Association between blood glucose control and risk factors of latent tuberculosis in the population with diabetes: Results from the National Health and Nutrition Examination Survey (NHANES) 2011–2012

doi:10.21203/rs.3.rs-3132617/v1

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Association between blood glucose control and risk factors of latent tuberculosis in the population with diabetes: Results from the National Health and Nutrition Examination Survey (NHANES) 2011–2012

https://doi.org/10.21203/rs.3.rs-3132617/v1

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Background

Diabetes has been conferred an increased risk of latent tuberculosis infection. However, the level of blood glucose control and associated risk factors for latent tuberculosis infection in diabetes population is poorly understood. This study aimed to determine the relationship between blood glucose control and the risk factors for latent tuberculosis infection (LTBI) in individuals with diabetes mellitus (DM) using the National Health and Nutrition Examination Survey datasets.

Methods

The association between blood glucose control and LTBI in patients with DM were investigated with logistic regression analysis. Additionally, covariates such as gender, age, education level, and ethnicity were also included in the analysis.

Results

A total of 2489 patients were included in this study, of which 76.3% were Non-Hispanic White, Black and Asia. 231 participants were positive with LTBI. Multivariable analysis demonstrated that the poor blood glucose control exhibited a 150% greater risk of LTBI in DM population. Besides, female gender in DM population would less likely occurring LTBI in DM population (AOR: 0.71, 95%CI: 0.55–0.91, P = 0.006). Meanwhile, with age increased, the risk of LTBI gradually raised. Comparing to patients aged 18 to 45 years old, the prevalence of LTBI in elderly more than 70 years old was much higher (AOR: 3.16, 95%CI: 2.11–4.74, P < 0.001). Furthermore, the ethnicity was also associated with LTBI in DM population. Non-Hispanic White and Black population with DM were less likely developing LTBI.

Conclusions

The findings of this study highlight the association between poor blood glucose control and the prevalence of LTBI in patients with DM. Furthermore, male, aging, and ethnicity were independent risk factors for LTBI in the DM population.

Latent tuberculosis infection

Diabetes mellitus

Poor blood glucose control

Risk factors

NHANES

Latent tuberculosis infection (LTBI) is defined as a persistent immune response to Mycobacterium tuberculosis (MTB) antigens without clinical manifestations of active tuberculosis (TB) disease. According to the World Health Organization (WHO), approximately one-quarter of the global population is latently infected with TB, of which 5%-10% may eventually develop symptoms and progress to active TB. In 2021, an estimated 10.6 million cases of active TB were diagnosed, resulting in 1.6 million TB-related deaths worldwide [1]. Given the goal of ending TB by 2035, it is crucial to explore the risk factors associated with LTBI. Identifying these risk factors is essential for the implementation of effective strategies to prevent the progression of LTBI to active TB and to reduce TB transmission.

Diabetes Mellitus (DM) is a widespread and potentially devastating medical condition that has experienced a significant increase in prevalence over the past few decades, presenting a major public health challenge in the twenty-first century [2]. It has been projected that the global prevalence of DM will reach 642 million by 2040 [3]. Several studies have demonstrated that individuals with DM are approximately three times more likely to develop active tuberculosis (TB) compared to the general population [4–7]. Moreover, emerging evidence suggests a significant association between DM and LTBI [8]. Population-based studies have reported that the prevalence of LTBI in adults with DM in the United States is more than twice that of adults without DM (11.6% vs. 4.6%) [9, 10]. Similarly, a community-based study conducted in China revealed an increased risk of LTBI in individuals with DM (AOR = 1.59, 95% CI: 1.11–2.28) [11]. Furthermore, a systematic review involving 38,263 participants confirmed the association between DM and LTBI [12].

Given the rapid increase in the global prevalence of DM and its association with high TB burdens, early identification and intervention targeting this co-epidemic would help prevent significant morbidity and mortality. However, the factors influencing the development of LTBI in individuals with DM are still unknown. To address this knowledge gap, our aim was to explore the levels of blood glucose control and other associated risk factors for LTBI in the DM population, based on the National Health and Nutrition Examination Survey (NHANES).

Study design and population

In this study, we conducted a cross-sectional analysis of LTBI in individuals with DM or pre-diabetes using data from the NHANES for the years 2011–2012. The NHANES is a series of population-based national surveys conducted by the Centers for Disease Control (CDC) and Prevention of America. It collected updated information on health and nutrition every 2 years. The NHANES utilizes a complex, stratified sampling design to select representative samples of non-institutionalized civilians in the United States. Our study focused on eligible adult participants (≥ 18 years old) who had completed interviews, health examinations, and had DM status results available. To ensure consistency in our analysis, individuals with glycated hemoglobin (HbA1c) levels ≤ 5.6 were excluded; furthermore, we excluded individuals who reported a history of active TB in the questionnaire and those with missing data for both TB skin test (TST) and QuantiFERON®-TB Gold In-Tube test (QFT-GIT) (Fig. 1). The Ethics Review Board of the National Center for Health Statistics Research approved the questionnaire and examination components, and all participants provided informed consent.

Measures and definitions

DM status of participants was determined based on self-reported diabetes status and blood glucose test, including HbA1c, OGTT, or fast blood glucose. Participants who reported a diagnosis of DM or pre-diabetes by a healthcare professional were classified as having DM or pre-diabetes, irrespective of the blood glucose test results. Participants without a self-reported history of DM or pre-diabetes were classified according to the American Diabetes Association guidelines. For HbA1c, individuals with values ranging from 5.7–6.4% were classified as having prediabetes, while those with values of 6.5% or higher were classified as having DM. For OGTT, individuals with values between 140 and 199 mg/dL were classified as prediabetes, and those with values of 200 mg/dL or higher were classified as DM. Lastly, for fasting blood glucose, individuals with values between 100 and 125 mg/dL were classified as prediabetes, while those with values of 126 mg/dL or higher were classified as DM.

Tuberculin skin testing (TST) was conducted on the volar surface of the arm for each participant by trained technicians following the relevant guidelines. Tubersol PPD (Sanofi, Bridgewater, NJ) was used as the antigen for all TSTs. The TST results were obtained between 46 and 76 hours after administration by NHANES technicians who were unaware of the participant's medical history or any history of TB contact. The induration size of the TST was calculated as the average of up to three recorded TST results. However, if only one TST result was recorded, that result was used for analysis. A positive TST was defined as an induration size of 10mm or greater.

For the QuantiFERON-TB Gold assay (QFT-GIT), it was performed and interpreted following the guidelines provided by the Centers for Disease Control and Prevention (CDC) for Interferon-Gamma Release Assays (IGRAs). To interpret the QuantiFERON-TB Gold assay as reactive, the following criteria had to be met: the Nil value (negative control) must be less than or equal to 8.0 IU gamma interferon (IF)/ml, and the difference between the TB antigen value and the Nil value must be equal to or greater than 0.35 IU gamma interferon (IF)/ml.

According to the United States Census Bureau reported in 2020, the income-to-poverty ratio serves as a measure to assess the severity of poverty and indicates the proximity of an individual’s or family’s income to their poverty threshold. This ratio is expressed as a percentage and compares the income of a family or individual with the relevant threshold based on the family size. When the income falls below the threshold, the income-to-poverty ratio is less than 1, with values closer to 1 indicating a closer approximation to meeting economic needs. On the other hand, individuals and families whose income meets or exceeds the threshold have income-to-poverty ratios equal to or greater than 1, with values greater than 1 denoting income that surpasses the poverty threshold.. Typically, the degree of poverty is evaluated based on the ratio value, which is classified into four levels: less than 0.5, 0.5 to 1, 1 to 2, and greater than or equal to 2.

Covariates

The covariates used in this study were extracted from the NHANES interviews, health examinations, and laboratory data. Information such as age, ethnicity, sex, income-to-poverty ratio, education level, body mass index (BMI), smoking status, and underlying diseases were obtained from the NHANES dataset. The Charlson Comorbidity Index (CCI) was calculated based on the underlying diseases.

Statistical analysis

All data were analyzed using R software version 3.6.2 (R Foundation for Statistical Computing). Quantitative variables were expressed as means and standard deviations (SD). Categorical variables were summarized as counts and proportions for each category. The characteristics of LTBI and non-LTBI DM patients were compared using Pearson’s χ2 test for categorical variables and t-test for quantitative variables. Pearson's correlation analysis was employed to examine the relationship between the factors (HAb1c, BMI, CCI, fast blood glucose, age, and income-to-poverty ratio) and IGRAs. To further evaluate the risk factors of LTBI in DM patients, with particular focus on blood glucose control level, univariable and multivariable logistic regression analyses were conducted. The variables for inclusion in the multivariable analysis were carefully selected based on statistically significant associations observed in the univariate analysis. The adjusted odds ratios (AOR) for the multivariable analyses were adjusted using stepwise selection. The results are presented as P-values, odds ratios (ORs), AOR, and 95% confidence interval (CIs). A P-value of < 0.05 was considered statistically significant.

Characteristics of Participant

In total, 2,563 patients diagnosed with diabetes or prediabetes from the NHANES 2011–2012 dataset were screened for this study (Fig. 1). Among them, 2,489 participants with a history of latent tuberculosis infection (LTBI) based on questionnaire responses or valid QFT-GIT/TST results were included. As shown in Table 1, out of the enrolled DM patients, 321 individuals (14.8%) were identified as having LTBI, with 59.5% of them being male. The mean age of the LTBI participants was significantly higher than that of participants without LTBI (P < 0.001). Notably, the non-Hispanic Asian race/ethnicity group exhibited a higher proportion of LTBI compared to the non-LTBI group (P < 0.001). Furthermore, an analysis of education levels revealed that patients with a lower education level were more likely to develop LTBI (P = 0.004). Most interestingly, patients with poor glucose control demonstrated a higher rate of LTBI (P < 0.001). No significant differences were observed in terms of household income, body mass index (BMI), smoking status, Charlson Comorbidity Index (CCI), and type of diabetes.

Table 1

Demographic of the DM participants with and without LTBI (N = 2489)
	Control(N = 2168)	LTBI(N = 321)	P-value
Gender
Male	1142 (52.7%)	191 (59.5%)	0.0258
Female	1026 (47.3%)	130 (40.5%)
Race/Ethnicity
Mexican American	204 (9.4%)	48 (15.0%)	< 0.001
Other Hispanic	213 (9.8%)	59 (18.4%)
Non-Hispanic White	809 (37.3%)	42 (13.1%)
Non-Hispanic Black	636 (29.3%)	84 (26.2%)
Non-Hispanic Asian	245 (11.3%)	84 (26.2%)
Others	61 (2.8%)	4 (1.2%)
Age (Years)
18–45	652 (30.1%)	56 (17.4%)	< 0.001
46–60	638 (29.4%)	91 (28.3%)
61–70	465 (21.4%)	98 (30.5%)
> 70	413 (19.0%)	76 (23.7%)
Ratio of Poverty
< 0.5	111 (5.1%)	20 (6.2%)	0.616
0.5-1	361 (16.7%)	56 (17.4%)
1–2	561 (25.9%)	84 (26.2%)
>=2	919 (42.4%)	123 (38.3%)
Education Level
Less than college degree	1100 (50.7%)	191 (59.5%)	0.004
College graduate or above	1068 (49.3%)	130 (40.5%)
BMI
Mean (SD)	30.6 (7.31)	29.9 (6.98)	0.0667
Active Smoking
No	1159 (53.5%)	285 (88.8%)	0.463
Yes	304 (14.0%)	36 (11.2%)
CCI
Mean (SD)	1.64 (1.70)	1.76 (1.57)	0.205
Glycosylated Hemoglobin (%)
< 5.7	688 (31.7%)	70 (21.8%)	< 0.001
5.7 ~ 6.4	975 (45.0%)	150 (46.7%)
>=6.5	505 (23.3%)	101 (31.5%)
>=200	75 (3.5%)	8 (2.5%)
Type of diabetes
Type 1	148 (6.8%)	22 (6.9%)	1
Type 2	2020 (93.2%)	299 (93.1%)
Note: Ratio of poverty was classified the ratio as four levels according to the United States Census Bureau: <0.5 stands for extremely poverty, 0.5 ~ 1 poverty, 1 ~ 2 not poverty, ≥ 2 wealthy.
DM, diabetes mellitus; LTBI, latent tuberculosis infection; BMI, body mass index. CCI: Charlson Comorbidity Index.

Correlation of LTBI with laboratory and basic parameters in DM patients

According to the results presented in Fig. 2, a positive correlation was found between LTBI and age, with a correlation coefficient of 0.1 (r = 0.1, P < 0.001). This implies that as age increases, the likelihood of LTBI also tends to increase. Conversely, no significant correlation was detected between LTBI and other factors, namely BMI, Fasting Glucose, HAb1c, CCI, and income-to-poverty ratio. These variables appear to be unrelated to the presence of LTBI in the studied population.

LTBI and associated risk factors in DM participants

Unadjusted analysis of risk factors associated with latent tuberculosis infection (LTBI) in patients with diabetes mellitus (DM) was conducted and summarized in Table 2. The findings revealed a statistically significant elevation in the risk of LTBI among elderly males with DM. Moreover, individuals of non-Hispanic white and black ethnicities with higher educational attainment demonstrated a notable reduction in the risk of LTBI. Additionally, poor glycemic control, as indicated by HbA1c levels in the ranges of 5.7 to 6.4 (OR: 1.70, 95% CI: 1.24–2.37, P = 0.001), 6.5 to 7.4 (OR: 2.25, 95% CI: 1.49–3.39, P < 0.001), 7.5 to 8.4 (OR: 2.38, 95% CI: 1.38-4.00, P = 0.001), and > = 8.5 (OR: 1.98, 95% CI: 1.19–3.22, P = 0.007), was found to be significantly associated with an increased risk of LTBI when compared to individuals with HbA1c levels below 5.7.

Table 2

The risk factors for LTBI in DM patients
Variables	Univariable		Multivariable
Variables	OR (95%CI)	P-value	AOR (95%CI)	P-value
Gender
Male	Reference	0.02	Reference	0.006
Female	0.76(0.60–0.96)		0.71(0.55–0.91)
Race/Ethnicity
Mexican American	Reference		Reference
Other Hispanic	1.18(0.77–1.81)	0.45	1.11(0.71–1.69)	0.72
Non-Hispanic White	0.22(0.14–0.34)	< 0.001	0.18(0.11–0.29)	< 0.001
Non-Hispanic Black	0.56(0.38–0.83)	0.003	0.50(0.34–0.74)	< 0.001
Non-Hispanic Asian	1.46(0.98–2.22)	0.06	1.44(0.96–2.17)	0.08
Others	0.28(0.008–0.71)	0.02	0.26(0.07–0.67)	0.01
Age (Years)
18ཞ45	Reference		Reference
46ཞ60	1.66(1.17–2.37)	0.004	1.67(1.16–2.41)	0.006
61ཞ70	2.45(1.74–3.50)	< 0.001	2.44(1.69–3.56)	< 0.001
> 70	2.14(1.49–3.10)	< 0.001	3.16(2.11–4.74)	< 0.001
Education Level
Less than college degree	Reference
College graduate or above	0.70(0.55–0.89)	0.003
Glycosylated Hemoglobin
< 5.7	Reference		Reference
5.7 ~ 6.4	1.70(1.24–2.37)	0.001	1.42(1.01–2.02)	0.043
6.5 ~ 7.4	2.25(1.49–3.39)	< 0.001	1.58(1.01–2.46)	0.043
7.5 ~ 8.4	2.38(1.38-4.00)	0.001	1.55(0.87–2.70)	0.12
> 8.5	1.98(1.19–3.22)	0.007	1.55(0.91–2.59)	0.09
Type of diabetes
Type 1	Reference
Type 2	1.10(0.66–1.73)	0.72
LTBI, latent tuberculosis infection; DM, diabetes mellitus; OR, odds ratios; AOR, adjusted odds ratios

For the adjusted analysis, a stepwise regression method was utilized to identify independent variables. The variables included in the analysis were gender, race, age, and HbA1c. Interestingly, even after adjusting for these variables, females exhibited a decreased likelihood of TB infection (adjusted odds ratio [AOR]: 0.71, 95% confidence interval [CI]: 0.55–0.91, P = 0.006). Non-Hispanic white and black individuals exhibited a significantly lower risk of LTBI, with risk reductions of 82% and 50%, respectively. Moreover, age was found to be positively associated with LTBI (P < 0.001), and higher levels of HbA1c were associated with an increased risk of LTBI among DM patients.

Emerging evidence suggests an association between DM and LTBI [13, 14]. In our study, the prevalence of LTBI is 14.8% in the U.S. population with DM was found to be 14.8%, which is more than twice as much as the general population [15]. Furthermore, blood glucose control level was identified as a factor related to LTBI. Meanwhile, gender, age, and ethnicity were also identified as risk factors in DM patients.

Maintaining optimal blood glucose control is crucial for disease prevention in DM patients. Poor blood glucose control has been proven to be associated with various diabetes complications, such as cardiovascular diseases, kidney disease, eye problems, nerve damage. Furthermore, the level of blood glucose control has been reported to be linked to the occurrence of pulmonary tuberculosis (PTB) and severe PTB [16]. However, although studies have shown that DM was associated with the increased prevalence of LTBI [8, 17, 18], the role of blood glucose control level in the prevalence of LTBI remains controversial. Two cross-sectional studies analyzing the risk factors for LTBI among DM patients did not find a significant difference in effective glycemic control between patients with positive and negative QuantiFERON-TB Gold In-Tube (QFT-GIT) results [19, 20]. In contrast, Gerardo et al. from Mexico obtained opposite results [21]. In our study, we did not primarily find a correlation between HbA1c and IGRAs; however, logistic regression analysis revealed a positive association between poor blood glucose control and the prevalence of LTBI. This finding is consistent with the results reported by Gerardo et al. To elucidate the underlying causes, it has been observed that blood glucose can influence the activity of macrophages [22]. Moreover, a negative correlation between glucose concentration and phagocytosis of MTB was observed when macrophages were cultured in different glucose concentrations [23].

It is well known that the regional variations exist in the occurrence of TB infection. In addition to environmental factors, there is no confirmed evidence suggesting a correlation between ethnicity and TB infection. Haddad et.al has reported the ethnic differences between diabetes and a positive test for TB infection [24]. Our study yielded similar results, indicating that the non-Hispanic population has a significantly lower risk of latent TB infection (LTBI) compared to Hispanic and Asian populations. Therefore, Hispanic and Asian patients with diabetes mellitus (DM) should pay more attention to screening for LTBI.

Interestingly, we identified the male gender and increased age as the consistent risk factors associated with LTBI. Male gender is a well-known risk factor for active TB disease due to the socio-cultural causes as well as biological differences compared to women [25, 26]. Although gender disparity has been investigated in LTBI, there is limited knowledge specifically in DM patients with LTBI. Pradipkumar et. al [27] screened for the prevalence of LTBI in type 2 DM patients in an Indian tertiary care hospital and found male gender to be a risk factor (72% vs 57%; P = 0.033). However, cross-sectional studies from Taipei did not find a gender disparity in patients’ composition [20]. The increase in LTBI prevalence with age is observed in patients with positive QFT-GIT/TST [28, 29]. Chang et.al [20] also found a trend of QFT-GIT positivity increasing after the age of 50 years. In our study, age showed a strong correlation with LTBI infection. Therefore, further randomized controlled trials (RCTs) are necessary to confirm male gender as a risk factor in the DM population, while age can be considered an independent risk factor in DM patients with LTBI.

Several limitations should be considered in our study. Firstly, the cross-sectional nature of the NHANES database used in our research prevents us from establishing a causative association. To verify causality, it is crucial to design more prospective cohort studies. Secondly, our investigation solely relies on the NHANES database, which represents the American population, thereby limiting the generalizability of our findings to other geographical regions. To determine the risk factors for DM with LTBI more comprehensively, additional comprehensive investigations should be conducted, particularly in areas with a high prevalence of tuberculosis. Lastly, while we found an association between poor glucose control and LTBI in the DM population, it's important to note that the p-value was marginally significant (p = 0.05). This could be attributed to the sample size of the population with poor glucose control. Hence, it is recommended to include a larger number of LTBI patients in the DM population in future studies.

In conclusion, our study suggests that poor glucose control is associated with LTBI in individuals with DM. Additionally, male gender, age, and ethnicity are identified as the risk factors for the prevalence of LTBI in DM patients. To further explore the role of poor glucose control in increasing the risk of LTBI and understand the potential underlying mechanisms, it is recommended to conduct future prospective cohort research.

Acknowledgements

Not applicable

Funding

This study was funded by the Basic Research and Frontier Exploration Project of Chongqing Yuzhong District Science &Technology Committee (No: 20180139), the Joint Science Project of Chongqing Science & Technology Committee-Health Bureau (No: 2018MSXM006), and the Medical Talents Program of Chongqing for Young and Middle-aged.

Author contributions

YF analyzed all the data and wrote the manuscript. YF and DT reviewed the literature. LT, XC, and GY collected the raw data. RG assisted in the statistical analysis. RG, JJ, and PW edited and supervised the writing of the manuscript. All authors contributed to the article and approved the submitted version.

Availability of data and materials

This study utilized publicly available data from the National Health and Nutrition Examination Survey. This data can be accessed using the following link: https://www.cdc.gov/nchs/nhanes/index.htm

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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No competing interests reported.

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Association between blood glucose control and risk factors of latent tuberculosis in the population with diabetes: Results from the National Health and Nutrition Examination Survey (NHANES) 2011–2012

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Background

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Background

Methods

Study design and population

Measures and definitions

Covariates

Statistical analysis

Results

Characteristics of Participant

Correlation of LTBI with laboratory and basic parameters in DM patients

LTBI and associated risk factors in DM participants

Discussion

Conclusions

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References

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