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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 11  |  Issue : 1  |  Page : 30-37

Uncommon manifestations in tuberculosis: An expanding clinical spectrum from North India


1 Department of General Medicine, Institute of Medical Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India
2 Department of Microbiology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India
3 Department of Pathology, Popular Multispecialty Hospital, Varanasi, Uttar Pradesh, India

Date of Submission06-Dec-2021
Date of Decision03-Jan-2022
Date of Acceptance22-Feb-2022
Date of Web Publication12-Mar-2022

Correspondence Address:
Anju Dinkar
Department of Microbiology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_242_21

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  Abstract 


Background: Despite being given the best by the health department to eradicate the disease, an alarming rise of tuberculosis (TB) remains a significant public health concern in India. Recently, highly variable clinical manifestations of TB have been reported. This study highlights the unusual presentations of TB with a comprehensive overview of epidemiology, demography and risk factors in the expended clinical spectrum of TB patients and their outcomes. Methods: It is a retrospective study using the records of 503 TB patients of all age groups of either sex from July 2017 to January 2021 at two tertiary care hospitals in North India. Results: Out of 503 cases, pulmonary, extrapulmonary, and disseminated TB were 77.7%, 19.5%, and 2.8%, respectively. Among all TB cases, 36 (7.2%) had uncommon manifestations, including the most common was pyrexia of unknown origin in 12 (33.3%) cases and liver abscess in 5 (13.9%) cases, followed by pancytopenia in 4 (11.1%) cases and chyluria in 3 (8.3%) cases. Atypical skin nodules and multiple swellings were also noted in three (8.3%) cases. Male sex (58%) and rural area (66.7%) were dominant in TB with uncommon manifestation (TBU) cases. The mean age in TBU cases was 46.92 years, whereas 34.26 years in all TB cases. It was extremely significant. The statistically significant risk factors in the TBU case were low socioeconomic status (24, 66.7%), inadequate nutrition (11, 30.6%), and smoking (19, 52.8%). Conclusions: Early recognition of uncommon presentations is imperative to respond better.

Keywords: Atypical presentation, disseminated tuberculosis, extrapulmonary tuberculosis, multidrug-resistant tuberculosis, pancytopenia, pyrexia of unknown origin


How to cite this article:
Singh J, Dinkar A, Gupta P. Uncommon manifestations in tuberculosis: An expanding clinical spectrum from North India. Int J Mycobacteriol 2022;11:30-7

How to cite this URL:
Singh J, Dinkar A, Gupta P. Uncommon manifestations in tuberculosis: An expanding clinical spectrum from North India. Int J Mycobacteriol [serial online] 2022 [cited 2022 May 20];11:30-7. Available from: https://www.ijmyco.org/text.asp?2022/11/1/30/339512




  Introduction Top


Most recently, World Health Organization (WHO) Global Tuberculosis Report (2021), India was listed among the group of top 20 high-burden countries in the year 2016, contributing global incidence 84%, high tuberculosis (TB)/human immunodeficiency virus (HIV) burden 85% and high multidrug-resistant (MDR) TB burden 84%. Globally, deaths among HIV-negative people were estimated as 1.3 million deaths in 2020 while 1.2 million in 2019. In addition, deaths among HIV-positive people were also increased slightly in the years 2020 (214,000 deaths) from the 209,000 deaths in 2019. The five risk factors attributing new cases of TB were identified as undernutrition, HIV infection, alcohol abuse, smoking (especially among men), and diabetes. In this TB report, the reduction in TB deaths (%) is targeted to 90% in 2025 and 95% in 2035 compared with deaths in the 2015 baseline. On the other hand, drug-resistance TB is another major health concern. Resistance to the two most effective first-line drugs (isoniazid and rifampicin) is defined as MDR-TB, which remains a public health threat. Consequently, MDR-TB or rifampicin-resistant TB (RR-TB) is treated with second-line antitubercular drugs. Globally, MDR-TB or RR-TB (MDR/RR-TB) is still stable. It is estimated that about 3%–4% of people diagnosed with TB for the first time and 18%–21% of those who had previously been treated for TB.[1] TB is the preeminent cause of mortality and morbidity by affecting one-third population of the world. In 2016, 10.4 million new TB cases were estimated worldwide, and India was on top with 27.9 lakh cases. The WHO Global TB report (2017) stated to have the highest number of TB cases in India throughout the world.[1],[2]

TB is the primitive disease of humanity caused by Mycobacterium tuberculosis, which primarily affects the lungs and can affect anybody system.[2] It involves organs other than the lung. It is called extrapulmonary TB (EPTB), which is not uncommon, especially in developing countries like India. It can present various manifestations. Over the past two decades, the world notified a striking change in the clinical pattern of TB.[2] Therefore, the present study has been attempted for a comprehensive overview to understand the demographic and clinical characteristics and treatment outcome under the Revised National Tuberculosis Control Program (RNTCP) of the unusual clinical spectrum of TB, emphasizing the importance of early diagnosis and a better outcome. It will also help to reduce both the mortality risk and the spread of infection to the community.

Pulmonary tuberculosis (PTB) is a highly communicable disease that remains a significant public health problem worldwide. Different aspects of it are unknown, and its atypical presentations delay diagnosis. The classical profile of PTB is the symptoms of evening pyrexia, cough with sputum, weight loss, anorexia, night sweats, and malaise that is usually present for a few weeks before the visit to clinicians. If tuberculous involvement is of two or more noncontiguous sites, it is disseminated TB. It may infect any body organ, but lungs, liver, and spleen (80%–100%), followed by kidneys (60%) and bone marrow (25%–75%) are commonly affected organs. Disseminated TB is uncommon in the immunocompetent host, but cases are reported from India.[2] This symptomology is not always present, diverting the clinician's attention to diagnose early. It usually happens with EPTB, which manifests organ and anatomic sites-specific symptoms and signs. Despite various programs for awareness, treatment, and control of TB, India has a unanimous high burden.


  Methods Top


Retrospective data of 503 TB patients were analyzed from July 2017 to January 2021 of indoor and outdoor patient departments at two tertiary care hospitals in Varanasi, Uttar Pradesh. Out of them, 445 cases were traced from popular hospital from July 2017 to August 2020, and the rest 58 cases were collected from the Institute of Medical Sciences, Banaras Hindu University (BHU) by the convenience sampling method. In addition, after starting the “Nikshay portal,” an online health facility provided by RNTCP, 426 cases were registered on this portal.

All data were assessed with a detailed history, demographics, and associated comorbidities. A thorough clinical examination and appropriate investigations were recorded accordingly. Suspected PTB was diagnosed by imaging, sputum for acid-fast bacilli (AFB), culture and GeneXpert. The clinical manifestations of EPTB were atypical and sometimes very difficult to suspect TB due to the involvement of occult sites. In suspected EPTB cases, every possible invasive or noninvasive attempt was made to get relevant tissue/body fluid for diagnostic testing. Basic investigations (blood routine, serum biochemistry, viral markers, and chest X-Ray) were done in all patients. Microbiological, cytopathological or histopathological methods demonstrated M. tuberculosis in different body tissues or fluids. Depending upon sites and need, body fluids (pleural fluid, cerebrospinal fluid, pericardial fluid, and other fluids) analysis and culture, imaging (plain radiograph, ultrasonography (USG), computerized tomography, and magnetic resonance Imaging), fine-needle aspiration cytopathology (FNAC), biopsy, echocardiography, and colonoscopy were done accordingly. Sputum and other body fluids/tissues were examined for AFB and GeneXpert for MDR TB at RNTCP centers Varanasi. Patients were treated as per the RNTCP guidelines and followed until the outcome. Cases with MDR TB were referred to the pulmonary medicine department of BHU.

Ethical issue

Though it was a retrospective study. Instead, informed and written consents were obtained from those whose images of any part of the body or investigation were used. Again, though, we care about not disclosing any patients' identities in any form.

Statistical analysis

Data analysis were done online by using GraphPad software Quick-Calcs version. The results of this study were calculated in percentages, mean and standard deviation. In addition, continuous data-descriptive statistics and mean confidence interval were calculated by t-test (unpaired). Finally, Fischer's exact test (two-tailed) was performed to test significance for categorical data.

Level of significance were represented as extremely significant (ES) (P < 0.001), very significant (VS) (P value 0.001–0.01), significant (S) (P value 0.01–0.05), not significant [NS] (P ≥ 0.05).


  Results Top


The present study enrolled 503 cases of TB of either sex attending outdoor and indoor. Out of 503 cases, pulmonary, extrapulmonary and disseminated TB were found as 391 (77.7%), 98 (19.5%) and 14 (2.8%), respectively. Age group 20–35 was most commonly infected with 188 (37.4%) cases, out of which 147 cases of pulmonary, 35 cases of ETB and 6 cases of disseminated TB were found. Male sex was dominant in PTB with 234 cases and disseminated TB with 11 cases, while female sex was dominantly involved in EPTB with 64 cases.

Rural dominancy was revealed in all cases of TB with PTB, 203 (51.9%) cases, EPTB 60 (61.2%) cases and 10 (71.4%) cases in disseminated TB [Table 1].
Table 1: Demographic characteristics of cases in different groups of tuberculosis

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Among all TB cases, 36 (7.2%) had uncommon manifestations. Out of which, the most common was pyrexia of unknown origin (PUO) in 12 (33.3%) cases and liver abscess in 5 (13.9%) cases, followed by pancytopenia in 4 (11.1%) cases and chyluria in 3 (8.3%) cases. In addition, atypical skin nodules and multiple swellings were noted in 3 (8.3%) cases, and other unusual manifestations are depicted in [Figure 1].
Figure 1: Uncommon manifestation in tuberculosis

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The mean age in uncommon TB cases was 46.92 years while 34.26 years in all TB cases. Age of uncommon TB cases was higher and ES on compression.

Male sex was dominant in TBU cases, with a male-female ratio of 1.4 (21/15). In more cases, 24 (66.7%) belonged to the rural area and were insignificant compared to all TB cases. Among risk factors, low socioeconomic status was found in 24 (66.7%) TBU while 152 (30.2%) cases of all TB cases. It was statistically ES. Due to poverty, inadequate nutrition was observed in 11 (30.6%) cases of TBU, while it was more in all TB with 274 (54.5%). This relation was also revealed statistically VS. Among TBU cases, 19 (52.8%) cases were a smoker. It was statistically VS compared to 142 (28.2%) cases of all TB. Among TBU, 9 (25%) cases and 44 (8.7%) TB cases had diabetes. The diabetic association between the two group cases was also statistically VS. Among TBU cases, none had HIV, while 2 (0.4%) cases were reported in all TB cases. History of chronic obstructive pulmonary disease was present in 4 (11.1%) TBU cases and 98 (19.5%) cases in all TB group. Chronic liver disease and chronic kidney disease were also in both groups, which were not statistically significant [Table 2]. Of 503 cases, 13 (2.6%) were of MDR TB. Most of them were male with rural dominancy (77%). Two cases (15.4%) have died. The rest were on treatment till analysis of data [Table 3]. MDR TB was not reported in TBU cases.
Table 2: A comparison of demographic and risk factors among cases of uncommon tuberculosis to all cases of tuberculosis

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Table 3: Demographic parameters of multidrug-resistant cases (n=13)

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  Discussion Top


In the present study, males and rural residents dominated TBU and all TB cases. However, rural and gender prominence were NS. The contributing factors to increasing incidence and prevalence of TB, especially in developing countries like India, are poverty, malnutrition, unhygienic living standards, crowding, drug abuse, the spread of HIV, immigration, chronic debilitating illness, immune status and genotype of M. tuberculosis strain.[2],[3]

Here, the most common risk factors among all TB cases were inadequate nutrition (54.5%) and low socioeconomic status (30.2%), followed by smoking (28.2%). On the other hand, in the TBU case, the most common risk factors were low socioeconomic status (66.7%) and smoking (28.2%), followed by inadequate nutrition (30.6%).

Tobacco use is negatively associated with TB outcomes in studies, and nearly 8% of TB cases are attributed to tobacco usage.[4] Overall, 28.2% of cases had a history of active smoking. Smoking was predominant in males, which may occur due to the social barrier as India is a dominant male country.

Diabetes attributes nearly two to three times more risk to TB. Furthermore, diabetes can affect the clinical course of TB and vice versa. In 2018 under RNTCP, 29% notified TB patients were screened and found nearly 8% cases of diabetes (newly diagnosed and already existing diabetes).[4] This study found diabetes 8.7% in all TB cases (10 new cases and 34 cases of preexisting diabetes), nearly the same as RNTCP. In contrast, diabetes was detected much more (25%) in TBU cases. Whereas, a retrospective analysis of abdominal TB from India revealed comorbidities as diabetes in 33.3% of cases, HIV infection in 45.2%, and chronic kidney disease in 11%.[5] Low socioeconomic status, smoking and diabetes were more common in TBU cases, and inadequate nutrition was lower than TB in all cases, and all these parameters were statistically significant.

Despite increasing public awareness with improved implementation of TB management, it continues to be the second leading cause of mortality due to infectious disease worldwide after HIV disease.[4] The burden of EPTB is reported 10%–20% in HIV-negative patients while it is 40%–50% in HIV-positive cases.[6],[7] Unfortunately, India has the third rank in the highest HIV burden worldwide.[4] In this study, all patients were screened for HIV and found 2 cases of HIV, one was an old male with PTB, and the other was a middle-aged female with disseminated TB. Fortunately, it was a very low incidence with 0.4%. None of the TBU cases had HIV infection. The other comorbidities such as chronic obstructive pulmonary disease, chronic kidney and liver disease were also found in TBU and all TB cases, but none was statistically significant.

As the trend of many studies in India, infections are the most common cause of PUO, and TB remains the most frequent.[8] We found 12 (33.3%) cases of PUO. On giving a trial of empirical antituberculous therapy to those patients, fever subsided to normal within 2 weeks. Six months of antituberculous treatment (ATT) was completed to the successful outcome without any adverse effects.

A retrospective analysis including 317 patients with abdominal TB showed luminal involvement in 49.5% cases as the most common, while solid visceral in 9.4% cases.[5] Diagnosing intestinal TB is a diagnostic challenge because of closely mimic Crohn's disease and colon cancer. In this dilemma, biopsy specimens often confirm that M. tuberculosis is detected in tissue.[9] A tuberculous liver abscess (TLA) is a rare entity but not an exceptional one. Mycobacterium bacilli infect the liver via a hepatic artery or the portal vein through respiratory and gastrointestinal tracts. Primary TLA without any evidence of TB infection in other body sites has been reported sporadically. Infiltration of antitubercular drugs to the target may hinder the presence of thick fibrous tissue around the abscesses. Despite that, ATT alone with or without percutaneous aspiration is wildly accepted therapeutic management of TLA.[10] The present study reported 5 (13.9%) cases of liver abscess with AFB positive in pus, two cases were primary TLA, and 3 cases were associated with disseminated TB [Figure 2]a. The abscess of all cases was drained percutaneously and resolved on ATT.
Figure 2: (a) Abscesses in both lobes of the liver with moderate ascites, (b) bone marrow aspiration examination showing pancytopenia, (c) yellowish white urine

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The various haematological abnormalities like anaemia of different types, pancytopenia, leukoerythroblastic anaemia, leukemoid reaction, rarely dissemination intravascular coagulation (disseminated intravascular coagulation), and myelofibrosis are reported in TB. However, pancytopenia was associated only with disseminated/miliary TB.[2] The study reported 4 (11.1%) cases of pancytopenia. Out of them, two were associated pulmonary and 2 cases with disseminated TB [Figure 2]b. The pancytopenia recovered spontaneously on ATT within 3–4 weeks and did not reoccur until the ATT completion.

Upper abdominal and mediastinal lymphadenopathy are rarely reported to cause thoracic duct obstruction, chylothorax, chylous ascites, and chyluria.[11] There were 3 (8.3%) cases of chyluria. Out of three, 1 case was associated with PTB, and one also had abdominal TB with chylous ascites. The third case was a known chronic alcoholic liver disease case who noticed suddenly white milky urine. On evaluation, he was found to have PTB with chyluria. Though AFB was not detected in urine or ascitic fluid in all cases, it turns in normal colour after 3–4 weeks of ATT initiation [Figure 2]c.

Cutaneous TB is a significant health concern in developing countries, especially lower socioeconomic groups.[12] There were 2 cases of disseminated TB having nonpruritic, nonpainful and pinhead-sized to 6 mm sized in diameters of erythematous macules, and papules types present all over the body, especially on the trunk thigh, genitalia, buttocks, and extensor extremities [Figure 3]a. This presentation is infrequent in literature and reported in immunocompromised patients.[13] Both cases had no evidence of immunocompromised status, which highlights further its rarity. For 1 month, the study reported a unique case of multiple soft, nontender swellings over the abdomen with constitutional symptoms [Figure 3]b. FNAC of large swelling was suggestive of TB with positive AFB. Interestingly, there were no detectable foci of TB in the lungs and other body sites, though this young boy had a history of taking steroids in a gymnasium. No similar case was found in the literature. Cutaneous TB is again uncommon, with 1%–2% of all extrapulmonary manifestations. Similarly, a 45-year-old immunocompetent woman presented with painful, warm nodules of various sizes on his body, later diagnosed as disseminated TB with polymorphous cutaneous lesions and tuberculous adenitis and bone TB.[14]
Figure 3: (a) Multiple nonpruritic papules on the neck, trunk, thigh, buttocks, and extensor extremities, (b) multiple nontender swellings over the abdomen, (c) Acid-fast bacilli in pus from the vulva

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Psoas abscess of tuberculous origin is a rare entity usually associated with spinal TB.[15] Here, 2 (5.6%) cases of psoas abscess were reported, one had spinal TB, and the other had PTB. It may be secondary to direct invasion from lumbar vertebrae or hematogenous spread. Ultrasound-guided percutaneous drainage was done in both cases. AFB was detected in the drained fluid of one case, while the second case had positive GeneXpert testing for M. tuberculosis without rifampicin resistance.

This study found tonsillar TB in 2 (5.6%) immunocompetent individuals. In one case, it was primary tonsillar TB in an otherwise healthy middle age, in whom no PTB was documented but had a history of teeth extraction twice before the illness. AFB was detected on Ziehl Neelsen staining in pus. Another case had bilaterally enlarged tonsils covered with yellowish-white plaque and bilateral significant cervical lymphadenopathy without any evidence of pulmonary involvement. FNAC from lymph node and histopathological examination of the resected specimen suggested chronic granulomatous inflammation due to TB. Isolated tonsillar TB in the absence of PTB is an infrequent clinical entity, as discussed in the literature. The predisposing factors are the direct contact of AFB positive sputum, dental extraction, low immunity, or hematogenous spread.[16] TB of the female genital system can involve  Fallopian tube More Detailss, endometrium and ovaries.[7] One more unique reporting of AFB was come out in pus from the abscess on the vulva of a young girl with PTB having low socioeconomic status and inadequate nutrition. However, the immunocompromised state was ruled out [Figure 3]c.

One more case of splenic abscess reported in this study was an infrequent entity among immunocompetent individuals.[17] He had a long-standing history of on and off fever and not responding to multiple antibiotics. His contrast-enhanced computed tomography abdomen revealed multiple well-defined abscesses in the spleen and mesenteric lymphadenopathy. USG-guided aspiration from the large lesion demonstrated AFB in pus. He responded well to a successful outcome on ATT.

Another cause of a young, healthy unmarried female was presented with loin pain and low-grade fever for 3 months. She was depressed about her illness as a diagnosis was not established. Later she was diagnosed with a right renal abscess and spinal TB without any evidence of TB in the lungs. She improved successfully by conservative management with ATT. Unfortunately, due to uncommon clinical manifestations, the disease was diagnosed late.

A young married woman was presented with low-grade fever, pain and swelling of the right breast for 2 months, followed by nipple discharge for 10 days. Rest local and systemic examinations were unremarkable. Her husband was also a known case of PTB and was on ATT for 1 month. USG of the breast showed a hypoechoic lesion in the retro areolar area. FNAC from the breast lump was suggestive of tuberculous pathology, and AFB was detected. The significance of this entity is due to its rarity and point to highlight that it may be misdiagnosed with other benign and malignant lesions of the breast. Brest TB is a rare disease with <0.1% in developed countries, ranging from 3% to 4% in the Indian sub-continent and Africa. Breast TB may be due to hematogenic, lymphatic spread by the adjacent tissues (thoracic wall or the axillary lymph nodes) or direct infection through traumatized skin or ducts.[18] Here, there is more likely to spread infection through skin abrasions or the main ducts of the nipple. A young, healthy boy was presented with recurrent low-grade fever and painless swelling of the right testis. He had completed an antifilarial course but still not improved. He had no trauma or significant medical history in the past. USG revealed most likely TB epididymitis with abscess formation. There was no clinical and laboratory evidence of TB involvement to any other site. FNAC also suggested TB, but no AFB was seen in pus. He cured completely with 6 months of ATT regimen. Isolated TB epididymitis is usually rare and challenging to diagnose. Though similar cases are reported from TB prevalent countries.[19] Furthermore, detailed clinical features, including uncommon manifestations of TB reported in the literature, are depicted in [Table 4].[6],[7],[11],[20],[21],[22],[23],[24],[25]
Table 4: Complications/sequelae and uncommon manifestations of tuberculosis

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Multidrug-resistant tuberculosis

Besides data collection, RNTCP provides nutritional support, free diagnostics, and treatment services for all TB patients. RNTCP, now called the National tuberculosis elimination program (NTEP) in December 2019, is working aggressively to eliminate TB from India targeting 2025.[4] It is an admirable concern for rising MDR TB cases. A study conducted on nine centres by the Indian Council of Medical Research revealed MDR TB ranging from 0.6% to 3.2% to initial drug resistance and 6% to 30% due to acquired drug resistance.[26] This study had 2.6% MDR TB, similar to previous studies. These cases were most of the rural residence. Additionally, a retrospective analysis of 1116 clinical isolates of newly diagnosed TB cases at TB laboratory, dubai, showed 4.5% MDR TB and diabetes cases were a risk factor of TB drug resistance.[27]

Limitation of the study: Although there are some limitations such as (i) small sample size, (ii) retrospective study, (iii) pattern of drug susceptibility and multidrug regimen in MDR cases, even though, authors have tried best to bring attention to the importance of such atypical presentations of TB and associated underlying risk factors. Furthermore, it is the only study including the largest cases of uncommon presentations and conducted at two centres.


  Conclusions Top


TB can manifest a variety of presentations. We conclude that there is a paramount need to strengthen the working association between diagnostics, treating clinicians, the private sector, religious bodies, and other voluntary nongovernment organizations for public awareness about TB's different aspects, including unusual manifestations. Health departments must ensure unauthorized practitioners prevent irrational use of ATT and encourage modern medicines to prevent MDR TB. Though, NTEP is working aggressively and vigilantly with promising results. Therefore, high clinical suspicion is required as unusual presentations of TB are not uncommon in India.

Acknowledgements

We thank Jaitik Dinkar Singh and Jenika Dinkar Singh for their kind support.

Ethical clearance

Waived. Though, informed and written consents were obtained from those whose images of any part of the body or investigation were used.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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