may proceed fairly expeditiously as the retraction can become greatly enhanced. In addition, after creating a hole in the gall bladder for stone retrieval, the retracting surgeon can either close the hole by grasping both sides of the hole with a bowel grasper to close the defect. In some cases in which the gall bladder wall is extremely thick, the assistant can actually grasp the wall of the cholecystomy to intensify the pull of the retraction. If the dissection in the Calot triangle is fraught with too much bleeding and suboptimal visualization, sometimes dissection in other areas of the gall bladder can create more mobilization of the gall bladder to facilitate the dissection. In this case, full division of the medial and lateral peritoneal surfaces the entire length of the gall bladder may be invaluable. This maneuver allows full mobilization of the gall bladder and may allow safe dissection at the cystic duct and the Calot triangle. Another commonly taught dictum is that the gall bladder should be dissected “from the top down” when the inflammation is too intense in the Calot triangle. However, the better strategy

Fig. 7. This picture captures a severely inflamed gall bladder with more than 150 gallstones of varying sizes. In this instance, the gall bladder is difficult to grasp with standard laparoscopic instruments and removal of the stones via a cholecystotomy facilitated the procedure such that it could be performed laparoscopically. Photograph by Soumitra R. Eachempati, MD. (Color version of figure is available online.)

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can sometimes be to dissect “from the middle down” and allow the top of the gall bladder to stay fixed on the liver bed to give counter traction. Dissecting from the middle down is performed by slowly dissecting each side of the gall bladder safely above the critical structures sequentially until a window exists behind the gall bladder anterior to the liver bed. For this maneuver to be accomplished properly, the gall bladder is not to be entered on the side of the liver bed. After this window is created, the surgeon can then cautiously dissect toward the neck of the gall bladder and the cystic duct. This maneuver can allow the gall bladder to be stretched and allow lengthening of the fundus and cystic duct to ensure proper visualization of the critical structures. If the surgeon cannot safely dissect the cystic duct or it is too large to clip safely, several options are available. First the skilled laparoscopic surgeon can suture the structure closed. However, this maneuver may not always be possible as sometimes the tissues are too friable. The surgeon can also attempt to divide the gall bladder higher above the cystic duct. As this area is generally too large for the standard 5- or 10-mm surgical EndoClips, the surgeon must use an Endo GIA Universal Stapler (Covidien, Dublin, Ireland) or an ENDOLOOP (Ethicon Endo-Surgery, Blue Ash, OH). Importantly, in all circumstances where the closure of the cystic duct or gall bladder fundus is suspect, a 10 F flat closed-suction drain should be placed to detect and control a potential postoperative biliary fistula before the patient develops bile peritonitis and becomes symptomatic. In all instances in which a cystic duct closure is suspect or bile is noted in the drain effluent, a low threshold should be given for investigation for a biliary leak by hydroxy iminodiacetic acid scan or imaging study. Detection of a biliary leak can allow the gastroenterology service to perform postoperative ERCP for biliary ductal decompression and possible stone retrieval or stenting. As mentioned earlier, LC in the setting of AC can be difficult with the potential for increased morbidity and conversion rates. The traditional teaching has been that if the “critical view” cannot be obtained during the dissection of the Calot triangle, conversion to an open cholecystectomy is advocated to prevent a bile duct injury.139 However, younger surgeons have limited experience in open cholecystectomies and may have difficulty in performing a safe procedure in a hostile field using an open approach. Furthermore, an open approach does not necessarily provide a better view of the anatomy in the difficult cases in which standard laparoscopic surgery is not feasible and sometimes the patient can receive the identical procedure laparoscopically without the need for recovery from the morbidity of an open incision. The last option admittedly employs principles of “damage control surgery” and is the laparoscopic partial or “subtotal” cholecystectomy (LPC). In aggregate, the all-encompassing indication for laparoscopic psychomotor skills is that safe standard progression is not possible laparoscopically and the patient will not receive better treatment for the disease process with open surgery. A related indication is that the patient is a poor candidate for open surgery or extended dissection because of anticipated extra time or blood loss. Factors warranting LPC can include severe congestion, edema and adhesions at the Calot triangle, tenacious fibrosis at the Calot triangle, or severe bleeding on performing any aspect of the operative dissection. Situations in which bleeding during LC can become prominent include intense inflammation in the Calot triangle, dense adherence of the gall bladder or posterior rind to the liver bed, and an operative field complicated by portal hypertension.140 LPC is sometimes chosen pre-emptively to avoid a major injury, such as to the right hepatic artery or bile duct while trying to dissect in a bleeding field with poor visualization of the important structures during LC. LPC incorporates the principles of damage control or abbreviated surgery into its components. Optimally, as much gall bladder as possible is removed and adequate closure of the cystic duct is performed in LPC. However, in many cases in which LPC is needed, adequate dissection to visualize enough cystic duct length to facilitate a secure closure is not possible. In LPC, a common strategy for LPC includes stapling of the gall bladder neck near the cystic duct, as previously described for thick tissues, above inflammation in the Calot triangle. Another common strategy entails leaving a portion of the gall bladder wall behind in situ on the liver bed to minimize the severe bleeding that may be encountered when trying to separate the gall bladder from the liver bed. When a portion of the gall bladder is left on the liver bed, attempts should be made to cauterize as much residual gall bladder mucosa as possible. Regardless of the


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individual characteristics of the technique, current reviews document that LPC is feasible in approximately 90% of patients undergoing a difficult resection.139 Importantly, LPC does not eliminate all the complications that could occur with LC.139,140 In the recent meta-analysis, the most common complication of LPC was postoperative bile leak, which occurred in 10.6% of patients.139 The authors noted that leaving the cystic duct open leads to higher postoperative bile leak rates, prolonged drainage, and more frequent necessity for percutaneous drainage. Additional complications after LPC include recurrent symptoms of gallstones (2.2%), immediate reoperation (2.7%), and the need for postoperative ERCP (7.5%) or postoperative percutaneous interventions (1.4%).139 Further analysis revealed that fewer bile leaks, less need for ERCP, and less recurrent symptoms of gallstones seemed to occur when the cystic duct and gall bladder remnant were closed. These data support a low threshold for postoperative ERCP with biliary decompression in cases of LPC and cautious inspection of a patient's physical examination, clinical status, and laboratory parameters before a potentially premature discharge.

Management strategy for AC in the sick patient An algorithm for the treatment of patients with acute calculous cholecystitis is given in Figure 8. Early cholecystectomy is the treatment of choice for acute calculous cholecystitis. For patients with sudden sickness or those with recurring illness who could benefit from medical optimization, initial nonoperative treatment should be attempted for acute calculous

Fig. 8. This figure represents an algorithm of the management strategy for acute calculous cholecystitis. The preferred treatment is urgent cholecystectomy unless the patient carries high operative risk, in which case, percutaneous drainage should be performed.

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cholecystitis. Risk stratification is important to ensure that patients who may benefit from surgery are appropriately chosen. ASA class, age, and various comorbidities should not be used alone when evaluating patients for cholecystectomy. When patients are considered to have unacceptable risk for anesthesia and surgery, other nonoperative approaches may be considered, including antibiotics with or without percutaneous drainage. If the patient's comorbidities can be treated and the patient optimized medically, then surgery may become an option. Additionally, for acute acalculous cholecystitis, nonoperative treatment with drainage should generally be the initial strategy. For those in whom the risk of surgery remains high, continued percutaneous drainage or removal of the drain depends on whether the cystic duct is open. Although PTGBD remains the standard of care for nonoperative gall bladder drainage, the external tube can be painful and limit the activities of daily living. Creation of a mature percutaneous transhepatic tract requires time, rendering removal of the tube and labor intensive. PTGBA does not require an external drainage tube. However, PTGBA can require multiple aspirations to achieve the same success as PTGBD. Patients with moderate ascites, coagulopathy, or aberrant anatomy may be better served using an endoscopic approach; however, these techniques are still in their infancy and should only be performed by skilled endoscopists. LPC should be reserved as an intraoperative damage control option, as this technique may minimize operative morbidity in high-risk patients without compromising operative utility for disease control. References 1. McArthur P, Cuschieri A, Sells RA, Shields R. Controlled clinical trial comparing early with interval cholecystectomy for acute cholecystitis. Br J Surg. 1975;62(10):850–852. 2. Yamashita Y, Takada T, Strasberg SM, et al. TG13 surgical management of acute cholecystitis. J Hepatobiliary Pancreat Sci. 2013;20(1):89–96. 3. Lahtinen J, Alhava EM, Aukee S. Acute cholecystitis treated by early and delayed surgery. A controlled clinical trial. Scand J Gastroenterol. 1978;13:673–678. 4. Jarvinen HJ, Hastbacka J. Early cholecystectomy for acute cholecystitis: a prospective randomized study. Ann Surg. 1980;191:501–505. 5. Norrby S, Herlin P, Holmin T, Sjodahl R, Tagesson C. Early or delayed cholecystectomy in acute cholecystitis? A clinical trial. Br J Surg. 1983;70:163–165. 6. van der Linden W, Sunzel H. Early versus delayed operation for acute cholecystitis. A controlled clinical trial. Am J Surg. 1970;120:7–13. 7. van der Linden W, Edlund G. Early versus delayed cholecystectomy: the effect of a change in management. Br J Surg. 1981;68:753–757. 8. Cuschieri A, Dubois F, Mouiel J, et al. The European experience with laparoscopic cholecystectomy. Am J Surg. 1991;161(3):385–387. 9. Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg. 1995;180(1):101–125. 10. Gutt CN, Encke J, Köninger J, et al. Acute cholecystitis: early versus delayed cholecystectomy, a multicenter randomized trial (ACDC study, NCT00447304). Ann Surg. 2013;258(3):385–393. 11. Kiviluoto T, Siren J, Luukkonen P, Kivilaakso E. Randomized trial of laparoscopic versus open cholecystectomy for acute and gangrenous cholecystitis. Lancet. 1998;351:321–325. 12. Berrgren U, Gordh T, Grama D, Haglund U, Rastad J, Arvidsson D. Laparoscopic versus open cholecystectomy: hospitalization, sick leave, analgesia and trauma responses. Br J Surg. 1994;81:1362–1365. 13. Zacks SL, Sandler RS, Rutledge R, Brown RS. A population based cohort study comparing laparoscopic cholecystectomy and open cholecystectomy. Am J Gastroenterol. 2002;97:334–340. 14. Flowers JL, Bailey RW, Scovill WA, Zucker KA. The Baltimore experience with laparoscopic management of acute cholecystitis. Am J Surg. 1991;161:388–392. 15. Everhart JE, Khare M, Hill M, Maurer KR. Prevalence and ethnic differences in gallbladder disease in the United States. Gastroenterology. 1999;117(3):632–639. 16. Gurusamy KS, Samraj K. Early versus delayed laparoscopic cholecystectomy for acute cholecystitis. Cochrane Database Syst Rev. 2013;6:CD005440. 17. Cheruvu CV, Eyre-Brook IA. Consequences of prolonged wait before gallbladder surgery. Ann R Coll Surg Engl. 2002;84(1):20–22. 18. Yuksel O, Salman B, Yilmaz U, Akyurek N, Tatlicioglu E. Timing of laparoscopic cholecystectomy for subacute calculous cholecystitis: early or interval—a prospective study. J Hepatobiliary Pancreat Sci. 2006;13(5):421–426. 19. Boerma D, Rauws EA, Keulemans YC, et al. Wait-and-see policy or laparoscopic cholecystectomy after endoscopic sphincterotomy for bile-duct stones: a randomised trial. Lancet. 2002;360(9335):761–765. 20. Lau H, Lo CY, Patil NG, Yuen WK. Early versus delayed-interval laparoscopic cholecystectomy for acute cholecystitis: a metaanalysis. Surg Endosc. 2006;20(1):82–87.


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Unsuspected Duplicated Gallbladder in a Patient Presenting with Acute Cholecystitis.

Acute acalculous cholecystitis in a patient with juvenile dermatomyositis.

[Acute acalculous cholecystitis in a patient without underlying pathology].

Acute cholecystitis in the elderly.

Acute cholecystitis.

Acute cholecystitis.

Acute Cholecystitis.

Radiography in the diagnosis of acute cholecystitis.

Postoperative acute cholecystitis in Japan.

Acute cholecystitis complicating trauma.

Postoperative acute acalculous cholecystitis.

Editorial: Acute cholecystitis in childhood.

Bile peritonitis in acute cholecystitis.

Acute typhic cholecystitis.

[Emergency checklist: acute cholecystitis].

The Surgical Clerkship and Medical Student Performance in a Standardized Patient Case of Acute Cholecystitis.

The radiologic diagnosis of acute cholecystitis.

Editorial: Treatment of acute cholecystitis.

Editorial: Management of acute cholecystitis.

Acute acalculous cholecystitis. A review.

Acute cholecystitis: WSES position statement.

Imaging of acute cholecystitis and cholecystitis-associated complications in the emergency setting.

Acute cholecystitis after a colonoscopy.

[Intravenous cholegraphy in acute cholecystitis (author's transl)].