CT values of contrast-enhanced CBBCT: A useful diagnostic tool for benign and malignant breast lesions

Abstract

Background

Computed tomography (CT) value studies of cone-beam breast CT (CBBCT) mainly focus on the enhancement value or enhancement rate, and there has been no study on the CT value (Hounsfield units [HU]) of the lesion itself.

Purpose

To investigate the CT values under contrast-enhanced CBBCT (CE-CBBCT) and non-contrast-enhanced CBBCT (NC-CBBCT) in scanning for the differential diagnosis of benign and malignant breast lesions.

Material and Methods

A retrospective analysis was performed on 189 cases of mammary glandular tissues that underwent NC-CBBCT and CE-CBBCT examination. The qualitative CT values of the lesions, standardized Δ(L-A), standardized Δ*(L - G), standardized Δ(L-A) (Post 1st-Pre), and standardized Δ*(L-G) (Post 2nd-Post 1st) between the benign and malignant groups were compared. Prediction performance was evaluated using receiver operating characteristic (ROC) curves.

Results

In total, 58 cases were included in the benign group, 79 cases were included in the malignant group, and 52 cases were included in the normal group. The best diagnostic thresholds of CT values for L (Post 1st-Pre), Δ(L-A) (Post 1st-Pre), and Δ*(L-G) (Post 1st-Pre) were 49.5, 44, and 64.8 HU, respectively. The Δ(L-A) Post-1st rate values of CBBCT had medium diagnostic efficacy (AUC = 0.74, sensitivity = 76.6%, specificity = 69.4%).

Conclusion

CE-CBBCT can improve the diagnostic efficiency of breast lesions compared with NC-CBBCT. The CT values (HU) of lesions do not need to be standardized with fat and can be directly used in clinical differential diagnosis. The first contrast phase (60 s) is recommended to reduce the radiation exposure.

Keywords

Breast value cone-beam breast computed tomography computed tomography

Introduction

In most countries, the incidence of breast cancer is increasing yearly, and breast cancer has become a hot issue of common concern in society (1). The early detection, appropriate treatment, and accurate differentiation between benign and malignant lesions are of great significance to improve the prognosis of breast cancers and can significantly increase the survival rate of patients.

Cone-beam breast computed tomography (CBBCT) is a new three-dimensional (3D) imaging tool for the non-invasive diagnosis of benign and malignant breast lesions. It not only reduces the influence of dense glandular tissue that overlaps lesions but also visualizes blood supply formation in breast lesions through enhanced scanning. The diagnostic value of non-contrast-enhanced (NC-CBBCT) and contrast-enhanced CBBCT (CE-CBBCT) for breast cancer has been gradually recognized by clinicians (2), who believe that the features of CE-CBBCT have unique prospects for the preoperative stage and stratification of risk of breast cancer (3). Moreover, CBBCT is helpful in differentiating benign and malignant lesions as well as histopathological and immunohistochemical subtypes of breast cancer (4). Compared with NC-CBBCT scanning, CE-CBBCT not only increases the display efficiency of pathological morphology but also provides more diagnostic information for the qualitative diagnosis of lesions by enhancing the hemodynamic information (5 –7). For dense breasts, CE-CBBCT is equal to nuclear magnetic resonance imaging (MRI) in diagnostic accuracy. Therefore, CE-CBBCT is considered an alternative examination for patients with contraindications to MRI (8).

However, studies of the CT value (Hounsfield units [HU]) of CBBCT mainly focus on the relative enhancement value or enhancement rate, and there has been no study on the CT value of the lesion itself by direct measurement (9,10). Therefore, the feasibility of evaluating HU values directly in breast lesions was explored in this study, and different parameters of enhanced CT values were analyzed for the differential diagnosis of benign and malignant breast lesions. The CT values of different phases—Δ(L-A) (lesions – fat) and Δ^*(L-G) (lesions – glandular tissues)—were used based on ΔHU (CT value) to obtain the best evaluation index.

Material and Methods

Participants

A retrospective analysis of the data of patients who underwent NC-CBBCT and CE-CBBCT examinations at Guangxi Medical University Cancer Hospital between June 2019 and December 2020 was performed. The inclusion criteria were as follows: (i) NC-CBBCT and CE-CBBCT scans were performed simultaneously, and the breast of the study side was in dual-phase enhanced scan mode (dominant breast); (ii) no biopsy or resection, radiotherapy, chemotherapy, or prosthesis implantation occurred before the examination; and (iii) the diagnoses of benign and malignant lesions were confirmed by gross postoperative pathology or biopsy pathology. There was no palpable mass in the normal control group, and no definitive lesion was found by CBBCT, MRI, ultrasound, or X-ray. This study was reviewed and approved by the ethics committee of Guangxi Medical University Cancer Hospital. All patients signed informed consent before the examination.

Scanning methods

A dedicated breast CT machine (KBCT 1000, Tianjin Corning Medical Equipment Co., Ltd., Tianjin, PR China) was used. This CBBCT system has been approved by the U.S. Food and Drug Administration and the China Food and Drug Administration. The CBBCT tube voltage was 49 kVp, and the tube current was automatically adjusted within the range of 50–160 mA according to the size and density of the patient's glandular tissues as previously published (9,10).

Image analysis

The Koning CT Image Viewer workstation was used to measure the CT values of the images and the CT values (HU) of the lesions, glandular tissues, and fat (in the same layer and on the same side as the lesions if no invasion was observed). For the CT value measurement of imaging, regions of interest (ROIs) were selected at the corresponding location of the same lateral, segment, quadrant, and layer of the breast lesion in different phases (NC-CBBCT and CE-CBBCT scans, ROI area of 5–10 mm²).

The baseline CT values (HU) of CBBCT were measured using the following parameters: precontrast = HU values of NC-CBBCT; first contrast phase = HU values of enhanced scanning was performed in 60 s; and second contrast phase = HU values of enhanced scanning was performed in 110 s. The standardized CT value (HU) values of CBBCT were measured using the following parameters: precontrast-enhanced = non-contrast-enhanced); L (Post 1st-Pre) = standardized HU values of the first contrast-enhanced phase minus the HU values of the precontrast-enhanced phase; L (Post 2nd-Pre) = standardized HU values of the second contrast-enhanced phase minus the HU values of the precontrast-enhanced phase; L (Post 2nd-Post1st) = standardized HU values of the second contrast-enhanced phase minus the HU values of the first contrast-enhanced phase; Δ(L-A) (Post 1st-Pre) = standardized HU values of Δ (lesions – fat) first contrast-enhanced phase – precontrast-enhanced phase; Δ(L-A) (Post 2nd-Pre) = standardized HU values of Δ (lesions – fat) second contrast-enhanced phase – precontrast-enhanced phase; Δ(L-A) (Post 2nd-Post 1st) = standardized HU values of Δ (lesions – fat) second contrast-enhanced phase – first contrast-enhanced phase; Δ^*(L-G) (Post 1st-Pre) = standardized HU values of Δ^* (lesions – gland) first contrast-enhanced phase – precontrast; Δ^*(L-G) (Post 2nd-Pre) = standardized HU values of Δ^* (lesions – gland) second contrast-enhanced phase – precontrast; Δ^*(L-G) (Post 2nd-Post 1st) = standardized HU values of Δ^* (lesions – gland) second contrast-enhanced phase – first contrast-enhanced phase; L(Post 1st rate) = standardized HU values of (1st contrast-enhanced phase – precontrast-enhanced phase)/precontrast × 100%; L(Post 2nd rate 1) = standardized HU values of (2nd contrast-enhanced phase – precontrast-enhanced phase)/precontrast × 100%; L(Post 2nd rate 2) = standardized HU values of (2nd contrast-enhanced phase – 1st contrast-enhanced phase)/1st phase contrast × 100%; Δ(L-A) Post 1st rate = standardized HU values of Δ (lesions – fat) (1st contrast-enhanced phase – precontrast)/precontrast × 100%; Δ(L-A) Post 2nd rate 1 = standardized HU values of Δ (lesions – fat) (2nd contrast-enhanced phase – precontrast)/precontrast × 100%; Δ(L-A) Post 2nd rate 2 = standardized HU values of Δ (lesions – fat) (2nd contrast-enhanced phase – 1st contrast-enhanced phase)/1st contrast-enhanced phase × 100%; Δ^*(L-G) Post 1st rate = standardized HU values of Δ^* (lesions – gland) (1st contrast-enhanced phase – precontrast)/precontrast × 100% (lesions – glands) = (lesions – gland); Δ^*(L-G) Post 2nd rate 1 = standardized HU values of Δ^* (lesions – glands) (2nd contrast-enhanced phase – precontrast)/precontrast × 100%; and Δ^*(L-G) Post-2nd rate 2 = standardized HU values of Δ^* (lesions – gland) (2nd contrast-enhanced phase – 1st contrast-enhanced phase)/1st contrast-enhanced phase × 100%.

Statistical analysis

All the original data were analyzed using SPSS 23.0 statistical software (IBM Corp., Armonk, NY, USA), and the statistical data were expressed as measures of frequency or central tendency and of dispersion or variation. The CT values (HU) of the lesions, Δ(L-A) and Δ^*(L-G), between the benign and malignant groups were statistically analyzed by independent sample t tests and univariate ANOVA tests. The HU values of the fat, glandular tissue, chest wall muscle, and nipple among the benign, malignant, and normal groups were tested by univariate ANOVA. If necessary, the LSD method was used for pairwise comparisons. P < 0.05 was considered significant. The receiver operating characteristic (ROC) curve was analyzed, and the area under the ROC curve (AUC) was used to evaluate its accuracy for benign and malignant diagnoses. The best diagnostic threshold was determined by the Youden index, and the highest point was at the top left of the curve.

Results

A total of 137 patients were enrolled in the study (137 women; mean age = 44.7 ± 10.7 years; 79 patients were enrolled in the malignant group and 58 patients were enrolled in the benign group.

CT values (HU) of the precontrast-enhanced and contrast-enhanced phases between the benign and malignant groups

There were differences in the first contrast-enhanced phase and second contrast-enhanced phase between the benign and malignant groups, and the values of the malignant group were higher than those of the benign group (Fig. 1). There were no significant differences in the HU values of the Δ(L-A) scan between the benign and malignant groups. The Δ^* HU values were significantly different in the precontrast-enhanced CBBCT and first and second contrast-enhanced phase groups between the benign group and malignant group, and the HU values of the malignant group were higher than those of the benign group.

There were significant differences in the HU values of the lesions, Δ(L-A) and Δ^*(L-G), between the benign group and the malignant group using univariate ANOVA (Table 2). Then, the LSD method was used for pairwise comparisons, and the HU values of the lesions, Δ(L-A) and Δ^*(L-G), between the benign and malignant groups showed the following patterns: there were significant differences between the precontrast-enhanced and first contrast-enhanced phases and significant differences between the precontrast-enhanced and second contrast-enhanced phases, while there were no significant differences between the first contrast-enhanced phase and second contrast-enhanced phase (Fig. 2, Supplemental Table 1).

Fig. 1.

Schematic diagram of CT value (HU) measurement of breast lesions, a, b, c axial view; d, e, f coronal view; g, h, i sagittal view. Note: Case of invasive ductal carcinoma in the upper quadrant of the right inner breast: a 53-year-old woman with 77.9 HU in the non-contrast-enhanced CBBCT scan, 120.4 HU in the first contrast-enhancement phase, and 115.7 HU in the second contrast-enhancement phase. CBBCT, cone-beam breast computed tomography; CT, computed tomography.

Fig. 2.

CT value (HU) comparison of different contrast enhancement scanning periods between benign and malignant groups (Precontrast-enhanced equal to non-contrast-enhanced). CT, computed tomography, (a) CT Value of Tumors; (b) Δ CT Value of Tumors; c, Δ* CT Value of Tumors.

Table 1.

Clinical and histopathological characteristics of 189 patients.

Variable	Benign (n = 58)	Malignant (n = 79)	Normal (n = 52)
Age (years)	39.2 ± 11.6	49.3 ± 9.4	43.9 ± 8.5
Median age (years)	41	49	45
Menopausal
Premenopausal	45	42	37
Postmenopausal	13	37	15
Histopathology
	Fibroadenoma (n = 35)	DCIS (n = 8)
	Benign lobular tumor (n = 2)	IDC (n = 48)
	Breast hyperplasia series (n = 12)	IDC + IC (n = 20)
	Inflammatory change (n = 8)	Malignant lobar tumor (n = 1)
	lipoma (n = 1)	Adenoid cystic carcinoma (n = 1)
		Invasive lobular carcinoma (n = 1)

Values are given as n or mean ± SD unless otherwise indicated.

DCIS, ductal carcinoma in situ; IC, intraductal carcinoma; IDC, invasive ductal carcinoma; SD, standard deviation.

Table 2.

Comparison of CT values (HU) of contrast-enhanced CCBCT scans between the benign and malignant groups (transverse comparison and longitudinal comparison).

CT value (HU)	Scan period	Benign	Malignant	P	t value
	Non-enhanced scan	76.2 ± 67.9	83.6 ± 53.2	0.485	−0.7
L	Enhancement phase 1	131.9 ± 80.1	169.53 ± 66.7	0.005	−2.86
	Enhancement phase 2	137.2 ± 77.6	173.3 ± 67.0	0.006	−2.81
	F	10.603	51.26
	P	0.000	0.000
	Non-enhanced scan	210.1 ± 66.4	224.2 ± 39.6	0.165	−1.4
Δ(L-A)	Enhancement phase 1	256.5 ± 81.2	301.9 ± 69.2	0.001	−3.43
	Enhancement phase 2	267.2 ± 76.2	303.6 ± 59.7	0.003	−3.07
	F	8.822	48.635
	P	0.000	0.000
	Non-enhanced scan	9.9 ± 56.2	36.1 ± 32.1	0.001	−3.4
Δ^*(L-G)	Enhancement phase 1	51.6 ± 67.8	114.2 ± 51.2	0.000	−6.01
	Enhancement phase 2	56.7 ± 67.1	115.3 ± 52.4	0.000	−5.62
	F	8.655	75.673
	P	0.000	0.000

A, fat; CBBCT, cone-beam breast computed tomography; CT, computed tomography; G, glandular tissues; L, lesion.

The CT values (HU) of glandular tissues in the precontrast-enhanced and contrast-enhanced phases between the normal, benign, and malignant groups

There were significant differences in the CT values (HU) of the glandular tissue precontrast-enhanced (precontrast-enhanced equal to non-contrast-enhanced) and two contrast-enhanced phases between the normal, benign, and malignant groups. The denser the glandular tissue, the higher the CT value of the glandular tissue (Table 3, Supplemental Table 1). There were no significant differences in the HU values of the fat and chest wall muscle among the three groups.

Table 3.

CT values (HU) of benign, malignant, and normal groups (fat, glandular tissue, chest wall muscle, nipple).

CT value of the same side and layer of the lesion (HU)	Scan period	Benign	Malignant	Normal	F	P
	Non-enhanced scan	−136.4 ± 39.7	−136.8 ± 30.6	−137.8 ± 25.5	0.061	0.941
Fat	Enhancement phase 1	−132.1 ± 40.0	−136.3 ± 31.3	−135.3 ± 29.0	0.29	0.749
	Enhancement phase 2	−137.7 ± 37.5	−130.3 ± 33.9	−135.6 ± 26.3	1.183	0.308
	F	0.297	1.023	0.454
	P	0.744	0.361	0.635
	Non-enhanced scan	68.9 ± 55.3	50.4 ± 47.9	93.2 ± 58.9	17.031	0.000
Glandular tissues	Enhancement phase 1	72.8 ± 59.9	53.9 ± 46.9	93.4 ± 62.7	12.835	0.000
	Enhancement phase 2	72.7 ± 58.6	58.4 ± 44.8	96.1 ± 60.5	13.167	0.000
	F	0.077	0.587	0.132
	P	0.926	0.557	0.877
	Non-enhanced scan	−56.4 ± 38.5	−59.7 ± 42.1	−59.5 ± 51.6	0.103	0.902
Chest wall muscles	Enhancement phase 1	−46.4 ± 35.8	−47.9 ± 43.1	−52.8 ± 53.2	0.296	0.744
	Enhancement phase 2	−46.1 ± 38.0	−44.8 ± 41.2	−47.8 ± 54.7	0.072	0.931
	F	1.283	2.755	0.637
	P	0.28	0.066	0.53
	Non-enhanced scan	247.7 ± 46.5	250.2 ± 46.5	268.4 ± 35.6	3.705	0.026
Nipple	Enhancement phase 1	256.2 ± 46.6	264.0 ± 55.3	274.1 ± 37.6	1.822	0.165
	Enhancement phase 2	359.8 ± 49.4	271.2 ± 59.6	287.4 ± 31.3	4.065	0.019
	F	0.926	0.066	4.066
	P	0.398	0.047	0.019

CT, computed tomography.

There were significant differences in the HU values of the nipple in the precontrast-enhanced and second contrast-enhanced phases among the three groups. There were significant differences in the longitudinal HU values of the nipple between the malignant group and the normal group (Table 3). There were no significant differences in fat, glandular tissue, or chest wall muscle in each phase within each group.

The LSD method was used for pairwise comparison of the glandular tissues between the normal, benign, and malignant groups. Regarding the HU values of glandular tissues, there were significant differences in precontrast-enhanced and dual-phase enhanced CBBCT between the benign and normal groups and the malignant and normal groups, but there were no significant differences between the benign and malignant groups (Supplemental Table 2). In terms of the HU values of the nipple, significant differences were shown in the precontrast-enhanced and second contrast-enhanced phases between the malignant group and the normal group, while there were no significant differences in the other enhanced phases (Supplemental Table 3). The older the patient, the lower the CT value of the glandular tissue (Table 3, Supplemental Table 1).

ROC curves based on the HU values of NC-CBBCT and CE-CBBCT between the benign and malignant groups

L (Post 1st-Pre), Δ(L-A) (Post 1st-Pre), and Δ^*(L-G) (Post 1st-Pre) had the same ROC curve for the differential diagnosis of benign and malignant lesions (both AUC = 0.77). The sensitivity and specificity of L (Post 1st-Pre) were 84% and 57%, respectively. The sensitivity and specificity of Δ(L-A) (Post 1st-Pre) were 86% and 66%, respectively. The sensitivity and specificity of L (Post 2nd-Post 1st), Δ(L-A) (Post 2nd-Post 1st), and Δ^*(L-G) (Post 2nd-Post 1st) differed greatly from each other and were not suitable for the differential diagnosis of benign and malignant lesions (Supplemental Table 4, Fig. 4a).

Using the pathological results as an independent variable, quantifiable HU values were used as the dependent variable to draw the ROC curve. The curves of L (Post 2nd rate 2), Δ(L-A) (Post 2nd rate 2) and Δ^*(L-G) (Post 2nd rate 2) were located below the reference line, while the remaining curves were above the reference line. The Δ(L-A) (Post 1st rate) had higher AUCs for the differential diagnosis of benign and malignant lesions, which were 0.77 and 0.69, respectively. However, the three indices of L (Post 2nd rate 2), Δ(L-A) (Post 2nd rate 2), and Δ^*(L-G) (Post 2nd rate 2) were not suitable for the differential diagnosis of benign and malignant lesions (Supplemental Table 5, Fig. 4b).

Discussion

CBBCT, as a new 3D breast imaging method, is superior to breast mammography (MG) in the coverage of the breast tissue and the comfort level during scanning (11 –14). However, standardized scan protocols and standardized CE-CBBCT acquisition protocols are still lacking (15). Moreover, there are no previous direct evaluations of the CT value of the breast lesion itself. For the first time, we directly evaluated the CT value (HU) of CBBCT for distinguishing benign and malignant breast lesions. The older the patient, the lower the CT value of the glandular tissue. The denser the glandular tissues, the higher the CT value of the glandular tissues.

Prionas et al. (16) proposed using fat normalization to evaluate the degree of enhancement of lesions of CBBCT and found that the mean ΔHU of malignant lesions was 38 HU higher than that of benign lesions, and the AUC of the subjects was 0.876.

In this study, the HU values of CBBCT in lesions were measured directly for the first time, and the HU values of Δ(L-A) and Δ^*(L-G) after normalization were also compared. The results showed that directly measuring the HU values of lesions is feasible, and the HU values of the malignant group were higher than those of the benign group (Table 1, Supplemental Figures 2 and 3). There were no significant differences before or after standardization by Δ(L-A) and Δ^*(L-G) for the differential diagnosis of benign and malignant lesions. The diagnostic efficacy of the HU values was consistent before and after Δ(L-A) standardization (Fig. 4). The HU values of fat tissue in the normal, benign, and malignant groups were not significantly different. Therefore, we suggest that the HU values of breast lesions could be directly measured by radiologists or AI software in the future. Clinicians can directly measure the CT values and do not need to calculate them, which will provide a more convenient auxiliary diagnostic method. Of course, the HU values of lesions, and the Δ(L-A) and Δ^*(L-G) standardized HU values can also be used for analysis to ensure the reliability of image evaluation.

Fig. 3.

CT value (HU) comparison of different contrast enhancement scanning periods between the benign, malignant, and normal groups (Precontrast-enhanced = non-contrast-enhanced CBBCT). CBBCT, cone-beam breast computed tomography; CT, computed tomography, (a) CT Value of Fat; (b) CT Value of Gland Tissues; (c) CT Value of Muscle; (d) CT Value of Nipple.

Fig. 4.

(a) The ROC curve of CT values (HU) between the benign and malignant groups. (b) ROC curves in benign and malignant groups (contrast-enhanced rate). Clinicians can directly measure the CT values and do not need to calculate them, which will provide a more convenient diagnostic method. CT, computed tomography; ROC, receiver operating characteristic.

Different research institutions are inconsistent in the selection of the time phase and enhancement parameters of enhanced scanning images, and there is no standardized and unified scanning scheme or evaluation index of CBBCT at present. In this study, 60 s and 110 s were used for dual-phase enhanced CT. The ROC curve results showed that the L (Post 1st-Pre) CT value, Δ(L-A) (Post 1st-Pre) CT value, and Δ(L-A) (Post 1st rate) were relatively high for the differential diagnosis of benign and malignant lesions, with AUC values of 0.77, 0.77, and 0.74, respectively (Supplemental Tables 4 and 5, Fig. 4).

The optimal dose of contrast agent and the delay from injection to scan have not been determined, and the need for two postcontrast scans has not been evaluated. Uhlig et al. (17) conducted a study of scans taken 2 min and 3 min after contrast agent injection. They argued that a 2-min enhancement could best distinguish malignant and benign breast lesions, but this study did not consider 1 min post enhancement. Seifert et al. (18) performed scans at 20-30 s and 60-70 s. The delay was eventually revised to 80 s because the second postcontrast scan showed only a negligible increase in enhancement over the first. Chen (19) studied changes in the CT values of the lesions and breast structure ΔHU (standardized by fat) at 1 min and 2 min after injection of the contrast agent. A comprehensive analysis showed that the best diagnostic efficiency was obtained after injection of contrast agent for 1 min. The present study also indicates that CE-CBBCT enhancement parameters are of great value in the differential diagnosis of benign and malignant breast lesions. All of the AUCs of the second contrast-enhanced phase (110 s) were lower than those of the first contrast-enhanced phase (60 s) in the HU value of lesions (Supplemental Tables 4 and 5). Therefore, the first contrast-enhanced phase (60 s) is recommended. This will help to reduce the higher radiation exposure caused by the second contrast-enhanced phase.

The present study has some limitations. First, this study used only single-center data, and the sample size was small. Second, as CBBCT is rarely used clinically at this time, there is no standard or guide for the CT value range and its variation rule, which may lead to deviation of results due to the selection of the measurement area of interest. Third, the diagnostic efficacy obtained in this study was slightly low. Therefore, large samples and multipathological data should be collected in the future. With the application of artificial intelligence, it is hoped that with the wider clinical application of CBBCT, a standardized scan collection scheme and standard guidelines will be formulated.

In conclusion, compared with non-contrast-enhanced CT, CE-CBBCT can improve the diagnostic efficiency of breast lesions. Enhanced CT value parameters can improve the differential diagnosis of benign and malignant breast lesions. The CT value of lesions does not need to be standardized with fat and can be directly used for clinical studies. The first contrast-enhanced phase (60 s) is recommended to reduce radiation exposure.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Guangxi Clinical Research Center for Medical Imaging Construction (Grant No. Guike AD20238096), the National Natural Science Fund of China (No. 32260241), Guangxi University middle-aged and young teachers’ basic scientific research ability improvement project (No. 2019ky0140), the self-financing research of the Health Department of Guangxi Autonomous Region (Grant No. Z20200803, Z20210631), Basic Ability Improvement Project for Young and Middle-aged Teachers of Guangxi Colleges and Universities (No. 2023KY0127), and Guangxi Medical and Health Appropriate Technology Development and Promotion Application Project (No. S2022123), and Joint Project on Regional High-Incidence Diseases Research of Guangxi Natural Science Foundation (No. 2023GXNSFBA026035).

ORCID iDs

Xian Lin Yi

DanKe Su

Supplemental Material

Supplemental material for this article is available online.

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