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Epidemiological characteristics, diagnosis and treatment effect of rifampicin-resistant pulmonary tuberculosis (RR-PTB) in Guizhou Province

BMC Infectious Diseases volume 24, Article number: 1058 (2024) Cite this article

Abstract

Background

Rifampicin-resistant pulmonary tuberculosis (RR-PTB) presents a significant threat to global public health security. China bears a substantial burden of RR-PTB cases globally, with Guizhou Province experiencing particularly alarming trends, marked by a continual increase in patient numbers. Understanding the population characteristics and treatment modalities for RR-PTB is crucial for mitigating morbidity and mortality associated with this disease.

Methods

We gathered epidemiological, diagnostic, and treatment data of all RR-PTB cases recorded in Guizhou Province from January 1, 2017 to December 31, 2023. Utilizing composition ratios as the analytical metric, we employed Chi-square tests to examine the spatiotemporal distribution patterns of RR-PTB patients and the evolving trends among different patient classifications over the study period.

Results

In our study, 3396 cases of RR-PTB were analyzed, with an average age of 45 years. The number of RR-PTB patients rose significantly from 176 in 2017 to 960 in 2023, peaking notably among individuals aged 23–28 and 44–54, with a rising proportion in the 51–80 age group (P < 0.001). Since 2021, there has been a notable increase in the proportion of female patients. While individuals of Han ethnic group comprised the largest group, their proportion decreased over time (P < 0.001). Conversely, the Miao ethnicity showed an increasing trend (P < 0.05). The majority of patients were farmers, with their proportion showing an upward trajectory (P < 0.001), while students represented 4.33% of the cases. Geographically, most patients were registered in Guiyang and Zunyi, with a declining trend (P < 0.001), yet household addresses primarily clustered in Bijie, Tongren, and Zunyi. The proportion of floating population patients gradually decreased, alongside an increase in newly treated patients and those without prior anti-tuberculosis therapy. Additionally, there was a notable rise in molecular biological diagnostic drug sensitivity (real-time PCR and melting curve analysis) (P < 0.001). However, the cure rate declined, coupled with an increasing proportion of RR-PTB patients lost to follow-up and untreated (P < 0.05).

Conclusions

Enhanced surveillance is crucial for detecting tuberculosis patients aged 23–28 and 44–54 years. The distribution of cases varies among nationalities and occupations, potentially influenced by cultural and environmental factors. Regional patterns in RR-PTB incidence suggest tailored prevention and control strategies are necessary. Despite molecular tests advances, challenges persist with low cure rates and high loss to follow-up. Strengthening long-term management, resource allocation, and social support systems for RR-PTB patients is essential.

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Introduction

As a significant global public health concern, pulmonary tuberculosis (PTB) remains a formidable challenge, particularly in China, where it ranks among the top 30 countries burdened with PTB [1]. Notably, the incidence of PTB in western China surpasses that of the eastern coastal areas, with a slower rate of decline observed in the former [2]. In regions like Guizhou Province in western China, the annual incidence of PTB exceeds 100 cases per 100,000 individuals [3,4,5].

However, the public health crisis extends beyond conventional PTB, as the emergence of drug-resistant tuberculosis (DR-PTB) exacerbates the situation, stemming from natural genetic variations or inappropriate drug utilization [6, 7]. The management of DR-PTB presents formidable challenges, with treatment durations extending up to two years [8, 9], a modest cure rate of approximately 63% [10, 11], and treatment costs exceeding those of standard PTB by over 100-fold [12, 13]. Among DR-PTB cases, multi-drug resistance/Rifampicin-resistant PTB (MDR/RR-PTB) constitutes the most prevalent subtype, with an estimated 410,000 individuals worldwide afflicted with MDR/RR-PTB in 2022. RR-PTB refers to PTB that is resistant to rifampicin, regardless of resistance to other anti-tuberculosis drugs, it essentially encompasses MDR-PTB. Alarmingly, 3.3% of newly diagnosed cases and 17% of previously treated patients globally exhibit MDR/RR-PTB [1], posing a formidable threat to global public health security. Efforts to understand the mechanisms and prevalence of DR-PTB are imperative for mitigating morbidity, mortality, and treatment expenses [14].

China shoulders a substantial burden of DR-PTB, ranking second globally in the number of RR-PTB cases, with approximately 25,000 cases reported in 2021 [15]. Notably, from 2015 to 2019, China witnessed a steady increase in the number of RR-PTB cases and detection rates [16], with a notable surge observed among students, particularly in western regions [17]. Guizhou Province, emblematic of western China, grapples with a particularly severe DR-PTB situation, marked by an annual rise in DR-PTB cases [18, 19]. However, the epidemiological study and the evaluation of diagnosis and treatment effect of RR-PTB population in this province have not been thoroughly carried out.

Therefore, the importance of this study is to provide a scientific basis for developing more effective RR-PTB prevention and control strategies to address this growing public health challenge.

Methods and materials

Ethics approval and consent to participate

Our study got the permission from the ethics committee. As the data were sourced from the Chinese Disease Prevention and Control Information System, researchers were subject to restrictions on access rights. Consequently, procedures for data retrieval, screening, and analysis were meticulously conducted to ensure the complete exclusion of patients’ identifiable information, including names, ID numbers, and residential addresses. Hence, the Ethics Committee of the Guizhou Center for Disease Control and Prevention deemed ethical approval and participant consent unnecessary for this study.

Participants and study design

The data were sourced from the China Disease Prevention and Control Information System, encompassing records of all documented cases of drug-resistant tuberculosis within Guizhou Province. Inclusion criteria comprised: (1) registration within the period spanning January 1, 2017, to December 31, 2023, (2) registration address located in Guizhou Province, and (3) registration indicating RR-PTB. Exclusion criteria were delineated as follows: (1) absence of documented evidence regarding drug sensitivity testing, and (2) absence of cases classified as RR-PTB.

Case data encompassed various parameters including registration time, gender, age, occupation, ethnic group, region, treatment classification, population mobility, anti-tuberculosis treatment history, drug sensitivity detection methods, and treatment outcomes. RR-PTB patient profiles, characterized by diverse attributes, were delineated through compositional ratios, with temporal analyses conducted to discern trends in these ratios over time.

Indicators and definitions

RR-PTB refers to mycobacterium tuberculosis from patients with tuberculosis that is resistant to rifampicin, regardless of resistance to other anti-TB drugs. The registration period is from 2017 to 2023; Gender is divided into male and female; The ages were divided into 0–10, 11–20, 21–30, 31–40, 41–50, 51–60, 61–70, 71–80, 81–90, 91-; Occupations are divided into peasant, housework and unemployment, and others; Ethnic groups are divided into Han, Miao, Tujia and others; The region covers 9 cities in Guizhou Province, including Guiyang, Zunyi, Tongren, Bijie, Qiandongnan, Liupanshui, Qiannan, Anshun, Qianxinan; The treatment was classified into primary treatment and retreatment; Population mobility is divided into local population and floating population, floating population includes the movement between counties, cities and provinces; Treatment history was divided into anti-tuberculosis treatment history and no anti-tuberculosis treatment history. The detection methods of drug sensitivity are divided into phenotype and molecular tests, molecular test methods mainly include real-time PCR and melting curve analysis of rpoB gene mutation, which are mainly for rifampin and isoniazid drugs. Treatment outcomes include cure, loss to follow-up, complete the course of treatment, untreated, death from non-tuberculosis, adverse reaction, cure, loss to follow-up, complete the course of treatment, untreated, death from non-tuberculosis, adverse reaction, under treatment, treatment failure, diagnostic change, death from tuberculosis, others. Composition ratio (%) as the index of analysis, composition ratio refers to the percentage of the number of a certain type’s cases of in the total number of cases.

Statistical analysis

The statistical analysis was conducted using SPSS version 26.0 to assess the changing trend in component ratios. The trend Chi-square test or Fisher’s exact probability method was employed for this analysis, with a significance level set at α = 0.05.

Results

Basic information of RR-PTB patients

We enrolled a total of 3396 cases of RR-PTB across 9 municipalities in Guizhou Province, comprising 2324 (68.43%) males and 1072 (31.57%) females, spanning ages from 1 to 96 years, with a mean age of 45 years (median 46 years). The incidence of RR-PTB rose from 176 cases in 2017 to 960 cases in 2023, with 42.22% falling within the 41–60 age group, specifically 22.23% aged 41–50 and 19.99% aged 51–60, making the 21–30 age bracket the third most affected, accounting for 17.76%. Predominantly, the occupation was farming (50.44%), the Han ethnic group represented 76.03%, retreatment cases constituted 62.69%, initial treatment stood at 37.31%, and 80.68% had a history of anti-tuberculosis treatment. Additionally, real-time PCR and melting curve analysis of rpoB gene mutation were conducted in 84.78% of cases for drug susceptibility. Regarding residency, Guiyang City contributed 31.80% of registered addresses, with 78.86% representing the local population and the remaining 21.14% comprising the floating population. The cure rate was 34.52%, while 19.96% were lost to follow-up, and 15.93% remained untreated (Table 1).

Table 1 Basic characteristics of rifampicin-resistant PTB patients (n = 3396)
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Gender and age characteristics of RR-PTB

During the period spanning 2017 to 2023, there was a higher incidence of RR-PTB among males compared to females, with both sexes demonstrating an increasing trend (Fig. 1A). Statistical analysis revealed no significant difference in the gender distribution of RR-PTB cases (P = 0.823). However, the proportion of females exhibited a noteworthy increase from 2021 onwards (Fig. 1B). Age distribution exhibited peaks at 23–28 years and 44–54 years, with fewer cases observed at younger and older age brackets (Fig. 1C). Notably, there was a declining trend observed among individuals aged 11–40 years (P < 0.05), while those aged 51–80 years demonstrated an increasing trend (P < 0.001). Conversely, the proportion of individuals aged 41–50 years remained relatively stable (P > 0.05).

Fig. 1
figure 1

Gender and age distribution of RR-PTB patients. (A) Number of male and female patients, (B) Proportion of male and female patients, (C) Age count, (D) Age group. * indicates that the composition ratio is decreasing and the difference is statistically significant, # indicates that the composition ratio is increasing and the difference is statistically significant

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Ethnic groups and occupational characteristics of RR-PTB

The proportion of Han ethnic group was the largest but showed a decreasing trend (P < 0.001), the proportion of Miao ethnic group ranked second and showed an increasing trend (P < 0.05), and the proportion of Tujia ethnic group maintained (P > 0.05) (Fig. 2A). Among the other ethnic minorities, Buyi accounted for 3.42% and Dong accounted for 3.3 (Fig. 2B). The proportion of farmers was the largest and showed an upward trend (P < 0.001), the proportion of housework and unemployment also showed an upward trend (P < 0.05), and the proportion of other occupations showed a downward trend (P < 0.001) (Fig. 2C). The student population is 4.33%, ranking third among all occupations (Fig. 2D).

Fig. 2
figure 2

Ethnic groups and occupational distribution of RR-PTB patients. (A) Ethnic group, (B) Other minorities, (C) Occupation, (D) Other occupation. * indicates that the composition ratio is decreasing and the difference is statistically significant, # indicates that the composition ratio is increasing and the difference is statistically significant

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Spatial and temporal distribution characteristics of RR-PTB

According to the registered addresses, the patients were predominantly located in Guiyang, Zunyi, and Tongren (Fig. 3A), as well as in southwest Guizhou, Anshun, Qiannan, Liupanshui, Qiandongnan, and Bijie. The overall proportion exhibited an increasing trend (P < 0.05), although the proportions in Zunyi and Guiyang showed a declining trend (P < 0.001) (Fig. 3B). Based on household addresses, patients were primarily concentrated in Bijie, Tongren, and Zunyi (Fig. 3C). The proportion of patients in Qianxinan and Anshun demonstrated a significant increase (P < 0.001), whereas the proportion in Zunyi and Bijie displayed a decreasing trend (P < 0.05) (Fig. 3D).

Regarding population mobility, there was a gradual decline in the proportion of the floating population, juxtaposed with a rise in the local population (P < 0.001) (Fig. 4A). Among the floating population, the proportion between counties was 12.75%, between cities 7.42%, and between provinces 0.97% (Fig. 4B).

Fig. 3
figure 3

Spatial and temporal distribution of RR-PTB patients. (A) Hotspot map registered address, (B) Proportion of registered address, (C) Hotspot map of household address, (D) Proportion of household address. * indicates that the composition ratio is decreasing and the difference is statistically significant, # indicates that the composition ratio is increasing and the difference is statistically significant

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Fig. 4
figure 4

Population mobility of RR-PTB patients. (A) Population mobility, (B) Classification of floating population

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Diagnostic and therapeutic characteristics of RR-PTB

Among the cohort of RR-PTB patients, there was an observed increase in the proportion of newly treated cases, coupled with a decrease in the proportion of retreated patients (P < 0.001) (Fig. 5A). Regarding treatment history, there was a gradual rise in the proportion of patients with no prior exposure to anti-TB therapy (P < 0.001) (Fig. 5B). Additionally, there was a progressive increase in the utilization of molecular biological diagnosis for drug sensitivity (P < 0.001) (Fig. 5C). Regarding treatment outcomes, as of 2021, there was a notable decline in the cure rate among RR-PTB patients (P < 0.05), alongside an increase in the proportion of patients lost to follow-up or untreated (P < 0.05) (Fig. 5D).

Fig. 5
figure 5

Diagnosis and treatment characteristics of RR-PTB patients. (A) Treatment classification, (B) Treatment history, (C) Drug sensitivity test methods, (D) Treatment outcomes. * indicates that the composition ratio is decreasing and the difference is statistically significant, # indicates that the composition ratio is increasing and the difference is statistically significant

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Discussion

Western China bears the brunt of PTB incidence, with Guizhou Province characterized by multi-ethnic clustering. An analysis of RR-PTB’s epidemiological characteristics, diagnosis, and treatment outcomes in Guizhou Province is pivotal for formulating evidence-based prevention and control strategies, with broader implications for tackling RR-PTB across western China.

Our findings reveal a concerning trend: the number of RR-PTB cases surged from 176 in 2017 to 960 in 2023 in Guizhou Province, diverging from the declining trend observed in overall PTB cases [20], it is apparent that RR-PTB is escalating at a markedly faster rate than that of the local population. Various factors potentially influence this discrepancy, encompassing enhancements in PTB surveillance and reporting [21, 22], the proliferation of drug resistance [23,24,25], and population mobility dynamics [26, 27]. Despite increasing popularity, PTB drug resistance screening remains inadequately comprehensive in Guizhou Province, indicating a severe prevalence of RR-PTB and the likelihood of undetected cases.Furthermore, RR-PTB patient demographics exhibit broad age distribution, with a notable concentration among individuals aged 41–60, indicative of specific susceptibility or risk factors within this age cohort [28,29,30]. Agricultural occupations predominate among RR-PTB patients, aligning with the rural-centric nature of TB incidence [31, 32], suggesting an intricate interplay between RR-PTB epidemiology and socioeconomic determinants [33, 34]. Moreover, the Han ethnicity constitutes the majority among RR-PTB patients, likely mirroring the demographic composition; however, further ethnic comparative studies are imperative to elucidate potential genetic or biological disparities [35,36,37].

Our findings reveal that the number of RR-PTB cases was higher in male than in female between 2017 and 2023, with both cohorts exhibiting an upward trajectory. Notably, a significant rise in the proportion of female patients emerged from 2021 onwards, suggesting potential gender-related determinants influencing RR-PTB epidemiology.Concerning age distribution, we observed peaks in patient numbers within the 23–28 and 44–54 age brackets, likely attributable to a complex interplay of lifestyle, environmental exposures, and other specific factors pertinent to these age cohorts [38, 39]. Moreover, a declining trend was noted in the proportion of patients aged 11 to 40 years, juxtaposed with an increasing trend among those aged 51 to 80 years, plausibly linked to population aging dynamics [40,41,42]. Our study underscores the potential utility of developing targeted strategies tailored to high-incidence age groups, alongside intensified surveillance and management protocols addressing gender and age differentials. Further exploration of the factors contributing to these disparities is warranted to inform comprehensive intervention strategies.

This study contributes valuable insights into the distribution of RR-PTB patients across diverse ethnic and occupational groups. The predominance of Han RR-PTB patients, albeit on a declining trajectory, is noteworthy, contrasting with an ascending trend among Miao patients, albeit less pronounced statistically. These shifts likely reflect population dynamics, environmental influences, or alterations in healthcare utilization [26, 27, 33, 34]. Moreover, there’s a notable rise in the representation of ethnic minorities. Buyi and Dong, however, exhibit relatively lower rates, potentially influenced by cultural, socioeconomic, and genetic factors warranting further investigation [43,44,45].Occupationally, farmers constitute the largest cohort, possibly due to the elevated RR-PTB incidence in rural regions and the substantial agricultural workforce [46, 47]. Yet, this demographic displays both declining and ascending trends. Housework and unemployment follow, exhibiting an increasing pattern, possibly indicative of intra-family transmission or familial environmental factors [48, 49]. Conversely, other occupational segments depict a downward trajectory, indicative of enhanced health protection and preventive measures within those sectors.Notably, students rank third among all occupations, comprising 4.33% of cases, potentially reflecting RR-PTB transmission within campus settings. Strengthening health education and preventive measures within the student populace is warranted [50,51,52].

This study aimed to elucidate the geographical distribution and population dynamics of RR-PTB patients by scrutinizing registered cases at both administrative and residential addresses within the Guizhou region. Our findings revealed divergent hotspots of RR-PTB incidence contingent upon the address type analyzed. Regarding administrative addresses, Guiyang and Zunyi emerged as primary foci, albeit exhibiting a declining trend in RR-PTB prevalence. Conversely, Tongren, Qianxinan, Anshun, Qiannan, Liupanshui, Qiandongnan, and Bijie witnessed an upward trajectory in RR-PTB prevalence. On the other hand, residential addresses showed a different pattern, with Bijie, Tongren, and Zunyi hosting a higher proportion of patients. Notably, Qianxinan and Anshun experienced an increasing prevalence, while Zunyi and Bijie observed a decline. These trends likely stem from multifaceted influences, including economic development [33, 34], population mobility [26, 27], and healthcare resource distribution [53, 54]. Our investigation unveiled that initially, only Guiyang and Zunyi possessed robust DR-PTB treatment capabilities, consequently attracting a disproportionate number of patients. However, with the establishment of DR-PTB treatment facilities across municipalities, patients increasingly sought care closer to their residences. Furthermore, our analysis of population mobility corroborated this observation, revealing a gradual decline in the floating population and a concurrent rise in local inhabitants. In the mobile population, inter-county migration dominates, succeeded by intra-city and inter-provincial movements, underscoring the regional essence of RR-PTB. Our study revealed a scarcity of DR-PTB treatment centers in each city, typically limited to one or at most two. The potential link between this paucity and the heightened rate of RR-PTB patient relocations across counties warrants deeper scrutiny. Nonetheless, these findings form a credible basis for advancing the diagnostic and therapeutic capabilities for DR-PTB at the county level, facilitating a more rational distribution of healthcare resources.

This study delves into the nuances of initial treatment, treatment history, molecular diagnostic drug sensitivity, and treatment outcomes among RR-PTB patients. Our findings reveal a progressive rise in the proportion of treatment-naive patients alongside a decline in retreatment cases, suggesting advancements in early PTB screening and treatment efficacy among known cases [55,56,57]. Moreover, a notable surge in patients with no prior antituberculosis treatment history underscores a potential increase in untreated new cases in certain regions, emphasizing the imperative to bolster early tuberculosis diagnosis and intervention efforts.

Simultaneously, there has been a gradual increase in the proportion of drug susceptibility diagnosed via molecular tests, potentially indicative of advancements in diagnostic methodologies and therapeutic approaches, thereby enhancing the accuracy and efficacy of drug-resistant TB detection and management [55,56,57,58]. Nevertheless, despite these strides, our study revealed a declining trend in the cure rate among RR-PTB patients in Guizhou Province until 2021, accompanied by a rise in the proportion of patients lost to follow-up or left untreated, influenced by various factors. These factors encompass patient adherence to treatment protocols [59, 60], the allocation and utilization of healthcare resources [53, 54], and the refinement of social support systems [61]. This underscores that while technological advancements have improved RR-PTB diagnosis, the downward trajectory in treatment outcomes and the uptick in missed visits highlight persisting challenges. Hence, to further enhance treatment efficacy and prognoses for RR-PTB patients, it is imperative to bolster long-term patient follow-up management, optimize the allocation and utilization of healthcare resources, and fortify the development of social support systems. This multifaceted approach aims to achieve a more holistic and effective tuberculosis prevention, control, and management strategy.

Limitations

This study is subject to certain limitations, including constraints related to data sources and potential information biases. Additionally, there was a failure to fully account for the influence of other potential contributing factors. Therefore, further analysis incorporating multiple factors and prolonged follow-up observations are warranted to achieve a more comprehensive understanding of the epidemiological characteristics and influencing factors associated with RR-PTB.

Conclusions

In Guizhou, the age groups of 23–28 years old and 44–54 years old exhibit heightened incidences of RR-PTB, underscoring the need for enhanced targeted monitoring and patient detection efforts. Disparities in the distribution among different nationalities and occupations suggest potential influences from cultural and environmental factors. Regional patterns in RR-PTB prevalence necessitate tailored prevention and control strategies based on distinct geographical characteristics. Despite advancements in molecular tests diagnostics, persistent challenges including low cure rates and high rates of loss to follow-up persist. Strengthening long-term follow-up management of RR-PTB patients, optimizing the allocation of medical resources, and fostering the development of robust social support systems are imperative measures moving forward.

Data availability

The data analyzed for this study can be found from the corresponding authors on reasonable request.

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Acknowledgements

We thank all members who participated in this work.

Funding

This study was supported by “Project for Public Health Talent Cultivation of China. Grant No. Guo Jikong Zong Ren Han [2024] 122” and “National Natural Science Foundation of China (Grant No. 82460695)”.

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Authors and Affiliations

  1. School of Public Health, the Key Laboratory of Environmental Pollution Monitoring and Disease Control, Ministry of Education, Guizhou Medical University, No.9 Beijing Road, Yunyan District, Guiyang city, 550025, Guizhou Province, China

    Jian Zhou, Yong Hu & Shijun Li

  2. Guizhou Center for Disease Control and Prevention, No.73, Bageyan Road, Yunyan District, Guiyang city, 550004, Guizhou Province, China

    Jian Zhou, Jinlan Li & Shijun Li

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  1. Jian Zhou
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  2. Jinlan Li
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  3. Yong Hu
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Contributions

JZ designed the study and analysis, and performed the statistical analysis and drafted the initial manuscript, and SJL，YH and JLL provided revisions, guidance, and funding support for the article. All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Jinlan Li, Yong Hu or Shijun Li.

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The authors declare no competing interests.

Conflict of interest

All the authors declared that there was no conflict of interest in the study.

Ethics approval and consent to participate

This study got the permission from the ethics committee. As the data were sourced from the Chinese Disease Prevention and Control Information System, researchers were subject to restrictions on access rights. Consequently, procedures for data retrieval, screening, and analysis were meticulously conducted to ensure the complete exclusion of patients’ identifiable information, including names, ID numbers, and residential addresses. Hence, the Ethics Committee of the Guizhou Center for Disease Control and Prevention deemed ethical approval and participant consent unnecessary for this study.

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Zhou, J., Li, J., Hu, Y. et al. Epidemiological characteristics, diagnosis and treatment effect of rifampicin-resistant pulmonary tuberculosis (RR-PTB) in Guizhou Province. BMC Infect Dis 24, 1058 (2024). https://doi.org/10.1186/s12879-024-09976-9

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Keywords

BMC Infectious Diseases

ISSN: 1471-2334

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