Global, regional and national burden of human cystic echinococcosis from 1990 to 2019: a systematic analysis for the Global Burden of Disease Study 2019

DOI: https://doi.org/10.21203/rs.3.rs-2842015/v1

Abstract

Background: Cystic echinococcosis (CE) is a neglected tropical parasitic disease that poses huge disease, social and economic burdens in the world. Although great strides have been achieved, multiple challenges remain to achieve the ambitious goal targeting CE set in the WHO roadmap for neglected tropical diseases 2021–2030. Estimates of the disease burden due to CE facilitate the progress towards eliminations; however, there is little knowledge on global morbidity, mortality and disability-adjusted life years (DALYs) of CE until now. This study aimed to present the most up-to-date data about the global, regional and national disease burden due to CE from 1990 to 2019 and to project trends in the next 10 years.

Methods: We measured the global, regional and national morbidity, mortality and DALYs of CE from 1990 to 2019 based on the Global Burden of Disease Study 2019 (GBD 2019) data, and we examined the correlation between socioeconomic development levels and the disease burden of CE. In addition, the disease burden due to CE was projected using Bayesian age-period-cohort analysis with integrated nested Laplace approximations from 2020 to 2030.

Results: The global number of CE cases increased from 134,980 [95% uncertainty interval (UI): (93,141 to 195,144)] in 1990 to 207,368 [95% UI: (6,347,183 to 8,769,520)] in 2019 [estimated annual percentage change (EAPC) = 0.54], and the age-standardized incidence rate (ASIR) of CE reduced from 2.65/105 [95% UI: (1.87/105 to 3.7/105)] in 1990 to 2.6/105 [95% UI: (1.72/105 to 3.79/105)] in 2019 (EAPC = ‒0.18). The number of deaths, DALYs, age-standardized mortality rate (ASMR) and age-standardized DALYs rate due to CE all appeared a tendency towards a decline from 1990 to 2019. A higher disease burden of CE was measured in women than in men in 2019. There was a significant difference in ASMR of CE in regions specified by socio-demographic index (SDI) and lower burdens of CE were estimated in high SDI regions. The global ASIR of CE was projected to appear a tendency towards a decline from 2020 to 2030; however, the ASMR and age-standardized DALY rate were projected to rise.

Conclusions: Our data may provide data-based evidence for public health officials and policy-makers to formulate and implement cost-benefit interventions to tackle the disease burden attributable to CE. More health resources are recommended to be allocated to low SDI regions, women and the elderly at ages of 55 to 65 years to reduce the disease burden of CE.

Background

Echinococcosis, caused by the larvae of the genus Echinococcus, is a global, neglected tropical zoonotic parasitic disease [1]. There are 9 Echinococcus species that have been characterized worldwide until know, and there are four of concerns in humans, including E. granulosus, E. multilocularis, E. oligarthrus and E. vogeli [2]. E. granulosus and E. multilocularis are the two most prevalent species, which cause cystic echinococcosis and alveolar echinococcosis, respectively, while E. oligarthrus and E. vogeli cause polycystic neotropical echinococcosis, which is limited in South America, Central America and North America [3].

As a neglected tropical disease, cystic echinococcosis is most prevalent in impoverished rural communities where animal husbandry is common [1]. Patients suffering from cystic echinococcosis may be asymptomatic at early stage, and clinical symptoms may present until hydatid cysts progress [4]. If inappropriately treated or untreated, a poor prognosis may be observed, with a post-surgical mortality rate of 2.2% and approximately 6.5% postoperative recurrence [5]. Cystic echinococcosis is widely prevalent across the world, and the incidence of human cystic echinococcosis is estimated to be more than 50/105 in endemic foci, while the prevalence may be as high as 5–10% in Argentina, Peru, eastern Africa, Central Asia and China [6]. The global burden was estimated to be 184,000 disability adjusted life years (DALYs) due to cystic echinococcosis each year, resulting in a loss of 760 million dollars a year [7]. In addition to huge economic burdens, this zoonotic parasitic disease poses extremely high global public health burdens [8].

Currently, vaccination in livestock and deworming of dogs are major interventions used for prevention of cystic echinococcosis [9]. Since there are no remarkable cystic echinococcosis-induced pathological alterations in livestock, a multisectoral collaboration is required for implementation of integrated cystic echinococcosis control programs, which suffers from a large number of difficulties [10]. Although great strides have been achieved, multiple challenges remain to achieve the ambitious goal targeting cystic echinococcosis set in the WHO roadmap for neglected tropical diseases 2021–2030 [11]. Estimates of the disease burden due to cystic echinococcosis facilitate the progress towards eliminations; however, there is little knowledge on global morbidity, mortality and DALYs of cystic echinococcosis until now. This study aimed to present the most up-to-date data about the global, regional and national disease burden due to cystic echinococcosis from 1990 to 2019 and to project trends in the next 10 years.

Methods

Data source

The incidence, age-standardized incidence rate (ASIR), mortality, age-standardized mortality rate (ASMR), DALYs and age-standardized DALY rate of cystic echinococcosis were captured in 204 countries from 1990 to 2019 based on the Global Burden of Disease Study 2019 (GBD 2019) data, which were retrieved from the Global Health Data Exchange tool (http://ghdx.healthdata.org/gbd-results-tool). All 204 countries were classified into 21 GBD regions and classified into five socio-demographic index (SDI) quintiles (low, low-middle, middle, high-middle, and high) based on SDI [12].

Statistical analysis

The global, regional and national pooled number, deaths, DALYs, ASIR, ASMR and age-standardized DALY rate of cystic echinococcosis were estimated per 105 populations. The overall trends in disease burden of cystic echinococcosis were evaluated using estimated annual percent change (EAPC) from 1990 to 2019, and the trends in regional and national ASIR of cystic echinococcosis from 1990 to 2019 were described with a heat map. To identify factors affecting EAPC, we examined the associations of EAPC and ASR of cystic echinococcosis with SDI, and a spline model was created to evaluate the association between age-standardized DALY rate of cystic echinococcosis and SDI [13]. In addition, the disease burden due to cystic echinococcosis was projected using Bayesian age-period-cohort analysis with integrated nested Laplace approximations from 2020 to 2030 [14]. All statistical analyses were performed using the software R package, and a P value of < 0.05 was considered statistically significant.

Results

Global trends in the disease burden of cystic echinococcosis

The global ASIR, ASMR and age-standardize DALY rate of cystic echinococcosis were 2.6/105 [95% uncertainty interval (UI): (1.72/105 to 3.7/105)], 0.02/105 [95% UI: (0.01/105 to 0.02/105)] and 1.56/105 [95% UI: (1.14/105 to 2.15/105)] in 2019, and the global incident cases, deaths and DALYs of cystic echinococcosis were estimated to be 207,368 [95% UI: (6,347,183 to 8,769,520)], 1,349 [95% UI: (987 to 1,762)] and 122,457 [95% UI: (89,244 to 168,556)] in 2019, respectively (Table 1).

The global number of incident cystic echinococcosis cases increased from 134,980 [95% UI: (93,141 to 195,144)] in 1990 to 207,368 [95% UI: (137,807 to 303,233)] in 2019, with an EAPC of 0.54% [95% UI: (0.42 to 0.7)], while the global deaths of cystic echinococcosis reduced from 2,839 [95% UI: (2,218 to 3,497)] in 1990 to 1,349 [95% UI: (987 to 1,762)] in 2019, an EAPC of ‒0.52% [95% UI: (‒0.66% to ‒0.34%)]. In addition, the global DALYs of cystic echinococcosis reduced from 210,044 [95% UI: (166,434 to 261,084)] in 1990 to 122,457 [95% UI: (89,244 to 168,556)] in 2019, an EAPC of ‒0.42% [95% UI: (‒0.57% to ‒0.23%)] (Table 2).

Although the global number of incident cystic echinococcosis cases appeared a tendency towards a rise from 1990 to 2019, the global ASIR of cystic echinococcosis appeared a tendency towards a decline [EAPC = ‒0.18%, 95% UI: (‒0.24% to ‒0.12%)], and both the global ASMR [EAPC = ‒4.64%, 95% UI: (‒4.85% to ‒4.43%)] and age-standardized DALY rate [EAPC = ‒3.38%, 95% UI: (‒3.54% to ‒3.26%)] of cystic echinococcosis appeared a tendency towards a decline (Table 2).

Country-specific ASIR of cystic echinococcosis  

Across 204 countries, the three highest ASIR of cystic echinococcosis were measured in Kazakhstan [127.6/105, 95% UI: (105.3/105 to 153.8/105)], Uzbekistan [123.5/105, 95% UI: (58.7/105 to 219.2/105)] and Tajikistan [121.9/105, 95% UI: (58.6/105 to 213.9/105)] from 1990 to 2019 (Figure 1A, Table S1). The largest increase in the number of incident cystic echinococcosis cases was seen in Italy (668.6% increase), Qatar (590.3% increase) and United Arab Emirates (459.3% increase), and the largest reduction was seen in Brazil (79.2% reduction), United Kingdom (64.5% reduction) and Japan (58.9% reduction) (Figure 1B, Table S1). In addition, the largest increase in the ASIR of cystic echinococcosis were measured was observed in Norway [EAPC = 2.42%, 95% UI: (1.75% to 3.11%)], Germany [EAPC = 1.87%, 95% UI: (1.28% to 2.28%)] and Sweden [EAPC = 1.37%, 95% UI: (0.76% to ‒1.98%)], and the greatest reduction was seen in Japan [EAPC = ‒3.79%, 95% UI: (‒4.57% to ‒3.01%)], United Kingdom [EAPC = ‒2.99%, 95% UI: (‒4.05% to ‒1.92%)] and Mexico [EAPC = ‒1.68%, 95% UI: (‒2.45% to ‒0.91%)] (Figure 1C, Table S1).

Age-specific burdens of cystic echinococcosis

The highest ASIR of cystic echinococcosis was found at ages of 50 to 59 years in 2019 [4.08/105, 95% UI: (2.27/105 to 6.86/105)], followed by at ages of 25 to 29 years [3.49/105, 95% UI: (1.79/105 to 6.32/105)], and the ASIR of cystic echinococcosis increased with age, with the highest seen at ages of 95 years and older [0.17/105, 95% UI: (0.01/105 to 0.48/105)]. In addition, the greatest age-standardized DALY rate of cystic echinococcosis was measured at ages of 60 to 64 years [2.17/105, 95% UI: (1.11/105 to 3.51/105)], followed by at ages of 1 to 4 years [1.97/105, 95% UI: (0.59/105 to 3.75/105)] (Table 2).

Association between age-specific burdens of cystic echinococcosis and SDI

The ASMR of cystic echinococcosis was found to correlate negatively with SDI in 21 GBD regions from 1990 to 2019 (R = ‒0.544, P < 0.01). The ASMR of cystic echinococcosis in high SDI regions and Australia was similar to the expected, while the ASMR of cystic echinococcosis in moderate SDI regions differed greatly from the expected (Figure 3). The ASMR of cystic echinococcosis was found to correlate negatively with SDI in 204 countries in 2019 (R = ‒0.546, P < 0.01), and the ASMR of cystic echinococcosis was much higher in few middle SDI countries than the expected (Figure 4). In addition, there were no associations found between the ASIR and age-standardized DALY rate of cystic echinococcosis and SDI (Figure S1, S2).

Projections of the global burden due to cystic echinococcosis from 2020 to 2030

The global ASIR of cystic echinococcosis was projected to appear a tendency towards a decline in both men and women from 2020 to 2030 based on Bayesian age-period-cohort analysis with integrated nested Laplace approximations from 2020 to 2030; however, a slight rise was projected in the global ASMR and age-standardized DALY rate of cystic echinococcosis (Figure 5).

Discussion

In the current study, we assessed the global disease burden due to cystic echinococcosis and measured the incidence, mortality and DALY rate of cystic echinococcosis in 204 countries during the period from 1990 to 2019. A total of 207,368 cystic echinococcosis cases were reported across 204 countries in 2019, which were significantly higher than in 1990 (134,980 cases). Our data showed that the global incidence, mortality and DALY rate of cystic echinococcosis all appeared a tendency towards a decline during the 30-year period from 1990 to 2019. However, the ASIR of cystic echinococcosis appeared a tendency towards a rise in low, low-middle, middle and high SDI regions, while the ASMR and age-standardized DALY rate of cystic echinococcosis remained a tendency towards a decline in all five SDI regions. Understanding of the trends in the epidemiology and disease burden of cystic echinococcosis is therefore of critical significance for public health officials and policy-makers to allocate reasonably medical resources.

In this study, we measured a continuous reduction in the global ASIR of cystic echinococcosis from 1990 to 2019, which is mainly attributed to the reduction in the global ASIR of cystic echinococcosis in the middle-high SDI region. Notably, the largest increase in the global ASIR of cystic echinococcosis was measured in the high SDI region, and Norway, Germany and Sweden were the three countries with the largest increase. A systematic review of scientific and grey literatures showed a tendency towards a remarkable rise in the incidence of cystic echinococcosis in Norway, Germany and Sweden from 1997 to 2021 [15]. The increase in the incidence of cystic echinococcosis in low endemic regions may be partly attributed to a number of immigrants from Syria and Afghanistan where cystic echinococcosis is highly prevalent [15], international travel and physicians’ increased knowledge about cystic echinococcosis control [14]. Therefore, the epidemics of cystic echinococcosis cannot be neglected in low-prevalence regions [16], where national echinococcosis control program is recommended to be launched [17].

In this study, we found a large reduction in the global ASMR and age-standardized DALY rate of cystic echinococcosis from 1990 to 2019 in relative to ASIR. This may be attributed to the release of the roadmap for the neglected tropical diseases by WHO in 2012 and 2020 [18, 19], and the signing of the London Declaration on Neglected Tropical Diseases in 2012 [20], which improved the emphasis on neglected tropical diseases throughout the world, including echinococcosis. In 2009, the expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans was reached by the WHO-Informal Working Group on Echinococcosis (WHO-IWGE) [21]. This consensus proposes the diagnostic and treatment options for echinococcosis, which facilitates the reduction in mortality and disease burden of echinococcosis. Recently, WHO has collaborated with veterinary and food security administrations to support the formulation of echinococcosis control programs under the One Health framework, which is of great importance to reduce the disease burden of echinococcosis and protect the food value chain [22–24].

Based on GBD2019 data, we found a higher ASIR and age-standardized DALY rate of cystic echinococcosis among women than among men, which is consistent with previous reports [13]. A recent meta-analysis showed that being female is a potential risk factor of human cystic echinococcosis [25]. This may be because women mainly work on feeding dogs, grazing animals, milking and collecting stools in many regions, resulting in a high risk of contamination with Echinococcus eggs [26–28]. Therefore, a higher priority for the management of cystic echinococcosis should be given to women. In addition, a high incidence rate of cystic echinococcosis was seen in individuals at ages of 55 to 65 years. This may be because residents at ages of 55 to 65 years are most active in animal husbandry [29], and cystic echinococcosis is a chronic infectious disease, which has a long course of disease. The clinical symptoms may present 5 to 20 years following Echinococcus infections, and individuals at ages of 55 to 65 years may be exposed to settings with contamination with Echinococcus eggs for a long period of time. Following the incubation period, the symptoms occur among individuals at ages of 55 to 65 years [26].

In this study, we measured that the ASMR of cystic echinococcosis appeared a tendency towards a reduction with SDI in 21 GBD regions and 204 countries, and there were no significant associations of SDI with ASIR or age-standardized DALY rate of cystic echinococcosis. In regions with higher SDI, better hygiene conditions and higher level of urbanization lead to a lower risk of exposure to echinococcosis. Education is an indicator of SDI, and a lower educational level is observed in lower SDI regions. It has been reported that echinococcosis is highly prevalent in underdeveloped communities with low education levels and high literacy rates or resource-poor communities [30]. Therefore, health education pertaining to echinococcosis control knowledge is of great importance for disease prevention and control. Nevertheless, readable health education materials are required given the low education level, in order to improve the acceptability and compliance [31].

In this study, we evaluated the temporal trends in the global disease burden of cystic echinococcosis from 1990 to 2019 and projected trends in the next 10 years based on the GBD2019 data. Our data showed a continuous decline in the ASIR, ASMR and age-standardized DALY rate of cystic echinococcosis during the 30-year period from 1990 to 2019, and the global ASIR of cystic echinococcosis was projected to decline from 2020 to 2030, which may be attributed to the global strengthening on echinococcosis prevention and control following the release of the WHO roadmap for neglected tropical diseases 2021–2030. In addition, the global ASMR and age-standardized DALY rate of cystic echinococcosis were projected to rise slightly, which may be attributed to the alteration of the population structure.

This study has some limitations. First, the source, analysis and assessment of the GBD2019 data have been adjusted for many times to improve the data accuracy comparability; however, there is inevitable bias in the integrity and accuracy of the GBD2019 data. Second, there are no available disability weights of cystic echinococcosis in the GBD2019 data, and the disability weights of liver cancer were employed in this study, which may cause bias in the study results. Third, cystic echinococcosis was included in the GBD2019 data, and no alveolar echinococcosis data were presented. Further studies to overcome these limitations are required to validate the findings from this study.

Conclusion

Our findings demonstrate the global disease burdens of cystic echinococcosis from 1990 to 2019 and project the future trends in the next 10 years. Our data may provide evidence-based information for public health officials and policy-makers to formulate and implement cost-benefit interventions to tackle the disease burden attributable to cystic echinococcosis. More health resources are recommended to be allocated to low SDI regions, women and the elderly at ages of 55 to 65 years to reduce the disease burden caused by cystic echinococcosis.

Declarations

Ethics approval and consent to participate

Not applicable. 

Consent for publication

Not applicable.

Competing interests

Xiao-Nong Zhou is an Editor-in-Chief of the journal Infectious Diseases of Poverty. He was not involved in the peer-review or handling of the manuscript. The authors have no other competing interests to disclose.

Availability of data and materials

All data generated or analysed during this study are included in the published article.

Author contributions

TT, WW, and XNZ designed the study. LM, TT, and WW conducted the data collections. LM, and TT performed data analyses. LM, TT, and WW wrote the original manuscript and WW, XNZ revised the manuscript. All authors read and approved the final manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (No. 2021YFC2300800, 2021YFC2300804), and the Integration and Innovation Fund of Shanghai Jiao Tong University (No. 2020-01).

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Tables

Tables 1 and 2 are available in the Supplementary Files section.