© 2002 The Society for Surgery of the Alimentary Tract, Inc. 1091-255X/02/$—see front matterPublished by Elsevier Science Inc. PII: S1091-255X(02)00063-X

Original Articles

862

Surgical Management of Abdominal Tuberculosis

Imran Hassan, Emmanouil S.

Brilakis, Rodney L. Thompson, Florencia G. Que, M.D.

Recent reports suggest an increased incidence of abdominal tuberculosis in the United States, particularlyin high-risk groups. The aim of this study was to review the spectrum of abdominal tuberculosis and itssurgical management at a tertiary referral center in the United States. The medical records of patientstreated for abdominal tuberculosis at our institution between January 1992 and June 2001 were retro-spectively reviewed. Eighteen patients were diagnosed with abdominal tuberculosis by microbiologicand/or histologic examination. The 10 men and eight women had a mean duration of symptoms of 4months (range 1 to 24 months). Five were born in the United States, and 13 were foreign born (7 Asiansand 6 Africans). The United States–born patients with abdominal tuberculosis, as compared to the for-eign-born patients, were older (mean age 74 years

vs.

35 years), more likely to have chronic medical ill-nesses (80%

vs.

7%), and had concomitant pulmonary tuberculosis (60% vs.

0%). Computed tomographywas the most frequent imaging modality (88%); findings suggestive of abdominal tuberculosis were me-senteric/omental stranding (50%), ascites (37%), and retroperitoneal lymphadenopathy (31%). Seven-teen of the 18 patients required operative intervention, and one patient underwent CT-guided drainageof a psoas abscess. Laparoscopy was useful for diagnosis in eight patients; laparotomy was performed forcomplications of abdominal tuberculosis in six patients and to obtain a tissue diagnosis in three patients.Abdominal tuberculosis continues to represent a diagnostic challenge to clinicians. Among native-bornwhite Americans, abdominal tuberculosis is primarily a disseminated disease of elderly, debilitated pa-tients with chronic illnesses. Among foreign-born individuals, abdominal tuberculosis occurs in young,immunocompetent patients from endemic areas. Characteristic CT findings should be evaluated for ab-dominal tuberculosis in the appropriate clinical setting. Laparoscopy is an effective modality for diagnosisof peritoneal tuberculosis. ( J G

ASTROINTEST

S

URG

2002;6:862–867.) © 2002 The Society for Surgery

of the Alimentary Tract, Inc.

K

EY

WORDS

: Abdominal tuberculosis, United States, management, laparoscopy, CT scans

During the second half of the twentieth century, asa result of improved nutrition, reduced crowding,public health measures, and effective chemotherapy, adramatic decrease in the incidence of tuberculosis wasseen in the United States. However, with the adventof the human immunodeficiency virus (HIV) in the1980s and an increase in the immigrant population inthe 1990s, there has been a resurgence of tuberculosisin this country.

1

HIV is a major risk factor for the de-velopment of clinical tuberculosis. It has been esti-mated that a person who is infected with both HIVand tuberculosis has a 7% to 10% chance per year ofdeveloping active tuberculosis, as opposed to the 10%lifetime chance of someone who is infected with tu-

berculosis alone.

2

At the same time, epidemiologicfigures have shown an increase in the number of for-eign-born persons with tuberculosis. In 1997, 39% ofthe cases of tuberculosis in the United States were inforeign-born individuals as compared to 27%, 5 yearsearlier.

3

Several reports have also shown a relativelyhigh incidence of extrapulmonary disease amongHIV-infected individuals and the immigrant popula-tion with tuberculosis.

4

As a result, the proportion ofcases of tuberculosis involving extrapulmonary sitesincluding the abdomen has steadily increased in theUnited States from 8% in 1964 to 26.6% in 1998.

3,5

Abdominal tuberculosis has protean manifesta-tions and is known to imitate a variety of intra-ab-

Presented at the Forty-Third annual meeting of The Society for Surgery of the Alimentary Tract, San Francisco, California, May 19–22, 2002(poster presentation) and published as an abstract in

Gastroenterology

.From the Department of Surgery (I.H., F.G.Q.) and Division of Infectious Diseases (E.S.B., R.L.T.), Mayo Clinic, Rochester, Minnesota.Reprint requests: Florencia G. Que, M.D., Department of Surgery, 200 First Street, SW, Mayo Clinic, Rochester, MN 55905. e-mail: que.florencia@mayo.edu

Vol. 6, No. 62002 Surgical Management of Abdominal Tuberculosis

863

dominal disorders.

6

Unless there is a high index ofsuspicion, this diagnosis is often overlooked, result-ing in significant morbidity and mortality. Recentstudies on the surgical management of abdominal tu-berculosis in the United States have come from re-gions where the incidence of HIV is high and wherethere are large immigrant populations.

5,7

The pur-pose of our review was to determine the spectrum ofabdominal tuberculosis and its surgical managementin an area where these groups are not as prevalent.

PATIENTS AND METHODS

From January 1992 to June 2001, 18 patients werediagnosed with abdominal or pelvic tuberculosis atour institution. Traditionally, reports of abdominaltuberculosis included infection of the gastrointesti-nal tract, peritoneum, mesentery, abdominal lymphnodes, liver, spleen, and pancreas. In addition tothese sites, we also included patients with pelvic dis-ease in this series. The diagnosis of abdominal tuber-culosis was made if tissue obtained during laparo-tomy or laparoscopy yielded positive cultures for

Mycobacterium tuberculosis

complex and/or acid-fastbacilli were seen on histologic examination of thespecimen along with strong clinical evidence. Pa-tients with

Mycobacterium avium

intracellulare (MAC)infections were excluded. Details of culture tech-niques have been described in detail previously

8

andwill be summarized as follows. Specimens weretreated with equal volume of BBL MycoPrep Re-agent (BD Diagnostic Systems, Sparks, MD) con-taining 2% NaOH and

N

-acetyl-

L

-cysteine mixedand incubated at 25

�

C for 15 minutes. After the ad-dition of MycoPrep buffer and centrifugation, thesupernate was removed and the sediment was sus-pended in 3 ml of MycoPrep phosphate buffer. Cul-tures were performed by inoculating 0.5 ml of sedi-ment into a MGIT tube and onto each side of abiplate that contained Middlebrook 7H10 agar andMiddlebrook 7H11 selective agar with antimicrobials(Remel, Lenexa, KS). After inoculation, tubes wereplaced into the BACTEC MGIT 960 System and in-cubated at 35 to 37

�

C for 6 weeks. Biplates weresealed in polyethylene bags and incubated at 37

�

C inthe presence of 5% to 7% CO

2

, and observed weeklyfor the presence of growth over an 8-week incubationperiod.

Patient histories including the surgeon’s operativenotes, hospital records, and follow-up data were re-viewed for variables including patient age, sex, nation-ality, presenting symptoms and duration, history oftuberculosis exposure, preoperative laboratory values,radiographic investigations, type of operation, micro-

biological stains, cultures and susceptibilities, postop-erative course, and follow-up.

RESULTSPatient Demographics

There were 10 men and eight women, whose av-erage age was 44 years (range 16 to 88 years); themean duration of symptoms was 4 months (range 1to 24 months) in the symptomatic patients. Five pa-tients were born in the United States and 13 wereforeign born. Among the foreign-born patients,there were seven immigrants: six from Africa (4 fromSomalia, 1 each from Ethiopia and Kenya) and onefrom India. The average duration of United Statesresidence of the immigrants prior to presentationwas 60 months (range 14 to 134 months). Six pa-tients had come from abroad for medical treatment,including four patients from the United Arab Emir-ates and one patient each from Saudi Arabia and Ku-wait. Therefore there were three main groups of pa-tients identified in our cohort. The first group (n

�

5) was comprised of patients who were native-bornwhite Americans and were, on average, older than therest of the patients (mean age 74 years). The secondgroup (n

�

7) included patients who had emigratedto the United States. These individuals were younger(mean age 26 years) than the others and were other-wise healthy. The third group (n

�

6) of patientswere those who had come to our institution for treat-ment from abroad and were of an intermediate agegroup (mean age 41 years). There was no differencein the duration of symptoms prior to diagnosis amongthe three groups.

Clinical Presentation

Abdominal pain (76%), weight loss (64%), fever(35%), and abdominal distention (24%) were themost common presenting signs and symptoms. Onepatient was asymptomatic at presentation (Table 1).Five patients had concomitant extra-abdominal sitesof tuberculosis: three patients with pulmonary tuber-culosis and one patient each with cervical lymphnodes and central nervous system involvement. Tu-berculosis was suspected preoperatively in 12 (66%) of18 patients. The preoperative diagnoses in the re-maining patients included lymphoma in three, ovariancystic mass in two, and disseminated intra-abdominalmalignancy in one. Five patients (27%) had a historyof prior tuberculosis exposure (two patients each fromgroups 1 and 3 and one patient from group 2).

Associated comorbid conditions included hemato-logic malignancies in two patients (chronic lympho-cytic leukemia and myelodysplastic syndrome in one

Journal of

864

Hassan et al. Gastrointestinal Surgery

patient each), diabetes mellitus, and long-term ste-roid use for polymyalgia rheumatica and alcoholismwith cirrhosis in one patient each.

Laboratory Investigations

Seventeen patients (94%) were anemic preopera-tively. The average hemoglobin concentrations formen and women were 12 g/dl and 10.6 g/dL, respec-tively (normal value for men, 13.5 mg/dl; normal forwomen, 11.5 mg/dl). Three patients had leukocytosis(

�

10

�

10

9

/L), and none had significant monocytosisor lymphocytosis. Ten patients (55%) had hypoalbu-minemia (serum albumin

�

3.5 g/dl). More than twicethe normal elevation in transaminases and alkalinephosphatase levels was seen in six patients (33%). Ele-vation (

�

30 mm/hr) in the erythrocyte sedimentationrate was seen in nine patients (50%). Results of tuber-culin skin testing were available for 14 patients; inter-mediate purified protein derivative (PPD) was positivein six patients and negative in eight. HIV serology inall 10 patients who were tested was negative.

Radiologic Findings

Six (33%) of the 18 patients had an abnormal chestradiograph. Abnormalities noted included pleural ef-fusion (2 patients), pulmonary infiltrate (2 patients),apical opacity (1 patient), and soft tissue prominencearound the gastroesophageal junction (1 patient). Thelatter was subsequently found to represent asymptom-atic retroperitoneal lymphadenopathy around the ce-liac artery and the aorta. All three patients with activepulmonary tuberculosis had an abnormal chest radio-graph.

CT scanning was the most frequently used ab-dominal imaging modality (16 patients) followed bygastrointestinal contrast studies (4 patients), colon-

oscopy (3 patients), and abdominal ultrasonography(3 patients). The most common CT findings in ab-dominal tuberculosis were ascites, lymphadenopa-thy, and omental/mesenteric stranding (Table 2).

Operative Findings and Management

Seventeen patients underwent surgical proce-dures, whereas one patient had CT-guided drainageof a psoas abscess. All operations were performedelectively, with the exception of one emergent sur-gery for a tuboovarian abscess. Of the patients re-quiring surgery, eight underwent a laparoscopic ex-ploration, whereas nine underwent a laparotomy.Seven (out of 8) patients undergoing laparoscopyhad peritoneal tuberculosis, with diffuse involvementof the visceral and parietal peritoneum and innumer-able peritoneal nodules or plaques, usually with as-cites. In these patients, laparoscopic peritoneal biop-sies were obtained to confirm the diagnosis.

Among the patients who underwent open explora-tory operations, two had pelvic tuberculosis withtuboovarian abscesses and required salpingo-oopho-rectomy. Two other patients had gastric outlet ob-struction from retroperitoneal and gastroduodenallymphadenopathy causing compression of the py-lorus. One patient required a gastrojejunostomy,whereas the other had a venting gastrostomy and afeeding jejunostomy. Two other patients were foundto have an ileocecal mass from lymphadenopathy inthe intestinal mesentery, resulting in narrowing of thebowel lumen and abdominal pain. Both of these pa-tients underwent a right hemicolectomy with primaryanastomosis. One patient each had lymphadenopathyin the small bowel mesentery forming a mass, retro-peritoneal lymphadenopathy along the celiac artery,hepatic artery, and aorta, and diffuse hepatic disease,respectively (Table 3). These three patients under-went excisional biopsies to establish a tissue diagnosis.

There was no significant operative morbidity ormortality among the patients who underwent surgery.

Table 1.

Presenting signs and symptoms in patients with abdominal tuberculosis

Signs and symptomsNo. of patients (%)

n

�

17*

Pain 13 (76)Weight loss 11 (64)Fever 6 (35)Nausea/emesis 5 (29)Fatigue 4 (24)Abdominal distention 4 (24)Anorexia 3 (18)Abdominal mass 3 (18)Night sweats 3 (18)Abdominal tenderness 3 (18)

*One patient was asymptomatic.

Table 2.

CT scan characteristics of patients with abdominal tuberculosis

CT findings

No.

of patients (%)n

�

16

Ascites 6 (37)Retroperitoneal lymphadenopathy 5 (31)Mesenteric stranding 4 (25)Omental stranding 4 (25)Mesenteric mass/lymphadenopathy 3 (19)Bowel wall thickening 2 (13)

Vol. 6, No. 62002 Surgical Management of Abdominal Tuberculosis

865

Pathology, Microbiology, and Chemotherapy

Pathologic examination of operative specimensshowed necrotizing and non-necrotizing granulomasconsistent with granulomatous disease in all patients.Patients were started on the standard four-drug antitu-berculous regimen after a clinical diagnosis of abdomi-nal tuberculosis, based on operative and pathologicfindings.

Mycobacterium tuberculosis

organisms were sub-sequently cultured in 17 patients and were fully sensi-tive to isoniazid, rifampin, ethambutol, pyrazinamide,and streptomycin in all cases. Drug regimens and dura-tion of treatment were then adjusted according to themicrobiological sensitivities, extent of extra-abdominalinvolvement, and resolution of symptoms. The meanlength of proposed treatment was 6 months (range 6 to18 months). Routine follow-up abdominal studies werenot performed in patients who responded appropriatelyto chemotherapy and were doing well clinically oncethey completed their treatment.

Two patients developed significant liver functionabnormalities after chemotherapy was initiated, ne-cessitating temporary discontinuation of therapy.Treatment was reinstituted at a lower dosage oncehepatic enzyme levels normalized.

Follow-Up

Mean follow-up was 18 months (range 1 to 60months). One patient died 4 years after diagnosis ofabdominal tuberculosis from his underlying hemato-logic malignancy. One female patient who had pelvictuberculosis developed infertility and is currently un-dergoing evaluation for in vitro fertilization.

DISCUSSION

Our review highlights several of the tribulationsthat the diagnosis and treatment of abdominal tuber-

culosis pose for physicians in the United States. In thefirst group, which consisted of native-born patients,abdominal tuberculosis was suspected preoperativelyin only one of them. The majority had concomitantactive pulmonary disease and associated chronic med-ical illnesses. These findings are similar to those ofprevious studies on tuberculosis among the native-born white American population. Reactivation diseaseis mainly seen in elderly debilitated patients withchronic illnesses, and these patients are more likely tohave disseminated multiorgan disease.

9

The presenting signs and symptoms, as well as thephysical findings in our series, were nonspecific andnondiagnostic, and this resulted in a significant delayin diagnosis. This observation is similar to those inpreviously published reports on this condition.

9–11

Patients had anemia and hypoalbuminemia, reflect-ing a chronic malnourishing process, although labo-ratory investigations could not reliably distinguishabdominal tuberculosis from other chronic diseaseprocesses. HIV infection was not identified in ourcohort and has a low prevalence in our patient popu-lation. All patients in this country who present withtuberculosis, however, must be screened for HIV.The incidence of liver enzyme abnormalities was notas high, as was reported in a recent series.

7

This mostlikely reflects differences in study populations, sincetheir cohort had several patients with HIV infectionin whom liver enzyme abnormalities may have beenthe result of the underlying disease, its complica-tions, or its treatment. It is important to monitor he-patic function in these patients during treatment fortuberculosis, because several first-line antituberculardrugs are hepatotoxic.

Tuberculin skin tests were positive in only 42% ofthe patients and could not be used as a dependablepredictor of disease. This test has been shown to havea lower specificity for abdominal disease as comparedto pulmonary tuberculosis.

11

Particularly in areaswhere tuberculosis is endemic, it has been found tohave a high false positive rate.

11

Furthermore, thetuberculin skin test cannot accurately differentiatebetween active disease and previous sensitization bycontact or vaccination.

10

In general, experience sug-gests that a positive PPD in a patient from an areawhere tuberculosis is endemic should be attributedto exposure and infection, not vaccination, whereas anegative PPD does not rule out disease in any case.The incidence of concurrent active pulmonary dis-ease in patients with abdominal tuberculosis was low(16%) in our series. Although some investigaors havenoted a higher incidence of active pulmonary in-volvement, there have been several recent reportsshowing a similar low incidence of active pulmonarytuberculosis in patients with abdominal tuberculo-

Table 3.

Intra-abdominal sites of tuberculosis involvement

Site of involvementNo. of patients (%)

n

�

18

Peritoneal 8 (44)Gastroduodenal 2 (11)Ileocecal 2 (11)Tuboovarian 2 (11)Retroperitoneum 2 (11)Liver 1 (6)Mesenteric 1 (6)

Journal of

866

Hassan et al. Gastrointestinal Surgery

sis.

6

The pathogenesis of abdominal tuberculosis ispresumed to involve hematogenous spread from aprimary focus in the lung, ingestion of infected spu-tum, or local reactivation of disseminated infectionat a much later date. It has therefore been suggestedthat these patients may have had previous undiag-nosed pulmonary tuberculosis, which has either re-solved or is just not radiologically apparent.

1

It isnecessary to consider the diagnosis of abdominal tu-berculosis, despite the absence of clinical or radio-logic evidence of active pulmonary tuberculosis.

CT scanning was the most common imagingstudy used in our series. Although CT was unable tospecifically differentiate this condition from otherintra-abdominal disorders, it was sensitive in detect-ing various intra-abdominal abnormalities that aretypical of abdominal tuberculosis. In the appropriateclinical settings, patients with a constellation of char-acteristic CT findings such as retroperitoneal lym-phadenopathy, bowel wall thickening, ascites, oromental and mesenteric stranding should be sus-pected of having abdominal tuberculosis and shouldbe evaluated accordingly. Colonoscopy and gas-trointestinal contrast studies were useful adjuncts indiagnosing patients with abdominal tuberculosis in-volving the gastrointestinal tract. Ultrasound wasable to detect abnormalities in the pelvis in both pa-tients with pelvic tuberculosis that presented as tu-boovarian abscesses. It is recommended that thesediagnostic modalities be considered in conjunctionwith clinical findings, laboratory investigations, andCT scans to establish a definitive diagnosis.

The role of surgery has traditionally been de-scribed as being limited to managing complicationsfrom abdominal tuberculosis.

9,12

In our series, com-plications resulting from abdominal tuberculosiswere seen in only six patients (33%). These includedgastric outlet obstruction from gastroduodenal ret-roperitoneal lymphadenopathy, intestinal obstruc-tion and pain from an ileocecal mass, and tuboova-rian abscesses. Surgery, and laparoscopy inparticular, however, was more commonly used as adiagnostic modality especially in patients with peri-toneal tuberculosis. The preoperative investigationsand radiographic findings in these patients are non-specific, and it is often not possible to differentiateperitoneal tuberculosis from a disseminated malig-nancy or primary liver disease. Ascitic fluid, which isusually present in these patients, can be obtained viaparacentesis, but the isolation rate for

Mycobacteriumtuberculosis

is only 20%,

13

whereas the sensitivity andspecificity of various chemical tests on the asciticfluid, such as the adenosine deaminase assay, are stillapproximately 80%.

13

In these patients, laparoscopicexploration provides an ideal opportunity to examine

the intra-abdominal contents and establish a clinicaldiagnosis while obtaining sufficient tissue for histo-logic and microbiologic examination.

Pelvic tuberculosis is not conventionally includedin discussions of abdominal tuberculosis. We believethat involvement of the pelvic organs is a continuumof the abdominal process demonstrating the poten-tial for this disease to affect any organ in the body.The significance of pelvic tuberculosis lies in itslong-term consequences with regard to the fertilityof female patients. A high incidence of infertility hasbeen reported in patients with pelvic tuberculosis,

14

and hence this should be kept in mind when treatingand counseling these patients.

With the increased incidence of tuberculosis incertain high-risk groups such as immigrants and HIV-infected individuals, the number of patients withabdominal tuberculosis will increase in this country.However, because of its nonspecific presentation andthe lack of reliable diagnostic tests, abdominal tuber-culosis will continue to present a challenge to the cli-nicians evaluating these patients. Immigrants or visi-tors from areas where tuberculosis is endemic whohave characteristic CT findings and symptoms shouldalways be evaluated for the possibility of abdominaltuberculosis. Laparoscopy is an effective modality fordiagnosis of patients with peritoneal tuberculosis andshould be considered in cases where there is a clinicalsuspicion of the disease. Mortality in these patients isrelated to the underlying disease process and not tothe abdominal tuberculosis itself. The outcome of im-munocompetent patients with abdominal tuberculosisis favorable, but long-term follow-up is important.

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