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 Table of Contents  
Year : 2022  |  Volume : 11  |  Issue : 4  |  Page : 448-453

A rare case series of HIV-negative patients with early relapsing cervical tuberculosis lymphadenitis

Department of Chest Diseases, Health Sciences University, Yedikule Chest Diseases and Thoracic Surgery Research and Training Hospital, Kazlicesme, Istanbul, Turkey

Date of Submission01-Sep-2022
Date of Decision25-Oct-2022
Date of Acceptance06-Nov-2022
Date of Web Publication10-Dec-2022

Correspondence Address:
Hulya Abali
Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital, Kazlicesme 34020, Istanbul
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmy.ijmy_165_22

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Most patients with early recurrent tuberculous lymphadenitis (RTL) can be overlooked due to the paucibacillary character of Mycobacterium tuberculosis complex (MTBC) causing difficulty in the differential diagnosis. Here, we present three cases with early RTL that occurred after completing pulmonary tuberculosis (TB) therapy with a cure, and that improved by early diagnosis and therapy. A 30-year-old migrant male, HIV-negative patient, who had used immunosuppressive drugs for Crohn's disease presented to the TB outpatient clinic with a new anterior cervical lymph node enlargement. Two months ago, his therapy for pulmonary TB and intra-abdominal tuberculous lymphadenitis (TL) was completed. Real-time polymerase chain reaction (RT-PCR) of purulent fine-needle aspiration (FNA) specimen from the anterior cervical lymphadenopathy (LAP) was detected positive for MTBC. Isoniazid (H) resistance was determined via the Seegene system. The 6 cm anterior cervical LAP regressed to a 1.6 cm LAP at the 4th month of initial therapy with first-line antitubercular drugs. A 25-year-old female, the HIV-negative patient, was admitted to the TB outpatient clinic with a bulge on the submandibular area 3 months after the cessation of pulmonary multidrug-resistance TB therapy lasting 2 years. She had an index case but no comorbidity. The cytomorphology of FNA biopsy from the submandibular LAP reported granuloma with necrosis. RT-PCR of the purulent FNA specimen was positive for MTBC. H and rifampicin (R) resistances were found via the Seegene system. The right submandibular 2.9 cm LAP improved to a 1.7 cm LAP 6 months after the initiation of second-line antitubercular therapy. A 19-year-old male, the HIV-negative patient, presented to the TB outpatient clinic with a new bulge on the left supraclavicular area 9 months after cessation of pulmonary TB. He had no comorbidity and index case. RT-PCR of the purulent FNA specimen was positive for MTBC. H and R sensitivities were determined via the Seegene system. After the initial therapy with first-line antitubercular drugs for 2 months, the 1.5 cm left supraclavicular LAP improved to a 1.2 cm LAP.

Keywords: Cytomorphology, fine-needle aspiration, pulmonary tuberculosis, real-time polymerase chain reaction, relapsing tuberculous lymphadenitis

How to cite this article:
Abali H, Ortakoylu MG. A rare case series of HIV-negative patients with early relapsing cervical tuberculosis lymphadenitis. Int J Mycobacteriol 2022;11:448-53

How to cite this URL:
Abali H, Ortakoylu MG. A rare case series of HIV-negative patients with early relapsing cervical tuberculosis lymphadenitis. Int J Mycobacteriol [serial online] 2022 [cited 2023 Feb 4];11:448-53. Available from: https://www.ijmyco.org/text.asp?2022/11/4/448/363161

  Introduction Top

Paradoxical lymph node (LN) enlargement can be presented during or after antitubercular therapy (ATT). Although its occurrence during ATT is common in human immunodeficiency virus (HIV)-positive patients, it is rare in HIV-negative patients.[1],[2],[3] The incidence of posttherapy lymphadenopathy (LAP) has been observed in a wide range of 2.8%–15.6% in previous studies.[2],[3],[4] After the completion of successful ATT, the rate of recurrent tuberculous lymphadenitis (RTL) has been declared 10%, whereas the rate of paradoxical reaction has been declared 12% in a high-burden setting.[5]

Tuberculous lymphadenitis (TL), the most prevalent type of extrapulmonary tuberculosis (TB), typically appears in the cervical site as a unilateral and painless bulge.[6],[7],[8] Lymphadenitis can be caused by nontuberculous mycobacterium (NTM) and Mycobacterium TB complex (MTBC) microorganisms. Lymphadenitis caused by NTM is often detected in children and rapid differential diagnosis is important since the therapy varies for both.[9] Delays in diagnosis can lead to superinfections[10] and complications, which can be life-threatening for especially immunosuppressive patients.

New or existing LN enlargement after completing ATT allows a clinician in a dilemma. Because posttherapy LAP may be a paradoxical response that develops due to immunologically mediated cellular response and does not require further therapy.[2] Microbiological recurrence is described as confirmed by a positive culture result after the end of ATT that resulted in cure. Clinical recurrence is described as no microbiological recurrence and improvement with retreatment. Thus, the clinician requires detecting microbiological or clinical recurrence for the decision to initiate and continue retreatment.

Culture samples generally have high specificity but low sensitivity, and the turnaround time for results is usually 3–8 weeks.[11] Polymerase chain reaction (PCR), the nucleic acid amplification test that reduces this time to 6–8 h, can improve sensitivity.[12],[13] Xpert mycobacterium tuberculosis/rifampicin (Xpert MTB/RIF, Cepheid, Sunnyvale, CA, USA), an automated cartridge-based rapid method, has high sensitivity and specificity.[14] Using Xpert MTB/RIF, conventional PCR, and Mycobacteria Growth Indicator Tube (MGIT), the identification rates of MTBC are 25.71%, 20.71%, and 17.85%, respectively.[15] However, Xpert MTB/RIF is not cost-effective compared to other diagnostic tests.[9]

Herein, the demographic, clinical, laboratory, imaging characteristics, and follow-up of three HIV-negative cases with relapsing tuberculosis lymphadenitis after the pulmonary TB therapy resulted in cure were presented.

  Case Reports Top

Case 1

A 30-year-old male patient presented to our TB outpatient clinic with a palpable bulge on the anterior side of his neck. The patient was nonsmoker, HIV-negative, and had no history of TB contact and COVID-19 history. He had treated with azathioprine and methylprednisolone for Crohn's disease 2 years ago. Except for mild increases in the sedimentation rate (42 mm/h), C-reactive protein (CRP) (14.5 mg/L), and potassium levels (5.3 mmol/L), laboratory findings were in reference ranges [Table 1].
Table 1: Demographical features and laboratory findings of the cases with relapsing tuberculosis lymphadenitis

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On the first admission to the TB outpatient clinic, the patient's complaints had been sweating and 10 kg of weight loss in 3 months. Infiltrates in the right lung lower lobe and lingula, bilateral hilar LAP, and right supraclavicular 1.4 cm LAP had been demonstrated in the thoracic computed tomography (CT) [Figure 1]a, and celiac LAP had been seen in the abdominal CT. Sputum culture had proliferated MTBC and real-time PCR (RT-PCR) of bronchoscopic lavage had been found positive for MTBC. The cytomorphology of the fine-needle aspiration biopsy (FNAB) from the celiac LAP had been reported a granuloma with necrosis. Isoniazid (H) resistance had been detected in the phenotypic resistance test via the MGIT system and he had been treated with H, rifampicin (R), pyrazinamide (P), and ethambutol (E) (2 months), then H, R, and E (7 months). In the 6th month of the therapy, the right enlarging supraclavicular LN with an abscess [Figure 2]a had been excised.
Figure 1: In the thoracic computed tomography on the first admission. (a) Right perihilar ground glass infiltrates and bilateral multiple centrilobular nodules of case 1. (b) Infiltrates in the superior segment of the right upper lobe, lingula, and posterior segment of the left lung of case 2. (c) Infiltrates in the bilateral lung upper lobes of case 3

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Figure 2: Lymphadenopathies of the first case. (a) Posttreatment right supraclavicular tuberculosis lymphadenitis. (b) Improvement of the posttreatment right supraclavicular tuberculosis lymphadenitis after excision and retreatment. (c) Relapsing anterior cervical tuberculosis lymphadenitis. (d) Improvement of the relapsing anterior cervical tuberculosis lymphadenitis after retreatment

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The therapy for pulmonary TB and TL was completed 2 months before the admission for the new neck bulge. In the ordered cervical ultrasound (USG), 3.8 cm dense loculation which tended to fistulize into the skin in the right supraclavicular area (excised LAP area), new right supraclavicular 1.3 cm LAP, left supraclavicular 1.2 cm LAP, and anterior cervical 6 cm LAP with abscess formation [Figure 2]c was shown. A 10 cc of FNA specimen with pus from the anterior cervical LAP was sent to the microbiology department to examine acid-fast bacilli (AFB) stain, culture, and RT-PCR for MTBC. RT-PCR was found positive, whereas AFB stain and culture were found negative for MTBC. H resistance was found in the genotypic resistance test via the Seegene system and H, R, P, and E were initiated as the therapy regimen. In the neck USG at the 4th month of the therapy, whereas loculation areas opening to the skin with a thickness of 1 cm caused by excised right supraclavicular LAP were observed in the surrounding soft tissue [Figure 2]b, the newly formed, anterior cervical 6 cm LAP with abscess improved to a 1.6 cm LAP that fistulized into the skin [Figure 2]d. The therapy and follow-up of the case continue in our reference chest diseases center.

Case 2

A 25-year-old female patient presented to the TB outpatient clinic for a palpable bulge on the right area of the neck. The nonsmoker HIV-negative patient was not previously infected with COVID-19. Her index case was her sister. Laboratory findings of the patient who had no comorbidity were within the reference ranges [Table 1].

The patient had admitted to the TB outpatient clinic for complaints of fatigue, cough, sputum, night sweating, and 6 kg of weight loss for 2 months about 3 years ago. Thoracic CT revealed bilateral infiltrates consisting right lung lower lobe, left lung upper lobe, and lingula [Figure 1]b. Right supraclavicular 2.2 cm LAP and multiple LAP of which the largest one was 3.2 cm in the right internal jugular and posterior cervical chains had been shown in the neck USG. MTBC proliferated in the sputum culture. H, R, and E resistances were determined in the phenotypic resistance test via the MGIT system. Moxifloxacin, amikacin, promid, cyclocaps, pyrazinamide (P), and para-aminosalicylic acid (PAS) were initiated as therapy, and amikacin was withdrawn 6 months later. The therapy period was completed in 2 years with other existing drugs.

Three months after the completion of the therapy, a right submandibular bulge appeared. Right submandibular 2.9 cm LAP with abscess [Figure 3]a foci had been observed in neck USG. The cytomorphology of FNAB from the submandibular LAP had resulted in granuloma with necrosis in another center. RT-PCR of purulent FNA specimen from this LAP was positive for MTBC. H and R resistances were found in a genotypic drug resistance test via the Seegene system. AAT including moxifloxacin, cyclocaps, promid, PAS, and linezolid was initiated. The right submandibular 2.9 cm LAP regressed to a 1.7 cm LAP [Figure 3]b in the neck USG 6 months later. The patient has been still treated and followed up in the TB outpatient clinic.
Figure 3: Lymphadenopathies of the second case. (a) Relapsing right submandibular multidrug-resistant tuberculosis lymphadenitis. (b) Improvement of the relapsing right submandibular multidrug-resistant tuberculosis lymphadenitis after retreatment

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Case 3

A 19-year-old male patient had a palpable bulge on the supraclavicular area on admission to the TB outpatient clinic. The nonsmoker HIV-negative patient had no comorbidities and COVID-19 history. The levels of sedimentation rate and CRP were observed to have increased (64 mm/h and 34 mg/L, respectively) moderately, and hepatitis B surface antibody (anti-HBs) was found positive via ELISA testing [Table 1].

The patient had been referred to our center from another center to examine the bilateral diffuse infiltrates 19 months ago. He had been suffered from cough, fever, and dyspnea for a month. Bilateral diffuse infiltrates that were common in the lung upper lobes and a 1 cm cavitary lesion in the apical posterior segment of the right lung upper lobe were detected in the thoracic CT [Figure 1c]. RT-PCR and culture of sputum were found positive for MTBC. The phenotypic resistance test via the MGIT system revealed no major drug resistance. Then, ATT was planned as H, R, P, and E (3 months) and H and R (7 months). However, since the radiological recovery had been under expectation, maintenance therapy had been initiated after 4 months. Two months after the maintenance therapy initiation, neck USG had been performed due to a bulge on the neck, and left submandibular 5 cm LAP with abscess foci had been examined. Core biopsy (Trucut needle biopsy) from this LAP had reported a granuloma with necrosis. RT-PCR of core biopsy was positive for MTBC.

The patient presented to our hospital with pus leaking from the existing fistulized submandibular LAP and a new left supraclavicular bulge 9 months after the completion of the pulmonary TB therapy. Thereupon, left submandibular 3.9 cm LAP with abscess foci and new left supraclavicular 1.5 cm LAP were observed in the ordered neck USG. RT-PCR of purulent FNA specimen from the supraclavicular LAP was positive for MTBC, and H and R sensitivities were found in the genotypic resistance test via Seegene. AFB testing and culture of the FNA specimen were negative for MTBC. ATT of H, R, P, and E (2 months) then H and R (4 months) were planned. After the completion of the initial therapy, the left submandibular LAP improved to 3.3 cm and the left supraclavicular LAP improved to 1.2 cm in the neck USG. The therapy management of the patient is carried out in our center.

Microbiological examination

AFB stain: LabChem Carbol-Fuchsin solution (Kinyoun), Cole-Parmer company, USA; RT PCR test: Anyplex™ II MTB/MDR Detection, Seegene, South Korea; and Culture: BD BACTEC™ MGIT™ automated mycobacterial detection system, Becton, Dickinson and Company, India.

  Discussion Top

Recurrent TB has two types consisting of relapse (produced by the initial strain) and reinfection (with another TB strain). A study reported that the majority of relapses developed within the first 4 years; however, the risk of reinfection TB persisted for 14 years.[16] There is no study on the rate of RTL in the literature. However, two peaks were observed in HIV-negative patients, with a relapse of 69% within 6 months after completing TB treatment, and another 89% within 1 year in a previous study.[17] The relapse of the first two patients occurred in the first peak period, whereas the third patient occurred in the second peak period.

Although there is no study on the risk factors for TB recurrence in high-burden settings, a study performed in low-burden settings reported low-socioeconomic status, foreign nationality, HIV-positive, and multidrug-resistant TB (MDR-TB) infections as risk factors. Moreover, a correlation between bilateral pulmonary TB and recurrent TB was found via univariate analysis (odds ratio [OR] 2.9, 95% confidence interval [CI] 1.5–2.7).[18] The migrant first patient used immunosuppressive drugs and the migrant third patient had a low-socioeconomic status. The second patient was diagnosed previously with MDR-TB. Furthermore, the common feature of all was the previous bilateral pulmonary involvement.

PR phenomenon is a pitfall for the diagnosis of RTL after completing pulmonary TB therapy. Patients' median interferon gamma-producing T-cell responses specific for TB decline to 6 months following the initiation of TB therapy in patients with pulmonary TB[19],[20] while it increases in those with extrapulmonary TB.[21] These results may support the low incidence of PR in pulmonary TB during therapy.[22] However, a previous study reported two peaks in the occurrence of PR in patients with extrapulmonary and pulmonary TB one during the therapy and one at the end of the therapy.[4] Initiation and withdrawal of the ATT may trigger an immunological response cascade. Thus, the occurrence of PR after the completion of therapy is also possible for pulmonary TB.

Culture and/or AFB testing positivity are essential for the diagnosis of TL. Detecting these results on FNA specimens is limited with a range of 10%[23] and 70%[24]. The detection of the MTBC using RT-PCR on FNA specimens has proven to be an effective molecular investigative tool, providing a definitive and comparable diagnosis of TL.[25] RT-PCR can also define H and R drug resistances quickly, offering the initiation of rapid and effective therapy. All of our patients had RT-PCR positivity for MTBC. With a sensitivity of 96.77%, a specificity of 100%, a positive predictive value (PPV) of 100%, and a negative predictive value (NPV) of 96.67%, FNA cytology was found to have good efficacy when compared to histology as the gold standard. The sensitivity, specificity, PPV, and NPV were 97.44, 100, 100, and 91.67%, respectively, when compared to bacteriology as a gold standard approach.[26] FNAB may eventually be replaced with FNA in TL diagnosis,[27] notably since it is a rapid, safe, painless, and cost-effective procedure.[28] The cytomorphological pattern on FNA, FNAB, and core biopsy of the patients was necrotic granuloma, which was the most frequently reported pattern in previous data.[25],[29],[30]

Tahseen et al. from Pakistan, which is like our country with a low HIV infection incidence and endemic for TB, reported that more than 95% of TL was diagnosed via a combination of the rapid molecular assay (Xpert) and cytopathology, compared to less than 60% via the Xpert alone.[31] We consider that these rates are valid for cytopathology and rapid molecular tests such as RT-PCR in our country.

  Conclusion Top

HIV-negative patients with RTL may increase rapidly in Turkey due to the increasing population of immigrants from TB-endemic areas. Therefore, cases with recurrent TL should not be overlooked to reduce misdiagnosis and the resulting health and socioeconomic burden. Demographic features and clinical, radiological, microbiological, and cytological examinations of the patients should be evaluated together.

Limitation of the study

The case reports of patients were presented while their therapies were proceeding, and no further follow-ups of the patients are available.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1]


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