Monitoring Measures in the Elimination of Malaria in Fujian, China: A Cost-Benet Analysis

Background: Malaria is an insect-borne infectious disease that spreads through bites from infected Anopheles mosquitos. The disease seriously endangers human health and economic development. The study focuses on Fujian Province, China, which entered the nal stage of malaria elimination stage in 2005. In order to understand the costs and benets of malaria monitoring measures during the elimination stage, the health economics of the monitoring measures should be examined. Methods: Data on the number of cases during the malaria elimination stage (2005–2019) in Fujian Province were collected and sorted. The basic economic data were obtained from the Fujian Statistical Yearbook. Based on the fundamental theories in health economics, a cost-benet analysis was conducted based on the data. Specically, the cost of monitoring measures during the malaria elimination stage was calculated by economic cost and compared to the benets, which were quantied based on economic and social benets of the monitoring measures. Results: The total cost of monitoring measures in the malaria elimination stage was estimated at 607,878,783.36 yuan (USD 87,534,544.80). The components of the total cost were: case detection and treatment, which accounted for 66.62% of costs, health education with 13.31%, epidemic monitoring, 10.05%, supervision and assessment, 5.15%, and training and meetings took 4.87%. The total benet of the monitoring measures in the malaria elimination stage was valued at about 116,123,417,911.81 yuan (USD 16,721,772,179.30). Direct economic benet accounted for 22.61% of the total, while the social benet was 77.39%. The cost-benet analysis of the malaria elimination stage showed that the net benet of monitoring measures was about 115,515,539,128.45 yuan (USD 16,634,237,634.50) and the benet-cost ratio was 191.03. The monitoring cost for residents was 1.08 yuan (USD 0.16) per capita, and the benet for residents was 206.12 yuan (USD 29.68) per capita. Conclusions: The monitoring measures conducted in the malaria elimination stage are a highly cost-effective intervention for reducing the negative impact of malaria in Fujian Province. Over the past 15 analysis approach allows us to understand the current input and output characteristics of malaria monitoring in Fujian Province and analyze the benets of monitoring measures in the malaria elimination stage. The study not only provides reference for future malaria elimination research but also a scientic basis for more rational formulations of malaria monitoring programs in Fujian Province. Future studies may use modications to this approach to obtain more precise results, which will serve as an even more comprehensive reference for the malaria monitoring work.


Background
Malaria is an insect-borne infectious disease caused by the Plasmodium parasite, which spreads to people through Anopheles mosquito bites. It is a complex disease that can spread rapidly and exhibit acute onset. Accordingly, it can easily cause local outbreaks and epidemics and seriously endanger human life and health, as well as social and economic development. In 2018, about 228 million malaria cases occurred worldwide, leading to about 405,000 deaths. The World Health Organization (WHO) observed that the African region accounted for 93.0% of all cases, followed by Southeast Asia and the eastern Mediterranean region. The global results of malaria elimination efforts are expanding, with 27 countries reporting fewer than 100 local cases and a growing number of countries reporting zero local cases [1,2]. This indicates that malaria elimination is nally within reach. The global burden of malaria is declining through effective control interventions, but monitoring is vital to maintain progress [3].
Since the implementation of the action plan for malaria eradication in China (2010-2020), remarkable achievements have been made in malaria elimination, with more than 95% of counties in China reporting incidence rates below 1 in 10,000 [4].
Fujian Province has not reported any local cases and is considered to have entered the stage of malaria elimination in 2005 [5].
However, imported malaria cases are often reported in Fujian Province due to frequent commercial exchanges and high mobility in coastal areas [6]. Therefore, it is still necessary to conduct a health economics evaluation of the monitoring measures in Fujian, even though it is in the malaria elimination stage. We reviewed and analyzed the literature on the economics of malaria and found that the differences between the nancial and economic costs were negligible; thus, only economic costs are presented here [7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23]. We calculated costs based on health economics theory and the malaria monitoring measures in this stage. We determined the economic analysis framework based on survey data, literature, and expert consultations [7][8][9]. This approach has allowed us to understand the current input and output characteristics of monitoring measures and analyze their costs and bene ts to the province during the malaria elimination stage.

Sources of Data
We collected malaria epidemic data during the nal stage of malaria elimination in Fujian Province (2005-2019). The annual malaria report is based on reports of monitoring work and epidemic investigations in various cities. Case investigation data were extracted from the reports of the China Disease Prevention and Control Information System network. Cases were counted according to the time of onset, and duplicate cases were excluded (Table 1). Demographic and economic data were obtained from the Fujian Statistical Yearbook (Table 1).

Cost De nition and Measuring Method
Cost was expressed in currency units (RMB 1 yuan = USD 0.144). In the case of this study, no substantial donated items were used and few capital goods were used. As such, the differences between nancial and economic costs were negligible and only economic costs are presented here. The basic economic data were obtained from the Fujian Statistical Yearbook. The professionals' wages were calculated according to the wage level of institutions in Fujian Province (Table 2). Based on the domestic and international malaria-related economics literature [5][6][7][8][9], discussions in the research team, consultations with malaria control experts, the Operation Manual of the Malaria Monitoring Program in Fujian Province, and general characteristics of malaria monitoring work, we divided monitoring measures into ve categories: 1) case detection and treatment, 2) epidemic monitoring, 3) health education, 4) training and meetings, and 5) supervision and assessment.

Case detection and treatment
Case detection costs included lab professional salaries, blood collection costs, blood smear costs, and microscopic examination costs. The care rate per patient was set at 1. The direct medical costs included drug treatment, care, and testing costs. The direct non-medical costs were calculated according to the consumption levels of Fujian Province in the same period, including transit fares, accommodation costs, and food expenses. Missed work costs due to hospitalization were converted into a monetary amount by the per capita national income method [9]: Missed work costs = days off work × (per capita national income /306) × 2.84. One patient missed work on 8 days to be treated for malaria [10].

Epidemic monitoring
Professional salaries and associated monitoring costs (e.g. materials, transportation etc.) were calculated in units of monitoring sites. The anti-mosquito drug costs for epidemic focus areas were calculated according to the actual amount used and the market price. The professional travel allowances were calculated according to the number of cases.

Health education
Since the Fujian Provincial Center for Disease Control and Prevention (FJCDC) carries out health education in Fujian every year, the costs included those of health education and personnel salaries. The health education activities were carried out on World Malaria Day (April 26th). The labor cost was approx. 50 yuan (USD 7.2) per capita.

Training and meetings
Trainings for clinicians, monitors, and lab professionals were held every year. The training costs (material, site, lecture, accommodation, transportation, etc.) were calculated by applying the comprehensive quota standard.
The amount of work to be conducted in the form of meetings at the malaria elimination stage is low compared to that of other infectious diseases, so the meeting costs were estimated at 5% of training costs.

Supervision and assessment
The mid-year supervision and year-end assessment costs included materials costs, personnel salaries, and travel allowances.

Cost-bene t Analysis Method
A cost-bene t analysis was conducted for this study, based on fundamental theories of health economics. The cost (C) of monitoring measures during the malaria elimination stage in Fujian Province was calculated and compared to its bene ts (B).

Cost-bene t Analysis of Malaria Monitoring per Capita
The per capita cost of malaria monitoring is calculated as follows: If BCR > 1 and NB is positive, the monitoring measures were bene cial to the economy. If BCR < 1 and the NB is negative, the monitoring measure cost was higher than the bene t, which means the implementation of those measures was economically burdensome at the malaria elimination stage and the monitoring measures should be adjusted [12,13].

Accounting Assumptions of Cost and Bene t Indicators
The work of monitoring is less intensive but more targeted in the malaria elimination stage. Thus, we could assume that without the monitoring, large xed assets would still need to be depreciated and this cost can be excluded from cost estimations. The statutory working hours of professionals can be fully utilized with effective monitoring measures. However, without them, all identi ed cases will require hospitalization and the assistance of a caregiver (with an assumed care rate of 1), and neither patients nor caregivers can work during hospitalization. We decided it would be practical to calculate the cost of training and health education activities according to the reported project costs. This estimation method did not signi cantly in uence the calculation of social bene ts in the cost-bene t analysis. The experts we consulted on the matter con rmed that the indicators that did not meet the inclusion criteria would not have a signi cant impact on the overall analysis.

Costs of Malaria Monitoring Measures
Costs of case detection and treatment:  The required annual blood test rate was not less than 2/100 in Nanping and Sanming, not less than 5/1,000 in the southern area, and not less than 1/1,000 in other cities. Cost of epidemic monitoring: Table 3  Hence, the total anti-mosquito drug cost was 770,000 yuan (USD 110,880.00).
The cases were investigated and veri ed by two professionals. This incurred a cost for professional travel allowance of 320,320.00 yuan (USD 46,126.08).
Cost of training and meetings: Table 3 shows that the training and meeting cost Hence, the total training cost was 19,722,390.00 yuan (USD 2,840,024.16) and the total meeting cost is estimated at 9,861,195.00 yuan (USD 1,420,012.08).
Cost of health education: Table 3 shows that the health education cost was 13.31% (80,929,064.00 yuan = USD$ 11,653,785.22) of total costs. Ninety-four professionals participated in health education every year. The health education activities cost was estimated at 20,000 yuan (USD 2,880.00) every year. Thus, the total health education cost was 300,000.00 yuan (USD 43,200.00). Further, the total professional salary cost for health education was 80,558,564.00 yuan (USD 11,600,433.22) and the total labor cost was 70,500.00 yuan (USD 10,152.00).
Cost of supervision and assessment: Table 3 shows that the supervision and assessment cost was 5.15% (31,303,416.00 yuan = USD$ 4,507,691.90) of the total cost. Thirty-six professionals conducted 188 supervisions and assessments every year. The total material cost was 112,800.00 yuan (USD 16,243.20), the total professional salary cost was 30,852,216.00 yuan (USD 4,442,719.10), and the associated total professional travel allowance cost was 338,400.00 yuan (USD 48,729.60).

Bene ts Achieved in the Malaria Elimination Stage
Economic bene ts: Without effective monitoring and control measures, the spread of a malaria epidemic would be very fast and seriously damage human health. All cases would need to be treated with anti-malaria drugs in hospitals. The control incidence rate in this study, which is 238.25/10,000, is based on the highest incidence of malaria in the years since 1972 [9]. In the malaria elimination stage, the permanent population of Fujian Province was 563.38 million, so the number of potential cases = It was assumed that, as a result of the health education activities, all residents would acquire prevention knowledge and avoid malaria infection. Combined with the survey results [10], it was estimated that the social bene t of this education was 100 yuan (USD 14.40) per capita. Accordingly, the total bene t of improving health protection awareness was calculated as 100 × 563,380,000 = 56,338,000,000.00 yuan (USD 811,267,200.00).
In sum, the total bene t achieved in the malaria elimination stage was 116,123,417,911.81 yuan (USD 16,721,772,179.30) (Fig. 2). As shown in Table 4

Discussion
Cost-bene t analysis is one of the most important tools in health economics research, and can be used to effectively evaluate the impacts of health and epidemic prevention efforts [14]. This study identi ed the characteristics of malaria elimination efforts in Fujian Province and comprehensively analyzed the inputs and outputs to monitoring in the malaria elimination stage.
Literature has shown that implementing more effective malaria monitoring and control measures can produce economic bene ts [15][16][17][18][19][20][21]. At present, malaria monitoring measures in Fujian Province have been incorporated into overall public health efforts. The malaria monitoring measures for imported cases have been strengthened and the diagnostic knowledge of clinicians and the ability of monitoring personnel and lab personnel, enhanced. Health education activities have been carried out through multiple channels, and the achievements in malaria control have been consolidated. Overall, the monitoring work has achieved enormous economic and social bene ts in the malaria elimination stage.
The study estimated the cost based on the monitoring measures, although some in uencing factors could not be taken into account. However, we assume that this did not signi cantly impact results. At present, Fujian Province is at the stage of malaria elimination and malaria-related efforts are gradually being reduced. If we had used traditional cost accounting, the accuracy of the results may have been adversely affected. Therefore, in our framework, we determined the cost structure according to the malaria monitoring measures. This approach was intended to more accurately re ect the direct cost of the monitoring measures, similar to the methods in other relevant studies [7,14]. and assessment costs were 5.15%, and training and meetings were the smallest cost factor at 4.87% of the total. As the population is generally susceptible to malaria, it was necessary to carry out blood tests on febrile patients, which explains why the case detection costs made the highest contribution to total cost. At present, the majority of imported cases in the province are falciparum malaria cases. The density of the Anopheles sinensis and the risk of re-transmission of falciparum malaria are very low. Therefore, the focus of the malaria elimination stage is discovering and treating the sources of infection and reducing mortality. This focus on infectious sources is different from malaria-endemic areas in Africa, which mainly emphasizes blocking infectious sources, controlling transmission routes, and protecting susceptible populations [19,22,23]. The study concludes that, for Fujian Province, monitoring personnel should adopt more targeted measures, focusing on the detection of imported cases in the malaria elimination stage. A malaria special working group should be set up to take more targeted monitoring measures and thereby, reduce the proportion of personnel salaries in the total cost equation. This will reduce the overall monitoring cost and enable costs to be accounted for more accurately. In this stage, the focus of training should be shifted to clinicians to improve their diagnostic ability.
The cost-bene t analysis of the malaria elimination stage showed that the cost of malaria monitoring for each resident was 1.08 yuan (USD 0. 16 14). Therefore, investments in health education could be increased. The health education workers should enhance the level of education on malaria prevention for the personnel who go to high-prevalence areas.
In the malaria elimination stage, different monitoring measures were applied according to different risk levels, thus strengthening the prevention and control for the imported cases. These measures conformed to the global malaria strategy (World Health Assembly 2015) and were also similar to those observed in past studies [16,20,24].
Given time and research capacity constraints, some potentially in uential factors (such as the policy environment) were not considered at this stage. Further, some data were estimated based on interview results, which may have interfered with the accuracy of the analysis results.

Conclusions
The monitoring measures conducted in the malaria elimination stage are a highly cost-effective intervention for reducing the negative impact of malaria in Fujian Province. The cost-bene t analysis of the malaria elimination stage shows that the NB of monitoring measures, which is 115,515,539,128.45 yuan (USD 16,634,237,634.50), as well as the BCR, which is 191.03. The monitoring cost for each resident is 1.08 yuan (USD 0.16) and the bene t is 206.12 yuan (USD 29.68). These values show that the per capita malaria monitoring cost is relatively low, and the effectiveness is positive. Although some limitations are present, this study remains signi cant. The cost-bene t analysis approach allows us to understand the current input and output characteristics of malaria monitoring in Fujian Province and analyze the bene ts of monitoring measures in the malaria elimination stage. The study not only provides reference for future malaria elimination research but also a scienti c basis for more rational formulations of malaria monitoring programs in Fujian Province. Future studies may use modi cations to this approach to obtain more precise results, which will serve as an even more comprehensive reference for the malaria monitoring work.
Abbreviations BCR: bene t-cost ratio; NB: net bene t; WHO: World Health Organization;

Declarations Ethics approval and consent to participate
This study is a health economics study on malaria monitoring measures, so it was only the aggregate total not individual subjects therefore "Not applicate".

Consent for publication
Not applicable Availability of data and materials The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Competing interests