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Clinical features of Tibetan adolescent tuberculosis at high altitudes: a retrospective study

BMC Pulmonary Medicine volume 24, Article number: 611 (2024) Cite this article

Abstract

Background

Adolescent pulmonary tuberculosis (TB) is considered inadequately recognized and underreported at high altitudes. This study aimed to investigate the clinical features of adolescent pulmonary TB patients at high altitudes in China.

Method

A retrospective analysis was performed at Linzhi People’s Hospital. Patients recruited were newly diagnosed with pulmonary TB. Detailed information, including demographics, medical history, presenting symptoms, laboratory results and pulmonary images, was collected. Sputum samples were collected to detect Mycobacterium tuberculosis via the GeneXpert MTB/RIF assay.

Result

A total of 63 adolescents and 192 adults were recruited. Compared with those in the adult group, typical TB-related manifestations were significantly less common in the adolescent group (all P < 0.05). The adolescent group had significantly more subclinical TB (23.8% vs. 8.3%, P = 0.001) and a higher previous tuberculosis exposure rate (38.8% vs. 8.3%, P < 0.001) than did the adult group. The erythrocyte sedimentation rate was significantly higher in the adolescent group than in the adult group (P = 0.026). Compared with adult patients, adolescent patients presented a lower rate of pleural thickening (P < 0.01). Compared with active adolescent patients, there were more female than male in the adolescent subclinical TB group (12/15 vs 27/48) and the positive rate of the sputum GeneXpert test was higher in subclinical TB group (6/15 vs 8/48).

Conclusion

Adolescent patients with pulmonary TB at high altitudes were prone to subclinical TB and have a higher previous TB exposure rate. Sputum GeneXpert test and ESR were important for the diagnosis of subclinical pulmonary TB.

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Introduction

Adolescence has been characterized by a substantial increase in the incidence of TB since the early twentieth century, especially in some low- or middle-income countries or regions [1]. Yearly, 850,000 adolescents (aged 10–19 years) have become infected with tuberculosis (TB) globally [2, 3] and in 2020, 226,000 children and young aolescents (aged 10–14 years) died due to TB [4]. A 6 years of experience at a hospital in Argentina found that 48% of individuals diagnosed with TB disease were adolescents [5]. Given substantially increased incidence of TB in adolescence [3], this population requires more attention. In TB surveillance systems, individuals aged < 15 years are grouped with children, and those aged ≥ 15 years are grouped with adults [3, 6]. Adolescents have not been considered a distinct population in TB policy or treatment services [3]. They have received little attention in TB research, and their vulnerability to the disease has been largely forgotten [1]. Few studies have explored the characteristics of tuberculosis in this age group (10–19 years old) [1.5]. Thus, adolescent TB is considered inadequately recognized and underreported [2].

Mycobacterium tuberculosis (MTB) is a facultative aerobic bacillus and low oxygen pressures inhibit the ability of MTB to survive and multiply. Its growth slows when MTB is exposed to hypoxia [7]. Previous studies showed that 10–20% of adolescents with TB disease have pleural TB, 10–20% have extrathoracic TB, and approximately 25% have lung cavitation [3, 8,9,10,11]. While few studies have investigated adolescent TB in high-altitude hypoxia so far. To identify the clinical features of adolescent TB in plateaus, we performed a comprehensive and retrospective analysis in this study.

Materials and methods

Study subjects

We conducted an observational and retrospective study in the department of infectious diseases of ** People’s Hospital, where the average elevation is 3000 m above sea level. Patients who were treated in the hospital between July 2019 to July 2021 were included. The presence of symptoms was evaluated by TB nurse specialists and physicians during hospitalization. Detailed information, including demographics, medical history, presenting symptoms, laboratory results, and radiological results, was collected by reviewing medical records. All study staff were trained on the study protocol.

The inclusion criteria for this study were as follows: (1) patients aged ≥ 10 years, (2) living in the Tibet Autonomous Region for more than 10 years, and (3) newly diagnosis of pulmonary TB during the study period. Exclusion criteria were as follows: (1) patients without lung computed tomography (CT) scans during the hospitalization, (2) patients whose medical records were found to be incomplete or were not accessible for analysis, (3) patients receiving immunosuppressive therapy, (4) patients complicated with HIV, diabetes mellitus and cancer, and (5) patients complicated with other infectious diseases.

Pulmonary TB was defined according to the National Health and Family Planning Commission of PRC diagnostic criteria launched in 2017 [12]. In brief, it was disease due to MTB that caused radiologic or microbiological abnormalities consistent with active TB, with or without TB-related clinical symptoms. Active pulmonary TB was referred to symptomatic pulmonary TB. Subclinical pulmonary TB was referred to disease caused by MTB without any symptoms but with detectable radiologic or microbiological abnormalities that could be used to diagnose active pulmonary TB [13,14,15]. The symptoms included but not limited to clinical TB-related symptoms such as cough, fever, night sweats, weight loss, or chest pain, regardless of symptoms duration. Extrapulmonary TB (EPTB) refers to TB involving organs other than the lungs (e.g., the lymph nodes, abdomen, joints and bone, genitourinary tract, skin, or meninges). Rifampicin-resistant TB was defined as resistance to at least rifampicin. Patients aged 10–19 years were classified into the adolescent group; those aged ≥ 19 years composed the adult group. The criteria of exposure to TB were individuals who had recent contact with someone with active tuberculosis and the cumulative duration of exposure was greater than eight hours in a confined space [4].

Sputum was collected for nucleic acid tests. When spontaneously expectorated sputum could not be obtained, induced sputum was collected for testing with the patient’s consent. Sputum induction was performed by TB nurse specialists in a isolation ward during hospitalization as previously described [16].

The study was designed in accordance with the Helsinki Declaration. The protocol and instruments were approved by the Ethics Committee of ** People’s Hospital (LZRY.NO.20210315 [001]). As this was a retrospective study and the data were anonymous, the requirement for informed consent was therefore waived.

Statistical analysis

Statistical evaluation was performed via SPSS software (IBM SPSS Statistics 21; SPSS Inc., Chicago, IL, USA). All the data were presented as the means ± standard deviations (SDs), as applicable. A t test was used to compare means between two independent groups, and the χ2 test was used for enumeration data comparison. Probability values (P) < 0.05 were considered statistically significant.

Results

Baseline information

In total, 255 patients (63 adolescents and 192 adults) were recruited. The mean age was 14.4 ± 2.4 years in the adolescent group and 39.9 ± 16.9 years in the adult group. Males accounted for 47.6% and 56.8% of the patients in the two groups, respectively (P > 0.05). The mean body mass index (BMI) was 18.94 ± 2.83 kg/m2 in the adolescent group and 21.09 ± 3.26 kg/m2 in the adult group (P < 0.01). The adolescent group were students from primary and secondary schools. The main occupations of the patients in the adult group were farmers (124, 64.6%) or college students (30, 15.6%). There were 11 (17.5%) EPTB patients in the adolescent group and 20 (10.4%) in the adult group, respectively (P > 0.05).

Clinical manifestation of adolescent patients with pulmonary TB

Patient symptoms were recorded. Compared with those in the adult group, typical TB-related manifestations such as sputum, weakness, chest pain and back pain were significantly less common in the adolescent group (all P < 0.05) (Table 1). All subclinical pulmonary TB patients were those who manifested chest X-ray abnormalities during active surveillance programme or health check-up. The chest X-ray abnormalities make them go to hospital for tuberculosis screening. Compared with patients in the adult group, there were significantly more patients with subclinical pulmonary TB in the adolescent group (23.8% vs. 8.3%, P = 0.001, χ2 = 10.639). Compared with the adult patients, the adolescent patients had a higher TB exposure rate (38.1% vs. 8.3%, χ2 = 31.769) (P < 0.001) (Table 1).

Table 1 Clinical manifestation of adolescent patients with pulmonary TB
Full size table

Blood laboratory examination of adolescent patients with pulmonary TB

Clinical laboratory data, including the white blood cell (WBC) count, percentage of neutrophils (N%), C-reactive protein (CRP), procalcitonin (PCT), and erythrocyte sedimentation rate (ESR), were collected. The ESR was significantly greater in the adolescent group than in the adult group (P = 0.026) (Table 2). There was no significant difference between the groups in CRP, PCT, N% or WBC count. In addition, Routine blood sugar test was done during hospitalization.There were no diabetes in the adolescent group.

Table 2 Blood laboratory examination of adolescent patients with pulmonary TB
Full size table

Lung CT of adolescent patients with pulmonary TB

Pulmonary computed tomography (CT) images were included in this study. Compared with adult patients, adolescent patients presented a lower rate of pleural thickening (P < 0.01) (Table 3). There was no significant difference in the location of the lesions or the pulmonary cavity between the two groups.

Table 3 Lung CT images of adolescent patients with pulmonary TB
Full size table

Results of the GeneXpert MTB/RIF assay of adolescent patients with pulmonary TB

Samples from 29 adolescent and 95 adult patients were tested via GeneXpert MTB/RIF. No significant difference was found in the results of GeneXpert MTB/RIF between the two groups (P > 0.05) (Table 4). In terms of rifampicin-resistant TB, there was no significant difference between the two groups (3.2% vs 7.3%) (P > 0.05).

Table 4 Results of the GeneXpert MTB/RIF assay of adolescent patients with pulmonary TB
Full size table

Clinical features of adolescent patients with subclinical pulmonary TB

There were 15 subclinical pulmonary TB patients and 48 active patients in the adolescent group. Compared with active adolescent patients, more subclinical patients were female (12/15 vs 27/48) (Table 5). Induced sputum was obtained from 9 of the 15 adolescent subclinical pulmonary TB patients and 20 of the 48 active patients via the GeneXpert MTB/RIF assay. The positive rate of the sputum GeneXpert test was higher in subclinical TB patients than in active TB patients (6/15 vs 8/48) (Table 5).

Table 5 Clinical features of adolescent patients with subclinical pulmonary TB
Full size table

Discussion

Human MTB infection is a continuous process involving metabolic bacterial activity and antagonistic immunological responses [14]. The natural progression of TB includes initial exposure, latent infection, incipient TB, subclinical TB and active TB [14]. In this study we found that adolescent pulmonary TB at high altitudes were prone to manifest as subclinical TB. According to Carril SS, tuberculosis in adolescents may present characteristics similar to those of adults, with a higher frequency of severe pulmonary disease leading to pulmonary sequelae [5]. While our results revealed significantly more subclinical pulmonary TB in Tibetan adolescents than in adults. Typical TB-related manifestations, such as sputum, weakness, chest pain and back pain, were less common in adolescents. Studies have shown that culture-positive TB can last up to 18 months before passive case presentation [17, 18], whereas symptoms are often reported only 2–3 months before diagnosis [19]. In a recent TB prevalence survey in Asia [20], symptoms were not reported by up to 80% of individuals with microbiologically confirmed infectious TB. As access to start the protocols for identifying active TB relied mostly on positive symptom screening (e.g., cough, fever, night sweats, weight loss), subclinical TB was usually missed [8]. Subclinical TB patients who persistently or intermittently carry lower bacillary burdens in the lungs may be sources of transmission in the community [18]. Previous study also showed that smear-positive subclinical tuberculosis contributes to MTB transmission [21]. Thus, as is shown in a modeling study, subclinical TB plays an important role in the transmission of TB and needs to be diagnosed and treated [22]. Diagnostic pathways only based on TB-related symptoms will delay diagnosis of subclinical adolescent TB at high altitudes. Paying attention to adolescent individuals with subclinical TB who have not yet sought health care could provide opportunities for therapeutic interventions to prevent progression to active TB disease and transmission of TB bacilli [14, 23, 24] in schools. In this study, there were no diabetes or receiving immunosuppressive therapy patients in the adolescent group. We also excluded patients with combination of HIV and cancer. Chinese adolescents spending most of their time at home and school, made it easier to perform active surveillance or health check-up. This might be probable mechanism of higher cases of subclinical TB in adolescents in this study.

There were more female adolescent subclinical TB patients in this study. This finding was consistent with previous research, which revealed that TB without cough was more common among women [25]. The maturation of the cough reflex is the result of structural and functional changes caused by endogenous and exogenous factors [26]. According to Plevkova et al., sex hormones are the main endogenous factors that impact the maturation of the cough reflex [26]. The cough threshold was similar between the sexes before puberty. It becomes lower at mid-puberty and significantly greater at late puberty in girls [27]. Our finding that there were more females among adolescent subclinical TB patients might be partly related to the changes in sex hormones in adolescence.

In this study, adolescent patients had a higher TB exposure rate than did adult controls. Chinese adolescents spend most of their time at home and school, making it easier to identify TB contacts. Given that a large proportion of transmission may occur outside household exposure [28], we consider that the high TB exposure of adolescents was related partly to accommodations at schools [29,30,31].

GeneXpert MTB/RIF assay was also performed for TB diagnosis in this study. Although there were more subclinical patients in the adolescent group than in the control group, the positive rate of the sputum GeneXpert MTB/RIF assay in the adolescent group was similar to that in the adult group. Our study was consistent with a recent meta-analysis, which revealed that approximately a quarter of pulmonary TB patients who did not report any cough had positive sputum smears [25]. Considering the bacillary burdens, molecular detection of MTB was important for adolescents with subclinical pulmonary TB. Our study also showed a higher number of subclinical cases with GeneXpert positive results as compared to active adolescent TB cases. We think that the different dependence on microbiological abnormalities in diagnosing pulmonary TB might lead to the dicrepancy.

ESR is a sensitive marker of the inflammatory response and is part of a well-established routine investigation for TB. A previous research showed that compared to healthy controls, ESR values were significantly increased in tuberculosis patients. To measure ESR is a simple and cost-effective method to predict TB [32]. A systematic review and meta-analysis also showed that elevated ESR in newly diagnosed TB patients helps physicians in early diagnosis [33]. In this study, the ESR was significantly higher in the adolescent group. Therefore, the ESR cannot be neglected when screening for adolescent TB.

In this study, adolescent patients presented a lower rate of pleural thickening than did adult patients. This finding was inconsistent with those of previous studies, which showed that cavitation and pleural effusion were more common in adolescent TB patients [3, 14]. The fact that those studies included recurrent TB patients and our study included newly diagnosed asymptomatic patients might be the reason for the difference.

There are some limitations in our study. First, the limited cases limited the representativeness in this study. According to the latest China population census report, there were 3 137 901 Tibetan resident in the Tibet Autonomous Region. The mean annual incidence of TB is 101.98 per 100 000 population and we estimated that the total number of TB patients in the Tibet Autonomous Region was about 3200. Thus we think that the 255 TB patients included in the study, which accounting for about 7.9% of the total number of TB patients, might have a certain representativeness. Second, as patients have seldom been performed DST in this study, we did not include these data in our analyses. Due to the limitation of testing technology, all patients did not conducted IGRAs. Low oxygen pressures inhibit the ability of MTB to survive and multiply in high-altitude. Due to the limitation of MTB culture technology, all patients did not conducted sputum culture. Third, The nearly 1:3 ratio between the two groups introduces a potential source of bias, particularly selection bias, which may affect the comparability of the results. The larger group could disproportionately influence the findings, potentially leading to an over- or underestimation of the effect size. Although statistical adjustments were not applied to balance the groups (such as propensity score matching or weighting methods), we performed multivariable analyses to control for key confounding factors. However, the risk of residual confounding remains, and the unequal group sizes may limit the generalizability of our findings. Future studies with more balanced group sizes or the application of advanced statistical methods would be beneficial to validate and strengthen the conclusions.

Our study included only hospitalized adolescent TB patients. Future research is needed to investigate the clinical features of adolescent TB patients in the community and develop alternative inexpensive, sputum-free tests for diagnosis of subclinical TB.

Conclusions

Adolescent patients with pulmonary TB at high altitudes were prone to subclinical TB and have a higher previous TB exposure rate. Paying attention to adolescent individuals with subclinical TB who have not yet sought health care could provide opportunities for early diagnosis at high altitudes. Sputum GeneXpert test and ESR were important for the diagnosis of subclinical pulmonary TB.

Data availability

Owing to reasons of sensitivity, the data that support the findings of this study are not openly available. Upon reasonable request, these data are available from the corresponding author.

Abbreviations

TB:

Tuberculosis

MTB:

Mycobacterium tuberculosis

EPTB:

Extrapulmonary TB

WBC:

White blood cell

N%:

Percentage of neutrophils

CRP:

C-reactive protein

PCT:

Procalcitonin

ESR:

Erythrocyte sedimentation rate

CT:

Computed tomography

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Acknowledgements

We would like to thank all the patients who participated in this study. We also thank Sheng Wang, Yuting Lin, all the doctors and nurses involved in the study.

Funding

This study was supported by a project funded by the Shenzhen Third People’s Hospital (No. G2022052 and No. G2022009) and the Shenzhen High-level Hospital Construction Fund.

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Authors and Affiliations

  1. Department of Respiratory Medicine, National Clinical Research Center for Infectious Disease, Shenzhen Third People’s Hospital, Shenzhen, Guangdong Province, 518112, China

    Min Shen, Wen Luo, Peiyan Zhang, Xuerong Chen & Peifen Chen

  2. Department of Infectious Diseases, Linzhi People’s Hospital, Linzhi, Tibet Autonomous Region, China

    Banjiu Luobu, Weiping Guo & Peifen Chen

  3. Hospital-Acquired Infection Control Department, Pu’er People’s Hospital, Pu’er, Yunnan, China

    Yirong Chen

  4. Beijing Normal University - Hong Kong Baptist University United International College, Zhuhai, Guangdong Province, 519000, China

    Ruisi Qiu

  5. Department of Gastroentestinal Surgery, the Third Affiliated Hospital of Sun Yat-Sen University, Guangzhou, China

    Weiping Guo

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Contributions

B. L., R.Q., W. G. and P. C. collected the data. M. S., W. L., P. Z., and X. C. wrote the main manuscript text. Y. C. completed the statistical work. All the authors reviewed the manuscript.

Corresponding authors

Correspondence to Weiping Guo or Peifen Chen.

Ethics declarations

Ethics approval and consent to participate

The study was designed in accordance with the Helsinki Declaration. The protocol and instruments were approved by the Ethics Committee of Linzhi People’s Hospital (LZRY.NO.20210315 [001]). As this was a retrospective study and the data were anonymous, the requirement for informed consent was therefore waived.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Shen, M., Luo, W., Luobu, B. et al. Clinical features of Tibetan adolescent tuberculosis at high altitudes: a retrospective study. BMC Pulm Med 24, 611 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03427-6

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BMC Pulmonary Medicine

ISSN: 1471-2466

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