Economic burden of measles and its influencing factors in Fujian, China

ABSTRACT

Background

Measles is a highly-contagious, serious diseases that can lead to potentially fatal illness, disability and death . We conducted an investigation to calculate the economic burden of measles cases from 2018 to 2019 and to analyze factors that influenced the total costs of measles cases in Fujian Province, China.

Methods

We investigated confirmed cases of measles by telephone interview, from 2018 to 2019, including demographic characteristics, therapeutic measures, self-treatment and nutritional supplement expenditure, transportation fees, and lost wages. Medical expenses in the hospitals were obtained from the hospital service charge system.

Results

A total of 131 measles cases were investigated, the average direct cost, indirect cost, and total cost were $518, $284, and $802, respectively. The total cost was 15.5% of Annual Per Capita Disposable Income of Households ($5 162) in Fujian. Hospitalization (OR = 98.6, 95%CI: 21.1 ~ 460.6) and complication (OR = 8.7, 95%CI: 1.3 ~ 58.0) significantly influenced the total cost according to binary logistic regression, and an outbreak of measles may pose a significant threat to household finances in a short term.

Conclusions

The economic burden of measles was high when compared with Annual Per Capita Disposable Income of Households. The resurgence of measles and measles outbreaks increased economic burden of household finances.

KEYWORDS:

• Economic burden
• measles
• cost influencing factors
• vaccine-preventable disease
• Fujian province

Introduction

China started to implement nationwide measles vaccination in 1978 with the start of the national Expanded Program on Immunization (EPI). With the mass vaccination, the incidence per 100 000 population decreased from 9.5 in 2005 to 2.8 in 2018^1,2. Fujian province considerably benefits from the EPI. The measles incidence rate dramatically decreased from 410.2 per 100 000 population in 1978 to 0.04 per 100 000 population in 2020.

Although the measles epidemic in Fujian Province has been stably controlled, the size and density of China’s population, the high transmissibility of measles virus, and the persistence of global measles virus transmission suggest that measles will remain in Fujian for years to come. The H1 measles genotype is the only genotype indigenous in Fujian province for over 20 years. In recent years, however, imported measles viruses have been detected, especially in 2019, it was found that 55.0% of genotyped measles viruses were B3 or D8, which was previously mainly prevalent in Germany, Australia, India, and Bangladesh^3–7. All of these could lead to resurgence of measles outbreak in Fujian Province, leading to a large increased households spending in a short term⁸.

Research on the economic burden of measles can provide evidence and data for measles prevention and control strategies and vaccine economic evaluation. Also, the health sector needs evidence-based data to optimize the limited allocation of health resources. But there is no empirical cost-of-illness study for measles in Fujian. So we conducted a survey to quantify the direct and indirect cost associated with measles. This study was designed to identify factors affecting economic burden of measles in Fujian and provide evidence gap research in Fujian.

Method

Subjects

According to the China Information System for Disease Control and Prevention, 141 laboratory-confirmed measles cases were reported in 2018–2019 in Fujian Province, of which 131 cases were investigated and 10 cases refused to participate. This study was approved by the ethics committee of the Fujian Provincial Center for Disease Control and Prevention. Informed consent was obtained from the adult participants or guardians of children prior to investigate.

Field investigation

The survey was conducted from October 2019 to January 2020. 131 measles cases were investigated by telephone interviews, which were performed by trained professional investigators. A standardized questionnaire was used to obtain information, including gender, age (<8 months, 8–23 months, 2–14 years, ≥15 years), hospitalization, visit at distance (go to the hospital which is not in the place of residence), vaccination, hospital exposure history (within 7–21 days), complication, self-treatment and nutritional supplement expenditure, transportation fees, and work-day loss. Medical expenses occurred in the hospitals were obtained from the hospital service charge system to rule out 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, and transportation fee. Indirect economic burden was defined as the economic loss caused by temporary disability, permanent disability, and death due to measles, and the economic loss caused by missing work or school due to illness in adults, or that due to taking care of their children, relatives, or friends who had measles were also included. All the costs were converted to U.S. dollars at the average exchange rate of 1:6.9 in 2019 according to the National Bureau of Statistics of China.

We estimated the economic loss based on the average annual income of a gainfully employed person from the Fujian Provincial Bureau of Statistics ($9,100). The per work-day economic loss was calculated by dividing the average annual income by the average number of work days per year ($9,100/250 days = $36.40 per day).

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

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

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

X4: economic loss because of taking care of patients = number of days off × average daily wage

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

Statistical analysis

All data were cleaned by Epidata 3.0 and analyzed by SPSS 20.0. Mann-Whitney U or Kruskal-Wallis H tests were used to compare the economic burden among different groups. The total costs were appropriately ranked as average or high according to the median, and binary logistic regression was applied to analyze factors influencing the total cost. Statistical significance was defined as P < .05. The annual discount rate was defined as 5%⁹.

Results

Base case analysis

The average age was 21.7 ± 16.6 y(4 months to 52 y), and 48.9% (64) were female. Among these, 45.0% (59) were hospitalized cases, and 38.9% (51) were treated in neighboring counties. Twenty-eight cases (21.4%) had immunization history with measles vaccine. 27 cases (20.6%) had hospital exposure history within 7–21 days before illness. 21 (16.0%) cases had complications. The Annual Per Capita Disposable Income of Households was $5162.5 in Fujian in 2019. Median duration of measles case were 10 days (5–33 days). (Table 1).

Table 1. Characteristics of the 131 measles cases in Fujian Province, 2018–2019

Characteristics	No. of cases	%
Gender
Male	67	51.1
Female	64	48.9
Age
<8 months	10	7.6
8 months-23 months	28	21.4
2 y-14 y	11	8.4
≥15 y	82	62.6
Hospitalization
Yes	59	45.0
No	72	55.0
Visit at distance
Yes	51	38.9
No	80	61.1
Vaccination
Yes	28	21.4
No	103	78.6
Hospital exposure history
Yes	27	20.6
No	104	79.4
Complication
Yes	21	16.0
No	110	84.0

Economic burden

The Table 2 showed the direct cost (DC), indirect cost (IC), and total cost (TC) for a single measles case were $518, $284, and $802, respectively. The direct cost accounted for 64.6% of the total cost and was significantly higher than the indirect cost (Z = 3.2, P < .05). Accounting for 55.1% of the total cost, hospitalization expense was the main contributor to the direct cost. No deaths and disabilities were found in the survey, so the economic loss due to death and disability were not taken into account. For adult cases, the economic loss due to measles did not significantly differ from that due to taking care of patients (Z = −0.4, P > .05).

Table 2. Costs of measles patient (USD) in Fujian, 2018–2019

Item	Overall	Average	% of total cost
Direct cost	67807	518	64.6
Outpatient expenditure	4555	35	4.3
Hospitalization expenditure	57872	442	55.1
Self-treatment and nutrition supplements	3700	28	3.5
Transportation fee	1680	13	1.6
Indirect cost	37223	284	35.4
Economic loss due to measles for adult cases	18354	140	17.5
Economic loss due to taking care of patient	18869	144	18.0
Total cost	105030	802	100.0

Influencing factors of measles economic burden

Mann-Whitney U and Kruskal-Wallis H tests indicated that gender, visit at distance, vaccination, hospital exposure history did not influence measles economic burden. Hospitalization cases had significantly higher direct costs and total costs than outpatient cases (P₁ < 0.001, P₂ < 0.001). In addition, economic burden of measles varied by age groups: significantly higher costs were observed in patients aged less than 8 months (P₁ < 0.01 for DC, P₂ < 0.001 for IC, P₃ < 0.01 for TC) compared to those aged over 15 y. Also, significantly higher costs were observed in patients with complications (P₁ < 0.001 for DC, P₂ < 0.05 for IC, P₃ < 0.001 for TC) compared to those without. Detailed univariate analysis of factors associated with measles economic burden are listed in Table 3.

Table 3. Univariate analysis of factors associated with the economic burden (USD) of measles in Fujian, 2018–2019

Influencing factor	Direct cost	Indirect cost	Total cost
Gender
Male	488	295	783
Female	548	273	822
Z	−0.6	−1.9	−0.2
p Value	0.54	0.05	0.84
Age
<8 months	1028	388	1416
8 months-23 months	654	329	983
2 y-14 y	529	263	791
≥15 y	407	259	666
X^2	10.8	28.0	14.8
p Value	0.01	0.00	0.00
Hospitalization
Yes	905	298	1203
No	200	273	473
Z	−8.5	−0.1	−8.1
p Value	0.00	0.91	0.00
Visit at distance
Yes	627	301	928
No	448	273	721
Z	−0.4	−0.4	−0.6
p Value	0.72	0.67	0.53
Vaccination
Yes	513	271	784.
No	519	288	807
Z	−0.6	−0.2	−0.5
p Value	0.54	0.85	0.59
Hospital exposure history
Yes	541	287	828
No	429	272	701
Z	−0.5	−0.3	−0.7
p Value	0.61	0.81	0.51
Complication
Yes	1410	368	1778
No	347	268	615
Z	−6.2	−2.7	−6.1
p Value	0.00	0.01	0.00

The previously listed variables were included in a multivariate analysis for total cost using binary logistic regression. According to the median total cost, we converted it to a two-level ranked variable (1: ≤$612; 2: >$612). Hospitalization (OR = 98.6, 95%CI: 21.1 ~ 460.6) and complication (OR = 8.7, 95%CI: 1.3 ~ 58.0) significantly influenced the total cost of measles (Table 4).

Table 4. Multivariate analysis on factors influencing the total cost of measles in Fujian, 2018–2019

Factors	β	SE	Wald	p Value	OR(95%CI)
Gender
Male					1.0
Female	1.1	0.7	2.3	0.13	3.0(0.7 ~ 12.4)
Age
<8 months					1.0
8 months-18 months	−0.5	1.2	0.2	0.68	0.6(0.1 ~ 6.6)
2 y-14 y	−0.2	1.0	0.1	0.84	0.8(0.1 ~ 5.4)
≥15 y	−0.3	1.4	0.1	0.81	0.7(0.5 ~ 10.7)
Hospitalization
No					1.00
Yes	4.6	0.8	34.1	0.00	98.6(21.1 ~ 460.6)
Visit at distance
No					1.00
Yes	−0.4	0.6	0.4	0.53	0.7(0.2 ~ 2.3)
Vaccination
No					1.00
Yes	1.0	1.1	0.9	0.34	2.7(0.4 ~ 21.3)
Hospital exposure history
No					1.00
Yes	1.1	0.8	2.0	0.16	2.9(0.7 ~ 12.5)
Complication
No					1.00
Yes	2.2	1.0	5.0	0.03	8.7(1.3 ~ 58.0)

Discussion

The high transmissibility of measles virus allows its circulation among relatively well-vaccinated populations, exposing population immunity gaps. Marcelo et al.¹⁰ reported that Brazil was declared measles-free in 2016, but the epidemic returned with a decline in vaccination coverage and the emergence of imported cases. Measles cases were all at low levels during the last decade in Fujian Province. However, measles outbreaks may occur due to high risk of importation and declining coverage rates as a result of vaccination hesitancy or omission, as well as immunization failure, which may result in a relatively high disease burden.

We investigated the direct and indirect economic burden of measles. The results showed the average direct, indirect, and total cost per single measles case were $518, $284, and $802, respectively, in Fujian Province. The total cost was higher, accounting for 15.5% of Annual Per Capita Disposable Income of Households ($5 162) in Fujian. Previous studies have indicated that, when illness-related economic costs are >10% of annual household income, it is considered catastrophic because it potentially forces households to cut consumption of necessities, and leads to increased debt or greater poverty.^11,12 The direct cost in our survey was higher than the indirect cost, which was consistent with the cost of measles in other investigations^13–15, Hospitalization expenditures were the major component (55.1%) in total cost, which may be related to higher treatment costs and longer duration of illness for inpatients. Costs associated with work loss is also noticeable. In China, measles cases are quarantined until 4 days after developing the rash, and patients should be stay in the hospital or at home during the quarantine⁹, Also, caregivers must spend a significant amount of time away from work and from the household to access care for measles treatment, hindering the household’s financial security.⁸

A survey investigating the economic burden of measles in Zhejiang China reported that the direct, indirect, and total cost were $747, $520, and $1 267, respectively, in 2015⁹ Results of our survey indicated that the economic burden of measles in Fujian was lower than that in Zhejiang. This disparity may be due to the higher cost of treatment, measles-related healthcare services and labor cost in Zhejiang. These evidence all emphasizes the resurgence of measles outbreaks was a substantial cost for households, requiring significant short-term expenditures, and maintaining high vaccination rates would likely alleviate most of this burden.

The binary logistic regression model indicated that hospitalization and complication had significant influence on the total economic burden of measles. Hospitalization expenditures accounted for more than half of the total cost, which included costs for clinical examination and medical treatment of inpatients, infection control required to stop nosocomial spread, and costs that are associated with the duration of illness. Patients with complication had significantly longer duration of disease and a higher economic burden. A survey investigating the economic burden of measles hospitalization in Italy reported that a higher mean cost per case ($3 023) was observed in hospitalizations with complication, compared to the average cost ($1 588) in those without complication¹⁶.

Although the remaining explanatory variables did not significantly influence the total cost in the regression model, they could explain differences in the univariate analysis to some extent. Patients of less than 8 months old had higher costs compared to patients aged over 15 y, because caregivers must spend considerable amount of time away from work and from the household to take care of babies 24 hours a day, and multiple caregivers are likely required.

There are several limitations of our study. First, measles epidemics have been stably controlled in Fujian Province, no deaths and disabilities were found in the survey. Therefore, loss of value caused by these two variables was not considered. Second, the sample size was small, although we included almost all measles cases in Fujian Province in 2018–2019 registered in the China information system. Third, this study did not include public health response costs, and the source of direct costs did not distinguish whether it came from out-of-pocket expenses to families, insurance company costs, or other costs. Fourth, some cost estimates were retrospective, such as self-purchased medicine cost and transportation fee, thus recall bias was possible in several cases.

Conclusion

This study improves our understanding of the magnitude of the economic burden of measles in Fujian Province. The economic burden of measles in Fujian is high when compared with Annual Per Capita Disposable Income of Households. The resurgence of measles outbreaks may require significant public expenditures in a short term and pose a significant threat to household finances. Preventing outbreaks through maintaining a high rate of vaccination coverage would likely alleviate most of this burden.

Authors’ contributions

Weiyi Pan and Junlei Chen conceived and designed the study. Junlei Chen, Weiyi Pan, Shanshan Ma, Yahong Chen and Changfu Chen performed the field investigation. Junlei Chen and Haimei Jia wrote the paper. All authors read and approved the manuscript.

Acknowledgments

We would like to express our deepest gratitude for participants in the study.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This publication was made possible with support from the Vaccine and Immunization Talent Project of Chinese Preventive Medical Association (CPMAQT_YM0218), the Fujian Provincial Science and Technology project (2015Y0049). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.