Cholecystitis in Pregnancy - Hindawi Publishing...

Infectious Diseases in Obstetrics and Gynecology 4:303-309 (1996)(C) 1997 Wiley-Liss, Inc.

Cholecystitis in Pregnancy

Brian M. Casey* and Susan M. CoxDepartment of Obstetrics and Gynecology, Universily of Texas Southasestern Medical Center,

Dallas, Texas

ABSTRACT

Biliary tract disease is a relatively uncommon, heterogenous disease in pregnancy. Specifical-ly, acute eholecystitis can be especially difficult to recognize in pregnancy. However, once diag-nosed, the initial management plan should be conservative and include antibiotic therapy. Subse-quent management depends on the gestational age at diagnosis. Surgical therapy, when indicated,should not be delayed and a planned intervention during the second trimester appears to offer abetter outcome than surgery performed under emergent conditions. Infect. Dis. Obstet. Gyneeol.4:303-309, 1996. (C) 1997 wiey-I.iss, Inc.

KEY WORDS

biliary tract disease; cholelithiasis; Escaericaia coli; Bacteroides species

holelithiasis is a condition which effects ap-proximately 20 million American women with

million new cases diagnosed each year. Womenof reproductive age are 4 times more likely thanmen of similar age to develop gallbladder disease,z

Epidemiologic studies indicate that the incidenceof cholesterol gallstones rises abruptly as womenenter the childbearing years.3 In fact, several stud-ies show a direct relationship between parity andrisk of developing biliary stones.4-6 Generallythough, biliary tract disease is a relatively uncom-

mon occurrence during pregnancy. A recent reviewof more than 45,000 pregnant women revealed theincidence of symptomatic biliary tract disease to be0.16% in pregnancy.7 Despite its relatively uncom-mon occurrence during pregnancy, 81% of womenwith symptoms of gallbladder disease had their firstattack within 1 year of pregnancy. Pregnancy thenseems to predispose women to developing biliarytract disease.

Biliary tract disease encompasses a continuumof pathologic entities which includes biliary sludg-ing, cholelithiasis, cholecystitis, choledocholithia-sis, and cholangitis. Biliary sludge or the supersatu-

ration of bile with cholesterol, is an important pre-cursor to gallstone formation. The exact prevalenceof cholelithiasis in pregnancy is essentially un-

known since 50% of women with gallstones are

asymptomatic. Efforts to identify asymptomaticcholelithiasis in pregnancy using ultrasound haveproduced variable results; however, the best esti-mate of incidence appears to be between 2.5% and4.5%.8-1o

In addition to pregnancy, several other factorsare strongly associated with gallbladder disease.

Ethnicity contributes to the risk for developing bil-

iary disease. In particular, 70% of Native Americanwomen older than 30 years of age develop choleli-thiasis. Mexican American women have an inter-

mediate prevalence of about 14% with Caucasiansand Black women at 4% and 5%, respectively. 1

Chilean women are also reported to be at high riskfor developing gallstones. e In addition, heredityhas been implicated as a contributing factor; 20% offirst degree relatives with cholelithiasis will de-velop symptomatic gallstones. 1 Finally, age andobesity are also commonly associated with biliarydisease.

*Correspondence to: Dr. Brian M. Casey, Department of Obstetrics and Gynecology, University of Texas SouthwesternMedical Center, 5323 Harry Hines Boulevard, Dallas, TX 75235-9032.

Received 10 July 1996Review Article Accepted November 1996

CHOLECYSTITIS IN PREGNANCY

As stated earlier, biliary disease, including acute

cholccystitis, occurs infrequently during the preg-nant state. In fact, the prevalence of acute chole-cystitis in pregnancy ranges from 1/1,000 to

1/10,000 births. 13,14 Cholclithiasis is obviously themajor etiologic factor in the development of acute

cholecystitis and it has been established that thepregnant state predisposes women to gallstone for-mation. In light of the key role they play in theetiology of acute cholecystitis, it is only appropriatethat a brief description of the pathogenesis of gall-stones be provided in this review.

PATHOGENESIS OF BILIARY STONESGallstones are composed of cholesterol, bilirubin,calcium salts, and protein. Each of these ingredi-ents occurs in various percentages. Specifically,there are cholesterol and non-cholesterol stones.

Non-cholesterol stones are frequently associatedwith a chronic hemolytic condition and contain a

higher bilirubin concentration. Brown pigmentnon-cholesterol stones are often associated with in-fection since bacteria are likely to hydrolyze con-

jugated bilirubin into calcium salts. This hydrolysisaccounts for the brown coloration of many non-

cholesterol gallstones.Cholesterol gallstones, 75% of all stones in the

Western world, form when cholesterol concentra-

tions exceed the ability of bile acids to maintaincholesterol in solution. At higher cholesterol con-

centrations, cholesterol micelles coalesce precipi-tating crystals. This coalescence yields gallbladdersludge, which is merely thickened mucoproteinwith entrapped cholesterol crystals. Sludge is an

important precursor to gallstone formation as thecrystals bind to the biliary proteins and ultimatelyresult in cholelithiasis, is

The increased risk of developing gallstones dur-ing pregnancy is due to several factors. First, thegallbladder volume is increased during the secondand third trimesters. Second, gallbladder motility isdecreased in pregnancy, possibly due to elevatedprogesterone levels. The evidence, however, isonly circumstantial as progesterone has beenproved only to inhibit gastrointestinal smoothmuscle contractility in vitro. 6

The theorized decrease in motility alone cannot

completely account for the increased bile volumenoted in pregnancy. Analysis of sequential films forgallbladder volume revealed a significant increase

CASEYAND COX

in residual volume after gallbladder emptying. 17

There is also a 50% increase in the bile acid poolassociated with a concomitant steroid-induced in-crease in cholesterol secretion during pregnancy.Together with the replacement of deoxycholic andchenodeoxycholic bile acids with cholcic acid, in-creased volume and decreased motility of the gall-bladder enhance the development of biliary stones.

When these pregnancy-induced changes occur

with a metabolic and/or hereditary predispositionto developing gallstones, the likelihood of biliarydisease is predictably high.

MICROBIOLOGY OF BILIARY DISEASE

Identifiable gallstones do not have to be present inorder to develop symptomatology. In fact, biliarysludge can precipitate biliary pain, acute cholecys-titis, or even pancreatitis. When sludge developsinto gallstones and they obstruct the cystic or com-

mon bile ducts, bacterial invasion can occur. How-ever, the primary cause of acute cholecystitis is not

bacterial invasion. Instead, it is frequently a chemi-

cal inflammation. After obstruction, inflammation,hyperemia, and edema of the gallbladder follow.Subsequent venous and lymphatic obstruction

yields ischemia. It is only after this secondary isch-emia that bacterial invasion and infection com-

monly occur. 8

The presence of organisms in the bile, per se,does not necessarily imply an active infection.Bactibilia has only been reported in up to 65% ofwomen with acute cholecystitis. In fact, most re-

ports state that only 50% of patients with acute

cholecystitis will have positive bile cultures. 9 Con-verscly, bactibilia is found in 20-30% of patientswith biliary concrements that have minimal or no

signs of obstruction. Therefore, the mere presenceof biliary calculi seems to support some bacterial

growth. 18,9 Ultimately, then, acute cholecystitiscan be thought of as a heterogeneous disease.

The incidence of bactibilia varies significantlywith the stage of disease and the patient’s age.Also, as expected, with infections originating in thegut, the array of organisms in acute cholecystitis is

broad. It includes both aerobes and anaerobes witha predominance of enteric gram-negative organ-isms (Table 1). Escherichia coli is the most common

organism found in all studies of men and women

diagnosed with acute cholecystitis. Klebsiella, Pro-teus, Enterococci, and Streptococci together with

304 INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY

CHOLECYSTITIS IN PREGNANCY CASEYAND COX

TABLE I. Common causes of cholecystitis8

AerobicEscherichia coliKlebsiella sp.EnterococciProteus sp.

AnaerobicBacteroides sp.Clostridium sp.Anaerobic cocci

E. coli account for 75% of all bacterial strains re-covered during acute cholecystitis. 18 There hasbeen a slow increase in anaerobic isolates which ismost likely due to improved culturing techniques.Nevertheless, of the anaerobes recovered, Bacte-roides and Clostridia are among the most com-

18mon.

Although the bacteria of acute cholecystitis are

undoubtedly enteric in origin, the route of entryinto the biliary tract remains uncertain. Ascendinginfection would seem to be the most likely expla-nation. However, there is good evidence that he-matogenous spread with direct infection throughthe thickened gallbladder walls also leads to acute

cholecystitis. 18

DIAGNOSIS

To effectively treat acute cholecystins you must

first recognize the clinical picture. Other than bil-iary disease, the differential diagnosis in a pregnantwoman with right upper quadrant pain includesprccclampsia, pyclonephritis, appendicitis, andeven gastric ulcer. After initial evaluation excludesthese and other less common entities from the dif-ferential diagnosis, the diagnosis of biliary diseaseshould be further investigated. As stated earlier,differentiating cholelithiasis from acute cholecysti-tis can be difficult. This is especially true whenpregnancy complicates the clinical picture. Someclinicians argue that differentiating between thetwo would not affect management. At any rate, theclinical manifestations of acute cholecystitis duringpregnancy are essentially the same as the non-

pregnant state.

HISTORY

An episode of biliary pain usually begins with rightupper quadrant or mid-epigastric pain which mayincrease in severity. Biliary colic begins quite sud-denly and may radiate to the interscapular area, to

the angle of the right scapula, or to the right shoul-der. It may be precipitated by a fatty meal or byconsumption of a large meal following a period offasting. Typically though, biliary colic occurs in a

diurnal pattern with pain peaking around midnight.Nausea and vomiting also frequently accompanyepisodes of colic. Finally, 70-80% of patients willhave a history of colic attacks and fatty food intol-erance. 13 Increasing severity of colicky pain, fever,or chills (rigors) usually implies an underlying com-plication, i.e., cholecystitis, pancreatitis, or cholan-gitis.

PHYSICAL EXAMINATION

Physical examination reveals right upper quadranttenderness. This is usually associated with an in-crease in pain to palpation upon deep inspiration(Murphy’s sign). Fever and tachycardia may indi-cate an underlying infection. The presence of peri-toneal signs, guarding, rigidity, and rebound, are

extremely ominous signs and may reflect rupture ofthe gallbladder.

LABORATORY FINDINGS

Laboratory evaluation may provide assistance in di-agnosis but it is clear that the clinical course willdictate the management plan. Laboratory studiescommonly performed when evaluating thesewomen include blood leukocyte count, evaluationof hepatic function, serum bilirubin, amylase, li-pase, and alkaline phosphatase. There are numer-ous alterations in several of these laboratory param-eters which normally occur in pregnancy and can

limit their usefulness. The blood leukocyte count

varies considerably during normal pregnancy. Val-ues can range from 5,000 to 12,000/ml and thesevalues may rise significantly with exercise or labor.Also, alkaline phosphatase activity nearly doublesduring normal pregnancy. Finally, postprandialplasma levels of total bile acids progressively in-crease during pregnancy. Therefore, laboratoryevaluation will only provide clues in the diagnosisof biliary tract disease during pregnancy. For ex-

ample, serum bilirubin may be mildly elevated andleukocytosis may be present. If bilirubin remainselevated with persistent jaundice, common ductstones should be suspected. If there is significantleukocytosis in addition, an underlying infectiousprocess should be considered. Finally, serum amy-

INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY 305


lase, lipase, and alkaline phosphatase may be ofsome assistance in identifying pancreatic involve-ment. 17

RADIOGRAPHIC EVALUATION

Ultrasound has revolutionized the accuracy andsafety of diagnosing biliary tract disease. It has allbut replaced oral cholecystography and intravenous

cholangiography as the standard for diagnosis of

gallbladder disease. Ultrasonography, as a rulethough, provides no direct evidence of acute cho-

lecystitis. Conversely, intravenous cholecystogra-phy gives a more functional diagnostic view of cho-

lecystitis by directly revealing blockage of the cys-tic duct and biliary stasis.

Additional sonographic findings may aid in dif-ferentiating cholelithiasis from acute eholecystitis.These include gallbladder wall thickening, gall-bladder distention, and tenderness upon deforma-tion of the gallbladder with the ultrasound trans-

ducer (sonographic Murphy’s sign). However, none

of these findings is an absolute indicator of acute

cholecystitis. In fact, when reviewing the literature,several studies both support and refute the use ofgallbladder wall thickening and sonographic Mur-phy’s sign to differentiate biliary colic from acute

calculous or acalculos cholecystitis,s’lg,z

In other words, ultrasound is imperfect in dem-onstrating biliary stones impacted in the cystic ductand this, unfortunately, is the cardinal sign of acutecholecystitis,e Nevertheless, ultrasound has no

known medical contraindications or adverse sideeffects and should be used as the first line of diag-nostic study. One study reported a 96% sensitivityand 88% specificity for ultrasound in the diagnosisof cholecystitis when combined with all of theclinical criteria previously described,e The overallaccuracy of ultrasound in diagnosing acute chole-cystitis is 93%. The same study cited above re-

ported an overall accuracy of intravenous cholecys-tography as 88%; however, this was felt to be due to

impaired hepatic excretion of contrast medium.

Finally, the use of intravenous contrast media

always runs the risk of hypersensitivity reactions. Itis, therefore, reasonable to conclude that ultra-sound is accurate, safe, and the most practicalmethod for diagnosing acute cholecystitis in preg-nancy.

TREATMENT

Medical Management

The primary issue in the management of acute

cholecystitis is when to intervene surgically. Initial

medical therapy is appropriate in all patients with

biliary tract disease, however, clinicians should not

procrastinate when surgery is indicated. Medical

therapy includes eliminating oral intake, nasogas-tric suction, correction of electrolyte abnormalities,and analgesia. Morphine analgesia and its deriva-tives should be avoided, as they may cause spasmof the sphincter of Oddi. This spasm may exacer-

bate an already painful condition. Finally, intrave-

nous antibiotic therapy is usually indicated in pa-tients with suspected acute cholccystitis, even

though superinfection of the bile/gallbladder maynot occur until the latter stages of disease.The combination of a penicillin and an

aminoglycoside has long been recommended as theinitial treatment of choice for patients with infec-tions of the biliary tract. This initial antibiotictherapy is empirically based on the bacterial floralikely to bc encountered in the biliary tract.

Aminoglycosides are used to treat gram-negativefacultativc biliary pathogens including pseudomo-nas. Penicillins offer adequate gram-positive cov-

erage. Specifically, ampicillin will cover most an-

aerobes and enterococcus species. Therefore, their

combination would empirically provide good anti-biotic coverage in patients with evidence of acute

cholecystitis.Concern about aminoglycosidc-induced nephro-

toxicity in patients with jaundice and sepsiscoupled with the development of newer, more ef-fective cephalosporins has challenged penicillinplus aminoglycoside use as the preferred treatment

in acute cholccystitis. Specifically, improved cov-

erage against Bacteroides sp. by some second andthird generation cephalosporins has led to their in-creased use in both prophylaxis and treatment re-

gimes. In one study, cefepime, a third generationcephalosporin, was compared to mezlocillin andgentamicin therapy in patients with acute chole-cystitis undergoing cholecystectomy. The resultsindicated that single drug therapy with cefepimcwas as effective as combination therapy with mcz-

locillin and gentamicin, el Cefepime, like manylater generation cephalosporins, requires 12 h dos-

ing and can achieve high bile, blood, and gallblad-



der levels. Ultimately, with increased cost con-

sciousncss, decreased drug monitoring and fewerdoses mean lower overall costs related to cephalo-sporin use.

Pipcracillin, an extended spectrum penicillin,has broad coverage against all organisms commonlybound in the biliary tract, excellent biliary excre-

tion, and negligible nephrotoxicity. It has also beenshown to be efficacious in patients with acute cho-lecystitis, zz,z’ The overall cure rate for acute cho-lecystitis in patients treated with piperacillin, am-

picillin and tobramycin, or cefopcrazonc was 92%with no difference in any of the three groups,zz

Hence, when considering antibiotic therapy in pa-tients with acute cholecystitis, the standard of a

penicillin and an aminoglycosidc remains an effec-tive regimen. However, when considering more

current issues such as cost containment, alterna-tives including extended spectrum penicillins or

third generation cephalosporins cannot be ignored.In managing acute cholecystitis in pregnancy,

many physicians advocate initial non-operativemanagement in an effort to prevent surgical inter-

vention prior to completion of the pregnancy. Thepregnancy outcomes are highly dependent on thetrimester during which the biliary symptoms occur.

One study evaluated 26 pregnant patients withacute cholecystitis in all three trimesters. Only 2 ofthe 7 patients who presented in the first trimesterhad pregnancies which went to term, whereas allpatients who presented in the third trimester com-

pleted a successful pregnancy,z4 Twenty of the pa-tients did not require operation before resolution ofthe pregnancy. Non-operative therapy has classi-

cally been the primary goal for pregnant women

with acute cholecystitis.Having said that, there is evidence to suggest a

high rate of recurrence of biliary pain in pregnancycomplicated by cholelithiasis and cholecystitis. In a

recent retrospective review of 44 women with bil-

iary colic or cholecystitis, experience with conser-

vative, non-operative therapy was not favorable.Twenty-six of the 44 patients were managed con-

servatively and 58% of those had recurrent symp-toms. Twenty-seven percent of these women were

rehospitalized two or more times during their preg-nancy. The average hospital stay for these womenwas 14 days as opposed to 6 days for the group with

surgical intervention,zs

Surgical ManagementThe implication is that cholecystcctomy should bcconsidered early in the management of thesewomen. With regard to non-obstetric surgicaltherapy, several comments can be made. Duringpregnancy appendicitis is the most common indi-cation for non-obstetric surgery followed by adnex-al masses and cholecystectomy,z6 Cholecystectomyis performed at a rate of 1-6/10,000 pregnancies,z7

In a review of approximately 50,000 pregnancies,the preterm delivery rate within 2 weeks of anysurgery was significantly higher in the third trimes-

ter than in the second trimester (25.7% vs. 8.2%).Also, there was a trend toward prcterm delivery forthose procedures performed emergently vs. thosethat were planned. Finally, in this study, tocolyticagents were not found to be beneficial,z7

Based on the current literature, the followingoverall recommendations can be made with regardto management of pregnant women with acute cho-lecystitis. First, prepregnancy cholecystectomy is

advised in those women with a history of choleli-thiasis. Second, biliary colic or acute cholccystitisoccurring during the first trimester of pregnancyshould initially be treated medically. If possible,elective surgery should be scheduled for the sec-

ond trimester. Biliary symptoms occurring in thesecond trimester should ideally be treated surgi-cally. Finally, symptoms of biliary colic or evidenceof acute cholecystitis in the third trimester shouldbe treated medically, when possible. Postpartumsurgical therapy should then be pursued,zs In con-

clusion, due to high recurrence rates of biliarysymptoms in pregnant women with acute cholecys-titis, surgery should be considered early in manage-ment as opposed to postponing definitive therapy.

Once the decision for surgical intervention hasbccn made, the question is which approach shouldbe used. The options include endoscopic retro-

grade cholangiopancreatography (ERCP) with

sphincterotomy and stone removal, laparoscopiccholecystectomy, or open cholecystectomy. Prior to

any of the above procedures, however, appropriateantibiotics should be instituted.

With respect to ERCP with sphinctcrotomy andstone removal, conventional wisdom is that due to

potential radiation-induced damage to the fetus,fluoroscopic procedures should be avoided. Severalstudies in the second and third trimesters, how-



ever, have reported successful pregnancy outcomes

following ERCP with biliary stone removal,zS,z9

Additionally, Hoffman and Cunningham3 re-

ported four pregnant women who underwentERCP during the first trimester. In this report, ra-

diation exposure after appropriate abdominalshielding was calculated and found to be well be-low levels at which damage to the fetus can occur."Ultimately, then, ERCP with sphincterotomy andstone removal and possible stcnting of the gallblad-der appears to be a safe procedure in pregnantwomen with uncomplicated cholelithiasis.31

In cases of acute cholecystitis or complicatedcholelithiasis, depending on gestational age at di-

agnosis, the surgical management may differ. Lap-aroscopic cholecystectomy in pregnancy was firstreported in 1991. 3z The laparoscopic approachtheoretically avoids potential postoperative compli-cations such as thrombophlebotic and embolic

events in the pregnant, hypcrcoagulablc state. This

report described a pregnancy in the early secondtrimester with the uterus at the pelvic brim. Thepatient was discharged on postoperative day with

an eventual successful pregnancy outcome)z Lap-aroscopic cholecystectomy has been performedsuccessfully in non-pregnant patients with acute

cholecystitis, common duct stones, previous surgi-cal history, obesity, coagulopathy, and dilatedbowel.33 Also, gynecologic laparoscopics are fre-quently performed during pregnancy.e Therefore,a laparoscopic cholecystectomy is a reasonable con-

sideration in pregnant women. Despite longer sur-

gery times, reduced morbidity and mortality alongwith decreased cost of hospitalization justifies itsuse in experienced hands. Pregnancy should not beconsidered an absolute contraindication to the lap-aroscopic approach in these patients.

There is no consensus, however, at what gesta-

tional age/uterine size laparoscopy would be con-

traindicated. Clear contraindications such as sepsis,cholangitis, common duct stones, and portal hyper-tension would still apply."’,4 If it is the opinion ofthe experienced surgeon that he or she cannot

safely place the trocar into the peritoneal cavity or

perform an open laparoscopy, the traditional lapa-rotomy approach should be the treatment ofchoice. As stated previously, tocolytic therapy hasbeen shown to be of no benefit in these patients,z6

CONCLUSION

Biliary tract disease in pregnancy is a relatively un-

common occurrence. Because of the heterogeneousnature of the disease, progression to acute chole-cystitis can be difficult to recognize. Once diag-nosed, the initial management plan should be con-

servative and include institution of antibiotictherapy. Then, depending on the gestational age at

diagnosis, the management plan may differ. Surgi-cal intervention, when indicated, should not be de-layed and a planned intervention during the secondtrimester appears to offer a better outcome thansurgery performed under emergent conditions,e6

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