Economic burden and associated factors of measles patients in Zhejiang Province, China

ABSTRACT

This study aimed to figure out the economic burden of measles patients and explore the associated factors for total cost in measles cases that occurred in the year 2015 from Jiaxing, Jinhua, and Taizhou cities in Zhejiang Province, China. Direct interviews were conducted to collect information on patient expenses during treatment, including outpatient expenses, hospitalization expenses, self-treatment fees, productivity loss, and transportation fees. Descriptive epidemiological methods and chi-square tests were used to assess the direct and indirect cost of measles patients. Ordinal logistic regression was applied to explore the possible factors contributing to cost. A total of 136 measles cases were investigated and the average direct cost, indirect cost, and total cost were #747.14, #520.12, and #1,267.26, respectively. Direct cost accounted for 58.96% of the total cost, which was significantly higher than the indirect cost (P < 0.001). In 2015, 1,386 confirmed cases were reported in the Zhejiang Province, and the overall direct, indirect, and total economic burden reached #1.04 million, #0.72 million, and #1.76 million, respectively. Quality-adjusted life years for measles patient were calculated to be 76.06 in Zhejiang, 2015. Hospitalization, occupation, complication, disease duration, age, and site had a significant influence on the total cost according to ordinal logistic regression, with the maximum contribution from hospitalization. Measles resulted in heavy economic burdens, and local public health departments or community health service centers should spare no effort to maintain a high rate of vaccination coverage and protect susceptible populations.

KEYWORDS:

• Measles
• economic burden
• cost associated factors
• Zhejiang province
• public health

Introduction

Measles is a highly contagious disease caused by the measles virus with symptoms including high fever, cough, runny nose, and skin rash. Before the measles vaccine licensure in 1963, an estimated 2.6 million worldwide deaths occurred annually, mostly a result of complications including severe diarrhea, encephalitis, and pneumonia.¹ There were approximately 110,000 deaths from measles in 2017, mostly in children less than 5 y old from developing countries.¹ These data show that while the vaccine is highly effective and in the current widespread use, measles still to this day causes a heavy burden to the society and family of patients.

In China, the incidence rate ranged from 200 to 1,500 cases per 100,000 people. Since the widespread use of the vaccine was adopted in 1978, the incidence rate has been reduced by 99% and epidemic outbreaks have significantly declined.² Zhejiang is an economically developed province in southeast China that has considerably benefitted from the National Expanded Program on Immunization (EPI). Due to effective vaccines and the sustained high vaccination coverage rates, the measles incidence rate sharply decreased from the highest value of 3,035.61 cases per 100,000 people in 1959 to a historical low of 0.58 cases per 100,000 people in 2017. The immunization schedule for measles in the Zhejiang Province is to receive the first dose of measles-rubella (MR) vaccine at 8 months of age and a second dose of measles-mumps-rubella (MMR) at 18 months of age, which were included in the Zhejiang provincial EPI program in 1978 and 2007, respectively.

Although the incidence rate of measles is well controlled in Zhejiang, the global disease burden is still high. There has been an increase in reports of imported cases with new genotypes in China, which have helped highlight the challenges and threats. In 2017, the first measles case with genotype D8 was found in Zhejiang, a genotype that was previously mainly prevalent in India, Bangladesh, Germany, and Australia.^3-6 In contrast, measles with H1 genotype was the main epidemic strain in China. A large population migrates to Zhejiang every year, which may weaken the immunity barrier of the public against the measles virus and increase the imported risk. The demographic structure of the province also changed as a result of this migration, leading to a high incidence rate of measles in adults and newborn babies less than 8 months old resulting in increased health-care investments.⁷

There is an increased government need for evidence-based data to optimize the allocation of health resources and enhance their utilization efficiency. Studies on disease burden not only help gather a better understanding of the impact of measles but also provide evidence and data for further economic evaluation of vaccines and strategies for measles prevention and control. In addition, it is important to determine the switching trend of disease characteristics. Measles disease burden in the Zhejiang Province with a particular emphasis on the economic costs of measles patients has not been evaluated. We conducted a survey to quantify the cost associated with measles, including direct and indirect costs, and to analyze the factors that influenced economic burden. This study provided evidence-based data that could be used in policies aimed to further measles elimination.

Results

Base case analysis

A total of 138 patients were investigated, of which two opted out of the study halfway due to revocation of consent, resulting in an overall effective rate of 98.55%. Death and permanent disability were not noted in the survey. Among 136 patients, 45 were from Jiaxing, 51 from Jinhua, and 40 from Taizhou cities within Zhejiang province. Hospitalized cases comprised 17.65% of the study population. The mean age was 29 y, and the majority of cases were either adults or babies less than 8 months of age. Female patients made up 73 (53.68%) cases, and 75 patients (55.15%) had insurance while 61 (44.85%) did not. Average household annual income was 17,687.86 dollars, while individual annual income was 4,796.08 dollars. Median days of illness were 11, while the shortest and the longest days were 5 and 36, respectively. Only six patients (4.41%) had clear immunization history with measles vaccine. Of the remaining cases, 39 patients (28.68%) were not vaccinated and 91 (66.91%) had unclear vaccination status. Complications were seen in 34 (25%) patients, including pneumonia (11.76%), diarrhea (11.76%), tracheitis (0.74%), and encephalitis (0.74%). Detailed patient characteristics are listed in Table 1.

Table 1. Characteristics of 136 measles cases in Zhejiang Province, 2015.

Characteristics	No. of cases	%
Gender
Male	63	46.32
Female	73	53.68
Age
<8 months	26	19.12
8 months–18 months	9	6.62
18 months–15 y	12	8.82
≥15 y	89	65.44
City
Jiaxing	45	33.09
Jinhua	51	37.50
Taizhou	40	29.41
Hospitalization
Yes	112	82.35
No	24	17.65
Occupation
Children, student	47	34.56
Civil servants, commercial service	21	15.44
Farmer, worker	48	35.29
Jobless, retired	20	14.71
Vaccination
Yes	6	4.41
No	39	28.68
Unknown	91	66.91
Major means of payment
Medical insurance	75	55.15
Self-pay	61	44.85
Complication
None	102	75.00
Pneumonia	16	11.76
Diarrhea	16	11.76
Tracheitis	1	0.74
Encephalitis	1

Economic burden

The direct cost (DC), indirect cost (IC), and total cost (TC) for a single measles patient were #747.14, #520.12, and #1,267.26, respectively, as shown in Table 2. Direct cost accounted for 58.96% of the total cost and was significantly higher than the indirect cost (Z = −4.04, P< 0.001). Hospitalization expenses mainly contributed to direct cost. According to our survey, death and disability were not noted and loss of value due to disability and death were not considered. The cost of work loss accounted for the majority of indirect cost (>95%). Only two patients (1.47%) hired health-care workers, and the rest were cared for by family members. The median work loss of family caregivers for adult patients (≥18 y old) was 3.5-person days, which was significantly lower (P < 0.001) than for minor patients (10-person days).

Table 2. Costs of measles patient (USD) in Zhejiang, 2015.

Item	Overall*	Average	% of total cost
Direct cost	101610.49	747.14	58.96
Outpatient expenditure	11464.56	84.30	6.65
Hospitalization expenditure	84846.43	623.87	49.23
Self-treatment and nutrition supplements	5299.50	38.97	3.07
Indirect cost	70736.81	520.12	41.04
Transportation fee	3038.92	22.34	1.76
The cost of work loss due to measles for adult cases	38528.37	283.30	22.36
The cost of work loss due to looking after patient	29097.27	213.95	16.88
The cost of hiring health-care worker	72.25	0.53	0.04
Total cost	172347.31	1267.26	100.00

Note: *Overall means all the 136 cases in the survey.

According to the China Information System for Disease Control and Prevention, 1,386 laboratory-confirmed measles cases were reported for all of 2015 in Zhejiang Province. Chi-square tests of the 136 samples were well representative of the measles cases in Zhejiang province in 2015. No significant differences were observed in age, occupation, and sex between samples and the population (χ²₁ = 5.019, P₁= 0.17; χ²₂ = 2.115, P₂= 0.146; χ²₃ = 5.304, P₃= 0.151, respectively). Therefore, the estimated direct, indirect, and total cost of measles patients in 2015 in Zhejiang province were extrapolated to be $1.04 million, $0.72 million, and $1.76 million, respectively.

Influencing factors of measles economic burden

Kruskal–Wallis H tests and Mann–Whitney U tests indicated that region, vaccination, or sex did not have significant statistical influence on economic burden. Although a significant difference was not observed in indirect and total cost, a significant difference was observed in direct cost by age. Further analysis indicated that direct cost of patients less than 8 months old (detailed in Table 3) was significantly higher than that of patients aged between 18 months to 15 y (P_adj= 0.026). Hospitalization cases had a significantly higher direct costs and total costs than outpatient cases (P₁< 0.001, P₂< 0.01), while no differences were observed for indirect costs between groups (P= 0.24). Significantly higher costs were observed in patients with complications (P₁< 0.001 for DC, P₂= 0.04 for IC, P₃< 0.001 for TC) compared to those without. Patients with pneumonia had a significantly longer duration of disease (Z = −2.770, P = 0.006), higher economic burden (Z = −3.765, P < 0.001) including direct (Z = −2.177, P = 0.029) and indirect (Z = −3.679, P < 0.001) costs. Patients with insurance had a significantly higher direct and total costs than those without (P₁< 0.001, P₂< 0.01, Table 3).

Table 3. Univariate analysis of the factors associated with the economic burden (USD) of measles cases in Zhejiang, 2015.

Influencing factor	Direct cost	Indirect cost	Total cost
City
Jiaxing	695.92	411.78	1107.70
Jinhua	763.64	508.63	1272.27
Taizhou	783.72	656.66	1440.39
χ^2	2.33	4.08	4.27
p Value	0.31	0.13	0.12
Age
<8 months (1)	986.95	355.86	1342.81
8 months–18 months (2)	543.11	295.54	838.65
18 months–15 y (3)	378.53	612.29	990.82
≥15 y (4)	720.52	573.95	1294.47
χ^2	8.62	4.60	1.32
p Value	0.04	0.20	0.73
Occupation
Children, student (1)	797.54	418.20	1215.74
Civil servants, commercial service (2)	615.61	582.71	1198.32
Farmer, worker (3)	793.79	678.43	1472.22
Jobless, retired (4)	654.80	314.00	968.81
χ^2	4.47	22.66	12.30
p Value	0.22	0.00	0.01
Vaccination
Yes	544.38	597.52	1141.90
No	860.87	392.72	1253.59
Unknown	711.76	569.62	1281.39
χ^2	0.99	3.09	0.12
p Value	0.61	0.21	0.94
Hospitalization
Yes	879.35	544.99	1424.34
No	130.13	404.10	534.24
Z	−7.46	−1.17	−5.59
p Value	0.00	0.24	0.00
Gender
Male	713.71	527.91	1241.62
Female	775.98	513.40	1289.39
Z	−0.32	−0.72	−0.27
p Value	0.75	0.47	0.79
Complication
With	1034.37	757.76	1792.13
Without	651.39	440.91	1092.30
Z	−3.15	−2.08	−3.38
p Value	0.00	0.04	0.00
Insurance
With	907.11	615.39	1522.50
Without	550.45	402.99	953.44
Z	−4.44	−1.91	−3.87
p Value	0.00	0.06	0.00

Spearman’s rank correlation analysis was conducted to analyze the correlation between various costs and non-normal continuous variables such as duration of disease and income. The longer the duration, the higher the costs (P< 0.001 for all three costs). Neither household annual income nor individual annual income had a significant influence on cost.

The previously listed variables were included in multivariate analyses for total cost using ordinal logistic regression models. According to the distribution, total cost was converted to a three-level ranked variable (1: <#642.26, 2: #642.26–#1,605.65, 3: ≥#1,605.65). Test of parallel lines and the likelihood ratio test met all demands (χ₁²= 4.440, P₁= 0.992; χ₂²= 99.375, P₂< 0.001). Age, duration days, site, occupation, hospitalization, and complication significantly influenced total cost (Table 4). Maximum contributors were hospitalization, followed by occupation, complication, duration days, age, and site (Odds ratios: 40.579, 9.673, 3.009, 1.187, 1.062, and 0.185, respectively).

Table 4. Analysis of ordinal logistic regression model on total cost in Zhejiang, 2015.

Factors	Estimate	OR	Std. error	Wald	df	p Value	95% CI
							Lower bound	Upper bound
Total cost = 1	5.422		1.303	17.308	1	0.000	2.868	7.977
Total cost = 2	9.459		1.541	37.661	1	0.000	6.438	12.480
Age	0.060	1.062	0.026	5.409	1	0.020	0.009	0.110
Income	−0.024	0.976	0.025	0.941	1	0.332	−0.074	0.025
Duration days	0.172	1.187	0.041	17.256	1	0.000	0.091	0.253
Site = Jiaxing	−1.688	0.185	0.555	9.269	1	0.002	−2.775	−0.601
Site = Jinhua	−0.763	0.466	0.531	2.067	1	0.150	−1.803	0.277
Site = Taizhou*	0				0
Sex = Male	0.165	1.179	0.419	0.155	1	0.694	−0.657	0.986
Sex = Female*	0				0
Occupation = 1	2.603	13.499	2.056	1.602	1	0.206	−1.427	6.632
Occupation = 2	1.585	4.882	0.824	3.698	1	0.054	−0.031	3.201
Occupation = 3	2.269	9.673	0.731	9.647	1	0.002	0.837	3.701
Occupation = 4*	0				0
Vaccination = No	−0.671	0.511	1.839	0.133	1	0.715	−4.276	2.933
Vaccination = Yes	0.279		2.009	0.019	1	0.889	−3.658	4.216
Vaccination = Unclear*	0				0
Hospitalization = Yes	3.703	40.579	0.704	27.659	1	0.000	2.323	5.083
Hospitalization = No*	0				0
Insurance = Yes	−0.382	0.683	0.488	0.613	1	0.434	−1.338	0.574
Insurance = No*	0				0
Complication = Yes	1.102	3.009	0.517	4.541	1	0.033	0.088	2.115
Complication = No*	0				0

Note:* was set to be the reference value.

QALYs

Using TTO valuation techniques in Japan, EQ-5D-3L status was converted to EQ-5D index score, which ranged from −0.111 to 0.848 with median score of 0.532. The first and third quartiles were 0.418 and 0.705, respectively. According to our survey, the median duration of measles was 11 d (0.030 y) which corresponds to the loss of survival years due to measles status. World health statistics in 2016 demonstrated that the 2015 life expectancy at birth in China was 76.1 y.⁸ Therefore, for a measles patient, the survival years of healthy status was 76.070 y. QALYs for measles patient were 76.086 y in Zhejiang, 2015 (Table 5).

Table 5. QALYs for measles patients in Zhejiang, 2015.

Status	Utility weights (wi)	Survival years (yi)	wiyi
Measles	0.532	0.030^a	0.016
Healthy	1	76.070^b	76.070
Total	-	76.100^c	76.086

Note: a survival years of measles status = the median duration days of measles patients.

b survival years of healthy status = c – a.

c Life expectancy at birth in China in 2015 was 76.1 y according to the World health statistics 2016.

Discussion

Measles is a highly infectious disease that can be eliminated with two-dose vaccination rates of 93% to 95%.^9,10 However, outbreaks still occur due to the difficulty in maintaining high coverage rates and high imported risk. Colzani et al.¹¹ reported a significant negative relationship between coverage and measles burden after comparing 29-member states of the European Union, emphasizing the importance of maintaining high national vaccination coverage. Recently, Europe observed a fourfold increase in measles cases in 2017 compared to the previous year, which affected 21,315 people and caused 35 deaths, following a record low of 5,273 cases in 2016. One in four European countries reported large measles outbreaks (>100 cases), and these outbreaks can continue to occur until every susceptible child and adult is vaccinated. Although reported vaccination rates have been greater than 90% during the last decade, Zhejiang (324 cases) still ranks fifth among all 31 provinces in China in 2017 with respect to most measles cases and has a relatively high disease burden.

We investigated the direct and indirect economic burden of measles and determined factors associated with costs of measles patients in Zhejiang Province. Our survey demonstrated that the mean direct, indirect, and total cost per measles case in 2015 were #747.14, #520.12, and #1,267.26, respectively. According to the China Information System for Disease Control and Prevention, 1,386 laboratory-confirmed measles cases were reported in 2015 in Zhejiang Province and resulted in extrapolated direct, indirect, and total costs of #1.04 million, #0.72 million, and #1.76 million, respectively. Direct cost was significantly higher than indirect cost, which may be due to the low mortality rate and low permanent disability rate as a result of vaccines. Hospitalization expenditures were the main cost (#623.87), followed by costs associated with work loss. In China, measles cases are isolated until the fourth day after rashes develop, during which time patients should be in the hospital or at home. Therefore, the cost of work loss is considerable. Nowadays, with the aid of vaccines, the population affected by measles in China has shifted from children less than 10 y to infants and adults. Stable changes in population distribution may affect total cost, and the results indicated the importance of measles elimination programs and corresponding high cost-benefits of measles immunization.

A study investigating the economic burden of 1945 measles cases in China reported that direct and total costs were CNY 1,186.6 and CNY 1,996.1, respectively, in 2004.¹² The estimated values were, respectively, CNY 1,932.85 and CNY 3,251.44 in 2015, considering the inflation rate of 5%, which were both 34% of the same value in our survey.¹³ This disparity may be due to high economic development and higher hospital costs in Zhejiang Province compared to the average cost in China.

A survey by Plass et al. investigating 1,217 cases between 2005 and 2007 revealed that measles resulted in an average of 740 annual DALY losses in Germany.¹⁴ An investigation of 1,749 measles cases in 2006 revealed that the average cost was EUR 373 per measles case and EUR 1,877 per hospitalization case.¹⁵ Discount to the year 2015 with the rate of 5%, the estimated cost per case was approximately the same in our survey.

A cost-benefit analysis of two-dose measles immunization in Canada demonstrated that direct and total cost per measles case was #301 and #929 in 1995, respectively, which was approximately #760.61 and #2,347.54 in 2015 after accounting for inflation.¹³ Direct cost was almost the same as that in our study. Difference was observed in indirect cost of #1,586.92 in 2015 for the Canadian measles cases, which was more than twice the direct cost. High wages of people and high caregiver labor costs in developed countries may have contributed to this observed difference.

Except for sporadic cases, Ortega-Sanchez et al. estimated the economic burden of measles outbreaks in the United States in 2011.¹⁶ A total of 16 outbreaks occurred in the US, with 107 confirmed cases. The total economic burden on local and state public health institutions ranged from an estimated #2.7 million to #5.3 million. It is alarming to note that measles outbreaks still occur even in developed countries with high coverage rates. This may partly be due to the persistent risk of imported measles and the presence of susceptible populations who are unvaccinated. Researchers in England also conducted a similar study to evaluate the total societal costs of outbreaks.¹⁷ In 2012, 2,458 measles cases were reported in Merseyside, and the estimated total cost of the outbreak was GBP 4.4 million, with health-care provider costs accounting for 15%, public health costs 40%, and societal productivity losses 44%. These studies all emphasized the importance of effective control and timely management of outbreaks by governments.^16-19

The ordinal logistic regression model indicated that age, disease duration, site, occupation, hospitalization, and complications had significant influence on the total economic burden. Hospitalization expenditure accounted for almost half the total cost. Older age along with increased numbers of the illness days equated to higher total cost. Compared with patients in Taizhou, the odds ratio for patients in Jiaxing with higher total cost was 0.185, indicating that total costs for cases in Taizhou were higher than those in Jiaxing. This may be due to increased relative economic development in Taizhou. The possibility of patients who were farmers or workers to have a higher total cost was 9.673 times that of non-working patients. Further comparison indicated that the difference mainly resulted from indirect costs, since non-working patients had much lower daily wages or no earnings, and farmers or workers had longer durations of illness. During this study, complications such as pneumonia (11.76%), diarrhea (11.76%), tracheitis (0.74%), and encephalitis (0.74%) were reported. Patients with pneumonia had a significantly longer duration of disease and a higher economic burden. Research in Italy revealed that pneumonia was the most common complication in measles patients less than 10 y old.¹⁸ The average hospitalization cost was EUR 1,700 in 2003 and would be much higher (EUR 2,721) if complications occurred.

Although the remaining explanatory variables did not significantly influence total cost in the regression model, they could explain differences in the univariate analysis to some extent. Patients with insurance had a higher direct and total cost possibly due to clinical overtreatment and unnecessary use of expensive antiviral drugs. In addition, some patients with mild disease may actively request hospitalization due to higher insurance reimbursement rates. Although vaccination did not affect total cost per case in this study, many cases and hospitalizations have been avoided with the help of measles vaccines. Annual incidence rates peaked at 3035.61/10⁵ cases without vaccination and sharply decreased to 2.52/10⁵ cases in 2015. Thus, vaccines provide an important role in benefiting patients and society with regard to reducing cost burden.

This study presents several limitations. First, measles epidemics are stably controlled in Zhejiang Province so far and the incidence rates were between 0.10 and 2.52 per 10,0000 people during 2010–2018, with no fatalities. Death and disability were not observed in the survey; therefore, loss of value caused by these two variables was not considered. According to some long-term sequelae studies, 20–30% of cases will have encephalitis as a complication.²⁰ Therefore, indirect costs were underestimated. Second, the sample size is small, especially in patients with complications. Although we included almost all measles cases reported in the China information system in the surveillance sites, more sample sites can be included, and the observation period can be extended to cover the entire year. Thirdly, we selected EQ-5D-3L instead of EQ-5D-5L to calculate the utility weight of different statuses. While EQ-5D-5L has increased sensitivity and reduced ceiling effect, the standard value set for China has not been established for our study time period.

Conclusion

In conclusion, this study quantifies the cost associated with measles in the Zhejiang Province of China. Direct, indirect, and total costs were $747.14, $520.12, and $1,267.26, respectively, in 2015. Furthermore, hospitalization, occupation, complication, disease duration, age, and site were found to significantly influence total cost. Local public health departments and community health service centers should spare no effort to maintain a high rate of vaccination coverage and protect susceptible populations, so as to reduce burden on medical resources and to provide an overall health benefit to the society.

Methods

Subjects

Jiaxing, Jinhua, and Taizhou were selected as surveillance cites considering their economic level and geographic location. New laboratory-confirmed cases were diagnosed based on standard case definitions according to the Chinese Measles Surveillance Program using measles IgM or measles RNA-positive result for any clinical specimen.¹⁷ A sample size of 116 was calculated for an estimated 20% cases who may not complete the whole survey, and to provide 90% power with statistical parameters (α= 0.05, β= 10%, σ= 0.5).²

This study was approved by the ethics committee of the Zhejiang Provincial Center for Disease Control and Prevention. Written informed consent was obtained from the adult participants or guardians of children prior to enrollment.

Field investigation

The survey was conducted from September to December 2015. All the laboratory-confirmed measles cases that occurred in 2015 were investigated through face-to-face interviews by trained professional investigators using specific questionnaires to obtain basic information, experience of treatment, nutritional supplement expenditure, transportation fees, and work-day loss. EQ-5D-3L was also included. Medical expenses occurred in the hospitals were obtained from the hospital service charge system to reduce recall bias.

Economic burden

Economic burden was classified into two categories: direct and indirect. Direct economic burden was defined as total outpatient and inpatient expenditures directly related to measles, including outpatient expenditure, hospitalization expenditure, prescription drug costs, self-treatment, and nutritional supplement expenditure. Indirect economic burden was defined as the loss of value caused by temporary disability, permanent disability, and death due to measles. This also included work loss of health-care workers, including the cost of work loss caused by disability or death due to measles in adults; cost of work loss for adults when their children, relatives, or friends had measles; transportation fees; and nursing fees if a health-care worker was employed. All costs were converted to U.S. dollars at the average exchange rate of 1:6.228 in 2015 according to the National Bureau of Statistics of China.

This method estimated the cost of work loss based on the average annual income of a gainfully employed person from the Zhejiang Provincial Bureau of Statistics ($7,730.41). The cost per work-day loss was calculated using the average annual income divided by the average number of work days per year ($7,730.41/250 days = $30.92 per day). The number of work days lost was based on information obtained from an epidemiological survey. Transportation fee was calculated based on an expense of $0.13 per kilometer when driving.

X1: loss of value caused by disability due to measles = (life expectancy ˗ age of disabled patient) × average annual income × disability weights

X2: loss of value caused by death due to measles = (life expectancy ˗ age of disabled) × average annual income

X3: cost of work loss due to measles for adult cases = number of days off × average daily wage

X4: cost of work loss because of caring for patient = number of days off × average daily wage

X5: transportation fee = $0.13 per kilometer × distance from home to hospital (roundtrip)

Indirect economic burden = X1 + X2 + X3 + X4 + X5; total economic burden = direct economic burden + indirect economic burden.

Quality-adjusted life years (QALYs)

The utility weight in QALYs was calculated using the EQ-5D-3L (EuroQol Research Foundation) from five domains: mobility, self-care, usual activity, pain/discomfort, and anxiety/depression. The EQ-5D questionnaire was widely used due to its simplicity to interpret, administer, and score in cost-utility analyses.²¹ The formula used for the computation of QALYs is given as follows:

(1) $QALY=\sum _{i=1}^n{w}_i{y}_i$(1)

where “n” is the number of functional status (two statuses were contained in this research: the condition of having measles and that of being healthy), “y_i” is the number of survival years of different functional statuses. Survival years of measles status was the median measles duration of measles patients. Survival years of healthy status was the difference between life expectancy and the survival years of measles status. Given that China is in Asia, and the time trade-off (TTO) valuation technique in Japan was widely used, the standard value set in Japan was used to convert EQ-5D states into EQ-5D index, where “w_i” represented the utility weight of every functional status.

Statistical analysis

All data were collected by Epidata 3.1 and analyzed by SPSS 23.0. Chi-square test or Fisher’s test for comparison of rates were used for statistical analysis. Kruskal–Wallis H test was used to compare the economic burden among different groups. The total costs were appropriately ranked as low, average or high according to the distribution, and ordinal logistic regression was applied to analyze factors influencing the total cost. Statistical significance was defined as P < 0.05. The annual discount rate was defined as 5%.¹³

Abbreviations

EPI	=	National Expanded program on Immunization
MR	=	Measles-Rubella vaccine
MMR	=	Measles-Mumps-Rubella vaccine
TTO	=	Time Trade-off
DC	=	Direct cost
IC	=	Indirect cost
TC	=	Total cost
QALYs	=	Quality-adjusted life years
DALYs	=	Disability-adjusted life years
CNY	=	China Yuan
EUR	=	European Dollar
GBP	=	Great Britain Pound
USD	=	United States Dollar
US	=	United States.

Disclosure of potential conflicts of interests

No potential conflicts of interest were disclosed.

Authors’ contributions

He, Deng and Zhou conceived and designed the study. He, Deng, Zhou, Yan, and Tang performed the field investigation. Deng wrote the paper. Xie, Fang, Zeng, and Fu provided technical guidance to the study and the manuscript. All authors read and approved the manuscript.

Acknowledgments

We sincerely thank the staff member from the Center for Disease Control and Prevention of Jiaxing, Jinhua, and Taizhou in Zhejiang province for all their assistance with this research. We would also like to express our deepest gratitude for those participants who took part in the study and provided the samples.

Additional information

Funding

There is no funding for this study.