Comorbidity and drug resistance of smear-positive pulmonary tuberculosis patients in the Yi Autonomous Prefecture of China: a cross-sectional study

doi:10.21203/rs.3.rs-3007578/v1

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Research Article

Comorbidity and drug resistance of smear-positive pulmonary tuberculosis patients in the Yi Autonomous Prefecture of China: a cross-sectional study

https://doi.org/10.21203/rs.3.rs-3007578/v1

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published 06 Sep, 2023

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Background

Tuberculosis (TB) has a high morbidity and mortality rate, and its prevention and treatment focus is on impoverished areas. The Liangshan Yi Autonomous Prefecture is a typical impoverished area in western China with insufficient medical resources and high HIV positivity. However, there have been few reports of TB and drug resistance in this area.

Methods

We collected the demographic and clinical data of inpatients with sputum smear positive TB between 2015 and 2021 in an infectious disease hospital in the Liangshan Yi Autonomous Prefecture. Descriptive analyses were used for the epidemiological data. The chi-square test was used to compare categorical variables between the drug-resistant and drug-susceptible groups, and binary logistic regression was used to analyse meaningful variables.

Results

We included 2263 patients, 79.9% of whom were Yi patients. The proportions of HIV (14.4%) and smoking (37.3%) were higher than previously reported. The incidence of extrapulmonary TB (28.5%) was high, and the infection site was different from that reported previously. When drug resistance gene detection was introduced, the proportion of drug-resistant patients became 10.9%. Patients aged 15–44 years (OR 1.817; 95% CI 1.162–2.840; P < 0.01) and 45–59 years (OR 2.175; 95% CI 1.335–3.543; P < 0.01) had significantly higher incidences of drug resistance than children and the elderly. Patients with a cough of ≥ 2 weeks had a significantly higher chance of drug resistance than those with < 2 weeks or no cough symptoms (OR 2.069; 95% CI 1.234–3.469; P < 0.01). Alcoholism (OR 1.741; 95% CI 1.107–2.736; P < 0.05) and high bacterial counts on sputum acid-fast smears (OR 1.846; 95% CI 1.115–3.058; P < 0.05) were significant in the univariate analysis.

Conclusions

Patients with Sputum smear positive TB who were hospitalised in this hospital had higher proportions of Yi nationality, smoking, HIV, and extrapulmonary TB. Ages 15–59 years and cough duration ≥ 2 weeks were risk factors for TB drug resistance. Meanwhile, alcohol abuse and high bacterial counts in sputum acid-fast smears may also be associated with TB drug resistance. These characteristics are related to poverty and insufficient health resources.

Sputum smear positive

Pulmonary tuberculosis

Impoverished area

Comorbidity

Drug-resistant

Tuberculosis (TB) is a major communicable disease worldwide, with high morbidity and mortality rates^{1, 2}. According to a global report, 5.8 million patients were newly diagnosed in 2020³. Before the COVID-19 pandemic, TB was the leading cause of death from an infectious disease^{3, 4}. TB is not only a health problem driven by poverty; it can also exacerbate poverty. Moreover, TB is the key point affecting the Sustainable Development Goals of poverty eradication^{5, 6}. Although high-income countries also have new TB cases annually, the World Health Organization (WHO)-listed high-burden countries are responsible for 80% of TB cases^{3, 7}. Most of these countries have low or middle income². Therefore, it is of great significance to control TB in poor areas. The WHO and the Chinese Center for Disease Control and Prevention have proposed long-term goals for TB prevention by 2030^{3, 5}. However, as the top three high-burden countries in terms of TB, achieving the goal of ending the TB epidemic is challenging⁸, especially in some impoverished areas in China where there are gatherings, underdeveloped healthcare resources, and high HIV prevalence.

The Liangshan Yi Autonomous Prefecture is located in southwest Sichuan Province and is the largest Yi community. The Yi people account for approximately 50% of the local permanent residents^{9, 10}. It is the largest gathering place of the Yi minority in China. The Yi nationality is the sixth largest ethnic group in China and an ancient ethnic group⁹. The Yi people are accustomed to living in high-altitude areas and have their own language and eating habits¹¹. Liangshan is one of the poorest areas in China, with poor local public health conditions¹². By 2021, 11 of 17 counties were in severe poverty¹³. Therefore, it is among the regions with the highest HIV prevalence in China¹⁴. HIV infection affects all aspects of TB, including the development of active, extrapulmonary TB, increased mortality, and TB drug resistance^15–18. A survival analysis of AIDS in this region showed that patients with TB had an increased mortality risk in recent years¹⁹. Despite being an area with a high incidence of infectious diseases, TB has rarely been reported.

We analysed the data of hospitalised patients to understand the epidemiological characteristics of sputum smear positive TB in this region. This type of TB is challenging to prevent and control as patients with sputum smear positive TB can expel Mycobacterium tuberculosis (M. tuberculosis) into the air by coughing, thus infecting others and spreading it further²⁰. Especially in areas with high clusters and high HIV prevalence, the infection and transmission of TB are prevalent³. In addition, drug resistance is a key point that hinders the prevention and treatment of TB³. The most common mono-drug resistance reported previously is isoniazid resistance²¹. However, the annually increasing occurrence of multidrug-resistant TB (MDR-TB), which is resistant to both rifampicin and isoniazid, can cause great harm²². Some factors associated with resistance include poor patient compliance, alcohol abuse, smoking, co-infection, diabetes, HIV/AIDS, and acid-fast bacilli (AFB) smear positivity^23–25. Therefore, this study summarised the occurrence of drug resistance and used logistic regression to analyse its risk factors in this group of patients.

Study area and population

We collected demographic and clinical data of patients with sputum smear positive TB who were hospitalised in the largest infectious disease hospital in the Liangshan Yi Autonomous Prefecture. The hospital is the only infectious disease hospital that provides tertiary care for patients with TB in the Liangshan Yi Autonomous Prefecture and is responsible for managing patients with TB in Liangshan city and surrounding regions. These clinical data came from the hospital 's his system, and included sex, age, ethnicity, disease course, living habits, comorbidities, smear results, and therapy. Living habits of alcohol consumption are defined here as chronic alcohol consumption and an average daily consumption of ≥ 15 g ²⁶. The resident population in this area is Yi and Han, with a ratio of approximately 1:1.

Study design

Criteria for admission

Data were collected from 1 January 2015 to 5 December 2021. The diagnosis met the following two criteria: AFB smear-positive sputum and lung computed tomography supported the presence of active pulmonary TB²⁷. At least two AFB sputum smear morning samples were collected from patients for testing. The Ziehl-Neelsen staining method and the grading standards promulgated by the National Health Commission of China were used for grading: Scanty, 1–8 on smear (300 fields examined); +, 3–9 in 100 fields (300 fields examined); 2+, 1–9 in 10 fields (100 fields examined); 3+, 1–9 per field of vision (50 fields examined); and 4+, ≥ 10 per field of vision (50 fields examined). For the analysis, we used the age groups 0–14, 15–44, 45–59, and > 60 years. Patients were divided into three groups according to whether they had a cough that lasted > 2 weeks. Missing values represent unrecorded values. We then screened patients after the hospital conducted drug resistance-mutated genes^{2, 28} on 6 May 2020. The drug resistance test was performed only for isoniazid and rifampicin at this hospital. Before genetic testing, drug resistance was determined through clinical treatment. After further excluding patients with unknown data, they were assigned to the drug-resistant and drug-susceptible groups according to the drug-susceptibility test results. The inclusion and exclusion data are illustrated in Fig. 1.

Statistical methods

Descriptive analyses were performed on the collected clinical data of all hospitalised patients, consistent with sputum smear positive TB. Age was not considered a continuous variable, but the patients were divided into different age groups. The chi-square test was used to compare categorical variables between the drug-resistant and drug-susceptible groups. Statistical significance was set at P < 0.05, but the binary logistic regression model included variables with P < 0.1. To identify significant variables affecting drug resistance, we used both univariate and multivariate binary logistic regression (backward stepwise logistic regression) to compare the included variables. A dummy variable for age-grouped was an ‘indicator-first’ of contrast selection, while cough selection was ‘deviation-first’. The TB smear was classified, and only 4 + positive patients were counted to determine whether the quantity of multiple bacteria affected drug resistance. Statistical analyses were performed using SPSS version 23.0 and GraphPad Prism 7.04 (GraphPad Software Inc., CA, USA).

Ethics statement

The study collected data from the patient’s hospital records and anonymised them. The acquisition of all clinical data and laboratory results, as well as the waiver of patient informed consent has been approved by the Ethics Review Committee of Sichuan Provincial Academy of Medical Sciences and Sichuan Provincial People's Hospital (Protocol 20220-254).

Characteristics of patients with sputum smear positive TB

During the data collection period, 2263 patients with sputum smear positive TB were hospitalised (Table 1). Among the patients, 63.2% were men, and most were Yi (79.9%). The patients’ ages ranged from 1 month to 94 years, 59.3% of whom were in the 15–44 age group, followed by 45–59-year-olds (19.1%), the elderly (17.9%), and children aged 0–14 years (4.1%). A history of smoking was observed among 37.3% of patients, while 26.7% had a history of alcoholism. Patients with type 2 diabetes accounted for 8.2% and HIV-positive patients accounted for 14.4%. Patients with extrapulmonary TB accounted for 28.5%, of whom 26.2% had multiple sites. The top five most common extrapulmonary TB cases were abdominal, genitourinary, pericardial, pleural, and lymphatic (Fig. 2A). Regarding treatment, 84.3% of the patients were administered first-line anti-TB therapy, whereas 7.1% were administered second-line anti-TB therapy. Another 8.7% of the patients had poor adherence, refusal, or discontinuation of the medication.

Table 1

Characteristics of 2263 tuberculosis patients in a infectious disease hospital of Liangshan Yi Autonomous Prefecture
Characteristic	Value (n = 2263)
Gender-n. (%)
Male	1430 (63.2)
Female	833 (36.8)
Age-Years
<14-n. (%)	92 (4.1)
15-44-n. (%)	1342 (59.3)
45-59-n. (%)	433 (19.1)
≥ 60-n. (%)	405 (17.9)
Ethnicity-n. (%)
Han	455 (20.1)
Yi	1808 (79.9)
Smoke-n. (%)
Yes	844 (37.3)
No	1402 (62.0)
Missing	17 (0.8)
Alcoholism -n. (%)
Yes	604 (26.7)
No	1644 (72.6)
Missing	15 (0.7)
Comobidites-n. (%)
COPD	142 (6.3)
Type 2 diabetes	185 (8.2)
HIV positive	326 (14.4)
Extrapulmonary tuberculosis	644 (28.5)
Treatment
First-line anti-TB drugs	1903 (84.3)
Second-line anti-TB drugs	176 (7.8)
Non-compliance with medical advice	184 (8.1)
Drug resistance
Yes	98 (4.3)
Drug susceptible	1438 (63.5)
Not clear	727 (32.1)

Characteristics of drug-resistant and drug-susceptible groups

Among the 2263 patients, 1405 were screened from May 2020, when genetic testing for isoniazid and rifampicin resistance was performed in this hospital. After excluding 557 (39.6%) undocumented patients who did not undergo this test, 91 of the remaining 848 patients showed drug resistance. The incidence rate of drug resistance was 10.7%. Among these drug-resistant patients, 73 (80.2%) were resistant to rifampicin, 4 (4.4%) were resistant to isoniazid, and 14 (15.4%) were resistant to both (MDR-TB) (Fig. 2B). Finally, 91 and 747 patients were included in the drug-resistant and drug-susceptible groups, respectively. There were no significant differences in sex, ethnicity, smoking, HIV positivity, extrapulmonary TB, or sputum smear between the two groups (Table 2). However, the P-value for HIV-positive and sputum smear results was < 0.1. There were statistically significant differences in age stratification (P < 0.001), alcohol consumption (P < 0.05), and cough status (P < 0.001) (Table 2).

Table 2

Demograhic and clinical characteristics after the hospital carried out drug resistance gene detection in 2020
Variable	Patients, No.(%)
	Drug-resistant (n = 91)	Drug-susceptible (n = 757)	P-value
Age-years			0.000***
≤ 14	1 (1.1)	38 (5.0)
15–44	63 (69.2)	449 (59.2)
45–59	25 (27.5)	136 (18.0)
≥ 60	2 (2.2)	135 (17.8)
Male	62 (68.1)	464 (61.3)	0.204
Yi Nationality	65 (71.4)	554 (73.2)	0.722
Smoke	38 (41.8)	283 (37.4)	0.417
Alcoholism	35 (38.5)	200 (26.4)	0.015*
HIV positive	17 (18.7)	89 (11.8)	0.059#
Compicated with extrapulmonary TB	14 (15.4)	169 (22.3)	0.128
Cough			0.000***
No	5 (5.5)	100 (13.2)
Cough for<2 weeks	3 (3.3)	81 (10.7)
Cough for ≥ 2 weeks	83 (91.2)	576 (76.1)
AFB sputum smear			0.099#
Scanty	5 (5.5)	58 (7.7)
+	23 (25.3)	264 (34.9)
2+	22 (24.2)	188 (24.8)
3+	17 (18.7)	124 (16.4)
4+	24 (26.4)	123 (16.2)
TB: tuberculosis; AFB: acid-fast bacilli.
: P-value< 0.05; : P-value< 0.01; **: P-value< 0.001; #: P-value< 0.1

Risk factor characteristics of drug-resistant patients with TB

After including significant variables in the binary regression model, we summarised the risk of developing resistance for these variables (Table 3 and Fig. 2C). Young patients aged 15–44 (multivariate analysis: OR 1.817; 95% CI 1.162–2.840; P < 0.01) and middle-aged patients aged 45–59 (multivariate analysis: OR 2.175; 95% CI 1.335–3.543; P < 0.01) were more likely to develop drug resistance than children and the elderly. A cough duration of ≥ 2 weeks was a risk factor for drug resistance relative to no cough and cough for < 2 weeks (multivariate analysis: OR 2.069; 95% CI 1.234–3.469; P < 0.01). These risk factors were meaningful in univariate and multivariate logistic regression analyses. However, alcohol (univariate analysis: OR 1.741; 95% CI 1.107–2.736; P < 0.05) and high bacterial counts in sputum smears (univariate analysis: OR 1.846; 95% CI 1.115–3.058; P < 0.05) were the only risk factors in univariate logistic regression but were not risk factors in multivariate logistic regression.

Table 3

Univariate and Multivariate logistic regression assessing risk factors for drug resistance of tuberculosis
Variable	Univariate		Multivariate
	OR (95% CI)	P-value	OR (95% CI)	P-value
Age-years#
<14 & ≥60	Ref	0.001**	Ref	0.003**
15–44	8.045 (2.493–25.958)		1.817 (1.162–2.840)
45–59	10.539 (3.116–35.645)		2.175 (1.335–3.543)
Alcoholism	1.741 (1.107–2.736)	0.016*	1.438 (0.898–2.302)	0.130
HIV positive	1.724 (0.973–3.054)	0.062	1.372 (0.758–2.481)	0.296
Cough##
No	Ref	0.008**	Ref	0.022*
Cough for<2 weeks	0.575 (0.251–1.317)		0.566 (0.245–1.304)
Cough for ≥ 2 weeks	2.238 (1.343–3.730)		2.069 (1.234–3.469)
AFB smear
4+	1.846 (1.115–3.058)	0.017*	1.557 (0.928–2.614)	0.093
AFB: acid-fast bacilli.
: P-value< 0.05; : P-value< 0.01; **: P-value< 0.001
#: contrast selection of dummy variables is “indicator-first”; ##: contrast selection of dummy variables is “deviation-

The 2263 patients with sputum smear positive TB were mainly Yi men aged 15–44 years, and sex characteristics were consistent with the previous reported male-to-female ratio of 2:1^{1, 4, 29}. However, compared with other regions of China or other ethnic minorities with tuberculosis, these patients are generally younger^30–33. China’s pulmonary TB group is dominated by people over 65 years of age³⁰, while our patients aged 15–44 account for 59.3%. The occurrence of TB in the 15–44 age group may be related to increased social activity, exposing them to risk factors such as smoking, drinking, and HIV. In our survey, we also observed that the number of smokers, alcoholism, and HIV-positive people are higher than those in previous surveys^{29, 34–36}. All these inconsistencies can be explained by approximately 80% of the Yi patients in the study group. This ratio far exceeds the 48.9% of the local Yi nationality resident population¹⁰. Unlike other nomadic minorities, the Yi people live in remote villages in the high-altitude mountains with their families¹¹. These mountain villages have poor sanitary conditions^{12, 37}. All these provide favourable conditions for the spread and development of TB. They mainly eat potatoes, oats, and buckwheat, eat little meat, and like to smoke and drink alcohol³⁸. Smoking and alcohol consumption are risk factors that cause great harm if they occur simultaneously^{39, 40}. The most important risk factor for TB is HIV positivity, which is also high in this nation. The incidence of HIV and TB co-infection in our study was 14.14%, which is higher than the global rate of 9% and China’s rate of 7.4%^{36, 41}.

Because of these risk factors, as well as the remoteness of living, these patients visit the hospital only after the symptoms manifest and significantly affect their work. In our study, more than 1/4 of the patients with extrapulmonary TB had complications at more than two sites, which was also higher than 14% in other data reported in China⁴². Moreover, the characteristics of this group of patients with extrapulmonary TB are very different from those previously reported. Firstly, the incidence of extrapulmonary TB is 28.5%, which is significantly higher than the values previously reported globally (14%) and in China (8.5%)^{27, 43}. Secondly, the occurrence sites of extrapulmonary TB identified in this study differed from those commonly reported previously, such as the lymph nodes and skeletal system^{27, 44}. The most common sites in our patients were in the abdomen (34.1%) and genitourinary system (17.3%), which is also inconsistent with the most common extrapulmonary TB in China in the pleura (49.8%) and bronchial TB (14.8%)⁴². Compared with genitourinary TB, which is also a common extrapulmonary TB⁴⁵, the incidence of abdominal TB is generally 1–3%⁴⁶. The reported rates of extrapulmonary TB globally and in China were 12% and 4.8%, respectively^{42, 47}. Gastrointestinal TB can spread through direct ingestion or distant spread in the blood, lymph, or adjacent tissues. Direct ingestion can be through sputum or contaminated food⁴⁸. The Yi people like to have meals together, regardless of tableware or with their hands, and have poor hygiene habits. These may be the reasons for the high rate of abdominal TB, consistent with the high incidence in developing countries of low socioeconomic status⁴⁹. In addition, HIV positivity is also a health factor for abdominal TB⁵⁰.

In this study, 15.9% of the patients were on second-line anti-TB treatment or had received no treatment because of poor compliance. Although the drugs for anti-TB treatment are free, travel expenses, examination fees, and lost work expenses remain a heavy burden for patients. Patients generally choose to stop medication after the symptoms have improved slightly, thus resulting in drug resistance and further aggravating the difficulty of treatment⁵¹. Approximately 10.7% of the patients in our study were drug-resistant, which is lower than the current global and domestic levels of drug-resistant TB⁵². However, this does not reflect the drug resistance of TB in this region because testing for drug resistance has been lacking. The hospital did not use rapid genetic detection of TB drug resistance until 2020, while the technology has been in use for almost 20 years⁵³. The traditional drug-susceptibility test for TB is not applicable in this region because of the long wait for culture results. Previous records of drug resistance and patients receiving second-line therapy have relied on physicians’ clinical experience. Among 91 cases of detected drug resistance, 80.2% were rifampicin-resistant (RR) TB and 15.4% were MDR-TB. This is different from isoniazid resistance predominant, and 80% of the RR eventually become MDR^{25, 54}. This difference may be due to a lack of laboratory tests.

In our regression model for the analysis of drug resistance-related risk factors, we still obtained the impact of living habits and poverty. The entire group of patients who are family labourers have a wide range of social activities and a significant increase in the incidence of drug resistance. Patients aged 15–44 and 45–59 years were 1.817 and 2.175 times more likely to develop drug resistance than children and the elderly, respectively. In studies of TB drug resistance in other regions of China, the highest incidence was found for those with low education levels, with low income, and aged 40–65⁵⁵. Because this age group is the source of the labour force at home, they may be forced to give up treatment for reasons such as continuing work and economic reasons, and compliance is poor. Although HIV is closely related to drug resistance in previous reports¹⁷ and is most frequently seen in the age group of 15–44 years¹⁴, our study did not identify it as a risk factor for TB drug resistance. Previous studies have shown that drug resistance mainly occurs in low-education, low-income, and poor populations²⁵. Our data revealed that those patients with cough for > 2 weeks developed drug resistance 2.08 times more likely than those without cough and within 2 weeks of duration of illness. The fact that the patients did not visit the hospital for more than two weeks after the cough appeared also showed that they did not pay enough attention to the disease because of local economic backwardness. These two risk factors for TB drug resistance explain the significant impact of the backward economy, poverty, and inconvenience of medical treatment in this region. The other two risk factors that only appeared in the univariate regression analysis were alcohol consumption and high bacterial count in the AFB smear test. Combined alcohol abuse, low education, and low income are predictors of MDR⁵⁶. Moreover, a high bacterial count in the AFB smear test might indicate a high organism burden and, thus, greater susceptibility to resistance^{57, 58}. However, it is also believed that a large number of acid-fast bacilli results from drug resistance rather than the cause⁵⁹. Therefore, it is essential to grade the initial sputum smear before treatment⁵⁸.

Our study only investigated hospitalised patients in an infectious disease hospital in the Liangshan Yi Autonomous Prefecture. Owing to poverty, poor sanitary conditions, and inconvenient medical treatment in the local area, many patients may seek medical treatment only when the disease is serious. This can lead to bias in patient selection and the absence of many patients with sputum smear positive TB. In addition, the drug resistance experiment in this hospital is not comprehensive and backward, and it may also affect the results of the regression model. However, this hospital accommodates most local inpatients with TB, and the epidemiological characteristics obtained and risk factors for TB drug resistance were within the interpretable range. Hopefully, these data will help to understand the clinical and treatment status of locally sputum smear positive TB and further help local TB prevention and treatment.

Patients with sputum smear positive TB who were hospitalised at the Liangshan Yi Autonomous Prefecture infectious disease hospital were mainly Yi men aged 15–44 years. Smoking, alcoholism, and HIV positivity had the highest proportions. The incidence of extrapulmonary TB is higher than in other regions in China, and the incidence site is different; abdominal TB is the most common. Because of local poverty and poor medical conditions, drug resistance gene testing has been recently carried out. The 15–59-year-old age group developed drug resistance two times higher than children and the elderly. A cough duration of > 2 weeks was also a risk factor for drug resistance. In addition, alcohol abuse and high bacterial counts in sputum AFB smears were also associated with drug resistance. However, these factors are related to local living habits, poverty, and insufficient healthcare resources.

Ethics declarations

Ethics approval and consent to participate

All methods were carried out in accordance with relevant guidelines and regulations. The acquisition of all clinical data and laboratory results, as well as the waiver of patient informed consent and study is approved by the Ethics Review Committee of Sichuan Provincial Academy of Medical Sciences and Sichuan Provincial People's Hospital (Protocol 20220-254).

Consent for publication

Not applicable.

Availability of data and materials

The datasets generated and/or analysed during the current study are not publicly available, but are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This study was supported by the Liangshan Science and Technology Bureau (Grant No. 21ZDY0058; No. 21ZDY0069), the Sichuan Provincial Cadre Health Research Project (Grant No. 2021-230)

Author’s contribution

Tao Wang and Chaoxin Zhou wrote the main manuscript text, Lan Shang prepared figures 1-2 and Table 1-3, and Xiyuan Zhou, who is the corresponding author, conceptualized, planned, and revised the article. All authors reviewed the manuscript.

Acknowledgements

We would like to thank the infectious disease ward, radiology department, and laboratory department of the First People’s Hospital of Liangshan Prefecture for providing relevant data.

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No competing interests reported.

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Comorbidity and drug resistance of smear-positive pulmonary tuberculosis patients in the Yi Autonomous Prefecture of China: a cross-sectional study

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Abstract

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Background

Methods

Study area and population

Study design

Criteria for admission

Statistical methods

Ethics statement

Results

Characteristics of patients with sputum smear positive TB

Characteristics of drug-resistant and drug-susceptible groups

Risk factor characteristics of drug-resistant patients with TB

Discussion

Conclusion

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References

Additional Declarations

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