|Year : 2016 | Volume
| Issue : 3 | Page : 115-121
Diagnostic challenges of tuberculosis peritonitis in upper Egypt
Nahed A Makhlouf1, Gamal A Makhlouf2, Ahmed Soliman2, Mahmoud F Sherif3, Hebat-Alla G Rashed4
1 Department of Tropical Medicine and Gastroenterology, Faculty of Medicine, Assiut University, Assiut, Egypt
2 Department of General Surgery, Faculty of Medicine, Assiut University, Assiut, Egypt
3 Department of Pathology, Faculty of Medicine, Assiut University, Assiut, Egypt
4 Department of Clinical Pathology, Faculty of Medicine, Assiut University, Assiut, Egypt
|Date of Submission||28-May-2016|
|Date of Acceptance||05-Jul-2016|
|Date of Web Publication||15-Feb-2017|
Nahed A Makhlouf
Assistant Professor of Tropical Medicine and Gastroenterology, Faculty of Medicine, Assiut University, Assiut, 71515
Source of Support: None, Conflict of Interest: None
Tuberculosis (TB) is a major global health problem. Peritoneal tuberculosis involves the omentum, intestinal tract, liver, spleen, or female genital tract in addition to the parietal and visceral peritoneum. It accounts for ∼1–2% of all cases of tuberculosis.
Aims of the study
The aims of this study was to analyze the clinical, laboratory, and imaging findings in patients with TB peritonitis and to evaluate the diagnostic methods.
Patients and methods
This prospective, observational study was carried out on patients with obscure ascites. All patients were subjected to history taking, clinical examination, and laboratory investigations. Ascitic fluid analysis and calculation of serum-ascites albumin gradient were done. Abdominal ultrasound (US) and computed tomography scans were performed. Laparoscopic-guided biopsies from peritoneal tubercle and unhealthy omentum were taken for histopathology and culture analysis.
The study included 22 cases. Approximately 77.3% were female. The mean age was 42.6±15.1. More than two-thirds of the cases had fever, pain, and abdominal swelling. No portal hypertensive ascites was found in 86.4% of cases. Ascitic fluid cytology revealed lymphocytes in 91%. In abdominal US, ascites was the only finding in 59% of cases; however, adhesion was found in 22.8% of cases. Lymphadenopathy was observed in 13.6% of cases undergoing abdominal US. During laparoscopy, small tubercles on the peritoneum, omentum, and/or intestine with extensive adhesions were the predominant findings. Regarding the histopathologic findings, TB granuloma was predominant in 80% of cases.
TB peritonitis was common among middle-aged females. Ascites and adhesions were the commonest findings. Laparoscopy and histopathology were the best diagnostic modalities.
Keywords: clinical features, diagnostic yield of laparoscopy, histopathology in tuberculosis, peritoneal tuberculosis
|How to cite this article:|
Makhlouf NA, Makhlouf GA, Soliman A, Sherif MF, Rashed HAG. Diagnostic challenges of tuberculosis peritonitis in upper Egypt. Al-Azhar Assiut Med J 2016;14:115-21
|How to cite this URL:|
Makhlouf NA, Makhlouf GA, Soliman A, Sherif MF, Rashed HAG. Diagnostic challenges of tuberculosis peritonitis in upper Egypt. Al-Azhar Assiut Med J [serial online] 2016 [cited 2020 Sep 30];14:115-21. Available from: http://www.azmj.eg.net/text.asp?2016/14/3/115/200148
| Introduction|| |
Tuberculosis (TB) is a major global health problem. It causes ill-health among millions of people each year. In 2014, there were an estimated 9.6 million new TB cases and there were also 1.5 million TB deaths worldwide. In Egypt, the incidence rate of TB (all forms of TB case) in 2014 was 15 in 100 000 populations and the mortality rate was 0.3 in 100 000 populations .
Abdominal TB is one of the most prevalent forms of extrapulmonary disease. Peritoneal TB is a form of abdominal TB that involves the omentum, intestinal tract, liver, spleen, or female genital tract in addition to the parietal and visceral peritoneum. It accounts for ∼1–2% of all cases of TB .
Peritoneal TB occurs in three forms: (i) wet type with ascites, (ii) encysted (loculated) type with a localized abdominal swelling, and (iii) fibrotic type with abdominal masses composed of mesenteric and omental thickening, with matted bowel loops felt as lumps in the abdomen. A combination of these types is also common . As TB peritonitis may have an insidious onset and nonspecific clinical presentation, it is a major diagnostic challenge .
| Aims of the study|| |
The aims of the study was as follows:
- To analyze the clinical, laboratory, and radiological findings in patients with TB peritonitis and
- To evaluate the diagnostic methods.
| Patients and methods|| |
This prospective, observational study was carried out through collaboration between Departments of Tropical Medicine and Gastroenterology, General Surgery, Pathology and Clinical Pathology, Assiut University Hospital, Assiut, Egypt, during a 1-year period from August 2014 to July 2015. The study was conducted on patients with obscure ascites.
All patients were subjected to the following:
- Complete history taking, with stress on the onset, course, duration of illness, presence or absence of fever and its grade, presence of pain and abdominal swelling, anorexia, loss of weight, change in the bowel habits, and symptoms of anemia.
- Thorough clinical examination, with stress on the presence of pallor, jaundice, fever, manifestations of hepatocellular failure, ascites and its amount, abdominal tenderness, palpable abdominal masses, and localized or generalized lymphadenopathy.
- Laboratory investigations including complete blood count, liver function tests and prothrombine time, and erythrocyte sedimentation rate.
- Ascitic fluid analysis, including physical appearance, total protein, albumin, calculation of serum-ascites albumin gradient (SAAG), and ascitic fluid cytology for types of cells. Staining of direct film from ascitic fluid by Ziehl–Neelsen stain searching for acid-fast bacilli.
- Abdominal ultrasonography (US) for the presence and amount of ascites, liver size, surface, echo pattern, focal lesions, and presence of adhesions or adherent bowel loopes or lymphadenopathy. Sometimes ascitic fluid aspiration was done under US guidance.
- Multislice contrast-enhanced computed tomography (CT) scan of the abdomen, with special stress on the presence of adhesions, dilated bowel loops, lymphadenopathy, peritoneal thickening, or deposits.
- Laparoscopy and laparoscopic-guided biopsies (four in number) from peritoneal tubercles or suspected unhealthy omentum or peritoneal thickening. Some were formalin fixed to be subjected to histopathology, and others put in normal saline for doing culture.
- Laparoscopy techniques:
The procedures were performed under general anesthesia. Infraumbilical incision port (10 mm in diameter) for camera and light source. Carbon dioxide was injected in the peritoneal cavity, meanwhile the pressure within the pneumoperitoneum apparatus was maintained at 8–12 mmHg all over the procedure. Two ports in the midclavicular lines at right and left sides of abdomen 3 cm above the level of umbilicus for grasper and hook were used. Exploration of the whole abdomen was done. A systematic survey was undertaken by the laparoscopy operator for the presence of ascites and peritoneal adhesions. A careful note was made of the liver (size, color, nodularity, localized suspicious lesions, etc.) and on the degree of vascularity of the falciform ligament. The surface of gall bladder, spleen, intestine, colon, and omentum as well as the pelvic cavity (ovaries, Fallopian tube More Detailss; uterus in females) were examined. The presence of abdominal masses was reported. Laparoscopic-guided biopsies by grasping biopsy forceps (four in number) were taken from peritoneal tubercles or suspected unhealthy omentum or peritoneal thickening for doing histopathology and culture analysis. The wound was closed by one or two mattress sutures. Immediately after that, report on the laparoscopic findings was written. The patients were observed for 24 h with regular check of blood pressure and pulse.
- Culture technique from tissue biopsy samples:
- Homogenize using a miniblender and inoculate into the medium (Löwenstein–Jensen medium).
- Incubate tubes at 36±1°C.
- Tubes should be incubated in a slanted position, with screw caps loose, for at least 1 week to ensure even distribution and absorption of inoculum. After 1 week of incubation, caps are tightened to minimize evaporation and drying of the media. Tubes may then stand upright to save space in incubators.
Reading and interpretation using solid media:
- Check colony formation every week, preferably twice within the first week.
- Report results immediately after detection and identification, and cultures should be kept for up to 8 weeks before being reported as negative.
- Ascitic fluid culture analysis for TB bacilli was also done.
- Cytological and histopathological study:
- Ascitic fluid:
Overall, 15 millilitre of aspirated ascitic fluid was centrifuged at 4000 rpm for 10 min. The pellets were removed and smeared on uncharged glass slides. The slides were stained by May-Grunwald-Giemsa and Papanicolaou stains for routine cytology evaluation. Another dried slide was prepared and stained with Ziehl–Neelsen (ZN) stain for detection of acid-fast bacilli.
- Laparoscopic omental biopsy specimen:
The laparoscopic-guided omental specimens were fixed in 10% buffered formalin, processed for tissue processing, and paraffin embedded. The slides were prepared by cutting 4-µm-thick sections and staining with hematoxylin and eosin for routine microscopic evaluation. If granulomatous reaction was seen in routine examination, another section was requested and stained with ZN stain for acid-fast bacilli. All cytologic and histopathologic slides were reviewed by the researcher.
The approval from medical ethical committee of Assiut Faculty of Medicine was taken. Each patient gave his/her written consent to participate in the study.
Categorical variables were described by number and percentage [n (%)], whereas continuous variables were described by mean and SD. A two-tailed P value less than 0.05 was considered statistically significant. All statistics were computed using SPSS version 20; SPSS Inc., Chicago IL, USA; Soft Ware.
| Results|| |
Our study included 22 cases with obscure ascites. [Table 1] shows the demographic and clinical data. Approximately 17 (77.3%) patients were female. The mean age was 42.6±15.1. More than two-thirds of the cases had fever, pain, and abdominal swelling. Approximately 54.5% had anemia (approximately two-thirds of cases with anemia had microcytic hypochromic anemia and 33.3% had macrocytic anemia). Moreover, three cases had liver cirrhosis and fever with refractory exudative ascites.
|Table 1 Demographic and clinical data of all patients with ascites (n=22)|
Click here to view
[Table 2] shows baseline laboratory data of all patients with ascites. Of 22 cases, 21 were exudative ascites. No portal hypertensive ascites was found in 86.4% of cases. Ascitic fluid cytology revealed predominant lymphocytes in 91% of cases. In abdominal US, ascites was the only finding in 59% of cases; however, adhesions were found in 22.8% of cases ([Table 3]).
Lymphadenopathy was observed in 13.6% of cases under abdominal US; however, in CT scan, it was observed in 40.9% of cases [enlarged mesenteric lymph nodes (LNs) in 22.7%, enlarged upper abdominal LNs in 4.6%, and enlarged mediastinal and abdominal LNs in 13.6%] ([Table 4]).
During laparoscopy, small tubercles on the peritoneum, omentum, and/or intestine, discrete or matted, with extensive adhesions, were the predominant findings ([Table 5] and [Figure 1]).
|Figure 1 Main laparoscopic findings. A: Confluent tubercles on the parietal peritoneum; B: Discrete tubercles with thin fibrous adhesions between both layers of the peritoneum.|
Click here to view
Regarding the histopathologic findings, TB granuloma was the predominant findings in 80% of cases ([Figure 2] and [Figure 3]), chronic nonspecific inflammation of the peritoneum with little reactive fibrosis was found in 15% of cases, and one case had omental fatty tissue with multiple small foci infiltrated with chronic inflammatory cells as shown in ([Table 6]).
|Figure 2 Omental laparoscopic biopsy showing the noncaseating granuloma with multinucleated giant cells [H&E stain, ×200 (inset ×400)].|
Click here to view
|Figure 3 Acid-fast dark red bacillus inside the multinucleated giant cell (black arrow).|
Click here to view
ZN staining of the ascitic fluid for detection of acid-fast bacilli was found to be positive in three (13.6%) cases ([Table 2] and [Figure 4]). Culture findings of ascitic fluid (two) and/or peritoneal biopsies (20) were negative for TB ([Table 2]).
|Figure 4 Smear from slide prepared from ascitic fluid pellet after cytocentrifugation showing two acid-fast dark red bacilli (black arrow).|
Click here to view
| Discussion|| |
Peritoneal tuberculosis should be suspected in high-risk patients with ascites, fever, unexplained generalized symptoms, and diffuse abdominal pain or tenderness .
The most common features were ascites (93%), abdominal pain (73%), and fever (58%). Abdominal pain and ascites were also the most common presenting features in several other reports ,. In the current study, more than 80% of cases had abdominal pain and abdominal swelling, and more than 70% of cases had fever.
Fever was more frequent in younger groups of patients (both young adults and middle-age patients) with either pulmonary or extrapulmonary TB .
In the present study, about 77.3% of cases were females with mean age 42.6±15.1. Similarly, in Makhlouf et al.  study, TB peritonitis was significantly lower in geriatric patients when compared with either young or middle-aged patients.
In the current study, weight loss was detected in 27.3%; 54.5% of cases had anemia, and three (13.6%) cases had TB peritonitis in addition to liver cirrhosis.
Mild to moderate normochromic, normocytic anemia is a frequent finding in TB peritonitis ,.
The risk of TB peritonitis is increased in patients with cirrhosis, HIV infection, diabetes mellitus, and underlying malignancy ,,,.
Tuberculous peritonitis should be considered in all patients presenting with unexplained lymphocytic ascites with a serum-ascites albumin gradient of less than 1.1 g/dl .
Examination of the peritoneal fluid may prove useful. In patients with tuberculous peritonitis, the ascitic fluid is straw colored with protein level of more than 3 g/dl, and total cell count of 150–4000/µl, consisting predominantly of lymphocytes (>70%) . ZN staining of the ascitic fluid for mycobacterial detection is positive in only ∼3% of cases with proven tuberculous peritonitis .
In the present study, 95.5% had exudative ascites, with ascitic fluid protein content of 5.2±1.2 g/dl and 86.4% had SAAG less than 1.1 gm/dl. However, only three (13.6%) cases had portal hypertensive ascites with SAAG equal to or more than 1.1 g/dl. Those three cases had TB peritonitis in addition to cirrhosis. Ascitic fluid cytology showed predominant lymphocytes in (91%) of cases. ZN staining of the ascitic fluid for mycobacterial detection was positive in three (13.6%) cases. Culture of ascitic fluid and/or peritoneal biopsies were negative for TB in 100% of cases. In contrast to our study, other studies showed that staining for acid-fast bacilli was positive in less than 3% of cases, and a positive culture finding was obtained in less than 20% of cases .
In the present study, abdominal US detected ascites, adhesions, peritoneal thickening, organomegaly, and lymphadenopathy. Ultrasonography can be very useful for imaging peritoneal TB . The following findings may be seen, usually in combination: (i) intra-abdominal fluid, which may be free or loculated, clear or complex (with debris and septae); (ii) club sandwich or sliced bread sign is because of the localized fluid between radially oriented bowel loops (interloop ascitis); (iii) lymphadenopathy may be discrete or matted, with mixed heterogeneity owing to caseation; and (iv) bowel wall thickening, best appreciated in the ileocecal region, may also be seen .
CT scan demonstrated ascites and adhesions similar to abdominal US in the current study. However, it was superior in demonstrating lymphadenopathy (nine cases in CT vs. three only in US), peritoneal thickening (three cases in CT vs. one case in US), stranding of omentum, mesentric fat, and dilated thickened bowel loops.
Thickened peritoneum and enhancing peritoneal nodules may be seen in CT scan . Mesenteric disease on CT scan was seen as a patchy or diffuse increase in density, with strands within the mesentery. LNs may be interspersed. Omental thickening is often seen as an omental cake appearance. A fibrous wall, called the omental line, could cover the omentum, developing from long standing inflammation. An omental line is less common in malignant infiltration .
Manifestations of TB in the abdomen are variable. CT reliably demonstrates the entire range of findings. Although no single CT feature is diagnostic of the disease, CT findings, interpreted in the light of clinical and laboratory data, can be a valuable tool in the diagnosis of abdominal TB .
Ascites with multiple tubercle studding the peritoneum and omentum with extensive adhesions were the commonest findings in laparoscopy in the present study (68.2%). TB granuloma was the commonest findings by histopathology (80%).
Bhargava et al.  found visual appearances to be more helpful (95% accurate) than either histology or culture (82. 3 and 37.5% sensitivity, respectively). Caseating granulomas may be found in 85–90% of the biopsies. The laparoscopic findings in peritoneal tuberculosis can be grouped into three categories: (i) thickened peritoneum with tubercles: multiple, yellowish white, and uniform sized (∼4–5 mm) tubercles diffusely distributed on the parietal peritoneum; (ii) thickened peritoneum without tubercles; and (iii) fibroadhesive peritonitis with markedly thickened peritoneum and multiple thick adhesions fixing the viscera.
Combined use of laparoscopic and bacteriologic examinations can approach 100% accuracy in the diagnosis of patients with tuberculous peritonitis. Laparoscopic examination (peritoneal tubercles) offers high diagnostic accuracy for diagnosis of TB peritonitis at 91.2% versus 86% for bacterial peritoneal culture and 64.9% for histopathology (TB granuloma) .
| Conclusion|| |
TB peritonitis was common in middle-aged females. The common clinical features were fever, abdominal pain, and abdominal swelling. More than half of cases had anemia. None portal hypertensive ascites and lymphocytes were suggestive findings. Ascites and adhesions were the commonest finding in US. Abdominal CT scan detect findings that were seen in the US in addition to the finding of lymphadenopathy. During laparoscopy, small tubercles on the peritoneum, omentum, and/or intestine with extensive adhesions were the predominant findings. TB granuloma was the predominant finding in histopathology.
The authors would like to thank staff members, specialists, and technicians in Radiology Department for routine performance and interpretation of CT findings, and nurses in Tropical Medicine Department, the laboratory workers in Clinical Pathology Department, and workers in Pathology Department for their help during the work.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
World Health Organization (WHO). Global tuberculosis report 2015. 20th ed. Geneva: WHO Press; 2015.
Mimidis K, Ritis K, Kartalis G. Peritoneal tuberculosis. Ann Gastroenterol 2005; 18:325–329.
Sharma MP, Bhatia V. Abdominal tuberculosis. Indian J Med Res 2004; 120:305–315.
Chau TN, Leung VKS, Wong S, Law ST, Chan WH, Luk IS et al.
Diagnostic challenges of tuberculosis peritonitis in patients with and without end-stage renal failure. Clin Infect Dis 2007; 45:e141–e146.
Evers BM. Diseases of the Peritoneum. In: Yamada T et al.
, editors. Textbook of gastroenterology. 2nd ed. Philadelphia, PA: JB Lippincott Company; 1995. pp. 2308–2309.
Demir K, Okten A, Kaymakoglu S, Dincer D, Besisik F, Cevikbas U et al.
Tuberculous peritonitis − reports of 26 cases, detailing diagnostic and therapeutic problems. Eur J Gastroenterol Hepatol 2001; 13:581.
Tanrikulu AC, Aldemir M, Gurkan F, Suner A, Dagli CE, Ece A. Clinical review of tuberculous peritonitis in 39 patients in Diyarbakir, Turkey. J Gastroenterol Hepatol 2005; 20:906.
Makhlouf HA, Makhlouf NA, Yousef HA. Clinical and radiological profile of geriatric tuberculosis. Egypt J Chest Dis Tuberc 2010; 59:1–8.
Shakil AO, Korula J, Kanel GC, Murray NG, Reynolds TB. Diagnostic features of tuberculous peritonitis in the absence and presence of chronic liver disease: a case control study. Am J Med 1996; 100:179–185.
Chow KM, Chow VC, Hung LC, Wong SM, Szeto CC. Tuberculous peritonitis-associated mortality is high among patients waiting for the results of mycobacterial cultures of ascitic fluid samples. Clin Infect Dis 2002; 35:409.
Aguado JM, Pons F, Casafont F, San Miguel G, Valle R. Tuberculous peritonitis: a study comparing cirrhotic and noncirrhotic patients. J Clin Gastroenterol 1990; 12:550.
Rieder HL, Snider DE Jr, Cauthen GM. Extrapulmonary tuberculosis in the United States. Am Rev Respir Dis 1990; 141:347.
Mehta JB, Dutt A, Harvill L, Mathews KM. Epidemiology of extrapulmonary tuberculosis. A comparative analysis with pre-AIDS era. Chest 1991; 99:1134.
Sanai FM, Bzeizi KI. Systematic review: tuberculous peritonitis-presenting features, diagnostic strategies and treatment. Aliment Pharmacol Ther 2005; 22:685.
Marshall JB. Tuberculosis of the gastrointestinal tract and peritoneum. Am J Gastroenterol 1993; 88:989–999.
Kedar RP, Shah PP, Shivde RS, Malde HM. Sonographic findings in gastrointestinal and peritoneal tuberculosis. Clin Radiol 1994; 49:24–29.
Jain R, Sawhney S, Bhargawa DK, Berry M. Diagnosis of abdominal tuberculosis: Sonographic findings in patients with early disease. Am J. Roentgenol 1995; 165:1391–1195.
Gulati MS, Sarma D, Paul SB. CT appearances in abdominal tuberculosis. A pictorial assay. Clin Imaging 1999; 23:51–59.
Ha HK, Jung JI, Lee MS, Choi BG, Lee MG, Kim PN et al.
CT differentiation of tuberculosis peritonitis and peritoneal carcinomatosis. Am J Roentgenol 1996; 167:743–748.
Sinan T, Sheikh M, Ramadan S, Sahwney S, Behbehani A. CT features in abdominal tuberculosis: 20 years experience. BMC Med Imaging 2002; 2:1–7.
Bhargava DK, Shriniwas , Chopra P, Nijhawan S, Dasarathy S, Kushwaha AK. Peritoneal tuberculosis: laparoscopic patterns and its diagnostic accuracy. Am J Gastroenterol 1992; 87:109–112.
El-Attar MM. Comparative study of diagnostic modalities in tuberculous peritonitis. Thesis submitted for the partial fulfillment of M.D. Degree in Tropical Medicine and Gastroenterology, Assiut University; 1999.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]