0Original Article
Pancreatic and peripancreatic tuberculosis presenting as hypoechoic mass and malignancy diagnosed by ultrasound-guided fine-needle aspiration cytology
ABSTRACT
Background: Pancreatic and peripancreatic tuberculosis is an extremely uncommon disease, presenting as hypoechoic mass on ultrasonography and imaging mimicking malignancy. Consequently, it represents a diagnostic challenge. Aims: To study 14 unusual cases of pancreatic and peripancreatic tuberculosis undergoing ultrasound-/endoscopic-guided fine-needle aspiration cytology (FNAC) in the 5-year period from 2006 to 2010.
Materials and Methods: Endoscopic-guided FNAC was done in two cases, while ultrasound-guided FNAC was performed in 12 cases using 22-G needles via a percutaneous transabdominal approach. The aspirated material was quickly smeared onto glass slides, air dried, and wet fixed in 95% ethyl alcohol for subsequent Papanicolaou staining. Results: All pancreatic and peripancreatic tuberculosis cases showed solid-cystic pancreatic mass. Smears showed epithelioid cell granulomas, multinucleated giant cells, mixed inflammatory cells and histiocytes against a necrotic background. The common anatomic locations were the head, peripancreatic, tail and body of the pancreas.
Conclusions: Ultrasound-/endoscopic-guided FNAC is a safe, reliable and cost-effective method for preoperative diagnosis of pancreatic and peripancreatic tuberculosis. Clinical symptoms and accurate diagnostic approach by ultrasound-/ endoscopic-guided FNAC of pancreatic and peripancreatic tuberculosis is needed to avoid performing redundant laparotomy. Despite its rarity, pancreatic and peripancreatic tuberculosis should be considered for differential diagnosis of pancreatic and peripancreatic cystic mass in endemic developing countries.
Key words: Cystic neoplasms; endoscopic; pancreas; pancreatitis; tuberculosis; ultrasound-FNA.
Introduction
Pancreatic and peripancreatic tuberculosis (PPT) is a rare non-neoplastic lesion and its clinical and radiological findings may be similar to those of pancreatic malignancy.!11 Therefore, diagnosis of the PPT is very difficult, and most of previously reported cases were diagnosed after exploratory laparotomy
for suspected pancreatic malignancy.[2] Tuberculosis (TB) is a potentially systemic disease that can affect any organ.[3] Abdominal infection with TB commonly affects the ileo-cecal region, spleen, liver and kidney. Pancreatic TB presents with a wide spectrum of symptoms such as abdominal pain, constitutional symptoms, obstructive jaundice, iron-deficiency anemia, pancreatic abscess, massive gastro-intestinal bleeding, acute/chronic pancreatitis, secondary diabetes, splenic vein thrombosis and a pancreatic mass mimicking malignancy. The frequency of PPT cases in developing countries has increased in recent years. We present a series of PPT cases to emphasize the differential diagnosis of a pancreatic mass and to discuss the role of ultrasound/endoscopic ultrasound-guided fine-needle aspiration cytology (US/EUS-FNAC) as a technique of good modality in preoperative diagnosis of PPT.
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R. N. Rao, Rakesh pandey, Manoj Kumar Rana1, praveer Rai2, Archna Gupta3
Departments of Pathology, 'Microbiology, Gastroenterology, and 3Radiodiagnosis, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
Address for correspondence: Dr. Ram Nawal Rao, Department of Pathology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India. E-mail: rnrao@sgpgi.ac.in
Materials and Methods
We analyzed a total of 14 diagnosed cases of primary TB involving the pancreas (7 cases) and peripancreatic region (7 cases). All the cases of PPT diagnosed by US/EUS-FNA of the pancreas over a period of 5 years (2006-2010) were retrieved from our hospital information system records. All the patients underwent US-FNAC except two cases (EUS-FNA), which was performed by the clinician, radiologist and the cytopathologist. The site of needle piercing was cleaned with spirit and betadine. A 22-gauge needle, 9 cm in length, was inserted into the lesion by the radiologist under ultrasound guidance. A 10/20 mL syringe fitted to a syringe holder was quickly attached, and the aspiration procedure was performed by the cytopathologist. A minimum of one to two FNA passes were taken from each lesion and the slides were immediately checked for adequacy of representative material. Both air-dried and alcohol-fixed smears were made (5-8 smears) from the aspirated material in each case. May-Grunwald-Giemsa (MGG), hematoxylin-eosin (H and E), Papanicolaou (Pap) stain, smears for fungus, acid-fast bacilli (AFB) along with FNA samples for culture, polymerase chain reaction (PCR) assay and cell blocks (if any) were evaluated. This included 10 males and 4 females with age ranging from 15 to 58 years (mean age 37 years), who were detected to have PPT from 2006 to 2010 at our institute. We reviewed the clinical, radiological [ultrasonographic, magnetic resonance imaging (MRI) and computed tomography (CT) features] and laboratory findings of all patients. In most of the cases, histopathological examination was not performed due to preoperative diagnosis of PPT. The cytological diagnosis was correlated with histopathological reports wherever available (cell blocks in two cases). On follow-up, ranging from 6 months to 1.5 years after anti-tubercular treatment (ATT), 12 patients showed good response to ATT, one patient had drug-resistant TB, and one patient was lost to follow-up.
Results
The male/female ratio was 2.5:1. Age ranged from 15 to 58 years. The majority of patients were in the fourth to fifth decade (30-45 years). The duration of symptoms spanned between 2 and 12 months, with a mean duration of 7 months. The most common symptom was abdominal pain localized to the epigastrium, fever and weight loss. All but one patient were seronegative for HIV-1 infection. All patients had history of TB displaying the isolated pancreatic (7/14 cases) and peripancreatic (7/14 cases) involvement as the primary manifestation [Table 1]. Ultrasonography (US) showed bulky homogenous pancreas in five patients and hypoechoic mass in nine cases. CT findings demonstrated hypodense collections within the pancreas in five patients and complex hypoechoic
pancreatic mass lesion in nine patients. CT findings in case 14 showed pancreatic mass with multiples lymph nodes and liver nodules. MRI was done in three cases and showed a sharply delineated mass with heterogeneous enhancement located in the pancreatic head. Endoscopic examination with FNA was done in two cases and showed a hypoechoic mass. Cytology smears showed necrosis in 12 cases in which predominant necrosis was found in 6 and focal necrosis in 6 cases, epithelioid cell granulomas in 8 cases, normal pancreatic acini in the background in 4 cases, and inflammatory cells comprising mainly polymorphs and lymphocytes in all cases. Necrosis, epithelioid cell granulomas and inflammatory cells [Figure 1] were seen in eight cases. Necrosis and inflammatory cells were seen in 12 cases. Multinucleated giant cells were seen only in one case. Ziehl-Neelsen stain (ZN stain) for AFB [Figure 2] was positive in 9 out of 14 cases. PCR was performed in 10 out of 14 cases, of which 8 cases showed Mycobacterium tuberculosis DNA in FNA samples [Figure 3]. Two cases showed inadequate sample for PCR assay. AFB culture was done in
Figure 1: Smear shows epithelioid cell granulomas, necrosis and inflammatory cells composed of neutrophils and lymphocytes (MGG, x400)
Figure 2: FNA smear shows necrosis and inflammatory cells. ZN stain for AFB is positive (ZN stain, x1000)
Table 1: Summary of US/EUS guided FNAC cases of pancreatic and peripancreatic tuberculosis (N=14)
Case Age Clinical Site Nature Mass Clinical Cytological ATT Period Prognosis
no. (year)/ sex symptoms (cm) diagnosis diagnosis/ZN stain for AFB
1 34/M Anorexia, fever, weight loss, pain and lump in epigastrium HOP Cystic 2x2 cm Pancreatic cancer, HIV+ Pan TB, positive INH, R-cin, PZA, CBT 12 months Good
2 44/F Fever, vitiligo PPLN Cystic 2x1.5 cm Pancreatic cancer GRLN, negative Yes Do Do
3 45/F Fever, pain and lump in epigastrium PPLN Cystic 2x1.6 cm Pancreatic cancer GRLN, negative Yes Do Do
4 40/M Anorexia, fever, weight loss HOP Cystic 3x2 cm Pancreatic cancer Pan TB, positive Yes Do Do
5 51/M Fever, weight loss, pain and lump in epigastrium HOP Cystic 2x1.5 cm Pancreatic cancer Pan TB positive Yes Do Do
6 58/M Fever and tail mass, jaundice tail Cystic 2x1 cm Pancreatic cancer Necrosis (Pan TB), positive Yes Do N/A
7 15/M Anorexia, fever HOP Cystic 3x2.5 cm Pancreatic cancer/lymphoma GRLN, negative Yes Do Do
8 34/F Fever, weight loss PPLN Cystic 2.5x1.5 cm Pancreatic cancer GRLN, negative Yes Do Resistant
9 45/M Fever, pain in epigastrium PPLN Cystic 2x1 cm Pancreatic cancer Pan TB, positive Yes Do Do
10 27/M Fever, numbness in both lower limbs, weakness HOP Cystic 2.5x1 cm Pancreatic cancer/Pan TB Pan TB, positive Yes Do Do
11 31/M Epigastric pain, fever, weight loss PPLN Cystic 1.5x1.5 cm Pancreatic cancer/metastatic Carcinoma Necrosis, negative Yes Do Do
12 28/F Fever and pain in epigastrium PPLN Solid-cystic 5.0x2.8 cm Pancreatic cancer, lymphoma Necrosis (Pan TB), positive Yes Do Do
13* 37/M Anorexia, fever and pain in epigastrium HOP Solid-cystic 2.5x1.5 cm Pancreatic cancer/Pan TB Pan TB, positive Yes Do Do
14* 35/M Fever and pain in epigastrium HOP Solid-cystic 2.0x1.2 cm Pancreatic cancer, lymphoma, Pan TB Pan TB, positive Yes Do Do
Pan TB: Pancreatic tuberculosis, GRLN: Granulomatous inflammation, HOP: Head of pancreas, PPLN: Peripancreatic lymph node, R-cin: Rifampicin, INH: Isoniazid, PZA: Pyrazinamide, CBT: Combutal, AFB: Acid-fast bacilli, ZN: Zeihl-Neelsen, N/A: Not available, *: Endoscopic ultrasound guided FNA cases
LANE 1 LANE 2 LANE 3 LANE 4 LANE 5 LANE 6
100 bp ^^^
Ladder +Ve Control - Ve Control Case 1 Case 2 Case 3
Figure 3: Polymerase chain reaction in pancreatic tuberculosis shows IS6110 gene (123 bp) in three FNA samples in lanes 4, 5 and 6. Lane 3 is negative control and lane 2 is positive control. Lane 1 is ladder (100 bp)
only one case. Cell blocks were made in two cases (2/14) and showed multinucleated giant cells, epithelioid histiocytes and necrosis. No histopathological examination was done due to preoperative cytological diagnosis of PPT and patients responded well to ATT. Case 9 had history of supraclavicular
tuberculous lymphadenopathy with positive ZN stain for AFB. Case 1 also had history of HIV infection. Follow-up was available in all cases up to 1.5 years, and 12 cases showed good response with ATT. Case 6 was lost to follow-up, and case 8 was drug resistant with ATT.
Precaution during procedure
Precaution on using diagnostic cytology in PPT is that the site of needle piercing should be cleaned with spirit and betadine. We should take consent from the patient before FNAC, and the patient should have normal prothrombin time (PT; 11-16 s) and activated partial thromboplastin time (APPT; 30-40 s) levels. Always 22-23 G spinal needle of 9 cm in length has to be used in the exact lesion by radiologist and cytopathologist team. Clinician should be present during the procedure to avoid any serious complication such as peritonitis, perforation, severe pain, major hemorrhage and exacerbation of pancreatitis.
Discussion
PPT is an unusual illness, particularly when it is isolated in the pancreas.[4] Extrapulmonary organ involvement by TB is
expected to occur in 10-15% of the patients non-infected by HIV. With the increasing use of immunosuppressant drugs and the emergence of AIDS, there has been a reappearance of TB and the frequency is about 50-70% in patients infected by HIV. The main symptoms at presentation of PPT in our cases were abdominal pain, weight loss, fever, recurrent vomiting and jaundice. Majority of our patients showed strongly positive tuberculin test (70%) and increased erythrocyte sedimentation rate (ESR). A previous study showed high ESR with positive tuberculin test in over two-thirds of the cases, authors also demonstrated that those patients had a strongly positive tuberculin test (50%) and normal sedimentation rate revealed elevated C-reactive protein in their other study.151 PPT presents with a wide spectrum of symptoms such as abdominal pain (100%), constitutional symptoms such as anorexia, weight loss and night sweat, fever, obstructive jaundice,161 iron-deficiency anemia, pancreatic abscess, massive gastrointestinal bleeding,171 acute pancreatitis, chronic pancreatitis, secondary diabetes, splenic vein thrombosis, and a pancreatic mass181 mimicking malignancy.191
Most of our patients (over ~75%) showed isolated pancreatic and peripancreatic mass mimicking pancreatic malignancy. Earlier studies showed that pancreatic mass mimicking pancreatic malignancy is seen in over 50% of patients.1101 The presence of fever with a pancreatic mass, as in our case, favors TB; however, malignant lymphoma should also be considered in such a clinical situation.
Most common location of PPT as a mass has been reported in the head or body as in our cases; however, occasionally isolated involvement of the pancreatic tail has also been described,!21 as in one of our case. Abdominal TB includes the infection of varying combinations of the intestinal tract, peritoneum, lymph nodes and solid organs such as the liver, spleen and pancreas. Involvement of solid abdominal organs is usually seen in association with miliary TB. Isolated abdominal organ involvement, especially of the pancreas, is unusual, even in the setting of miliary disease (ranging from 2.1 to 4.7%).[1]
A definitive diagnosis of PPT will prevent unnecessary surgery, and in the setting of suspected malignancy will change the diagnosis to one of a treatable infection; however, a definitive diagnosis of PPT is only achieved with histological confirmation. PPT is usually not suspected prior to laparotomy. Most patients have been diagnosed at laparotomy, however, if TB is suspected and confirmed, then surgery is not necessary, making FNAC a very useful diagnostic technique.!111 The success rate of image-guided percutaneous FNAC of previous studies in diagnosing pancreatic TB is less
than 50%,[9,12,13] while our series established the diagnosis in ~70 to 86% by FNA cytology.
EUS-FNA cytology/biopsy has proven to be an excellent tool for the cytological diagnosis of pancreatic and peripancreatic masses in 80-95% of cases.1141
AFB were identified only in 20-40% of cases and culture results were positive in 77% of cases even when intraoperative specimens were sent for direct smear and culture.1101 ZN staining for AFB was identified in ~65% of our cases.
A study showed caseating granulomas in 75-100% of cases161 while other study of 21 consecutive patients with pancreatic/ peripancreatic TB by EUS-FNA showed 13 patients (61.9%) with granulomatous inflammation on histopathological examination, and 10 of 15 patients (66.7%) were positive on a TB PCR assay. ZN staining was positive in 4 of 15 patients (26.7%), and 3 of 8 patients (37.5%) had cultures positive for M. tuberculosis.[151
In a previous case report, contrast-enhanced CT abdomen in a 24-year-old male showed pancreatic head mass invading portal vein, splenic artery and hepatic artery. On EUS, a pancreatic head mass infiltrating portal vein was seen. With provisional diagnosis of unresectable carcinoma of pancreas, EUS-FNAC was performed and the smear was suggestive of TB. Patient was started on ATT, to which he responded well
and was cured.1161
A chest radiograph may be helpful for TB. It should be suspected clinically in patients with a pancreatic mass, particularly if the patient is young, not jaundiced, coming from an endemic area with a normal endoscopic retrograde cholangiopancreatography (ERCP).1171
US and CT scan may show a diffusely enlarged pancreatic mass lesion. These findings are non-specific and may be seen with focal pancreatitis of any etiology, similar to pancreatic carcinoma.161 The imaging findings may suggest the possibility of TB, but none of the findings are pathognomic for pancreatic TB. CT scan findings include hypodense lesions and irregular borders usually in the head of the pancreas, diffuse enlargement of the pancreas or enlarged peripancreatic lymph nodes. The presence of hypodense lymph nodes with rim enhancement in the peripancreatic region, ascites and/or mural thickening affecting the ileo-cecal region may suggest the possibility of TB.1181 MRI findings of focal pancreatic TB include a sharply delineated mass located in the pancreatic head, showing heterogeneous enhancement. These lesions usually are hypointense on fat-suppressed
T1-weighted images and show a mixture of hypointensity and hyperintensity on T2-weighted images.[19] The common bile duct and the pancreatic duct have been reported to be normal in patients with pancreatic TB, even if the tuberculous mass is centrally positioned in the pancreatic head.
Radiological features including US, CT or endoscopic ultrasound (EUS) usually show multicystic pancreatic masses, most frequently in the head of the pancreas. Pancreatic lesions resulting from M. tuberculosis infection are often heterogeneous and multicystic and can mimic pancreatic cystic neoplasm.!201 When the diagnosis is suspected, a detailed screening for tuberculosis and US-FNA of the pancreatic lesions can confirm the diagnosis, and therefore avoid an unnecessary explorative laparotomy or pancreatic resection.[21] Because of the rarity of this disease, there are no specific treatment guidelines. The majority of cases of pancreatic TB respond well to 6-12 months of ATT and their prognosis is good.[22]
US-guided FNA was performed in pancreatic head mass in a 31-year-old female with history of HIV positivity, and 50 mL of purulent, turbid fluid was aspirated. The value of amylase in the cyst fluid was 33,801 U/l. The smears showed proteinaceous fluid and abundant acute inflammatory cells. ZN stain revealed AFB in the smears.[23]
A series of three EUS-guided FNA PPT cases and review of current literature on clinical presentation, diagnostic dilemmas and the role of EUS were studied. Authors concluded that endoscopic ultrasound is the diagnostic modality of choice for pancreatic tuberculosis facilitating high resolution imaging, as well as sampling of tissue for staining, cytology, culture and polymerase chain reaction assay.[24] CT-guided FNA in two female cases was done with history of epigastric pain radiating to back, and smears revealed caseous necrosis with positive AFB on ZN staining.[25,26] Earlier single case reports showed epithelioid cell granulomas and smears were positive for AFB in ZN Stain. AFB culture and PCR studies were also positive in these cases.[27,28]
PCR is a recent diagnostic-based assay test which detects M. tuberculosis DNA in the resected specimens. It is a highly specific assay and may give a positive result even when special staining techniques and culture of these tissues are negative. PCR was performed in 10 of our 14 cases, of which 8 cases showed M. tuberculosis DNA in FNA samples. These tests are more sensitive and more quickly available for definitive diagnosis, compared to microscopy and culture. Two cases showed inadequate sample for PCR assay. All the patients showed a good response to ATT, except one (drug resistant) in our study.
Most cases of pancreatic tuberculosis respond well to ATT as a primary treatment or after surgery, with Isoniazid/ Rifampin/Pyrazinamide/Ethambutol or Streptomycin for 6-12 months,[29] as in our cases. Twelve of 14 cases showed good response to ATT in our study, except 2 in which one case was lost to follow-up and other one was drug resistant.
The approach for noninvasive diagnostic techniques in pancreatic TB relies mainly on US and CT abdomen. US reveals focal hypoechoic lesions or cystic lesions of the pancreas. CT scan findings reveal hypodense lesions and irregular borders mostly in the head of the pancreas, diffuse enlargement of the pancreas or enlarged peripancreatic lymph nodes. In contrast to noninvasive techniques, invasive diagnostic techniques like EUS-guided biopsy, CT/US-guided percutaneous biopsy and surgical biopsy (open or laparoscopic) are more reliable and definitive for microbiological and pathological examination.!301
Conclusions
US-FNAC is a safe, reliable and cost-effective method for preoperative diagnosis of PPT. Clinical symptoms and accurate diagnostic approach by US-FNAC of PPT are the primary techniques which are needed to avoid performing redundant laparotomy. Despite its rarity, PPT should be considered for differential diagnosis of pancreatic and peripancreatic cystic mass in endemic developing countries.
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How to cite this article: Rao RN, Pandey R, Rana MK, Rai P, Gupta A. Pancreatic and peripancreatic tuberculosis presenting as hypoechoic mass and malignancy diagnosed by ultrasound-guided tine-needle aspiration cytology. J Cytol 2013;30:130-5.
Source of Support: Nil, Conflict of Interest: None declared.
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