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ORIGINAL ARTICLE
Year : 2023 | Volume
: 12
| Issue : 1 | Page : 28-32
Osteoarticular tuberculosis in Central India: Changing epidemiological profile and emerging challenges
Vivek Kumar Kori, Deepanshu Bandil, Mohit Asthana, Deepak Singh Maravi
Department of Orthopaedics, Gandhi Medical College, Bhopal, Madhya Pradesh, India
Correspondence Address:
Deepanshu Bandil
B-10 Dwarikapuri, Phoolbagh, Gwalior - 474 002, Madhya Pradesh
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/ijmy.ijmy_233_22
Background: Osteoarticular tuberculosis (OATB) is a form of extrapulmonary tuberculosis (TB) affecting bones and joints. There is a paucity of data on skeletal TB epidemiology in the annual TB reports and current literature. Many atypical presentations of the disease have also emerged. This necessitates periodic observation of the epidemiological profile of OATB. The aim of this study is to analyze the prevailing epidemiological trends of OATB in Central India. Methods: The 5-year ambispective observational study was conducted at the department of orthopedics of a tertiary care center in Central India. Records of patients diagnosed with OATB from January 2017 to December 2021 were analyzed for demographic factors, site of lesion, comorbidities (pulmonary TB, human immunodeficiency virus, and diabetes), etc., Chi-square test for linear trend was used to determine whether a linear trend exists in the number of diagnosed cases. Results: Two hundred and ten skeletal TB lesions were found in 208 patients included in the study. OATB was highly reported in young adults and females. Spinal lesions were three times more common than extraspinal OATB lesions. The lumbar spine was the most affected region. Hip was the most common extraspinal site. Unusual sites such as sternoclavicular joint and ischial tuberosity were also involved. Conclusion: The burden of OATB is increasing, especially spinal TB. The involvement of atypical sites insists on strong clinical suspicion for early diagnosis. The practice of empirical antitubercular chemotherapy needs to be reviewed considering the risk of drug resistance.
Keywords: Epidemiology, extrapulmonary, extraspinal, osteoarticular, spinal, tuberculosis
Osteoarticular tuberculosis (OATB) is a severe form of extrapulmonary tuberculosis (EPTB) and refers to infection of the bone and/or joints, most commonly by Mycobacterium tuberculosis bacillus. Nontuberculous mycobacterial osteoarticular infections, although infrequent, also occur.[1] OATB usually results from paucibacillary hematological dissemination. Diagnosis requires high clinical suspicion owing to indolent course, nonspecific imaging signs, inadequate tissue for histopathology, and negative microscopy findings in a paucibacillary lesion. Delay in diagnosis and treatment of skeletal TB can lead to significant morbidity and disability causing serious occupational and socioeconomic problems. This is especially true with TB of the spine which can lead to serious neurological consequences if not diagnosed early and managed properly.
According to the Global TB Report 2020, India contributed the highest burden of tuberculosis (TB) cases in the world, almost 26%.[2] According to a report from the Revised National TB Control Program (RNTCP), EPTB accounts for 20% of total TB cases in India.[3] Skeletal TB constitutes 2% of all TB cases according to a study conducted by the TB Research Centre, Chennai.[4] However, the true incidence of OATB is unknown due to the paucity of data on skeletal TB in the national statistics in annual TB reports and current literature.
Vertebral TB is the most common form of skeletal TB followed by hip, knee, foot, elbow, hand, shoulder, bursal sheaths, and others. Compared to yesteryears, the clinical picture of skeletal TB has changed a lot with many atypical forms and presentations of the disease.[5] In recent research, it has been debated that the incidence of bone involvement has dropped over time, bony lesions have become less frequent in the spine, and extraspinal lesions have increased.[6]
OATB and its complications remain one of the major problems to be dealt with in any orthopedic center in our country.[7] There is a need for regular observation of the epidemiological profile of OATB for the successful implementation of the National TB Elimination Program. Through this observational study, we aim to analyze the prevailing epidemiological trends of OATB and identify the diagnostic and therapeutic challenges to improve the patient care provided in a tertiary care center.
MethodsThis single-center 5-year ambispective observational study was conducted at the department of orthopedics of a tertiary care teaching institute in Central India after permission from the Institutional Ethical Committee. The study included all the patients diagnosed with OATB at our center from January 2017 to December 2021. Diagnosis of OATB was based on suggestive clinical findings and hematological tests (erythrocyte sedimentation rate, C-reactive protein, complete blood count, and differential leucocyte count); supportive radiological evidence (X-ray and magnetic resonance imaging); positive histopathological and microbiological evidence; and molecular detection methods such as Xpert MTB/RIF assay of biopsy sample whenever feasible. Case records of OATB patients diagnosed from January 2017 to December 2019 were collected retrospectively from the TB register and electronic TB database maintained at our department and district TB center whereas the case record of patients diagnosed from January 2020 to December 2021 was collected prospectively through patient's case sheets and record cards. Data were recorded on a predesigned patient pro forma, arranged in Microsoft Office Excel format, and analyzed retrospectively on the basis of demographic factors (such as age, sex, residence, and occupation), site of tubercular lesion (joint or bone involved), antitubercular drug resistance status, associated comorbidities (pulmonary TB, human immunodeficiency virus [HIV], and diabetes), complications of OATB, and other parameters. All the patients included in the study received antitubercular drugs as per RNTCP guidelines.
Type of sampling and reason for selection
All the patients diagnosed with OATB at our center from January 2017 to December 2021 were recruited in our study so that fair epidemiological trends could be analyzed.
Statistics
Categorical variables were presented as numbers and percentage. Chi-square test for linear trend was used to determine whether a linear trend exists in the number of cases over a period of time. P < 0.005 was considered statistically significant.
ResultsOut of 208 cases of OATB included in the 5-year study, 22 were diagnosed in the 1st year, 41 in the 2nd year, 49 in the 3rd year, 45 in the 4th year, and 51 in the 5th year, respectively. The majority of cases (38.46%) were in the 21–30-year age group [Table 1]. The mean age of patients at the time of presentation was 33.90 ± 15.4 years, with the youngest patient being 6 years old and the oldest being 78 years old. There were 140 females (67%) and 68 males (33%) in the study group. The number of females diagnosed with OATB was higher than males in each year of the study period [Figure 1]. Most of the cases were from urban areas (64.4%), particularly the urban slums followed by rural areas (35.6%). Regarding occupation, most of the cases were homemakers (36%) followed by students (24.27%), skilled employees (18.3%), laborers (17%), and unemployed (5%). The duration of symptoms ranged from 1 month to 24 months in our study. The mean duration of symptoms was 5.096 months and the maximum duration of symptoms was 24 months in a case. Localized pain was the most common presenting complaint followed by swelling and deformity. Constitutional symptoms such as fever, weight loss, and loss of appetite were quite uncommonly seen.
Figure 1: Sex distribution of OATB patients (2017–2021). OATB: Osteoarticular tuberculosisTwo hundred and ten skeletal TB lesions were present in 208 patients. Two patients had multifocal skeletal TB. One patient had tubercular dactylitis in one foot and an ankle TB lesion on the opposite side. The second patient had a wrist TB lesion and tubercular osteomyelitis of the radius on the same side. Spinal involvement (n = 150) was nearly three times more common than extraspinal (n = 60) OATB lesions in all age groups.
The lumbar spine was the most affected region, followed by the dorsal and dorsal-lumbar spine. The time trend showed a significant increase in the trend of lumbar spine TB [Table 2]. The cervical and lumbosacral regions were the least affected. Twenty-one percent of all spinal TB cases had neurodeficit in the form of paraparesis and paraplegia with male patients being predominantly affected. Kyphosis was observed in 14 patients of spinal TB, more commonly with dorsolumbar involvement. Nine cases had pus discharging sinus, with ankle and foot being the most common locations.
Among extraspinal tubercular lesions, hip (n = 24) was the most frequently affected site followed by the knee (n = 16) and wrist (n = 4) [Table 3]. Tubercular dactylitis of the foot (n = 2) and hand (n = 1) was more prevalent in females. Tubercular osteomyelitis of long bones was noted in only two cases. Unusual sites such as sternoclavicular joint (n = 1) and ischial tuberosity (n = 1) were also involved.
There were 174 “new” cases whereas 34 patients had been “previously treated” for OATB. HIV antigen test was reported as “reactive” in 7 cases (3.36%) while 12 cases (5.8%) were found diabetic. Concurrent pulmonary TB was found in only 12 cases in our study. Rifampicin resistance was detected through GeneXpert MTB/RIF in five cases while multidrug resistance (MDR) OATB was noted in three cases.
DiscussionOATB comprises 1%–4.3% of total TB cases and 10%–15% of all EPTB cases.[8] Yoon et al. reported bone and joint TB as the third most common type of EPTB.[9] In Western countries, there has been a significant reduction in bone and joint TB with less frequent localization to the spine.[10] However, in India, the incidence rate of skeletal TB has not shown any decline.[4],[11] EPTB cases need more investigations and invasive procedures for definitive diagnosis and hence are reported more in tertiary centers.[11] OATB remains a major problem for both, the patients and the treating orthopedic doctors in India, mainly because of the difficult diagnosis and nonuniform treatment protocols followed. Several observations can be made in the context of the disease in the orthopedic department of a teaching tertiary medical institute in Central India where the presentation of skeletal TB is high. In the present study, there was a gradual increase in the number of OATB cases diagnosed each year. The count was marginally less in the year 2020 which could be attributed to the coronavirus (COVID-19) pandemic since the health facilities offering TB diagnostic and treatment services were reallocated to the COVID-19 response.
Previous studies reported that OATB affected the older population.[12] In the present study, nearly half of the participants were in the second and third decades of life [Figure 2]. This was coherent with the findings of recently published studies on the epidemiology of skeletal TB.[4],[8],[13] This makes the situation worrisome because TB of bones and joints, especially in the young and working individuals, contributes to deformities and consequent functional disabilities that impose several socioeconomic challenges, affecting their quality of life. The rate of OATB was higher in females than males throughout the study period. This could be attributed to undernutrition and poor living conditions among females in representing population. Female predominance was also reported in studies by Chopra et al. and Prakasha et al., but the percentage of female cases was highest in the present study (67.30%).[4],[11] This contrasts with the findings of Tuli et al. and Gogia and Gupta. where the percentage of male patients was high.[7],[13] The majority of cases in our study were residents of urban slums followed by rural areas. These facts articulate the need for special efforts to address TB in vulnerable and disadvantaged groups. TB care in urban areas, especially in migrant urban slum dwellers, has remained a challenge, owing to failure in administration, financial management, and monitoring and tracking the patients.
Figure 2: Age distribution of OATB patients by gender. OATB: Osteoarticular tuberculosisOut of 208 patients included in the study, 83.60% were new cases without any prior history of antitubercular treatment and the remaining 16.34% had previously received antitubercular treatment. Spinal TB is uncommon in the Western world.[4] However, an increasing trend in the incidence of spinal TB is reported in Indian studies. The rate of spinal TB (72.11%) was higher than extraspinal (27.88%) OATB in our study [Table 1].
Among the extraspinal sites of skeletal TB in the present study, joints were more frequently affected than long bones, with hip being the most commonly affected joint followed by the knee, wrist, ankle, elbow, and sacroiliac joint. The knee joint was the most common extraspinal site of skeletal TB in studies by Tuli et al.,[7] Huang et al.,[14] and Chopra et al.[4] Ankle and foot TB is a very uncommonly reported type (<5%) of OATB because of wide range of conditions such as pyogenic osteomyelitis, inflammatory arthritis, and Charcot arthropathy mimicking it.[15] In contrast, Barik et al.[16] observed the ankle joint as the most common extraspinal site TB. Dhillon et al. reported nine cases of sternoclavicular joint TB with males predominantly affected.[17] In the present study, only one case of sternoclavicular joint TB was diagnosed, in a 45-year-old female. TB of short tubular bones of the foot and hand, also known as tubercular dactylitis, is very rare and was diagnosed in only three patients in our study.
In Tuli et al.'s series, the dorsal spine was the most commonly involved site of spinal TB.[7] However, the lumbar region (40%) was the most commonly affected spinal segment in the present study. Similar rates of lumbar involvement were reported in studies by Bodapati et al. (54%) and Charde et al. (42.5%).[18],[19] Lower lumbar spine and lumbosacral spine were the most commonly affected spinal TB sites in another study conducted at PGIMER, Chandigarh, India.[20] These findings contradict the fact published in previous literature and books that dorsal spine and dorsolumbar spine are the most common sites involved in spinal TB.
Immunity of the host is a major risk factor for EPTB.[21] Approximately 5% of the incident TB cases have comorbidity with HIV, though this proportion varies depending on the HIV prevalence of the population.[22] The role of HIV and diabetes as predisposing risk factors for OATB was not so obvious in our study. Only 3.26% of cases were reactive to HIV testing and 5.8% were diabetic. This suggests that OATB can occur in immunocompetent individuals, without any constitutional symptoms or pulmonary TB lesion.
Rifampicin resistance was noted in five cases and MDR-TB in three cases. Despite the availability of molecular detection methods of diagnosis such as GeneXpert MTB/RIF, many cases were diagnosed on a clinicoradiological basis as fewer biopsy samples were collected and processed. Preconception of poor culture yields due to paucibacillary tubercular lesions of bone could be the reason behind inclination toward clinicoradiological diagnosis. Although this practice is noninvasive and economical but carries a significant risk of missing TB mimics and developing drug resistance. Recent researches in India suggest increasing drug resistance in skeletal TB. Maurya et al. reported a high prevalence of MDR-TB (38.8%) both in new cases (29.1%) and previously treated cases (43.3%) of OATB.[23] Agashe et al. reported increased resistance even to second-line antitubercular drugs.[24] Hence, it is prudent to recognize the challenge of drug resistance in OATB, review the treatment guidelines, and improve the mycobacterial culture and drug sensitivity facilities at all hospitals.
ConclusionBone and joint TB burden in the Indian population is showing an increasing trend as evident from the year-wise increase in the number of diagnosed cases, especially spinal TB. The involvement of atypical sites such as ischial tuberosity and sternoclavicular joint is also becoming ubiquitous and insists on strong clinical suspicion for early diagnosis. All efforts are to be undertaken for microbiological/molecular confirmation of the diagnosis. The practice of empirical antitubercular chemotherapy needs to be reviewed, considering the risk of emergence of drug resistance patterns in the bone and joint TB lesions. A universal treatment protocol along with improved infrastructure is crucial.
Limitation of the study
Although the study findings point toward increasing burden and changed pattern of OATB in the community, the results of this single-center study cannot be universalized because of low sample size. True prevalence of antitubercular drug resistance could not be determined as tubercular lesion was not biopsied in every case.
Ethical clearance
This study was approved by the Institutional Ethical Committee, letter number – 473/MC/IEC/2020, date – January 4, 2020, and did not have any ethical issues.
Patient consent statement
Informed consent was obtained from all patients prior to recruitment.
Acknowledgment
The authors wish to acknowledge the contributions of Dr. Manoj Verma and his team, District TB Centre, Bhopal, and also the RNTCP staff and Community DOTS Providers of Hamidia Hospital, Gandhi Medical College, Bhopal, for help with data corroboration.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
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