Incidental peritoneal tuberculosis: surgeon’s dilemma in endemic regions

Abstract

Background:

Peritoneal tuberculosis has varying clinical manifestations. The study was conducted to highlight the entity of incidental peritoneal tuberculosis. Diagnostic and therapeutic dilemma is likely to occur on detection of unexpected peritoneal nodules.

Materials and methodology:

Incidental peritoneal tuberculosis was defined as peritoneal tuberculosis (peritoneal tubercles or ascites) detected intraoperatively in patients undergoing surgical exploration for other indications with no preoperative suspicion of abdominal tuberculosis or active tubercular lesions anywhere in the body. Retrospective analysis of patients operated in our department from June 2016 to November 2017 was performed.

Results:

Of the 409 patients operated, 5 patients (1.2%) had incidental peritoneal tuberculosis. The primary indication of surgery was laparoscopic cholecystectomy in three, restoration of bowel continuity in one and laparoscopic appendectomy in one. Two patients had remote history of antitubercular therapy for pulmonary and nodal tuberculosis, respectively. The three patients planned for laparoscopic cholecystectomy had their procedures deferred on suspicion of peritoneal carcinomatosis. Subsequently, all the three underwent cholecystectomy after completion of antitubercular treatment. None of the resected specimen (gallbladder/appendix/colon) had evidence of tuberculosis (acid fast bacilli positive or caseating granuloma). Antitubercular treatment for 6 months was completed in all the patients with active peritoneal disease.

Conclusion:

Incidental peritoneal tuberculosis represents an uncommon form of peritoneal tuberculosis. Absence of prior tuberculosis does not preclude the diagnosis of peritoneal tuberculosis. In an endemic region of tuberculosis, surgeons must be aware of the entity on encountering such finding. Frozen section can help in guiding appropriate management.

Introduction

Peritoneal tuberculosis is a form of abdominal tuberculosis affecting both visceral and parietal peritoneum. The spectrum of manifestations ranges from chronic subacute states to surgical emergencies. ¹ Little is known about the apparently asymptomatic individuals with peritoneal tuberculosis diagnosed during surgical exploration. We present five cases of incidentally detected peritoneal tuberculosis in individuals undergoing abdominal surgery for other indications and three of whom had no prior history or exposure to tuberculosis.

Methodology

Retrospective analysis of patients who had undergone surgery between June 2016 and November 2017 was done. We included cases where peritoneal tuberculosis was detected unexpectedly for surgery done for other indication.

Diagnosis of peritoneal tuberculosis

Diagnosis of ‘definite peritoneal tuberculosis’ was made in patients with atleast one of the following:

Figure 1.

Panel of histopathological images. (a) Low-power microscopic image (10×) showing multiple epitheloid cell granulomas. (b) High-power microscopic image (40×) showing scattered multinucleated giant cells (black asterisk). (c) and (d) Low-power (10×) and high-power (40×) images showing epitheloid cell granulomas with central areas of necrosis (black asterisk) surrounded by multinucleated giant cells with lymphocytic cuffing. Histopathology was suggestive of TB.

1. Histopathology examination of suspected nodule (peritoneum or omentum) showing the presence of caseating granulomatous inflammation with or without demonstration of acid fast bacilli (AFB).

Diagnosis of presumed peritoneal tuberculosis was made in the absence of histological confirmation with all of the following:

1. The presence of peritoneal calcification in the absence of known etiologies (e.g. peritoneal dialysis) with remote history of antitubercular medication or tubercles or yellow–white miliary nodules over parietal and/or visceral peritoneum ² or thick membrane encasing bowel loops (cocoon).

2. The presence of granuloma or ascitic fluid analysis having adenosine deaminase greater than 39 IU/ml with no atypical or malignant cells ³ or a response to antitubercular therapy with resolution of ascites or peritoneal nodules ⁴

Criteria for incidental peritoneal tuberculosis: (1) definitive or presumed peritoneal tuberculosis, (2) no preoperative suspicion of abdominal tuberculosis and (3) no active tubercular lesions anywhere else in the body.

Results

A total of 409 cases were operated during the period of which 5 (1.2%) patients had incidentally detected peritoneal tuberculosis (1 confirmed and 4 presumed). During the same period, 31 (7.6%) patients had undergone surgical intervention for symptomatic abdominal tuberculosis. Details of these cases are given in Table 1. Three patients were planned for laparoscopic cholecystectomy. In all these cases, the planned procedure was deferred on suspicion of peritoneal carcinomatosis intraoperatively. Two of these patients had complete resolution following antitubercular treatment (ATT) and subsequently underwent laparoscopic cholecystectomy. The other underwent open cholecystectomy in view of dense adhesions. Laparoscopic appendectomy was performed in one patient, and one patient had peritoneal tuberculosis on exploration for restoration of bowel continuity. None of them evidence of tuberculosis (AFB) positive or caseating granuloma) in the resected specimen (gallbladder/appendix/colon). ATT for 6 months was completed in all the patients with active peritoneal disease. At median follow up of 9 months, all patients were asymptomatic and doing fine.

Table 1.

Summary of clinical details of the patients with incidental peritoneal tuberculosis.

S. no.	Cases	Prior TB	ATT	Presenting complaints	Surgical procedure		Operative findings	Histopathology	Additional investigations
1	31/F	No	No	Biliary colic with dyspepsia	1	LC (attempted)	Multiple peritoneal nodules	Granulomas with multinucleated giant cells, occasional AFB positivity (Figure 1(a) and (b))	None
					2	LC (after completion of ATT course)	Complete resolution	Chronic cholecystitis
2	35/F	No	No	Biliary colic	1	LC (attempted elsewhere)	Multiple peritoneal nodules	NA	ADA – 66.3 IU/L (Ref. range <37 IU/L)CECT abdomen-calcified portal lymph nodes with mild ascites
					2	LC (at our institute after 2 months of ATT)	Complete resolution	Chronic cholecystitis
3	27/M	No	No	Blunt trauma abdomen	1	Primary repair of jejunal perforation and divided transverse loop colostomy	1 × 1 cm perforation in proximal jejunum and devascularized mid transverse colon; no peritoneal pathology	Ischeamic bowel (transverse colon)	None
					2	Restoration of bowel continuity (6 months later)	Multiple nodules on the peritoneal surface and all over the viscera with inter-bowel adhesions	Granulomatous inflammation consistent with tuberculosis (Figure 1(c) and (d))
4	55/M	Lymph node (cervical)	6 months (completed 20 years back)	Biliary colic	1	LC (attempted)	Hard mass in umbilical region, dense adhesions and multiple peritoneal nodules (Figure 2(a))	Frozen section of peritoneal nodule – calcified mass; no evidence of malignancy	FDG PET CT-calcified mass (3.6 × 8 cm in umbilical region) with multiple calcified granulomas in mesentery of small and large bowel (Figure 2(b)). No FDG uptake anywhere in the body
					2	OC	Uneventful	Chronic cholecystitis
5	25/M	Pulmonary TB (sputum+)	6 months (completed 2 years back)	Right iliac fossa pain.Appendicular lump	1`	Laparoscopic appendectomy	Multiple omental and peritoneal tubercles (Figure 2(c)). Moderate ascites (Figure 2(d)), appendix thickened and inflamed	Appendix – chronic appendicitisOmental nodule – granulomatous inflammation	ADA – 123 IU/L (Ref. range <37 IU/L)AFB stain of ascitic fluid – smear negative

ADA, adenosine deaminase; AFB, acid fast bacilli; ATT, antitubercular treatment; CECT, contrast enhanced computed tomography; FDG, fluorodeoxyglucose (18 F); LC, laparoscopic cholecystectomy; NA, not available; OC, open cholecystectomy; PET-CT, positron emission tomography/computed tomography; TB, Tuberculosis.

Discussion

Peritoneal tuberculosis, a form of abdominal tuberculosis, occurs in three forms (wet type with ascites, dry type with adhesions and fibrotic type with omental thickening and loculated ascites). ¹ It accounts for about 1–2% of all cases of tuberculosis. ⁵ The mechanisms postulated for tubercle bacilli’s entry into the peritoneal cavity are transmurally from affected bowel, via lymphatic channels from infected mesenteric lymph nodes, from tuberculous salpingitis or by hematogenous spread from a pulmonary focus. ⁶

Peritoneal tuberculosis is suspected in following clinical scenarios:

1. Secondary peritoneal involvement in patients diagnosed with pulmonary and/or extrapulmonary tuberculosis; ⁷

2. Unexplained ascites; ⁶

3. Bowel obstruction due to band or adhesions (with or without concomitant intestinal tuberculosis); ⁶

4. Misdiagnosed as peritoneal carcinomatosis; ⁵

5. Incidentally detected peritoneal tuberculosis.

Though reported, definition of this distinct entity, incidental peritoneal tuberculosis, has not been well described. ⁸ Incidental peritoneal tuberculosis is when peritoneal tuberculosis (peritoneal tubercles or ascites) is detected intraoperatively in patients undergoing surgical exploration for other indications with no preoperative suspicion of abdominal tuberculosis or active tubercular lesions. Two major problems arise on encountering such a finding. First, it poses diagnostic dilemma. Second, hesitation to proceed with the original surgical plan on encountering such a finding is likely.

Diagnosis is usually based on systemic evidence of tuberculosis and abdominal findings suggestive of tuberculosis. Constitutional symptoms and abdominal complaints suggestive of peritoneal tuberculosis were not present in any of the patients. This might be due to the either latent phase of pathogenesis or because of good immune status. Four patients had diffusely distributed peritoneal tuberculosis with minimal ascites. One patient had possible sequelae of unintentionally treated peritoneal tuberculosis in the form of calcific lesions predominately involving the parietal wall. There were neither gross bands nor adhesions that might cause intestinal obstruction. Neither gross-free fluid was present to cause symptomatic ascites.

Peritoneal carcinomatosis remains the most serious confounding diagnosis. Three patients in our series had their planned procedure deferred in view of suspected peritoneal carcinomatosis. In most instances, the decision to perform cholecystectomy is based on clinical examination and ultrasonogram. Given the poor sensitivity of ultrasound in diagnosing early gallbladder carcinoma, detection of peritoneal nodules intraoperatively will raise the suspicion of peritoneal metastasis, especially in an endemic region of gallbladder carcinoma. In a case series of gallbladder tuberculosis, one patient also had peritoneal tuberculosis leading to suspicion of gallbladder carcinoma with peritoneal carcinomatosis. ⁹ For diagnosis of peritoneal tuberculosis, histological demonstration of mycobacterium tuberculosis (MTB) is the gold standard. ⁷ However, owing to the low yield of peritoneal fluid culture and slow growth of MTB (considered gold standard), surgical visualization of nodules has been found to be more accurate than histology (95% versus 82%).^2,7 Small white tubercles over the peritoneum, inflammatory adhesions involving peritoneal surfaces and greater omentum thickening and retraction are some of the laparoscopic findings in peritoneal tuberculosis. ¹ In the preoperative setting, smooth peritoneal thickening with dirty omentum in computed tomography favours peritoneal tuberculosis. Peritoneal carcinomatosis tends to have nodular peritoneal thickening. ¹⁰ When confronted with such suspicious nodules in asymptomatic individuals, Koc and colleagues ⁵ suggest frozen section to distinguish between them. However, none of our patient underwent frozen section due to unavailability of frozen section at that time.

The dilemma to proceed even after ruling out peritoneal carcinomatosis can persist. Concern of port site or incision site tuberculosis in patients with peritoneal tuberculosis exists. ¹¹ None of our patients had such a complication. Initiation of ATT in the immediate postoperative period could be the reason.

Two patients had interesting presentations. The third patient in our series had no evidence of peritoneal pathology during the first surgery following trauma but manifested peritoneal tuberculosis during the second surgical exploration. Silent reactivation of peritoneal foci and postoperative flare of peritoneal tuberculosis have been described.^1,8 Rafoth and colleagues ⁸ demonstrated eight patients who underwent laparotomy for various indications but later developed symptomatic tuberculosis. The fourth patient had multiple calcific peritoneal nodules (Figure 2(a)) with one dominant calcific mass in umbilical region. None of the common causes of peritoneal calcification (peritoneal dialysis, prior peritonitis) were a possibility in the given patient. ¹² Given the presence of calcified mesenteric nodes and prior history of nodal tuberculosis, sequelae of healed tubercular granuloma were considered the first possibility. Interestingly, he had no abdominal complaints during the time of his nodal tuberculosis diagnosis.

Figure 2.

Panel of images showing peritoneal nodules. (a) Patient 4 – intraoperative laparoscopic image showing multiple whitish peritoneal nodules (long black arrow). (b) Patient 4 – computed tomography axial bone window section depicting calcified mass in parietal wall (red block arrow) and calcified mesenteric node (short red arrow). (c) Patient 5 – intraoperative images showing peritoneal, omental and serosal nodules (black curved arrow). (d) Patient 5 – intraoperative image showing ascitic fluid (black asterisk).

History of previous ATT was present in two patients. Both were diagnosed nodal or pulmonary tuberculosis based on histological evidence. The response has been documented based on clinical and microbiological bases. The second patient probably highlights the state of quandary in deciding whether longer duration of ATT in abdominal tuberculosis is warranted. ¹³

Response assessment in these individuals is difficult given the lack of clinical features and accurate imaging modality for peritoneal tuberculosis. The first two patients had complete resolution of peritoneal tuberculosis after ATT as evidenced by the absence of tubercles during their respective surgery. However, diagnostic laparoscopy for response assessment in otherwise asymptomatic individuals might be unwarranted. Thus, periodical clinical examination including monitoring of weight gain and selective investigations are required during follow-up.

Conclusion

Incidental peritoneal tuberculosis represents an uncommon form of peritoneal tuberculosis. The absence of prior tuberculosis does not preclude the diagnosis of peritoneal tuberculosis. In an endemic region of tuberculosis, surgeons must be aware of the entity on encountering such finding. Frozen section can help in guiding appropriate management.