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Comparison of fine-needle aspiration technique with Ziehl-Neelsen stains in diagnosis of tuberculous lymphadenitis.

Abstract

Background: Lymphadenopathy is one of the most common clinical presentation among patients. In developing countries such as India, tuberculous (TB) lymphadenitis is one of the common causes of lymphadenopathy. Cytomorphology with acid-fast staining is a valuable diagnostic tool in cases of tuberculosis.

Objective: To describe pattern of TB lymphadenitis presentation, and to compare results of fine needle aspiration cytology (FNAC) and Ziehl-Neelsen (ZN) stain in the diagnosis of TB lymphadenitis.

Materials and Methods: Total 351 patients of lymphadenopathy referred to the Department of Pathology, GMERS Medical College & Hospital, Vadodara, Gujarat, India, between March 2011 and December 2013included. FNAC was performed in all these patients and smears were prepared. Smears were stained with hematoxylin and eosin stain. ZN staining for acid-fast bacilli (AFB) was carried out on separate slide.

Results: Maximum number of patients (162; 46.15%) were from age group of 11-30 years. Total 351 cases [179 (50.99%) females and 172 (49.00%) males] were included in the study. Of 351 cases, 173 (49.28%) had tuberculosis, 141 (40.17%) had lymphadenitis other than tuberculosis, and 37 (10.54%) had malignant lymphadenopathy, including 2 (0.56%) cases of primary malignancy (i.e., lymphoma) and 35 (09.97%) of metastasis to lymph nodes. Overall, 119 (33.90%) cases were found to be positive for AFB on ZN staining.

Conclusion: FNAC is an optimally selected, efficient, easy to perform, and economical test for initial diagnostic workup in patients with TB lymphadenitis. Supplementation of ZN stain with FNAC increases the rates of diagnosis.

KEY WORDS: Tuberculosis, lymphadenopathy, fine-needle aspiration cytology, Ziehl-Neelsen stain

Introduction

India has the highest burden of tuberculosis in the world as reflected by the World Health Organization statistics for 2011, giving an estimated incidence of 2.2 million cases of tuberculosis for India of a global incidence of 8.7 million cases.[1]

In extrapulmonary tuberculosis, the most common presentation is cervical lymphadenopathy, especially among the Asian populations.[2,3] Lymph node enlargement could be due to tuberculosis, other inflammatory disease or fungal infection, or some underlying malignancy.[4] In general, tuberculous (TB) lymphadenitis is diagnosed using conventional methods such as histopathology on basis of caseous necrosis and granuloma formation. The chances of acid-fast bacilli (AFB) identification in tissue section are less because xylene and formalin affect the sensitivity of Ziehl-Neelsen (ZN) method to detect Mycobacterium tuberculosis in histopathology sections.[5]

Fine-needle aspiration cytology (FNAC) is a simple, quicker, reliable, minimally invasive, and relatively cheap diagnostic modality with minimal risk of complications.[6] The efficacy of FNAC to diagnose TB lymphadenitis is directly proportional to presence of purulent material in sample.[7] AFB are commonly seen in purulent samples, which may not contain granuloma, caseous necrosis, or epithelioid cells. In the absence of ZN staining, sample can be wrongly diagnosed as acute suppurative lymphadenitis.[3]

The aims and objective of this prospective study were (1) to describe presentation pattern of TB lymphadenitis and (2) to compare results of FNAC and ZN stain in the diagnosis of TB lymphadenitis.

Materials and Methods

Total 351 clinically diagnosed patients of lymphadenopathy referred to the Department of Pathology, GMERS Medical College & Hospital, Vadodara, Gujarat, India, between March 2011 and December 2013 were included in this study. The variables included in the study were age, sex, and site of lesion. Relevant history and examination of nodes were recorded. Nodes were aspirated after all aseptic measures with sterile disposable 23-G needle attached with 10 cc disposable syringe. Multiple smears were prepared with part of aspirated material; two to three smears were stained with hematoxylin and eosin (H&E) stain and ZN staining was performed on separate slide. All data were grouped and analyzed. Smears stained with H&E stain were examined under microscope for the presence of granuloma, necrosis, Langhans giant cells, plasma cells, lymphocytes, macro-phages, and neutrophils. Smears stained with ZN stain were examined under oil immersion objective for AFB. Presence of sheets of epithelioid cells with lymphocytes and plasma cells with or without multinucleated giant cells were diagnosed as granulomatous lymphadenitis, and eosinophilic granular material containing inflammatory cells and necrotic cell debris was defined as caseous necrosis.[7] The TB abscess was described as degenerate caseous necrosis and/or liquefied necrotic material with marked degenerating and viable inflammatory cell infiltration without epithelioid granuloma.[8]

Results

Aspirates from 351 patients were enrolled in this study with clinically diagnosed cases of lymphadenopathy. A majority of patients (162; 46.15%) were from 11-30 years age group [Table 1]. There were 179 (50.99%) female and 172 (49.00%) male patients with female/male ratio approximately 1.04:1. The most common site involved in lymphadenopathy was cervical in 339 (96.58%) cases followed by axillary in 8 (02.27%) and inguinal in 4 (01.13%) [Table 2]. TB lymphadenitis was found in 173 (49.28%) cases, inflammatory lymphadenitis other than tuberculosis in 141 (40.17%), and malignant lymphadenopathy in remaining 37 (10.54%) cases, consisting 2 (00.56%) cases of primary malignancy (i.e., lymphoma) and 35 (09.97%) of metastasis to lymph node [Table 3]. Of 314 cases of lymphadenitis, ZN stain was found to be positive for AFB in 119 (33.90%) cases [Table 4].

Discussion

India has the highest TB burden as shown in the 2011 World Health Organization (WHO) statistics.[1] The diagnosis of extrapulmonary tuberculosis still remains to be more of a clinical decision. Not many clinically sensitive tests are available in India to assist the treating physician. For accurate diagnosis of M. tuberculosis, isolation and culture of organism is gold standard, but as M. tuberculosis is slow growing organism, culture on conventional Lowenstein-Jensen medium takes 6-8 weeks. Middlebrook medium isolates growth of organism comparatively more rapidly. Mean duration to yield positive culture is about 3 weeks. But for the disease such as tuberculosis, this is too long to wait for results of culture as it is necessary to start treatment at the earliest. Therefore, comparatively rapid diagnostic strategies need to be established for diagnosis of TB lymphadenitis.[9] FNAC is a well-established diagnostic technique for lymphadenopathy evaluation. It is cost effective, safe, minimally invasive, and rapid method of diagnosing not only TB lymphadenitis but also other pathologies. It also avoids the possible physical and psychological complications of an excision biopsy.[9,10] In this prospective study, we have examined 351 cases of lymphadenopathy referred to the Department of Pathology. The finding that the majority of the patients (162; 46.15%) were from 11-30 years age group correlates with those of the other studies conducted by Bezabih and Mariam,[4] Lobo et al.,[12] Teklu et al.,[13] Hart et al.,[14] and Majeed and Bukhari.[15] Most common site involved was cervical region in 339 (96.58%) cases, which also correlates with the findings of other studies carried out by Bezabih et al.,[4] Lau et al.,[7] and Chen et al.[16] Tuberculosis was the most common finding in 173 (49.28%) cases, followed by other inflammatory lymphadenitis in 141 (40.17%). ZN stain was found to be positive for AFB in 119 (33.90%) cases, which correlates with the findings of other studies conducted by Majeed and Bukhari,[15] Kheiry and Ahmed,[17] and Rajwanshi et al.,[18] which reported ZN positivity of 37.4%, 59.4%, and 40% respectively. Most common cytological pattern observed was epithelioid granuloma with caseous necrosis and with or without Langhans giant cells in 125 (35.61%) cases, which is similar to the study conducted by Gupta et al.[19] Highest AFB positivity was seen in 119 (33.90%) cases with necrosis with or without granuloma and inflammatory cells. Few cases (54; 15.38%) with necrosis and granuloma showed AFB negativity whereas 36 (10.25%) smears that showed necrosis and polymorphs were reported as suppurative lymphadenopathy and 105 (29.62%) cases that did not show necrosis or granuloma and also were negative for AFB were reported as chronic nonspecific lymphadenitis, which is also similar to the study conducted by Gupta et al.[19] AFB were mostly visible in purulent aspirate whether acellular or accompanied by granuloma, and in the absence of ZN staining, case can be misinterpreted as an acute lymphadenitis.[20]

Conclusion

Cytomorphological features of FNAC on H&E stain have significant diagnostic yield. FNAC is an optimally selected, efficient, easy to perform, and economical test for initial diagnostic workup in patients with TB lymphadenitis. Supplementation of ZN stain with FNAC increases the diagnostic yield. AFB were mostly seen in purulent aspirate whether acellular or accompanied by granuloma. In the absence of ZN staining, case can be misinterpreted as an acute lymphadenitis.

References

1. TB Facts.org. TB Statistics India, 2012. Available at: http://www.tbfacts.org/tb-statistics-india.html (last accessed August 21, 2014).

2. Ng WF, Kung ITM. Clinical research pathology of tuberculous lymphadenitis: a fine needle aspiration approach. J Hong Kong Med Assoc 1990;42(1):18-21.

3. Metre MS, Jayaram G. Acid fast bacilli in aspiration smears from tuberculous lymph nodes. Acta Cytol 1987;31:17-9.

4. Bezabih M, Mariam DW, Selassie SG. Fine needle aspiration cytology of suspected tuberculous lymphadenitis. Cytopathology 2002;13(5):284-90.

5. Singh UR, Bhatia A, Gadre DV, Talwar V. Cytologic diagnosis of tuberculous lymphadenitis in children by fine needle aspiration. Indian J Pediatr 1992;59:115-8.

6. Shamshad SA, Shakeel A, Kafil A, Shano N, Tariq M. Study of fine needle aspiration cytology in lymphadenopathy with special reference to acid-fast staining in cases of tuberculosis. JK Science 2005;7:1-4.

7. Lau SK, Wei WI, Hsu C, Engzell UC. Fine needle aspiration biopsy of tuberculous cervical lymphadenopathy. Aus N Z J Surg 1988;58(2):947-50.

8. Dlipk DAS. Lymph nodes. In: Comprehensive Cytopathology, Bibbo M, Wilbur D (Eds.), 2nd edn. Philadelphia, PA: WB Saunders, 1997. pp. 707-9.

9. Mudduwa LKB, Nagahawatte Ade S. Diagnosis of tuberculous lymphadenitis: combining cytomorphology, microbiology and molecular techniques--a study from Sri Lanka. Indian J Pathol Microbiol 2008;51(2):195-7.

10. Finfer M, Perchick A, Burstein DE. Fine needle aspiration biopsy diagnosis of tuberculous lymphadenitis in patients with and without acquired immune deficiency syndrome. Acta Cytol 1991; 35:325-2.

11. Gupta AK, Nayar M, Chandra M. Critical appraisal of fine needle aspiration cytology in tuberculous lymphadenitis. Acta Cytol 1992;36:391-4.

12. Lobo J, Mulu G, Demmissie A. Immune response of tuberculous lymph adenitis patients to mycobacterial antigens. Abstract of 36th Annual Ethiopian Medical Association Conference; May 24-26, 2000; Addis Ababa, Ethiopia.

13. Teklu B, Habte D, Giday Y. Tuberculosis in children. In: Pulmonary Tuberculosis: The Essentials. Addis Ababa, Ethiopia: Ababa University Press, 1980. p. 24.

14. Hart CA, Beeching NJ, Dueren BI. Tuberculosis in the next century. J Med Microbiol 1996;44:1-34.

15. Majeed MM, Bukhari MH. Evaluation for granulomatous inflammation on fine needle aspiration cytology using special stains. Patholog Res Int 2011;2011:851524.

16. Chen YM, Lee PY, Su WJ, Perng RP. Lymph node tuberculosis: 7-year experience in Veterans General Hospital, Taipei, Taiwan. Tuber Lung Dis 1992;73:368-71.

17. Kheiry J, Ahmed ME. Cervical lymphadenopathy in Khartoum. J Trop Med Hyg 1992;95:416-9.

18. Rajwanshi A, Bhambhani S, Das DK. Fine needle aspiration cytology diagnosis of tuberculosis. Diagn Cytopathol 1987;3:13-6.

19. Gupta AK, Nayar M, Chandra M. Critical appraisal of fine needle aspiration cytology in tuberculous lymphadenitis. Acta Cytol 1992;36(3):391-4.

20. Pandey P, Dixit A, Mahajan NC. The diagnostic value of FNAC in assessment of superficial palpable lymph nodes: a study of 395 cases. Al Ameen J Med Sci 2013;6(4):320-7.

How to cite this article: Patel JM, Patel KR, Shah K, Patel NU, Baria H, Patel PD. Comparison of fine-needle aspiration technique with Ziehl-Neelsen stains in diagnosis of tuberculous lymphadenitis. Int J Med Sci Public Health 2015;4:400-403

Source of Support: Nil, Conflict of Interest: None declared.

Jignasha M Patel(1,) Kamini R Patel(1), Kamlesh Shah(1), Niraj U Patel(2), Hinal Baria(3), Prashant D Patel(4)

(1) Department of Pathology, GMERS Medical College & Hospital, Vadodara, Gujarat, India. (2) Department of Biochemistry, GMERS Medical College & Hospital, Vadodara, Gujarat, India. (3) Department of Community Medicine, GMERS Medical College & Hospital, Vadodara, Gujarat, India. (4) Department of Dentistry, SSG Hospital, Vadodara, Gujarat, India. Correspondence to: Jignasha M Patel, E-mail: dr.jignashapatel@gmail.com

Received September 11, 2014. Accepted November 23, 2014

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Website: http://www.ijmsph.com

Table 1: Age- and sex-wise distribution of cases of lymphadenopathy

Age (in years)     Male    Female    Total    Percentage

0-10                17       12       29        08.26
11-20               29       49       78        22.22
21-30               34       50       84        23.93
31-40               34       29       63        17.94
41-50               26       18       44        12.53
51-60               22       13       35        09.97
61-70               08       08       16        04.55
470                 02       00       02        00.56
Total              172      179      351       100
Percentage          49.00    50.99   100         -

Table 2: Site of lymph node involvement

Site                     No. of cases     Percentage

Cervical lymph nodes       339              96.58
Axillary lymph nodes        08              02.27
Inguinal lymph nodes        04              01.13
Total                      351             100

Table 3: Various cytomorphological picture in cases of lymphadenopathy

Type of lesion                   Cytomorphological diagnosis

Nonneoplastic                     Tuberculous lymphadenitis
(inflammatory lymphadenitis)
                                  Chronic nonspecific lymphadenitis
Acute lymphadenitis                             36
Neoplastic                        Metastasis to lymph node
(malignant lymphadenopathy)       Hodgkin's lymphoma
Non-Hodgkin's lymphoma                          01
Total                                          351

Type of lesion                   No. of cases    Percentage

Nonneoplastic                       173            49.28
(inflammatory lymphadenitis)
                                    105            29.91
Acute lymphadenitis                  10.25
Neoplastic                           35            09.97
(malignant lymphadenopathy)          01            00.28
Non-Hodgkin's lymphoma               00.28
Total                               100

Table 4: AFB positivity in various cytomorphological subpatterns in
cases of lymphadenitis

Cytomorphological picture      AFB positive cases   AFB negative cases
Epithelioid granuloma                71                    54
with caseous necrosis
Necrosis only without                08                    00
inflammatory cells
Necrosis with polymorphs             40                    36
Neither necrosis                     00                   105
nor granuloma
Total                               119                   195
Percentage                           33.90                 55.55

Cytomorphological picture      Total     Percentage

Epithelioid granuloma           125        35.61
with caseous necrosis
Necrosis only without            08        02.27
inflammatory cells
Necrosis with polymorphs         76        21.65
Neither necrosis                105        29.91
nor granuloma
Total                           314        89.45
Percentage                        -        89.45
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Title Annotation:Research Article
Author:Patel, Jignasha M; Patel, Kamini R; Shah, Kamlesh; Patel, Niraj U; Baria, Hinal; Patel, Prashant D
Publication:International Journal of Medical Science and Public Health
Article Type:Report
Date:Mar 1, 2015
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