Cost-benet analysis of the monitoring measures for the malaria elimination stage in Fujian, China

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. Against the background of eliminating malaria in Fujian Province, in order to understand the cost and benet of malaria monitoring measures, the health economics of the monitoring measures should be examined.. Methods The malaria epidemic data 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. A cost-benet analysis was conducted for this study, based on the fundamental theories in health economics. Moreover, the Cost (C) of monitoring measure during the malaria elimination stage was calculated, and the Benet of malaria elimination stage (B) was analyzed.

entry-exit personnel), and enhancing residents' awareness about prevention and personal protection. The work should continue to be consolidated for the elimination of malaria. The framework and results of this study conform to the principles of health economics and have a certain reference value for current malaria monitoring practices.

Background
Malaria is an insect-borne infectious disease caused by the Plasmodium parasite, which spreads to people during bites from Anopheles mosquitos or blood transfusions from an infected person. It is a complex disease that can spread rapidly and exhibit acute onset, which are factors that can easily cause local outbreaks and epidemics and seriously endanger human life, health, and social and economic development. In 2018, about 228 million malaria cases occurred worldwide, with about 405,000 deaths.
The WHO African region accounted for 93%, 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, which indicates that malaria elimination is nally within reach (1,2). Global malaria burden is reducing with effective control interventions, and surveillance is vital to maintain progress (3). Since the implementation of the China Action Plan for the Elimination of Malaria (2010-2020), remarkable achievements have been made in malaria elimination, with more than 95% of counties (cities, districts) in China reporting incidences below 1 in 10,000 (4). Fujian Province has not reported any local cases since 2005, and they have since advanced to the malaria elimination stage (5). However, imported malaria cases are often reported due to frequent commercial exchanges in the coastal areas of the province, resulting in the high mobility of personnel (6). Therefore, it was necessary to conduct a health economic evaluation of the surveillance measures of Fujian Province's malaria elimination phase. We calculated costs based on health economics analysis theory and the current status of malaria elimination in Fujian Province. We used the content of the malaria surveillance measures as the main body and determined the economic analysis framework based on the survey data, literature, and expert consultations (7)(8)(9). This approach allowed us to understand the current input and output characteristics of malaria surveillance in Fujian Province and analyze the bene ts of surveillance measures in the malaria elimination stage. Our study provides a reference for further malaria elimination work and also provides a scienti c basis for more rational formulations of malaria surveillance programs in Fujian Province.

Sources of data
We collected malaria epidemic data during the malaria elimination stage in Fujian Province from 2005 to 2019. The annual malaria report is based on reports of surveillance work and epidemic investigations in various cities of Fujian Province. Malaria case investigation data were from direct reports from the China Disease Prevention and Control Information System network. Cases were counted according to the time of onset, and duplicate cases were excluded. Demographic and economic data were obtained from the Fujian Statistical Yearbook.

Cost De nition and Measuring Method
Costs were expressed in currency units (yuan, RMB). The basic economic data was obtained from the Fujian Statistical Yearbook. The labor cost of personnel was calculated by 50 yuan per person. 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 Surveillance Program in Fujian Province, and general characteristics of malaria surveillance work, we divided surveillance measures in the malaria elimination phase into ve categories: 1) case detection and treatment; 2) epidemic surveillance ; 3) health education; 4) training meetings; and 5) supervision and assessment.

Case detection and treatment
The cost of a blood test includes the cost of blood collection, lm preparation, evaluation, and so on. It is estimated that a single blood smear slide is about 10 yuan.
The accompanying rate of case treatment was set at 1, and direct medical costs included the cost of drug treatment (staffed by a person) such as with primawaline and clowax and the cost of hospitalization/observation stay (drugs, nursing care, laboratory costs, etc.). These were approximately 300 yuan per case. Direct non-medical costs, including transportation, communication, and catering expenses, were calculated according to consumption levels in Fujian Province in the same period. The cost of hospitalization-related labor loss for patients and their family members was a missed work fee converted into a monetary amount by the per capita national income method(9): Cost of missed work = days off work × (annual per capita net income/306) × 2.84. Each patient missed about eight days of work (10).

Epidemic surveillance
The wages of the two professionals were measured according to wage levels in institutions in Fujian Province during the same period. Material, transportation, and labor costs for media control and surveillance were measured and calculated in units of surveillance sites. The cost of disinfection drugs to treat locations of epidemics was calculated according to the actual amount used and the market price at that time. Material costs were for case veri cation and investigation, and labor costs were for the two professionals.

Health education
The Centers for Disease Control and Prevention conducts "National Malaria Day" health education activities on April 26 each year to measure the costs of health education activities and materials, staff salaries, and labor.

Training meetings
Because the workload in the malaria elimination phase is less than that for other infectious diseases, conference fees were converted to 5% of the training course cost. The cost of the training (for materials, sites, lectures, accommodation, transportation, etc.) was calculated by applying the comprehensive quota standard (130 yuan per day from 2005 to 2014; and 400 yuan per day from 2014 to 2019).

Supervision and assessment
These were the mid-year supervision and end-of-year assessment costs for materials, staff wages, and labor as well as for transportation and accommodation.

Determining Bene t Indicators
We reviewed the domestic and international literature on the economic evaluation of malaria(9, 11, 12), had discussions with the research team, consulted experts, and then determined the economic and social bene t indicators. Economic bene ts included the direct treatment bene ts from avoiding illness-related hospitalization, the indirect non-medical bene ts from avoiding illness-related hospitalization, and the bene ts of avoiding illness-related work absence. Social bene ts included the malaria staff bene ts from improvement in surveillance capacity, the bene ts from residents' improved health levels, and the bene ts from residents' improved awareness of malaria protection.

Cost-bene t analysis method
Based on fundamental theories in health economics, we used a cost-bene t analysis method for the study. We calculated the annual average cost (C) of surveillance measures in Fujian Province's malaria elimination phase to analyze the corresponding annual average reduction in incidence and created bene ts (B).

Cost-bene t analysis of malaria surveillance per capita
The cost of malaria surveillance per capita of residents = average annual surveillance cost / number threatened by malaria infection; the bene t of malaria surveillance per capita of residents = average annual bene t / number threatened by malaria infection.

Bene t-Cost Ratio (BCR) = B/C = Average Annual Bene t/Average Annual surveillance Cost Net Bene t (NB) = B-C = Average Annual Bene t -Average Annual surveillance Cost
When the BCR is higher than one, and the NB is positive, it is economically advantageous to implement the measure. When the BCR is less than one and the NB is negative, the cost of the measure is higher than its e ciency. In other words, the implementation of this measure is economically burdensome, and the strategy should be adjusted (12,13).

Assumptions of cost-bene t accounting
Surveillance is less intensive but more targeted in a malaria elimination phase. Thus, we could assume that without the surveillance work, large xed assets would need to be depreciated and could be excluded from costing. Statutory working hours of relevant staff can be fully utilized with effective surveillance measures. However, without them, all identi ed cases will require hospitalization and the assistance of a caregiver (with a 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 project, and the estimation method did not signi cantly interfere with the social bene ts in the costbene t analysis model. Regarding the cost-bene t analysis framework for the surveillance measures, the expert we consulted believed that the indicators that did not meet the inclusion criteria had no signi cant impact on the overall analysis model.

Costs of malaria surveillance
Costs of case detection and treatment: According to the number of personnel required by the surveillance program (8) was not less than 2% in Nanping and Sanming, not less than 5/1,000 in southern Fujian, and not less than 1/1,000 in other cities (8). From 2010 to 2019, if the annual blood test rate was not less than 5/10,000, the annual number of blood tests was 110,178, and the annual cost of blood tests for febrile patients was about 2,203,560.00 yuan.

Economic and Social Bene ts of Malaria Surveillance
The average annual resident population of Fujian Province from 2005 to 2019 was 37.56 million. We used the incidence rate of 1,972 (238.25/10,000) as the study control and calculated that 894,867 cases were avoided due to malaria surveillance (8). The actual number of reported cases was 1,191 (about 119 cases per year); thus, from 2005 to 2019, the annual average number of cases actually avoided was 894,748 cases.
We assumed that without effective malaria surveillance, all cases would have been hospitalized for antimalarial treatment. The direct treatment cost of each case was 319.35 yuan, and the annual average bene t of avoiding hospitalization was about 285.74 million yuan. The direct non-medical cost of each case was 218.94 yuan with an accompanying rate of 1, so the annual average direct non-medical bene ts avoided was about 391.79 million yuan. The indirect cost of each case was 1,407.05 yuan with an accompanying rate of 1, so the bene t of avoiding hospitalization-related work absence was about 2.52 billion yuan, as shown in Table 2.
We used the number of professionals trained in Fujian Province from 2005 to 2019 multiplied by the per capita training bene t to calculate the bene t of improving professionals' surveillance ability. The estimated per capita training bene t was about 250 yuan. The total number of professionals trained from 2005 to 2019 was 18,542, and the average annual bene t of improving their surveillance ability was about 309,033.33 yuan. Combining the level of per capita health care expenditure and the results of a resident survey in Fujian Province during 2005-2019, it was estimated that residents would be willing to pay about 300 yuan to avoid the health loss caused by malaria. According to the actual number of cases avoided in this stage, we estimated that the average annual bene t of improving residents' health level was about 268 million yuan. We supposed that through different forms of health education and propaganda, the residents acquired enough knowledge about malaria protection to avoid malaria infection and suppress malaria incidence, and the per capita social bene t was estimated at 100 yuan. Then, the average annual bene t of the residents' awareness of malaria protection was about 3.756 billion yuan. As shown in Table 2, the total economic bene t was about 3.195 billion yuan, accounting for 44.26% of the total bene t. The social bene t was about 4.025 billion yuan, accounting for 55.74% (notably more than 50%).

Cost-bene t analysis of malaria surveillance
The average annual cost of malaria surveillance measures in Fujian Province during 2005-2019 was about 481.635 million yuan, and the total annual bene t obtained was about 722 billion yuan. Thus, the per capita cost of malaria surveillance for residents was 1.28 yuan, and the per capita bene t of malaria surveillance for residents was 192.23 yuan. This shows that the investment per capita cost of malaria surveillance measures in Fujian Province was lower than the per capita bene t that was obtained. Hence, the effect of the malaria surveillance work was very bene cial.
By subtracting the annual average cost from the annual average total bene t, we calculated that the annual average net bene t resulting from malaria surveillance was 7.172 billion yuan. We calculated an annual average bene t-cost ratio of 149.91:1, which indicates that every input of 1 yuan for malaria surveillance could produce social bene ts of 149.91 yuan.

Discussion
Cost-bene t analysis is one of the most important tools in health economics research, and it can be used to effectively evaluate the impacts of health and epidemic prevention efforts (14). This study identi ed characteristics of malaria elimination efforts in Fujian Province and comprehensively analyzed inputs and outputs. The results of the analysis can help managers and decision-makers reduce the costs and improve the bene ts of their programs.
Literature has shown that implementing more effective malaria surveillance and control methods can result in greater economic bene ts (15)(16)(17)(18)(19)(20)(21). Presently, malaria management in Fujian Province is incorporated into overall public health efforts. The surveillance and management of imported malaria cases has been strengthened; the knowledge and skills of clinicians, prevention and control personnel, and inspectors have been increased. Health education and promotion activities have been carried out through multiple channels, and the achievements at the malaria elimination phase have been consolidated. In all, enormous economic and social bene ts have been achieved.
The study estimated the cost inputs based on the surveillance measures, though some in uencing factors could not be taken into account. We assume there was no signi cant interference. 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 item classi cations in the malaria surveillance measures. This approach was intended to more accurately re ect the direct cost inputs of the surveillance measures, similar to the accounting methods in other relevant studies (7,14).
The results showed that the annual average cost of surveillance measures during the malaria elimination phase from 2005 to 2019 was about 48.1635 million yuan. Although the cost of surveillance measures was large, it was still within a reasonable range for infectious disease control and prevention. The cost of case detection and treatment accounted for 71.53% (34.4521 million yuan/year) of the total cost, health education accounted for 12.28%, epidemic surveillance accounted for 8.84%, supervision and assessment accounted for 4.48%, and training meetings accounted for 2.87%. The proportion of cost for case detection and treatment was the highest. The population is generally susceptible to malaria. At present, the majority of imported malaria cases in Fujian Province are falciparum malaria cases. The vector density of the Anopheles sinensis mosquitoes is very low, it is generally believed that the risk of retransmission of falciparum malaria is very low in Fujian Province. Therefore, the current focus of Fujian Province's elimination phase is discovering and treating the sources of infection and reducing the mortality. This focus on infectious sources is quite different from that in parts of Africa that are still in the epidemic stage. Malaria-endemic areas in Africa mainly concentrate on epidemic surveillance, which emphasizes blocking infectious sources, controlling transmission routes, and protecting susceptible populations (19,22,23). In the malaria elimination phase, on the other hand, staff should adopt more targeted surveillance measures, focusing on the screening and detection of imported infectious sources. Staff should also consider forming a special malaria working group to carry out surveillance measures to reduce the proportions of wages and investments in the total surveillance costs and scienti c accounting. In malaria surveillance in Fujian, the focus of training should be shifted to continuously improving the surveillance capacity of clinical medical staff. In addition, cost investments in health education should be increased, speci cally in the area of health education in malaria prevention for personnel traveling to high-prevalence areas. This would improve residents' knowledge level of malaria prevention and enhance their personal protection awareness.
A cost-bene t analysis of Fujian Province's malaria elimination phase showed that the annual average total bene t value of malaria surveillance from 2005 to 2019 was about 7.22 billion yuan. The net social bene t of malaria surveillance was about 717,200 yuan, with an average annual BCR of 149.91:1. This indicates that the surveillance measures in the elimination stage are economically favorable and that the incidence of imported case reports will tend to increase with lower-cost investment. Further, the surveillance measures in the elimination stage appear to have good prevention and control effects, and high sensitivity is maintained in case surveillance.
The study results show that health education investment only accounted for 12.28% of the total cost, while the bene t from improving residents' awareness of malaria prevention accounted for 52.02% of the total bene t, indicating that the cost-output ratio for health education was relatively high. Therefore, in Fujian Province's malaria surveillance efforts and particularly during the health education activities on National Malaria Promotion Day, we should focus on increasing residents' knowledge about malaria prevention and personal protection to improve the cost-effectiveness ratio of malaria surveillance. We should do this especially in gathering places for entry-exit personnel. Meanwhile, the cost and bene t of malaria surveillance per capita are 1.07 yuan and 192.23 yuan, respectively. This indicates that the cost per capita of malaria surveillance was relatively small, while the effect of malaria surveillance was positive.
In sum, Fujian Province can effectively control and manage malaria cases based on various risk levels, with a particular focus on the surveillance and management of imported cases. The surveillance measures being implemented in the elimination stage of malaria are feasible and effective, and strong economic and social bene ts have been achieved. These ndings are in line with the global malaria strategy put forth at the World Health Assembly in 2015 and are also similar to many studies (16,20,24) .
To date, very few health economics evaluations have been conducted in the context of malaria surveillance. The framework and results of this study conform to the principles of health economics, and they have a certain reference value for current malaria surveillance practices. Given time and research capacity constraints, some potentially in uential factors (such as the policy environment) were not considered at this stage. Some data were estimated based only on the actual situation and interview results, which may have interfered with the accuracy of the analysis model. It is hoped that in the future, modi cations to this approach will allow for more precise results, which will serve as an even more comprehensive reference for the real work of malaria surveillance.

Conclusion
A cost-bene t analysis approach allowed us to understand the current input and output characteristics of malaria surveillance in Fujian Province and analyze the bene ts of surveillance measures in the malaria elimination stage. The framework and results of this study conform to the principles of health economics, and they have a certain reference value for current malaria surveillance practices. Our study provides a reference for further malaria elimination work and also provides a scienti c basis for more rational formulations of malaria surveillance programs in Fujian Province.

Declarations Ethics approval and consent to participate
This study belongs to the study of health economics and does not involve ethical requirements.  Figure 1 The proportion of cost structure of annual average surveillance measures for malaria elimination in Fujian Province