Global patterns of the burden of zoonotic infectious diseases of poverty based on GBD 2021

doi:10.21203/rs.3.rs-4646782/v1

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Research Article

Global patterns of the burden of zoonotic infectious diseases of poverty based on GBD 2021

https://doi.org/10.21203/rs.3.rs-4646782/v1

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Background

The zoonotic infectious diseases of poverty (zIDPs) continue to be a significant factor contributing to global poverty, with a broad distribution and a significant impact on a substantial population. We aimed to assess the global, regional, and national burden and trends of zIDPs utilizing Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) 2021, providing scientific support for policy making and resource allocating.

Methods

We retrieved data from GBD 2021 on the prevalence, disability-adjusted life-years (DALYs) of zIDPs (schistosomiasis, cystic echinococcosis [CE], cysticercosis, foodborne trematodiases particularly referring to opisthochiais, clonorchiasis, paragonimiasis, fascioliasis, fasciolopsis) in 204 countries and territories from 1990 to 2021. Estimated annual percentage changes in the age-standardized prevalence and DALY rates of zIDPs by age, sex, and Socio-demographic Index (SDI), were calculated to quantify the temporal trends. Spearman correlation analysis was used to examine the relationship between age-standardized rates and SDI.

Results

Globally, there are an estimated 151 376 744 schistosomiasis cases (95% Uncertainty Interval (UI) 109 062 891 to 198 666 395), 633 404 CE cases (95% UI 517 477 to 782 468), 4 357 190 cysticercosis cases (95% UI 3 150 315 to 5 716 430), and 44 466 329 (95% UI 40 017 218 to 50 034 921) foodborne trematodiases cases, respectively. The number of DALYs due to schistosomiasis, CE, cysticercosis and foodborne trematodiases worldwide in 2021 was 1 746 333 (95% UI 1038122 to 2984204), 105 072 (95% UI 78 967 to 133 309), 1 235 939 (95% UI 787 769 to 1 808 363) and 998 029 (95% UI 569 766-1 638 112), respectively. The age-standardized prevalence rate and DALYs of schistosomiasis, cysticercosis and foodborne trematodiases decreased year by year significantly globally during 1990 to 2019. The highest number of cases and DALYs occurred in: Sub-Saharan Africa for schistosomiasis; South Asia, East Asia (only cases), North Africa and Middle East, Eastern Sub-Saharan Africa (only DALYs) for CE; South Asia (only cases), East Asia and Central Latin America for cysticercosis; East Asia, Southeast Asia (only cases), High-income Asia Pacific (only cases) for foodborne trematodiases. The age-standardized prevalence rates of the zIDPs exhibited three different patterns with the increases of SDI, whereas the age-standardized DALY of the zIDPs (excluding foodborne trematodiases) decreased with the rise of SDI.

Conclusion

The prevalence and DALYs of zIDPs presented decrease trends in most endemic regions globally by year. The regions and countries with low SDI should prioritize reducing the burden of zIDPs in light of the WHO's aim to control or eliminate NTDs.

global burden of disease

zoonotic infectious diseases of poverty

disability-adjusted life year (DALY)

prevalence

age-standardized rate

Infectious Diseases of Poverty (IDPs) are a group of infectious diseases that thrive in conditions of poverty and socioeconomic inequality, severely impacting on the health of the affected populations [1, 2]. These diseases encompass, but are not limited to, malaria, AIDS, tuberculosis, dengue fever, and Neglected Tropical Diseases (NTDs). The global epidemic situation of IDPs is complex and diverse, while they are primarily prevalent in low- and middle-income countries, particularly in sub-Saharan Africa, South Asia, Southeast Asia, and Latin America [3]. The distribution and prevalence of IDPs are often closely linked to impoverished conditions that frequently lack basic sanitation facilities, clean drinking water, and effective medical services, while living environments may also be overcrowded and have poor hygiene conditions, all of which provide a breeding ground for the spread of infectious diseases [4, 5]. Additionally, poverty restricts individuals' capacity to acquire the necessary resources for the prevention and treatment of these diseases, encompassing vaccines, medications, and diagnostic tools [6]. IDPs also hamper the social and economic development, resulting in a loss of labor force, decreased productivity, and increased financial strain on families and communities [1, 4, 6]. These regions, burdened by substantial disease, face greater difficulties in escaping poverty, perpetuating a vicious cycle. To this day, IDPs continue to pose a significant challenge to global public health. Compared to other IDPs, zoonotic IDPs, such as schistosomiasis, cystic echinococcosis (CE), cysticercosis, foodborne trematodiases including opisthochiais, clonorchiasis, paragonimiasis, fascioliasis, fasciolopsis, etc., pose a greater challenge for monitoring and control due to their multiple hosts and complicated transmission route [7], thereby emphasizing the necessity of comprehending their disease burden to understand of the impact of diseases on population health and assess progress towards international health targets [8–10].

GBD led by the Institute for Health Metrics and Evaluation (IHME) at the University of Washington in the United States, remains the most comprehensive disease burden research effort and valuable global health data resource to date [11, 12]. Since the early 1990s, GBD has systematically and comprehensively released estimates of global health and health loss across stratified age groups, locations, and sexes [13]. The availability of disease burden estimates offers evidence-based global health assessments, enabling the identification of health disparities and the formulation and implementation of interventions aimed at mitigating diseases. Moreover, the GBD database is an important foundation for global health research, promoting extensive academic and applied research for providing detailed health data which supported disease burden analysis, health risk assessment, and intervention effect research to all researchers [14]. GBD 2021 is an update based on 2019, highlighting emerging and existing health threats that are prioritized in the international public health agenda, especially in the context of COVID-19 having shifted from a new threat that requires urgent response to an infectious disease that requires population coexistence and management [15].

In this study, we selected zIDPs for detailed burden description from GBD 2021. In the zIDPs, schistosomiasis, also known as bilharzia, is an acute and chronic disease caused by blood flukes (trematode worms) of the genus Schistosoma. It is recognized as most dangerous parasitic disease after malaria, being prevalent in 78 countries and territories worldwide, especially in poor communities without access to safe drinking water and adequate sanitation [16]. Human echinococcosis is caused by the tapeworms of the genus Echinococcus. In the 4 forms of echinococcosis, cystic echinococcosis (CE), also known as hydatid disease, is caused by the infection of the larvae of Echinococcus granulosus. CE can cause harmful, slowly enlarging cysts in the liver, lungs, and other organs that often grow for years without significant signs or symptoms, resulting in expensive and complicated treatment which may require extensive surgery and/or prolonged drug therapy. CE is globally distributed and found in every continent except Antarctica [17]. Cysticercosis is a parasitic infection caused by the larvae (immature worm) of the tapeworm, Taenia solium. People get infection by consuming tapeworm eggs. These eggs hatch and develop into larvae, and then penetrate (move through) the host’s intestinal wall and move to tissues like muscle, eyes, or brain. The at-risk populations are distributed worldwide, and the people living in the areas in developing countries in Africa, Asia, and Latin America have higher risk of infection [18]. Foodborne trematodiases are a group of parasitic diseases of opisthochiais, clonorchiasis, paragonimiasis, fascioliasis and fasciolopsis. These parasitic flukes have a complex life cycle involving diverse definitive hosts and one or two intermediate hosts. Foodborne trematodes cause infection in humans via the consumption of contaminated food (raw fish, crustaceans or vegetables), resulting in severe liver and lung disease. Globally, foodborne trematodiases are most prevalent in East Asia and South America [19].

The World Health Organization (WHO) has published the “Ending the neglect to attain the Sustainable Development Goals: A road map for neglected tropical diseases 2021–2030”, which aims to address schistosomiasis elimination as a public health problem, and control of cystic echinococcosis, cysticercosis and foodborne trematodiases [20]. Based on GBD 2021, this research aims to reveal the prevalence and DALYs of those zIDPs and explore the effects of the socio-demographic index (SDI), geographic location, gender, and age on the burden related to zIDPs, providing reference for policy making.

Study population and data collection

The GBD 2021 provided estimates of the worldwide burden of 371 diseases and injuries across 204 nations and territories from 1990 to 2021. Using the Global Health Data Exchange (GHDx) results tool (http://ghdx.healthdata.org/gbd-results-tool), we retrieved data from GBD 2021 on the prevalence and disability-adjusted life-years (DALYs) of zIDPs (schistosomiasis, cystic echinococcosis, cysticercosis and foodborne trematodiases) in 204 countries and territories from 1990 to 2021. In GBD2021, the foodborne trematodiases are a group of diseases that result from infection with parasitic worms of the class Trematoda, also known as flukes, via consumption of contaminated food, including opisthochiais, clonorchiasis, paragonimiasis, fascioliasis and fasciolopsis.

To determine the overall level of health-related social and economic circumstances in each region, the Socio-demographic Index (SDI) is computed in GBD 2021. Based on country-level estimates of SDI in 2021, the 204 countries and territories included in the GBD were divided into five categories: low, low-middle, medium, high-middle, and high. Twenty groups of people ranged in age from 0 to 100 years old, and each group was separated by five years. In addition, 204 countries or territories were subdivided into 21 subnational regions, taking into consideration geographical characteristics.

Statistical analysis

Based on the age structure of standard populations, the GBD 2021 produced age-standardized rates (ASRs) per 100,000 persons. These rates were based on the average age of the population. To summarize, the ASR was determined by applying the formula that is presented below:

$$ASR=\frac{{\sum }_{i=1}^{N}{\alpha }_{i}{W}_{i}}{{\sum }_{i=1}^{N}{W}_{i}}$$

The variable α_i represents the age-specific rate in a specific age group. At the same time, W_i denotes the number of individuals (or weight) in the same age group within the GBD standard population. The value of N represents the total number of age groups. The 95% uncertainty intervals (UIs) were determined by identifying the 25th and 975th values from the ordered set of 1000 draws.

Smoothing splines models were utilized to evaluate the association between the burdens of forward-stated four NTDs among various age groups and SDIs throughout 21 regions and 204 nations and territories. The predicted values were determined by considering the SDI and the disease rates obtained from every location. We used the Locally Weighted Scatterplot Smoothing (LOWESS) technique to fit the smooth splines. This approach automatically estimates the degree, quantity, and placement of nodes (knots) depending on the data and span parameters. The r indices and P values of ASR related to SDI were estimated using Spearman correlation analysis. A P-value of less than 0.05 was determined to be statistically significant. Data analysis and mapping were all conducted using R software (version 4.3.2).

Prevalence burden of zIDPs

Globally, there were an estimated 151 376 744 schistosomiasis cases (95% UI 109 062 891 to 198 666 395), 633 404 CE cases (95% UI 517 477 to 782 468), 4 357 190 cysticercosis cases (95% UI 3 150 315 to 5 716 430), and 44 466 329 (95% UI 40 017 218 to 50 034 921) foodborne trematodiases cases, respectively. The age-standardized prevalence rate was 1 914.3 (95% UI 1378.9 to 2510.8) per 100 000 population for schistosomiasis, 7.7 (95% UI 6.3 to 9.5) for CE, 51.3 (95% UI 37.2 to 67.3) for cysticercosis, and 526.7 (95% UI 473.7 to 593.3) for foodborne trematodiases. From 1990 to 2019, the age-standardized prevalence rates of schistosomiasis, cysticercosis, and foodborne trematodiases showed significant global declines, averaging -22.6% (95% CI -0.33 to 0.13), -25.1% (95% CI -0.29 to 0.20), and -50.1% (95% CI -0.53 to 0.47) per year, respectively. Conversely, the prevalence of cystic echinococcosis remained stable over the same period, with a global average change of 4.4% (95% CI -0.03 to 0.10) per year. In addition, the number of cases and the age-standardized prevalence rate of schistosomiasis were markedly higher than those of CE, cysticercosis and foodborne trematodiases (Table 1).

In GBD 2021, the Western Sub-Saharan Africa reported the highest schistosomiasis cases (61 534 853, 95% UI 44 035 020 to 81 338 005), followed by that of Eastern Sub-Saharan Africa (46 949 044, 95% UI 33 903 446 to 61 048 520) and East Asia (11 459 581, 95% UI 8 953 886 to 15 054 894, Fig 1A). Western Sub-Saharan Africa also had the highest age-standardized prevalence rate of schistosomiasis at 13 433.6 per 100 000 population (95% UI 9 651.8 to 17 812.1), followed by Eastern Sub-Saharan Africa (11 617.6, 95% UI 8 558.00 to 15 093.1) and Central Sub-Saharan Africa (7 947.5, 95% UI 5 702.6 to 11 151.9). Furthermore, the age-standardized prevalence rates of schistosomiasis decreased across all GBD regions from 1990 to 2021, except in the Caribbean. The region with the highest average decrease rate was North Africa and the Middle East (-0.83, 95% CI -0.88 to 0.78, Table 1).

For CE, the highest number of cases was observed in South Asia (199 794, 95% UI 161 370 to 248 813), East Asia (114 589, 95% UI 86 308 to 147 199) and North Africa and Middle East (94 754, 95% UI 77 603 to 117 793, Fig 1B). The regions with the highest age-standardized prevalence rates were Southern Latin America (38.2 per 100 000 population, 95% UI 32.0 to 45.2), Central Asia (23.0, 95% UI 18.7 to 28.2) and Eastern Sub-Saharan Africa (17.2, 95% UI 13.8 to 21.7, Table 1). Additionally, six out of 21 GBD regions showed increased trends in age-standardized prevalence rate from 1990 to 2021, with East Asia experiencing the highest average annual increase of 153.6% (95% CI 1.3 to 1.8, Table 1).

In 2021, the regions with the highest number of cysticercosis cases were South AsiaS (755 683, 95% UI 551 993 to 972 079), East Asia (725 883, 95% UI 494 719 to 1 018 980) and Central Latin America (562 969, 95% UI 410 577 to 708 799) (Table 1, Fig 1C). Central Latin America (216.4 per 100 000 population, 95% UI 160.3 to 271.4), Southern Sub-Saharan Africa (208.3, 95% UI 155.3 to 258.4) and Central Sub-Saharan Africa (191.4, 95% UI 144.1 to 235.0) had the highest age-standardized prevalence rate. From 1990 to 2021, the age-standardized prevalence rate of cysticercosis decreased in all GBD regions except High-income North America, with the largest decrease observed in North Africa and Middle East (average annual change -51.9%, 95% CI -0.561 to 0.478, Table 1).

In 2021, the regions with the highest number of foodborne trematodiases cases were East Asia (33 317 223, 95% UI 29 251 039 to 38 353 602), Southeast Asia (4 708 038, 95% UI 4 280 246 to 5 159 478) and High-income Asia Pacific (1 974 178, 95% UI 1 750 147 to 2 202 860, Table 1). The regions with the highest age-standardized prevalence rates were Andean Latin America (2 606.1, 95% UI 2 127.3-3 171), East Asia (1 862.4, 95% UI 1 640.7-2 161.6), and High-income Asia Pacific (821.5, 95% UI 731.3 to 915.2, Table 1). From 1990 to 2021, an increase in the age-standardized prevalence rate of foodborne trematodiases was observed in High-income Asia Pacific (average change 11.0% per year, 95% CI 0·01 to 0·22) and Eastern Europe (0.4%, 95% CI -0.02 to 0.03).

DALYs burden of zIDPs

In 2021, the global number of DALYs (Disability-Adjusted Life Years) due to schistosomiasis was 1 746 333 (95% UI 1 038 122 to 2,984,204), with an age-standardized rate of 21.9 DALYs (95% UI 12.9 to 37.3) per 100 000 population. The age-standardized DALY rate for schistosomiasis significantly decreased from 1990 to 2021, with an average annual change of -0.41 (95% CI -0.52 to -0.32) globally (Table 2). Similarly, in 2021, the number of DALYs due to cystic echinococcosis (CE) was 105 072 (95% UI 78 967 to 133 309), with an age-standardized rate of 1.3 DALYs (95% UI 1.0 to 1.7) per 100 000 population, showing an average annual decrease of -0.72 (95% CI -0.8 to -0.6) from 1990 to 2021. For cysticercosis, the number of DALYs in 2021 was 1 235 939 (95% UI 787 769 to 1 808 363), with an age-standardized rate of 14.6 (95% UI 9.3 to 21.3), and an average annual decline of -0.39 (95% CI -0.47 to -0.29) from 1990 to 2021. Regarding foodborne trematodiases, the number of DALYs in 2021 was 998 029 (95% UI 569 766 to 1 638 112), with an age-standardized rate of 11.8 (95% UI 6.7 to 19.5). The age-standardized DALY rate for foodborne trematodiases also declined, with an average annual decrease of -0.54 (95% CI -0.60 to -0.45) from 1990 to 2021 (Table 2). Overall, the DALY burden (both the number of DALYs and the age-standardized DALY rate) of schistosomiasis was higher than that of cystic echinococcosis, cysticercosis, and foodborne trematodiases.

In 2021, regions of sub-Saharan Africa (central, eastern, and western) had the highest number of DALYs and age-standardized DALY rates (per 100,000 population) for schistosomiasis (Fig. 2A). All schistosomiasis-endemic GBD regions exhibited a decline in the age-standardized DALY rate, with the largest decreases occurring in North Africa and the Middle East (average annual change -0.82, 95% CI -0.85 to -0.78).

For CE, the highest number of DALYs was observed in South Asia (34 006, 95% UI 25 804 to 43 190), Eastern Sub-Saharan Africa (17 337, 95% UI 12 042 to 23 167), and North Africa and the Middle East (17 319, 95% UI 13 165 to 21 974, Fig 2B). The highest age-standardized DALY rates were found in Eastern Sub-Saharan Africa (4.2, 95% UI 3.0 to 5.4), North Africa and the Middle East (3.0, 95% UI 2.3 to 3.7), and Southern Latin America (3.0, 95% UI 2.0 to 4.2). All GBD regions showed obvious decreases in the age-standardized DALY rate, with the highest average annual change in Western Sub-Saharan Africa (-0.81, 95% CI -0.89 to -0.69, Table 2).

In 2021, the highest number of DALYs due to cysticercosis occurred in East Asia (176 228, 95% UI 101 465 to 284 693), Central Latin America (157 382, 95% UI 98 523 to 228 880), and Eastern Sub-Saharan Africa (94 863, 95% UI 64 603 to 129 428, Fig 2C). The highest age-standardized DALY rates were observed in Central Sub-Saharan Africa (72.0, 95% UI 46.4 to 103.7), Southern Sub-Saharan Africa (66.8, 95% UI 42.7 to 94.3), and Central Latin America (60.3, 95% UI 37.9 to 87.3, Table 2). Most regions (except High-income North America) showed decreases in the age-standardized DALY rate for cysticercosis, with the largest decreases in North Africa and the Middle East (-0.65, 95% CI -0.74 to -0.52), East Asia (-0.54, 95% CI -0.67 to -0.40), and South Asia (-0.55, 95% CI -0.63 to -0.43, Table 2).

For foodborne trematodiases, East Asia had the highest number of DALYs (768 297, 95% UI 383 883 to 1 367 826), significantly higher than other regions. Andean Latin America had the highest age-standardized DALY rate (56.1, 95% UI 19.0 to 106.1), followed by East Asia (42.6, 95% UI 21.3 to 77.0, Table 2). The increase in the age-standardized DALY rate was only found in High-income Asia Pacific (average change 0.170 per year, 95% CI 0.042 to 0.319) and Eastern Europe (0.005, 95% CI -0.040 to 0.048), while other regions showed a decreasing trend (Table 2).

The burden of zIDPs by age

For schistosomiasis, the 10-29 age groups had the highest number of cases. The age-standardized prevalence rate showed an upward trend until the 15-19 age group, after which it presented a downward trend with increasing age (Fig 3A). Additionally, the number of male schistosomiasis cases exceeded that of females in all age groups. The maximum number of DALYs for schistosomiasis was found in the 15-34 age groups. The age-standardized DALY rate exhibited an upward trend until the 20-24 age group, and then a downward trend with increasing age (Fig. 3E).

For CE, the 30-49 age groups had the highest number of cases, with the peak of the age-standardized prevalence rate also occurring in these age groups. Interestingly, the number of male cases was less than that of females across all age groups (Fig 3B). The <5 years age group had the highest number of DALYs (both females and males each had more than 5,000). The age-standardized DALY rate did not change much across age groups but showed a significant decrease from the <5 years age group to the 15-19 age group (Fig 3F).

For cysticercosis, the maximum number of cases were concentrated in the 55-74 age groups, while the age-standardized prevalence rate increased with age. Additionally, male cases of cysticercosis were fewer than female cases across all age groups (Fig 3C). The number of DALYs was concentrated in the 20-84 age groups, with the age-standardized DALY rate showing a continuous upward trend with age. Furthermore, the number of DALYs in females was higher than in males across all age groups (Fig 3G).

For foodborne trematodiases, the 45-59 age groups had the highest number of cases and DALYs. The age-standardized prevalence rate and DALY rate both initially rose (in the age groups <5 to 69) and then declined (in those over 69 years old). Additionally, the number of cases and DALYs in males across almost all age groups (except those over 80) were higher than in females (Fig 3D, H).

The burden of zIDPs by SDI

In the five categories of SDI regions (high, middle-high, middle, low-middle, low), the age-standardized prevalence rate of schistosomiasis showed an upward trend in the high SDI region and a downward trend in the other regions from 1990 to 2021. The age-standardized prevalence rate of foodborne trematodiases exhibited a downward trend in the middle SDI region, but rebounded in 2015 in the high and middle-high SDI regions. The age-standardized prevalence rates of CE and cysticercosis remained stable from 1990 to 2021 (Fig 4A).

The age-standardized DALY rate of CE showed no significant change in the five SDI regions from 1990 to 2021. The age-standardized DALY rate of schistosomiasis showed a downward trend in the low, low-middle, and middle SDI regions, and remained stable in the high-middle and high SDI regions. The age-standardized DALY rate of cysticercosis showed a slight downward trend in the low-middle, middle, and high-middle regions. The age-standardized DALY rate of foodborne trematodiases showed a significant downward trend only in the middle SDI region (Fig 4B).

The relation between burden of zIDPs and SDI

The age-standardized prevalence rates of the zIDPs exhibited three distinct patterns with increasing SDI at the national level. Schistosomiasis showed a linear decline in prevalence. The prevalence of cysticercosis was divided into two zones: increasing (<0.6) and decreasing (>0.6), with an SDI threshold of 0.6. The prevalence of CE and foodborne trematodiases showed no significant changes. The highest age-standardized prevalence rates were observed in Mauritius for schistosomiasis (30.8 per 100 000 population, 95% UI: 21.6 to 41.2), in the Republic of Moldova for CE (107.4, 95% UI: 86.2 to 131.6), in Mexico for cysticercosis (281.4, 95% UI: 206.3 to 352.0), and in the Lao People's Democratic Republic for foodborne trematodiases (4 028.8, 95% UI: 4 585.0 to 494.3, Fig 5A, C, E, G).

At the regional level, Western, Central, and Southern Sub-Saharan Africa had higher-than-expected age-standardized prevalence rates of schistosomiasis despite an overall decline. The age-standardized prevalence rates of CE showed a curve that first decreases, then rises, and then decreases again, with higher-than-expected rates in Eastern Sub-Saharan Africa, Central Asia, and Southern Latin America. For cysticercosis, the prevalence decreased with increasing SDI, and Central and Southern Sub-Saharan Africa, Andean and Central Latin America, and High-income North America had higher-than-expected rates. The prevalence rates of foodborne trematodiases showed an initial rise and then a decrease at an SDI of 0.5, with higher-than-expected rates in Latin America, East Asia, Southeast Asia, Eastern Europe, and High-income Asia Pacific (Fig 5B, D, G, H).

At the national level and regional level, the age-standardized DALY of the zIDPs decreased with increases in SDI except foodborne trematodiases (Fig 6). The African countries have higher age-standardized DALYs rates compared to the countries in other regions, and the Central African Republic had the highest rate for schistosomiasis (401.6 per 100 000 population, 95% UI: 289.8 to 540.6), South Sudan for CE (12.3, 95% UI: 8.4 to 17.1), and Zimbabwe for cysticercosis (98.7, 95% UI: 60.2 to 146.5). The Lao People's Democratic Republic had the highest age-standardized DALYs rate of foodborne trematodiases (Fig 6 A, C, E, G).

Sub-Saharan Africa, North Africa and Middle East and Tropical Latin America had higher-than-expected age-standardized DALY rates of scistosomiasis based on the SDI between 1990 and 2021. South Asia, Central Asia, North Africa and Middle East, Southern Latin America and Eastern Europe had higher-than-expected age-standardized DALY rates of CE. For cysticercosis, Central and Southern sub-Saharan Africa, Andean and Central Latin America and High-income North America had higher-than-expected age-standardized DALYs rates. For foodborne trematodiases, Latin America, East Asia, Southeast Asia, Eastern Europe, High−income Asia Pacific had higher-than-expected age-standardized DALY rates (Fig 6B, D, G, H).

GBD 2021 is a comprehensive and updated work that assesses global health losses. It provides estimates for 371 diseases and injuries by utilizing indicators such as prevalence, incidence, years lived with disability (YLDs), years of life lost (YLLs), disability-adjusted life-years (DALYs), and healthy life expectancy (HALE) across various age groups, genders, and locations [12]. In comparison to other diseases such as emerging infectious diseases and cardiovascular and cerebrovascular diseases, the burden of disease caused by zIDPs may be significantly underrecognized, particularly during the COVID-19 global pandemic [15, 21, 22]. The majority of zIDPs reside in remote rural areas with inadequate sanitation in low- and middle-income countries in tropical or subtropical regions. The COVID-19 pandemic is likely to deprive these regions of funding and policy attention for NTDs. In this study, we first present the burden estimates of zIDPs utilizing GBD 2021. We speculate that analyzing the global burden of zIDPs is crucial in enhancing understanding of their impact on population health and assessing progress towards national and global control or elimination goals. This analysis may result in support for policy making or allocating resources reasonably such as funds, personnel, and drugs etc.

Among the zIDPs, schistosomiasis presented the highest disease burden (prevalence and DALYs) worldwide in 2021, necessitating the allocation of additional resources towards its control. WHO unveiled “Ending the neglect to attain the Sustainable Development Goals: A road map for neglected tropical diseases 2021–2030” in 2021. According to the roadmap, schistosomiasis is targeted for elimination as a public health problem (WHO currently defined as < 1% proportion of heavy intensity schistosomiasis infections), while CD, cysticercosis and foodborne trematodiases are targeted for control [20]. Although the goal for schistosomiasis is more radical in terms of disease burden, the elimination of the disease as a public health problem is achievable, as demonstrated by countries like China that have achieved this through the implementation of integrated strategies focusing on infection source control [23, 24]. Clearly, this success is attributed to the continuous investment of political, financial, physical, and human resources. Globally, the burden of these zIDPs has shown a decline, particularly in low SDI regions and countries, providing evidence-based data support for the realization of the ambitious roadmap goals for zIDPs.

The primary focus of schistosomiasis control remains in sub-Saharan Africa, where the prevalence and DALYs are significantly higher than in other regions. Additionally, while the SDI in the Tropical Latin America and Caribbean region is higher than in sub-Saharan Africa, more resources should be allocated towards schistosomiasis control. East and Southeast Asia may be considered as the leading regions in achieving the WHO roadmap goals for schistosomiasis. Despite the presence of a certain number of patients in the region, the DALYs (Disability-Adjusted Life Years) have significantly decreased compared to the 1990s and other regions. Notably, major endemic countries such as China, Laos, and Cambodia have issued national elimination plans for schistosomiasis [23, 25, 26]. Furthermore, the prevalence and DALYs of schistosomiasis primarily affect individuals aged between 15 and 59, making them a critical population for intervention. As the WHO new guideline for control and elimination of human schistosomiasis issued in 2022 recommended to extend the population targeted for preventive chemotherapy to all individuals at risk of infection, more praziquantel tablets and other interventions are required to accelerate the process of schistosomiasis elimination as a public health problem by 2030 globally. In addition, we noticed that the age-standardized prevalence rate increased in high SDI regions, indicating that the disease spread from rural areas to urbans due to climate change or social-economic activities. Monitoring and intervention activities also should be strengthened in these regions.

The burden of CE was distributed in the regions of Eastern Sub-Saharan Africa, North Africa and Middle East, Southern Latin America, Central Asia and South Asia. This burden may be attributed to the thriving livestock breeding, slaughtering, and trade activities in these regions. Notably, the burden of CE (prevalence, incidence, DALYs) does not exhibit a significant correlation with SDI, with a conspicuous surge in the incidence of CE observed in high SDI regions between 1990 and 2021. Moreover, the elevated age-standardized DALYs and mortality rates among children under the age of 5 (data not depicted) are another area that demands immediate attention and intervention. Furthermore, public health professionals, in collaboration with veterinarians, should focus on promoting health of guardians, administering deworming to dogs, facilitating early diagnosis, and enhancing nutritional status [27, 28].

Unlike schistosomiasis and CE, some regions with high SDI and high income, such as high-income North America and Eastern Europe, also exhibit a certain prevalence rate of cysticercosis and a certain number of DALYs, in addition to sub-Saharan Africa (central, southern, eastern, and western) and Latin America (central, Andean, and tropical), which are the primary contributors to the disease burden. Out of the 21 GBD regions, Australasia is the only region without any prevalence or DALYs related to cysticercosis. The absence of cysticercosis burden can likely be attributed to a series of regulations within the framework of One Health [8, 29, 30], which include stringent animal quarantine and management measures for pig farming and canine animals, sophisticated healthcare infrastructure such as water supply, sanitation infrastructure, and food hygiene systems, a robust medical and veterinary service system, waste management, and strict legal oversight.

Asia, especially East Asia, bears the most burden of foodborne trematodiases primarily due to the region's dietary patterns, including the consumption of raw fish or other foods as a traditional or signature dish in certain areas [31, 32]. Furthermore, our analysis uncovers that the correlation between the burden of foodborne trematodiases and SDI is less pronounced compared to other zIDPs, suggesting that preventing and managing these diseases could be more intricate and difficult. Therefore, it is crucial to emphasize that in certain high SDI countries where raw fish and crustaceans are often consumed, heightened surveillance is advised for community members and intermediate hosts [33–35]. A prolonged campaign against foodborne trematodiases also should be conducted with integration of deworming, health education and behavior changes, improving sanitation etc.

Despite the varying modes of infection and transmission, as well as differing disease burdens, all diseases pertaining to zIDPs invariably engage multiple interfaces between humans, animals, and the environment. To effectively control or eliminate zIDPs, it is crucial to underscore the significance of the One Health framework [29, 36, 37]. This involves emphasizing effective communication, collaboration, and coordination at the managerial level, as well as the concurrent involvement of various departments and disciplines in practice. This analysis of the burden of zIDPs offers evidence-based priorities for the future control of zIDPs, and contributes to the WHO's roadmap to end neglected tropical diseases and the global One Health joint action plan.

The study retrieved data from GBD 2021 on the prevalence and DALYs of zIDPs from 1990 to 2021. This is likely the first comprehensive characterization of the burden associated with zIDPs to date. Meanwhile, estimated annual percentage changes in the age-standardized prevalence and DALY rates of zIDPs by age, sex, and SDI, were calculated to present the temporal changes. The results showed that the prevalence and DALYs of zIDPs declined from 1990 to 2021, although there were regional and demographic disparities. Similarly, the prevalence and DALYs of these zIDPs each exhibits distinct characteristics in terms of age and gender distribution. Moreover, the prevalence and DALYs of zIDPs (except prevalence of CE) were decrease with the SDI increase. Schistosomiasis had the most severe burden of prevalence and DALYs of the zIDPs and should allocate more control resources. Regions and countries with low SDI should be the focus for reducing the burden of zIDPs in the control activity. In addition, high or high-middle regions should strength the surveillance to mitigate or eliminate the health risks posed by zIDPs.

Acknowledgements

The authors would like to thank all participants for participating in this study.

Authors’ contributions

JX and ML conceived and designed analysis. CL, YC, and ZC performed the whole data integration, ML, WC, NZ, YC, YL and WD participated in data analysis and content discussion. CL, YC, and ZC wrote the first draft of the manuscript. JX and YZ edited the manuscript. All authors approved the submitted version.

Funding

This study is partially supported by International Joint Laboratory on Tropical Diseases Control in Greater Mekong Subregion (no. 21410750200) from Shanghai Municipality Government and the Scientific research project of Shanghai Health Commission (20204Y0050).

Availability of data and materials

The datasets used and/or analyzed during this study are available from the corresponding author upon reasonable request.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that there are no competing interests.

Author details

¹National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), National Health Commission Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai, China (Chao Lv, Yinlong Li, Wangping Deng, Jing Xu)

²School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China (Yiwen Chen, Zile Cheng, Min Li, Weiye Chen, Nan Zhou, Yiming Chen, Xiaokui Guo, Yongzhang Zhu)

³School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, China (Chao Lv, Yiwen Chen, Zile Cheng, Min Li, Weiye Chen, Nan Zhou, Yiming Chen, Xiaokui Guo)

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Global patterns of the burden of zoonotic infectious diseases of poverty based on GBD 2021

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