ABSTRACT
Regular, comprehensive, and effective cost analyses of immunization services are essential for evaluating whether current policy subsidies are suitable for these services. However, such studies are relatively limited in China. This study is the first comprehensive investigation of the costs of immunization services in Guangzhou City. Through stratified random sampling, we selected 84 vaccination clinics covering 11 administrative districts, including routine, adult, and rabies vaccination clinics. Investigate the vaccination service costs of various types of outpatient clinics. The cost investigation adopts the top – down full cost method to examine the labor costs, operating costs, and fixed – asset depreciation costs of each vaccination unit. In addition, it is need to clarify that vaccine procurement costs were not included in the scope of this cost analysis. Key findings revealed that the costs per dose (293.70 CNY,$41.66) and per person (433.96 CNY,$61.55) were significantly higher at adult vaccination clinics than routine vaccination clinics (per dose: 64.88 CNY($9.20); per person: 153.66 CNY($21.80)) and rabies vaccination clinics (per dose: 252.15 CNY($35.77); per person: 867.13 CNY($123.00)). For all surveyed vaccination units, labor costs accounted for the largest proportion of total costs (75.02%), and was followed by operational costs (19.67%) and fixed assets (5.31%). Univariate and multivariate regression analyses identified several factors influencing service costs. An increase in the standard number of staff per week was associated with higher vaccination service costs. Factors associated with lower vaccination service costs included clinics that were privately operated, served larger population sizes, offered services on more days per week, or had moderate to large vaccination areas. This comprehensive analysis provides valuable insights for optimizing resource allocation, improving vaccination accessibility across the life course, and informing policy development to support sustainable immunization programs.
KEYWORDS: Vaccination service, cost analysis, investigation, resource allocation, Guangzhou city
Introduction
Since the implementation of the immunization program in 1978, China has made remarkable achievements in vaccination.1,2 Vaccination remains the most economical and effective measure to prevent and control infectious diseases3,4; as public awareness of disease prevention has increased, vaccination services have expanded to cover the entire lifespan. In China, governmental funding is the primary source of financial support for vaccination programs. With the continued expansion of immunization planning, the scope of work and task volume have increased, and the corresponding costs of vaccination services have dynamically changed. These cost dynamics are consistent with the costing described in frameworks such as the World Health Organization’s Comprehensive Multi-year Plan (cMYP), which emphasizes sustainable vaccine delivery through standardized cost tracking.5 Ensuring reasonable cost input is crucial for maintaining high-quality immunization services, and regular monitoring and analysis of these cost changes are essential for optimizing policy formulation and funding allocation decisions.6,7
Internationally, the cost of vaccine delivery in Southeast Asian countries was $1.35 (US$0.40-US$3.48)8; the cost of vaccine delivery in Tanzania was US$1.38 per dose7; and the full course of vaccination in India ranged from US$20.08 to US$34.81.9 However, specific research examining the costs of preventive vaccination services in China is limited. Existing evidence includes only a few studies, such as those reporting vaccination service costs at 27.4 CNY($3.89) per dose in Shenzhen (2015) and 18.84 CNY($1.25) per dose in Chengdu (2016). Additionally, most of the existing literature has focused on cost estimates for basic public health services.10,11 Existing data span wide timeframes and cannot accurately reflect the current real-world complexity. The cost of vaccination services is influenced by multiple factors, including regional economic development levels and the operational models of various types of vaccination institutions. Moreover, the emergence of new circumstances, such as the recent decline in birth rates in China12 and the gradually increasing demand for adult vaccinations,13 may lead to changes in the current costs of preventive vaccination services. Therefore, there is an urgent need to conduct a timely and comprehensive cost assessment and recalculate the cost structure of vaccination services to establish baseline data and provide information for the government to promptly adjust the distribution patterns and resource allocation of various types of clinics.
Currently, Guangzhou has 257 routine, 74 adult, and 153 rabies vaccination clinics, which deliver 8.4, 0.36, and 0.97 million doses annually, respectively, according to 2023 data. This survey on vaccination cost services encompasses three distinct clinic types: routine, adult, and rabies vaccination clinics – including both public and private establishments. This study aims to estimate the unit costs of vaccination services in Guangzhou and explore how clinic type and operational characteristics influence service costs. To the best of our knowledge, this research is the first city-wide specialized survey on the cost of vaccination services carried out in Guangzhou, China. This study provides useful baseline data on service delivery costs, which can indirectly inform policy decisions, particularly around clinic configuration and personnel planning.
Method
Questionnaire design
This study used the self-designed Guangzhou Vaccination Service Cost Survey Questionnaire,investigate the delivery cost of vaccination services in Guangzhou in 2023. In the early stages of questionnaire design, we referred to the WHO guidelines on immunization costs, and relevant domestic and international literature on cost surveys, and we conducted small-scale field pre-surveys and in-depth interviews. The final version of the questionnaire was optimized and determined on the basis of advice from professionals and experts, as well as on-site research findings. Details regarding the questionnaire items are provided in Supplementary Figure S1.
Sample selection and sample size calculation
The study targeted all public and private clinics providing vaccination services in Guangzhou. Inclusion criteria were: (1) clinics officially registered with the local health authority; (2) clinics open to the general public; and (3) clinics that had been in operation for at least one year prior to the study. Exclusion criteria included: (1) outpatient clinics that are only for certain people to be vaccinated (e.g., foreign nationals, collective organizations); and (2) vaccination clinics operating for less than one year. The sample size for this study was determined using a two-pronged approach that combines preliminary statistical estimation with methodological principles specific to costing studies. First, according to the literature review6 and preliminary survey results, the sample size was calculated using the formula for cross-sectional quantitative data. The significance level (α) was set at 0.05, the allowable error (δ) was set at 10, and Z1-α/2 = 1.96. The expected variability in cost per dose, represented by the standard deviation from the preliminary survey (SD = 40.79 CNY), which reflects the underlying heterogeneity in service costs across clinics, was used as a key input in the sample size calculation. A higher value of standard deviation implies a larger required sample size to achieve greater statistical precision and power. This yielded an initial sample size calculation of 64 vaccination units. Secondly, in cost research, especially in the field of immunization service delivery, it is emphasized that there is a need to comprehensively consider the diverse characteristics of the operating environment, cost structure, and service models, rather than focusing solely on statistical sampling based on variability and power calculations. These sampling decisions are supported by previous immunization costing studies.9,14 As stated in the consensus statement on vaccine delivery costs led by the World Health Organization and related literature,6,8,15 the adequacy of samples in cost research should be judged based on cost relevance (i.e., including cost drivers that influence differences) and saturation logic (i.e., covering all meaningful differences among various facility types, ownership models, and service environments). Therefore, cost accounting research at the facility level needs to focus on the diversity of service models, operating environments, and cost structures. We further optimized the sampling strategy, highlighting the differences in cost relevance and diversity saturation among clinic types and attributes. A stratified random sampling design was used to cover three types of clinics (general clinics, adult clinics and rabies specialty clinics) in 11 administrative districts, taking into account factors such as different sizes, service radius and public and private medical institutions. The final sample size was expanded to 84 clinics, aiming to ensure the representativeness of different service scenarios, maximize the display of differences in cost drivers, and improve the external validity of the research. In addition, our sample size also includes vaccine inoculation clinics with high and low inoculation doses, which not only ensures that cost outliers are fully presented, but also more comprehensively reflects the cost differences under different service models. The final sample of 84 medical institutions not only meets the needs of statistical estimation, but also fully presents the diverse characteristics of various immunization service models and cost structures. The distribution of vaccination clinic types is provided in Supplementary Table S1. This survey was sent through the government system to contact all units for cooperation, and all the selected vaccination units cooperated to complete this survey.The sampled proportions by clinic type and attribute were consistent with the overall distribution of vaccination clinic types and attributes in Guangzhou.
Cost calculation
In this study, cost refers to the cost incurred during the vaccination service from the perspective of the vaccination unit, that is, the cost of service provision. Therefore, the cost in this study does not include the cost of the vaccine itself. This investigation divides the total cost into three categories: labor cost, operating cost, and fixed asset depreciation. The calculation of labor costs incorporates the ‘standard manpower’ method. This concept is adapted from the Full-Time Equivalent (FTE) approach used in human resource cost accounting,16 implemented to address the complex and nonstandard staffing arrangements across vaccination clinics. The number of standard manpower refers to the number of personnel required to complete all vaccination tasks scheduled for a given day, based on the clinic’s operational workflow and daily practices. Clinics are required to report weekly the actual standard manpower needed for each morning/afternoon session, distinguishing between workdays and non-workdays. Combined with clinic-specific staff compensation data, this metric allows for the calculation of daily labor costs and enables the aggregation of total labor costs. The labor cost accounting framework aligns with the full costing methodology. Operating cost includes the total of relevant expenses such as rent, daily work consumption (electricity, water, transportation, etc.) and office supplies. Fixed asset depreciation is calculated using the straight-line method. The useful life of each asset type was determined according to China’s national accounting standards for public health institutions (e.g., 5 years for medical equipment, 10 years for infrastructure). The specific composition details of the above three types of costs can be found in the text description part of Supplementary Figure S1. For shared costs, allocation was based on the proportion of square footage used for immunization services relative to the total clinic area. This approach is consistent with WHO’s costing guidelines for immunization programs.6 The cost per dose is the total cost of the vaccination unit in 2023/the number of vaccination doses in 2023, and the cost per person is the total cost of the vaccination unit in 2023/the number of vaccinated people in 2023. All costs are expressed in 2023 Chinese Yuan (CNY). To facilitate international comparison, costs have been converted into US dollars (USD) using the annual average exchange rate of 7.05 (CNY to USD) for 2023.
Survey method
The survey implementation involved questionnaire training, questionnaire completion, and rigorous quality control. During the questionnaire completion process, investigators from the Center for Disease Control (CDC) provided guidance and explanations to the personnel responsible for filling out the forms at the investigated vaccination units, and informed them of standardized methods and precautions. The questionnaires were jointly completed through consultation of financial records by public health personnel and financial staff at the vaccination clinics who had received standardized training, to avoid subjective biases in the data.The questionnaires were conducted through both online and offline methods. Cost data were primarily collected through a hybrid approach that combined official financial records and structured interviews. Specifically, data such as staff salaries, utility bills, clinic operating expenses, and vaccination volume were directly extracted from official financial and operational records maintained at each clinic. In contrast, operational details including weekly staff allocation, manpower per session were obtained through in-person or telephone interviews with clinic personnel. To ensure data reliability, all cost data underwent a two-step verification process. First, clinic staff were instructed to extract cost values directly from official financial records, including ledgers, salary registers, and utility bills. Second, trained CDC investigators reviewed each questionnaire for internal consistency and cross-checked the submitted figures with source documents where available. In cases of discrepancy or missing data, follow-up telephone calls or on-site verification visits were conducted. This approach ensured that cost figures aligned with underlying financial records and minimized reporting bias. The complete analytical workflow is illustrated in Figure 1. All questionnaires were compiled into standardized datasets using Microsoft Excel 2017 (Microsoft Corp., Redmond, WA, USA), and all subsequent cost analyses were performed using SPSS (IBM Corp.) software.
Figure 1.

Flowchart of the vaccination cost analysis survey in Guangzhou city.
Statistical analysis
Baseline characteristics across all vaccination clinics were described using descriptive statistics, with continuous variables reported as mean ± standard deviation for normally distributed data and median ± interquartile range for non-normally distributed data, while categorical variables were described as frequencies and percentages. Specific statistical tests were applied as follows: Kruskal-Wallis H test for comparing three clinic types with non-parametric continuous variables, Mann-Whitney U test for pairwise comparisons (public vs. private clinics) with non-parametric continuous variables, and chi-square test for categorical variables comparisons. Univariate linear regression was used for preliminary screening of cost-influencing factors, and multivariate linear regression with backward selection was used to establish adjusted models. Prior to regression modeling, we assessed key assumptions. The Durbin-Watson test was employed to examine autocorrelation among the independent variables. Multicollinearity was examined using the variance inflation factor (VIF), with all independent variables showing VIF < 5, indicating no serious multicollinearity. Normality of residuals was evaluated using histograms and P-P plots, and homoscedasticity was assessed by plotting standardized residuals against predicted values. All diagnostic checks indicated acceptable adherence to regression assumptions. All cost data were analyzed in their original scale without transformation. The skewness of cost distributions was assessed through visual inspection of histograms and quantile-quantile (Q-Q) plots. Although the data exhibited moderate skewness, we retained the original scale for interpretability, as the central limit theorem and the moderate sample size (n = 84 clinics) support the robustness of linear regression. To account for operational logic differences among three types of vaccination clinics, we employed a linear mixed-effects model with clinic type as a random intercept. Fixed effects included clinic attributes, service radius, number of people served, etc, while the random component captured unobserved variance specific to each clinic type. To test the robustness of the findings, we performed two sensitivity analyses: (1) Labor costs were adjusted, assuming a 5%-20% change in labor costs, and total service costs were reassessed; and (2) we excluded clinics in the top 5% of cost per dose and cost per person distributions to determine the influence of high-cost outliers on the regression results. All analyses were performed using SPSS 26.0 (IBM Corp.) with statistical significance set at P < .05, and graphical representations were created using GraphPad Prism 8.0. Model performance was evaluated using R2 and diagnostic residual plots (see Results section and Supplementary Table S2–S3, Figures S2-S4,Figures S5-S7).
Results
The basic information for the vaccination clinics in this sample survey is shown in Table 1. Routine immunization clinics had the smallest service radius (4.00 ± 3.00 km), and were followed by rabies vaccination clinics (5.00 ± 7.75 km) and adult vaccination clinics (10.00 ± 21.77 km), Compared to routine immunization clinics, the differences were P < .05 for rabies clinics and P < .01 for adult clinics. Rabies vaccination clinics had significantly longer service hours (operating 7 days per week) than the other two types of clinics (P < .001 for both). Routine immunization clinics had the largest vaccination area (210 ± 97.00 square meters), and were followed by adult vaccination clinics (184.63 ± 117.08 square meters), whereas rabies vaccination clinics had the smallest area (62.97 ± 44.98 square meters). Compared to routine immunization clinics, the differences were P < .05 for adult clinics and P < .01 for rabies clinics. In contrast, public clinics covered a significantly larger population (7.66 ± 7.39 ten thousand people) than private clinics (5.87 ± 4.43 ten thousand people) (P < .01), but offered significantly fewer average service days (4.00 ± 2.75 days) than private clinics (5.00 ± 2.80 days) (P = .01).
Table 1.
Basic information for vaccination service cost survey sites in Guangzhou.
| Basic Information | Total | Routine Immunization Clinic | Adult Vaccination Clinic | Rabies Vaccination Clinic | Kruskal-Wallis H | p-Value | Public Clinic | Private Clinic | Mann-Whitney U | p-Value |
|---|---|---|---|---|---|---|---|---|---|---|
| Service radius | 5.00 (2.50,7.00) | 4.00 (2.00,5.00) | 10.00 (5.00,25.00) | 5.00 (5.00,15.00) | 14.59 | <.01 | 5.00 (2.45,7.50) | 4.00 (2.38,5.75) | 517.00 | .31 |
| Service days (per week) |
4.00 (4.00,6.00) | 4.00 (4.00,5.00) | 4.00 (3.00,6.00) | 7.00 (7.00,7.00) | 39.31 | <.001 | 4.00 (4.00,6.00) | 5.00 (4.00,7.00) | 900.50 | .01 |
| Covered population (per 10,000 population) |
7.34 (5.00,11.54) | 7.10 (5.00,9.59) | 6.00 (1.40,16.74) | 11.54 (6.68,17.67) | 5.19 | .08 | 9.16 (5.60,13.52) | 5.68 (2.16,7.80) | 370.50 | <.01 |
| Vaccination area (square meters) |
180.00 (108.00,247.00) | 210.50 (163.00,200.00) | 120.00 (98.50,200.00) | 56.00 (24.25,88.90) | 37.39 | <.001 | 180.00 (105.00,256.26) | 164.80 (103.50,215.43) | 584.00 | .37 |
We conducted a comprehensive survey to collect data on the educational backgrounds, professional expertise, and professional titles of all staff members working in vaccination units (results in Table 2). The distribution of employees’ educational qualifications was concentrated at the bachelor’s degree level (68.96%), followed by junior college (23.41%), technical secondary school (4.61%), and graduate degree or above (3.02%). Compared with other clinics, routine immunization clinics had higher percentages of staff with bachelor’s degrees (74.28%) and engaging in preventive medicine (32.15%) (P < .001 for both). In contrast, adult vaccination clinics and rabies vaccination clinics had more personnel specialized in clinical medicine (30.43% and 34.63%, respectively; P values < 0.001 for both). Most staff across all sampled vaccination clinics held intermediate and junior professional titles (total proportion of 91.70%). Regarding employment status, the proportion of nonpermanent staff was significantly higher at adult vaccination clinics (81.16%) than the other two types of clinics (P < .001 for both). In contrast, public vaccination clinics, compared with private vaccination clinics, had higher percentages of employees with bachelor’s degrees (75.16%) and permanent positions (69.33%) (P < .001 for both). However, private clinics had significantly higher percentages of nurses (62.78%) and staff with junior titles (57.14%) than public clinics (P < .001 for both).
Table 2.
Personnel information obtained for the various surveyed vaccination clinic types in Guangzhou.
| Personnel Information Conditions | Total | Routine Immunization Clinic | Adult Vaccination Clinic | Rabies Vaccination Clinic |
x2 | p-Value | Public Clinic | Private Clinic | x2 | p-Value | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Education Level | Technical secondary school | 55 (4.61%) | 35 (4.59%) | 10 (14.49%) | 10 (2.77%) | 50.78 | <.001 | 24 (2.59%) | 31 (11.65%) | 94.91 | <.001 |
| Junior college | 279 (23.41%) | 146 (19.16%) | 20 (28.99%) | 113 (31.30%) | 176 (19.01%) | 103 (38.72%) | |||||
| Bachelor’s degree | 822 (68.96%) | 566 (74.28%) | 36 (52.17%) | 220 (60.94%) | 696 (75.16%) | 126 (47.37%) | |||||
| Graduate degree or above | 36 (3.02%) | 15 (1.97%) | 3 (4.35%) | 18 (4.99%) | 30 (3.24%) | 6 (2.26%) | |||||
| Major | Preventive medicine | 269 (22.57%) | 245 (32.15%) | 8 (11.59%) | 16 (4.43%) | 154.86 | <.001 | 236 (25.49%) | 33 (12.41%) | 29.96 | <.001 |
| Nursing | 636 (53.36%) | 390 (51.18%) | 36 (52.17%) | 210 (58.17%) | 469 (50.65%) | 167 (62.78%) | |||||
| Clinical medicine | 241 (20.22%) | 95 (12.47%) | 21 (30.43%) | 125 (34.63%) | 181 (19.55%) | 60 (22.56%) | |||||
| Other | 46 (3.86%) | 32 (4.20%) | 4 (5.80%) | 10 (2.77%) | 40 (4.32%) | 6 (2.26%) | |||||
| Professional Title | Junior professional title | 521 (43.71%) | 321 (42.13%) | 30 (43.48%) | 171 (47.37%) | 16.83 | <.01 | 370 (39.96%) | 152 (57.14%) | 25.79 | <.001 |
| Intermediate professional title |
572 (47.99%) | 386 (50.66%) | 30 (43.48%) | 157 (43.49%) | 477 (51.51%) | 96 (36.09%) | |||||
| Associate senior professional title or above | 92 (7.72%) | 50 (6.56%) | 6 (8.70%) | 31 (8.59%) | 72 (7.78%) | 15 (5.64%) | |||||
| Non-titled | 7 (0.59%) | 5 (0.66%) | 3 (4.35%) | 2 (0.55%) | 7 (0.76%) | 3 (1.13%) | |||||
| Employment Status* | Established post | 656 (55.03%) | 475 (62.33%) | 13 (18.84%) | 168 (46.54%) | 63.47 | <.001 | 642 (69.33%) | 14 (5.26%) | 340.16 | <.001 |
| Non-established post | 536 (44.97%) | 287 (37.66%) | 56 (81.16%) | 193 (53.46%) | 284 (30.67%) | 252 (94.74%) | |||||
*Established post = permanent staff positions,Non-established post = contract positions.
Figure 2(A–C) show the average labor, operational, and fixed assets per clinic for the three types of vaccination clinics. Compared to routine vaccination clinics, adult vaccination clinics exhibited the lowest labor cost (1.22 million CNY($173,049.65) vs. 0.56 million CNY ($79,432.62), P < .001). Routine vaccination clinics incurred the highest operational and fixed costs, amounting to 0.34 million CNY ($48,227.27) and 0.09 million CNY($12,765.96), respectively. In contrast, rabies vaccination clinics had the lowest costs in both categories, at 0.12 million CNY ($17,021.28) and 0.04 million CNY($5,673.76), respectively (P < .001 for both). Adult vaccination clinics showed intermediate levels, with operational and fixed costs of 0.23 million CNY ($32,624.11)and 0.05 million CNY($7,092.20), respectively (P < .05 for both). Among the surveyed vaccination clinics, labor costs accounted for the highest proportion of total costs (75.02%), and was followed by operating costs and fixed assets (19.67% and 5.31%, respectively; Figure 2(F)). The average cost per dose and per person, with the number of vaccination doses or the number of vaccinated individuals in 2023 as the denominator, were compared among vaccination clinic types. The average cost per dose and per person were lowest in routine vaccination clinics (64.88 CNY($9.20) and 153.66 CNY($21.80), respectively), followed by rabies vaccination clinics [252.15 CNY($35.77) (P < .001) and 867.13 CNY($123.00) (P < .05), respectively]. The costs were highest for adult vaccination clinics (293.70 CNY($41.65) and 433.96 CNY($61.55), respectively; P < .001) (Figures 2(D–E)).
Figure 2.

Cost and cost composition of different types of outpatient vaccination services. Labor costs (A), operating costs (B), fixed assets (C), cost per doses (D), and cost per person (E), by vaccination clinic type. Cost composition of various vaccination clinic types (F).
VC = vaccination clinic, **P < .05; ***P < .001 (compared with group A); △P < .05 (compared with group B).
Private routine vaccination clinics had lower labor costs (133.49 thousand CNY($133,490.00) vs. 84.42 thousand CNY($11,977.30)), lower costs per dose (71.54 CNY($10.15) vs. 43.39 CNY($6.15)), and lower per person costs (171.32 CNY($24.30) vs. 96.61 CNY($13.70)) than public clinics (all P < .01; Figure 3(A, D-E)).
Figure 3.

Comparative analysis of clinic vaccination service costs by institutional attributes. Labor costs (A), operating costs (B), fixed assets (C), cost per doses (D), and cost per person (E), by vaccination clinic attributes.
VC = vaccination clinic, **P < .05; ***P < .001 (compared with group A); △P < .05 (compared with group B).
Furthermore, we conducted univariate and multivariate analyses to identify the factors influencing the average cost per dose (Table 3) and average cost per person (Table 4) at the vaccination clinics. Prior to conducting multiple linear regression, we performed diagnostics to verify the model’s underlying assumptions. Durbin-Watson test statistics of 2.088 and 2.168 for the per-dose cost and per-visit cost models, respectively, indicated an absence of autocorrelation. All variance inflation factor (VIF) values remained below 5, confirming no evidence of multicollinearity among independent variables (see Supplementary Table S2 and S3). Normality of residuals was evaluated using histograms and P-P plots, and homoscedasticity was assessed by plotting standardized residuals against predicted values (see Supplementary Figures S2-S4, Figures S5-S7). The R2 values for the final multivariate linear regression models were 0.532 for cost per dose and 0.525 for cost per person, indicating a satisfactory level of model fit. The inclusion of R2 values and residual diagnostic plots further supports the robustness and validity of our regression analyses.
Table 3.
Factors influencing vaccination cost per dose in Guangzhou.
| Univariate Linear Regression Analysis |
Multiple Linear Regression Analysis |
|||||
|---|---|---|---|---|---|---|
| Variable | β | P | β | P | 95.0% Confidence Interval |
|
| Lower Bound | Upper Bound | |||||
| Vaccination Clinic Type | ||||||
| Routine vaccination clinic (Ref.) | / | / | / | / | / | / |
| Adult vaccination clinic | 228.81 | <.001 | 282.88 | <.001 | 176.03 | 389.72 |
| Rabies vaccination clinic | 187.26 | <.001 | 353.90 | <.001 | 217.54 | 490.26 |
| Vaccination Clinic Attributes | ||||||
| Public clinic (Ref.) | / | / | / | / | / | / |
| Private clinic | −30.44 | .49 | −84.40 | .02 | −157.43 | −11.38 |
| Coverage population (per 10,000 population) | 1.10 | .67 | −5.11 | .02 | −9.55 | −0.68 |
| Responsibility service radius (kilometers) | 5.08 | <.001 | 2.79 | .01 | 0.66 | 4.92 |
| Service days (per week) | 10.89 | .45 | −58.03 | <.01 | −100.76 | −15.30 |
| Standard Manpower (per week) | −2.72 | .09 | 5.52 | <.01 | 2.37 | 8.65 |
| Vaccination area*(square meters) | ||||||
| Relatively small area (Ref.) | / | / | / | / | / | / |
| Relatively medium area | −91.25 | .04 | −84.34 | <.01 | −145.70 | −22.99 |
| Relatively large area | −110.56 | .03 | −93.05 | .02 | −171.76 | −14.33 |
*Classification of vaccination area is based on tertiles of the percentile values for the area among vaccination clinic types as a reference standard.
Table 4.
Factors influencing vaccination cost per person in Guangzhou.
| Univariate Linear Regression Analysis |
Multiple Linear Regression Analysis |
|||||
|---|---|---|---|---|---|---|
| Variable | β | P | β | P | 95.0% Confidence Interval |
|
| Lower Bound | Upper Bound | |||||
| Vaccination clinic type | ||||||
| Routine vaccination clinic (Ref.) | / | / | / | / | / | / |
| Adult vaccination clinic | 280.30 | .04 | 543.13 | .001 | 227.69 | 858.57 |
| Rabies vaccination clinic | 713.47 | <.001 | 831.14 | <.001 | 606.72 | 1055.57 |
| Vaccination clinic attributes | ||||||
| Public clinic (Ref.) | / | / | / | / | / | / |
| Private clinic | −145.32 | .24 | −355.72 | <.01 | −572.15 | −139.28 |
| Coverage population (per 10,000 population) | 4.72 | .52 | −14.97 | .04 | −28.83 | −1.11 |
| Responsibility service radius (kilometers) | 9.78 | .01 | / | / | / | / |
| Service days (per week) | 112.36 | <.01 | / | / | / | / |
| Standard manpower (per week) | −1.81 | .69 | 10.46 | .02 | 1.89 | 19.02 |
| Vaccination area* (square meters) | ||||||
| Relatively small area (ref.) | / | / | / | / | / | / |
| Relatively medium area | −310.30 | .01 | −304.01 | .002 | −496.05 | −111.97 |
| Relatively large area | −348.56 | .01 | −325.74 | <.01 | −566.56 | −84.93 |
*Classification of vaccination area is based on tertiles of the percentile values for the area among vaccination clinic types as a reference standard.
Multivariate analysis indicated that the adjusted average cost per dose at adult and rabies vaccination clinics was higher than that at routine vaccination clinics, by 282.88 CNY ($40.12) (β = 282.88, 95% CI: 176.03–389.72, P < .001) and 353.90 CNY ($50.20) (β = 353.90, 95% CI: 217.54–490.26, P < .001), respectively. Private clinics had average costs per dose 84.40 CNY ($11.97) less than those of public clinics (β = −84.40, 95% CI: −157.43 to −11.38, P = .02). For every additional 10,000 people covered by clinics, the cost decreased by 5.11 CNY($0.72) (β = −5.11, 95% CI: −9.55 to −0.68, P = .02). For each additional kilometer in clinic service radius, the cost per dose increased by 2.79 CNY ($0.40) (β = 2.79, 95% CI: 0.66–4.92, P = 0.01). Each additional clinic service day per week decreased the cost per dose by 58.03 CNY($8.23) (β = −58.03, 95% CI: −100.76 to −15.30), P < .01), and each additional standard manpower per week increased the cost per dose by 5.52 CNY ($0.78) (β = 5.52, 95% CI: 2.37–8.65, P < .01). Clinic service area was categorized into three levels. Clinics covering moderate or large areas had lower cost per dose than those covering small areas (cost savings of 84.34 CNY ($11.96) (β = −84.34, 95% CI: −145.70 to −22.99, P < .01) and 93.05 CNY ($13.20) (β = −93.05, 95% CI: −171.76 to −14.33, P = .02), respectively).
Multivariate analysis demonstrated that the adjusted average cost per person at adult and rabies vaccination clinics was higher than that at routine vaccination clinics, by 543.13 CNY($77.04) (β = 543.13, 95% CI: 227.69–858.57, P = .001) and 831.14 CNY ($117.89) (β = 831.14, 95% CI: 606.72–1055.57, P < .001), respectively. Private clinics had an average cost per person 355.72 CNY($50.46) less than that at public clinics (β = −355.72, 95% CI: −572.15 to −139.28, P < .01). For each additional standard manpower per week increased the cost per person by 10.46 CNY($1.48) (β = 10.46, 95% CI: 1.89–19.02, P = .02). Clinic service area was categorized into three levels, and clinics covering moderate or large areas were found to have lower costs per person than clinics covering small areas (cost savings of 304.01 CNY($43.12) (β = −304.01, 95% CI: −496.05 to −111.97, P = .002) and 325.74 CNY($46.20) (β = −325.74, 95% CI: −566.56 to −84.93, P < .01), respectively). A mixed linear model analysis was conducted to determine the factors influencing the average cost per dose and the average cost per person in the vaccination clinics, as shown in Table 5. The results of mixed linear model test are generally consistent with those of multiple linear regression model test. Compared with the public vaccination clinics, the average cost per dose in the private vaccination clinics decreased by 85.9 CNY($12.18) (β = −84.40, 95% CI: −155.02 to −16.88, P = .015). For every additional 10,000 people receiving clinic services, the cost decreased by 4.93 CNY ($0.70)(β = −4.93, 95% CI: −9.15 to −0.72, P = .022). For every additional kilometer of the clinic service radius, the cost per dose increased by 2.94 CNY($0.42) (β = 2.94, 95% CI: 0.92–4.95, P = .005). For every additional clinic service day per week, the cost per dose decreased by 50.26 CNY($7.13) (β = −50.26, 95% CI: −89.44 to −11.01, P = .001), while for every additional standard manpower per week, the cost per dose increased by 5.13 CNY($0.81) (β = 5.13, 95% CI: 2.17–8.09, P = .001). The clinic service areas are divided into three grades, and the average cost per dose in the clinics covering medium or larger areas is lower than that in the clinics covering smaller areas, saving 96.70 CNY($13.72) (β = −96.70, 95% CI: −171.11 to −22.29, P = .012) and 85.80 CNY(($12.17) (β = −85.80, 95% CI: −144.16 to −27.44, P = .004), respectively. Compared with the public vaccination clinics, the average cost per person in the private vaccination clinics decreased by 310.77 CNY ($44.08) (β = −310.77, 95% CI: −525.41 to −96.14, P = .005). For every additional 10,000 people receiving clinic services, the cost decreased by 15.66 CNY($2.22) (β = −15.66, 95% CI: −28.78 to −2.54, P = .020), while for every additional standard manpower per week, the cost per dose increased by 13.67 CNY($1.94) (β = 13.67, 95% CI: 4.49–22.85, P = .004). The clinic service areas are divided into three grades, and the average cost per dose in the clinics covering medium or larger areas is lower than that in the clinics covering smaller areas, saving 312.12 CNY($44.27) (β = −312.12, 95% CI: −543.31 to −80.93, P = .009) and 285.22 CNY($40.46) (β = −285.22, 95% CI: −466.93 to −103.51, P = .003), respectively.
Table 5.
Analysis of factors affecting average agent cost and number of agents cost by mixed linear model.
| Variable | β | SE | t-Value | P | 95.0% Confidence Interval |
|
|---|---|---|---|---|---|---|
| Lower Bound | Upper Bound | |||||
| Cost per Dose | ||||||
| Intercept | 432.761 | 124.232 | 3.512 | .005 | 159.700 | 705.822 |
| Vaccination Clinic Attributes | ||||||
| Public clinic (Ref.) | / | / | / | / | / | / |
| Private clinic | −85.947 | 34.689 | −2.478 | .015 | −155.017 | −16.878 |
| Coverage population (per 10,000 population) | −4.931 | 2.116 | −2.330 | .022 | −9.146 | −0.716 |
| Responsibility service radius (kilometers) | 2.935 | 1.014 | 2.894 | .005 | 0.916 | 4.954 |
| Service days (per week) | −50.262 | 19.67 | −2.555 | .013 | −89.436 | −11.088 |
| Standard Manpower (per week) | 5.132 | 1.486 | 3.454 | .001 | 2.174 | 8.089 |
| Vaccination area*(square meters) | ||||||
| Relatively small area (Ref.) | / | / | / | / | / | / |
| Relatively medium area | −96.703 | 37.370 | −2.588 | .012 | −171.112 | −22.294 |
| Relatively large area | −85.801 | 29.301 | −2.928 | .004 | −144.160 | −27.442 |
| Cost per person | ||||||
| Intercept | 811.146 | 355.574 | 2.281 | .042 | 36.312 | 1585.981 |
| Vaccination Clinic Attributes | ||||||
| Public clinic (Ref.) | / | / | / | / | / | / |
| Private clinic | −310.772 | 107.805 | −2.883 | .005 | −525.407 | −96.136 |
| Coverage population (per 10,000 population) | −15.661 | 6.588 | −2.377 | .020 | −28.783 | −2.540 |
| Responsibility service radius (kilometers) | 5.103 | 3.154 | 1.618 | .110 | −1.178 | 11.383 |
| Service days (per week) | −53.648 | 60.438 | −0.888 | .378 | −174.165 | 66.869 |
| Standard Manpower (per week) | 13.669 | 4.610 | 2.965 | .004 | 4.493 | 22.845 |
| Vaccination area*(square meters) | ||||||
| Relatively small area (Ref.) | / | / | / | / | / | / |
| Relatively medium area | −312.117 | 116.123 | −2.688 | .009 | −543.307 | −80.926 |
| Relatively large area | −285.220 | 91.232 | −3.126 | .003 | −466.929 | −103.511 |
*Classification of vaccination area is based on tertiles of the percentile values for the area among vaccination clinic types as a reference standard.
To assess the robustness of the cost estimates and regression results, two sensitivity analyses were performed. First, we varied labor cost inputs by 5%, 10%, and 20%, given that labor constitutes the largest share of total service costs (75.02%). The changes in cost per dose across different types of clinics were consistently lower than or comparable to the predefined reference variation, indicating that the results are robust. The conclusions regarding cost differences among routine, adult, and rabies vaccination clinics remained consistent across all levels of variation (Supplementary Table S4). Second, we examined the influence of high-cost outliers by excluding the top 5% of clinics based on cost per dose and cost per person. The direction, magnitude and statistical significance of most coefficients remained stable, indicating that the results were not driven by a few extreme values (Supplementary Table S5).
Discussion
At present, the subsidy for the government-supported immunization program is 5 yuan per dose (cost recovery gap reached 96.26%), and the standard service fee for non-immunization program vaccines is 21 yuan per dose (cost recovery gap reached 84.28%). The findings from this first comprehensive cost analysis survey of vaccination services in Guangzhou indicated an average cost per vaccine dose of 133.56 CNY($18.95), a value higher than the known vaccination service costs in other cities in China10,17,18 (19.08–27.4 CNY($2.71–3.89) per dose in cities such as Shenzhen, Zhuhai, and Chengdu). This finding might potentially have resulted from the inclusion of both adult and rabies vaccination clinics, which tend to have relatively high service costs. However, the average cost was notably higher than the vaccination service costs in 94 low- or middle-income countries, which have been estimated by a model to range from 1.43 to 1.51 USD per dose.19 In comparison to high-income countries, the overall average cost was slightly higher than the mean vaccination cost of USD 14 reported in a 2019 survey conducted across 14 clinics in the United States.20 A study from the United Kingdom covering nine outpatient clinics reported an average cost per dose of 18.20 GBP for childhood vaccinations and 14.05 GBP for adult vaccinations21, whereas the corresponding figures in Guangzhou were CNY 64.88($9.20) and CNY 293.70($41.66), respectively. Moreover, directly using exchange rates for currency conversion may not fully reflect the differences in vaccination service costs between countries. To improve comparability, per capita GDP or purchasing power parity (PPP) are used for standardization. The average cost of a vaccine dose for children in Guangzhou is $9.2, which is approximately 0.040% of Guangzhou’s 2023 per capita GDP of $22,938. In contrast, the cost of a vaccine dose for children in the UK is £18.2, or $22.75, which is about 0.047% of the UK’s 2023 per capita GDP of $48,885. For adults in Guangzhou, the average cost of a vaccine dose is $41.66, which is roughly 0.182% of Guangzhou’s 2023 per capita GDP of $22,938. In the UK, the cost of a vaccine dose for adults is £14.05, or $17.56, which is about 0.036% of the UK’s 2023 per capita GDP of $48,885. This discrepancy might be attributable to variations in urban economic development levels; the extent of investment in healthcare resources; the allocation of resources within vaccination clinics; and government policies, including higher coverage rates for free adult vaccinations in high-income countries.9 Although all these studies were based on clinic-level cost estimates, cross-country comparisons should be interpreted with caution due to potential differences in cost structures, accounting standards, and system characteristics across nations. In addition to high-income countries, comparisons are made with neighboring low-and middle-income countries, especially those with similar service delivery environments. For example, studies in India using service-level costing and annualization methods have reported per-dose delivery costs ranging from USD 1.11 to USD 2.64 across various immunization programs.15,22 These figures are considerably lower than our findings in Guangzhou. However, such differences may stem from urban cost structures, labor intensity, and broader service mandates in China. According to a study conducted in Thailand, the cost per dose for routine immunization services ranges from USD 1.42 to USD 2.55,23 depending on the type of vaccine and the setting. The cost structure in Thailand is similar to Guangzhou in terms of labor costs being a significant portion of total costs. However, the overall cost per dose is still lower, possibly due to differences in economic development and healthcare resource allocation. These cross – national differences in the cost of vaccination services may be partly due to differences in wage structures and government subsidy policies. For example, in large cities like Guangzhou, China, the labor costs of public health workers include wages, bonuses, and social insurance. Additionally, the service fees for vaccination services in China are relatively standardized, especially for non – National Immunization Program (NIP) vaccines. In contrast, many high – income countries either provide full government funding for vaccines or allow cost recovery through market pricing, which may reduce cost differences at the clinic level.6 When comparing unit costs across countries, these structural differences in financing and labor compensation should be taken into account.
Our findings indicated that labor costs accounted for the majority (75.02%) of total vaccination service costs in Guangzhou City; this fraction was higher than those reported in some regions of China (58.29%),24 and in six countries in Africa, Central America, and Eastern Europe (14–69%).15 This difference might have been because our survey was based on comprehensive annual income, including salaries, bonuses, performance-based pay, and social insurance and housing funds. Gap analyses reveal notable cost differences across clinic types. For instance, the adjusted average cost per person in public clinics was 355.72 CNY (USD 50.46) higher than in private clinics, and the cost per dose was 84.40 CNY (USD 11.97) higher. These gaps highlight the potential for cost-saving through optimizing public clinic operations or encouraging private sector participation. Notably, the high proportion of established staff in public clinics, along with their higher qualifications, could be contributing to higher labor costs. Specifically, the higher qualifications and job permanency of public clinic staff likely result in increased salaries and benefits, thereby raising overall labor costs. In contrast, private clinics, which employ a higher proportion of nonpermanent staff, tend to incur lower labor costs. This observation highlights the importance of human resource management in controlling the costs of vaccination services. Optimizing staffing patterns and balancing the ratio of permanent to nonpermanent staff may help reduce labor costs while maintaining service quality. Additionally, Guangzhou, an economically developed city, attracts and retains highly qualified medical professionals, thus entailing high labor costs.
Our exploration of the factors affecting the cost of vaccination shows that private-type clinics, clinics with higher population coverage, clinics with medium and large vaccination areas have lower per-dose costs and per-person vaccination service costs, while clinics with higher weekly standard manpower have higher per-dose costs and per-person service costs. These findings are consistent with previous multi-country studies showing that factors such as clinic type, service scale, and operating model significantly influence vaccination delivery costs.9,15 In addition, we also found that the increase in the radius of responsible vaccination services can increase the cost of vaccination services, and the increase in the number of service days per week will reduce the cost of vaccination services. There are mainly the following reasons. First of all, the salary and manpower of private clinics are lower than those of public clinics, which leads to lower labor costs and lower service costs. Secondly, outpatient clinics with higher population coverage and more opening hours mean more doses and visits, so that the same fixed capital can be allocated to more doses of vaccines, resulting in lower service costs. In addition, clinics with medium and large vaccination areas can usually vaccinate more people, achieve higher service efficiency, provide a better vaccination experience, and attract more people to choose,25 thereby reducing the cost per dose and per person. Finally, a higher service radius will increase transportation costs, resulting in poor vaccine accessibility, and indirectly affect the willingness to vaccinate, thereby affecting the amount of vaccination26 and increasing service costs. The above findings suggest that the staffing of vaccination clinics should be optimized. In addition to the length of time set by the government, clinics can reasonably increase the opening time according to their own conditions. In addition, when building new vaccination clinics, appropriate population coverage and service radius should be considered to avoid smaller vaccination areas. This will be an effective measure to reduce vaccine costs, increase vaccination volume and ensure the provision of high-quality vaccination services in the future.27,28 Future studies with larger sample sizes could explore potential interaction effects – such as between clinic type and staffing or population coverage – to uncover differential cost drivers across settings.
The cost analysis of immunization programs includes three main aspects: vaccine costs, supply chain costs, and service delivery costs.19,29 In this study, the cost refers to the cost incurred during vaccination services from the perspective of vaccination units; i.e., the cost of service delivery. Consequently, this study has several strengths and limitations. The study limitations include that comprehensive cost data are not provided for the entire immunization program in Guangzhou City, thus preventing the government from assessing the complete expenditures of the city’s vaccination program.Another potential limitation is that the cost data were self-reported by clinics through a structured questionnaire. However, as the data were facilitated and verified by CDC staff through a rigorous review process, the risk of major inaccuracies is significantly reduced. While the sample of 84 clinics is robust and representative, it is important to note that it remains a sample. Although theoretical concerns about non-response or refusal could introduce some bias, the high sampling fraction and active involvement of the CDC have minimized the likelihood of such issues. For units that have not yet responded, multiple follow-up methods will be employed to contact them, explain the purpose of the investigation, and encourage their participation in the cost survey in order to reduce non-response rates. The study adopted a stratified random sampling approach to ensure representation across key clinic characteristics, such as region and clinic type. Nevertheless, the generalizability of the findings should be interpreted with caution if unmeasured differences exist between sampled and non-sampled clinics. Additionally, owing to difficulties in locating original cost records from previous years of vaccination clinics engaged in grassroots work, we investigated data for only the year 2023. The results of cross-sectional surveys can only reveal the factors influencing costs and cannot make causal inferences about these cost-influencing factors. In addition, a standard human resource method that follows the principles of full cost accounting is adopted. In future research, the transparency and accuracy of labor cost estimation can be improved by introducing time-motion analysis or employee-reported human resource allocation data. However, this study has substantial value in that it comprehensively and carefully investigated the cost of vaccination services, and it provides information on cost composition and influencing factors. Our findings might facilitate further exploration of factors affecting costs and optimization of the implementation of grassroots vaccination work, and the data provided might support the government in formulating and updating relevant health policies, and conducting economic evaluation of vaccination throughout the city.
Current policy analysis, future outlook, and policy recommendations: (1) Vaccination service fees in China are uniformly set by provincial governments based on their specific circumstances. Vaccines under the immunization scheme in all provinces cost 5 yuan/dose, in which case the government directly subsidizes the concerned vaccination clinics. Meanwhile, the service fees for vaccines not covered under the immunization scheme range from 18 to 28 yuan and are borne by citizens. As indicated by the survey results of this study, the service fee cost in Guangzhou is significantly higher than the current service fee standards stipulated by the government. One of the reasons causing this phenomenon is that the health management department pays more attention to vaccination safety, which makes the construction of outpatient clinics and the demand for personnel upgrade, under the requirements of China’s Vaccine Management Law. The second reason is that the charging standards for vaccination service fees in China are government led, and the revision of service fees involves the multi-departmental coordination, which is different from the scenario in other countries where prices are market-oriented and medical providers set their own service fees.30,31 Under the current zero markup policy mandated by the government for all vaccines, failure to enhance existing service subsidy standards may gradually degrade service quality and public satisfaction in vaccination clinics, especially in private vaccination clinics paying for labor costs on their own. Therefore, it is recommended that the government should conduct comprehensive investigations across different clinic types, establish a service cost accounting system, periodically evaluate price fluctuations and labor cost changes, coordinate with financial and health authorities to adjust subsidy standards accordingly, and implement differentiated increases in current vaccination service fees. (2) Due to the fact that from 2000 to 2018, the number of children born in China had remained above 15 million and the demand for vaccines among adults had also been rising year by year, the Chinese government officially proposed in 2019 to build adult clinics to alleviate the pressure at vaccination clinics. However, recent years have witnessed a gradual decline in the number of births in China, which fell steeply to 9.02 million in 2023, resulting in a decline in the vaccination volume at routine vaccination clinics. Meanwhile, service costs at adult clinics are found by this survey to be the highest. Continued existence of these circumstances will lead to further wastage of public health resources. Thus, it is suggested that the government merge adult clinics and general clinics in the future to create full life cycle clinics that are more accessible to families. Our regression results provide empirical support for this policy direction. Specifically, clinics with larger service areas and higher population coverage – features typical of mixed-service or consolidated clinics – were significantly associated with lower costs per dose and per person. For example, clinics with medium-to-large service areas showed a cost reduction of up to 96.70 CNY ($13.72) per dose (Table 5), suggesting that resource sharing and service integration may achieve substantial cost savings.
Based on the cost-influencing factors identified in this study, vaccination clinics can implement targeted actionable recommendations to lower current service costs. First, while building vaccination clinics, prioritize consider constructing medium-sized and large-sized ones as they will incur lower per dose cost and per person service cost. Second, when it comes to staffing, adopt a mixed model of employment that comprises long-term workers and contract workers to reduce wage burdens without compromising on service quality. Meanwhile, promote the deployment of automated digital tools to reduce labor costs and to further boost labor efficiency. Additionally, regarding the operation of the clinics, extend service hours during peak hours and establish resource sharing centers with surrounding clinics to optimize the utilization of facilities. These measures align with WHO recommendations for sustainable immunization financing, while Supplementary Table S6 provides a CHEERS 2022 framework-structured implementation roadmap to better support evidence-informed decision-making by health authorities and planners.
Conclusion
This study reports the first comprehensive examination of the service delivery costs associated with various types of vaccination clinics in Guangzhou, China. It is important to note that the costs discussed in this study refer solely to service delivery and do not include the cost of vaccines. The cost disparities among diverse vaccine clinics were elucidated, and their respective cost composition characteristics and potential influencing factors were delineated. This research not only provides granular scientific data to support Guangzhou’s immunization strategy and facilitate efficient resource allocation, at the same time, policymakers should consider using these findings to modify and improve the current subsidy level and clinic service model in Guangzhou, which will contribute to the sustainable and high-quality implementation of immunization programs. In addition may serve as a valuable reference for decision-making and optimization efforts in related fields in other municipalities.
Supplementary Material
Biographies
Wenji Wang, Ph.D., obtained her doctoral degree from Harbin Medical University and completed her postdoctoral research in clinical medicine at Fudan University. She primarily focuses on life-course health and vaccinology epidemiology. She has participated in the execution of several national and provincial-level research projects and has published over 15 papers in SCI-indexed journals and core Chinese journals.
Zhoubin Zhang, MPH, is a Chief Physician (Level 3) in Disease Control. He serves as a master’s supervisor at Sun Yat-sen University and Southern Medical University. He is recognized as a Key Medical Talent in Guangzhou and is the academic leader of the Guangzhou Key Medical Discipline – Laboratory for Rapid Detection and Early Warning of Infectious Diseases. Currently, he holds the positions of Party Secretary and Director at the Guangzhou Center for Disease Control and Prevention (Guangzhou Health Supervision Institute). His primary research focuses on the prevention and control of infectious diseases, emergency response to public health incidents, immunization programs and vaccination, as well as public health issues in Xinjiang. To date, he has published 88 papers as the first author or corresponding author, including 43 papers indexed by SCI, with a cumulative impact factor of 250.764. He has led major scientific projects under the National Key R&D Program of the Ministry of Science and Technology and the Guangzhou Key R&D Program. Additionally, he has presided over key R&D projects funded by the Guangzhou Science and Technology Bureau and participated in multiple national, provincial, and municipal projects, as well as targeted scientific and technological assistance initiatives.
Funding Statement
Supported by The Key Project of Medicine Discipline of Guangzhou [No 2025–2027-11], Guangdong Provincial Medical Science and Technology Research Fund Project [No. B2023260], Guangzhou Health Science and Technology Program [20241A011063] and Guangzhou Science and Technology Plan Project [No. 2024A03J0422].
Author contributions
Chunhuan Zhang: Conceptual framework, Writing Original draft, Key data collection; Zeyu Liu: Writing Original draft, Investigation, Data collection and organization; Yong Huang: Data analysis; Zhiwei Zheng: Data analysis; Wenji Wang: Article writing and revision, Data collection, Data visualization; Zhoubin Zhang: Resources, Supervision. All authors have read and agreed to the published version of the manuscript.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Supplementary Information
Supplemental data for this article can be accessed online at https://doi.org/10.1080/21645515.2025.2545031
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