ABSTRACT
Rabies remains a major public health issue. Yet, trends in rabies burden associated with age, period, and cohort effects remain unknown, and the association between animal rabies vaccination and rabies burden is unclear. We aimed to understand the long-term spatio-temporal trends in global rabies burden, the impacts of age, periods, and birth cohorts, and the association between animal rabies vaccination and burden. Rabies burden data were extracted from Global Burden of Disease Study 2019. We used joinpoint regression to assess temporal trends in rabies burden and age-period-cohort model to evaluate age, period, and cohort effects on rabies incidence and mortality. Animal rabies vaccination data were obtained from World Animal Health Information System. The association between the ratio of vaccinated animals and age-standardized incidence rate was explored. From 1990 to 2019, the global rabies incident cases, deaths, and disability-adjusted life years (DALYs) decreased by 43.12%, 47.20%, and 54.59%, respectively. Age-standardized rates of incidence, mortality, and DALYs declined in all socio-demographic index (SDI) regions, yet consistently remained the highest in low SDI region. The highest rabies incidence rate and mortality rate were observed in children aged 0–9 years. Population living during 1990–1994 had the highest rabies incidence and mortality risks. Countries and territories with high rabies age-standardized incidence rate generally had low ratios of vaccinated animals. Globally, rabies burden decreased over past 30 years, yet disparities in rabies burden regarding gender, age, period, cohort and SDI region existed. Targeted strategies are needed, especially in low SDI region and among children aged 0–9 years.
KEYWORDS: Rabies, global burden of disease study, joinpoint regression, age-period-cohort analysis, age-standardized rate
1. Introduction
Rabies is an acute fatal disease caused by lyssavirus infection and transmitted through bite or scratch of infected animals [1]. Domestic dogs are the major source of most human rabies deaths cases [2]. The rabies virus infects the central nervous system of mammals, including humans, ultimately causing brain inflammation and death. Incubation period of rabies could be weeks to months after infection, varying with specific type of virus, the place where lyssavirus invades, and viral load. Once the clinical symptoms occur, the disease is virtually 100% fatal [3]. Timely vaccination of animals plays a crucial role in rabies control [4]. The World Health Organization (WHO) recommends achieving a minimum vaccination coverage of 70% of the dog population through annual immunization as a crucial step toward the elimination of rabies [5].
Globally, rabies remains a major public health issue. According to previous studies, rabies causes the death of more than 59 000 people annually and results in an economic burden of over 8.6 billion dollars worldwide [6]. Asia and Africa are the continents hardest hit by rabies, with estimated 35 172 and 21 476 human deaths due to dog-mediated rabies per year, respectively [6,7]. In the European Union and the European Economic Area (EU/EEA), the majority of human rabies cases occur among travelers bitten by dogs in countries where rabies is endemic, primarily in Asia and Africa [8].
The risks of rabies incidence and mortality can be further decomposed into age effect, period effect, and birth cohort effect. Risks of rabies incidence and mortality vary in different age groups [9,10]. Advances in rabies-related health policies, disease diagnostics, and treatments affect the risk of rabies incidence and mortality in different periods [4,11]. The risks of rabies incidence and mortality also vary among different birth cohorts, influenced by their exposure to distinct social events [12]. Therefore, an in-depth analysis of trends in global rabies incidence and mortality with particular focus on association with age, period, and cohort effects can deepen understanding of rabies epidemiology, as well as to identify potential gaps in different aspects of rabies prevention, treatment, and management. Furthermore, large-scale canine rabies vaccination has been proved an important way to control rabies [4]. By analyzing the association between animal rabies vaccination and human rabies burden, evidence can be provided for current progress in rabies prevention and control.
The Global Burden of Disease Study (GBD) provides a comprehensive assessment of diseases and risk factors. Based on GBD database, a recent study systematically reported global burden of rabies in 204 countries and territories [13]. Another study explored the global rabies burden and further predicted absolute number of rabies cases for 2030 [14]. Yet, trends in rabies burden associated with age, period, and cohort effects remain unknown, and the association between animal rabies vaccination and human rabies incidence is still unclear.
In this study, based on data obtained from GBD 2019, we aimed to assess the trends in rabies burden associated with age, period, and cohort effects. In addition, combined with data extracted from World Animal Health Information System (WAHIS), we further explored the association between ratio of animals vaccinated against rabies and the age-standardized incidence rates of rabies from 2005 to 2019. We utilized joinpoint regression analysis and age-period-cohort (APC) model to gain a more in-depth understanding of the effectiveness of rabies vaccination in animals, with a focus on regional disparities in animal vaccination coverage and the influence of rabies-related public health policies. Findings would have important implications for policy-makers to optimize strategies and measures against rabies.
2. Methods
2.1. Data source
The data of rabies burden were obtained from GBD 2019. The GBD 2019 provided a comprehensive assessment of 369 diseases and injuries by sex, age, location, and year from 1990 to 2019 across 204 countries and territories. Details on the methods used to estimates the results for each disease and injury could be referred to previous studies [15]. Data sources of rabies in GBD 2019 are from mortality database, literature reviews, and reports. All available cause of death data were standardized and pooled into a single database, from which estimates of the rabies mortality were subsequently generated through algorithms. Symptomatic infections are modeled, not including those infections in which the onset of symptomatic disease was prevented by intervention. Estimates of the number of symptomatic rabies infections (i.e. those not averted through prophylactic vaccination) were generated based on rabies mortality estimates, assuming 99% case fatality. All cases are assumed to be severe [15].
Data on animals vaccinated against rabies were obtained from World Animal Health Information System (WAHIS), the global animal health reference database of the World Organization for Animal Health (WOAH). WAHIS data reflect validated information on terrestrial and aquatic diseases, emerging diseases, and zoonoses in domestic and wild animals, reported by member and nonmember national and territorial veterinary authorities since 2005. The types of animals vaccinated vary by country, with dogs being the predominant species.
2.2. Measurements
In GBD 2019, rabies was diagnosed basing on the 10th edition of the International Classification of Diseases (ICD-10), codes A82-A82.9, Z20.3, and Z24.2. The Socio-demographic Index (SDI) is a composite indicator of social background and economic condition. Countries and territories were classified into five SDI levels in GBD 2019, i.e. low, low-middle, middle, high-middle, and high SDI levels. We extracted incident cases, age-standardized incidence rate (ASIR), deaths, age-standardized mortality rate (ASMR), disability-adjusted life years (DALYs), and age-standardized DALYs rate (ASDR) of rabies with 95% uncertain intervals (UIs) by sex, age, geographic regions, SDI quantiles, countries and territories from 1990 to 2019.
WAHIS registers various kinds of animal diseases, with relevant number of species, emerging outbreaks, cases, susceptible animals and vaccinated animals, etc. We extracted records of the number of animals vaccinated against rabies from 2005 to 2019 by country.
2.3. Statistical analysis
2.3.1. Joinpoint regression analysis
Joinpoint regression analysis has been widely applied to explore the temporal trends in disease burden [16,17]. This method identifies changes in data trends by connecting different segments on a log scale at ‘joinpoints’ (the points with the best fit). Each joinpoint indicates a significant change in the trend [18]. Two key indicators were calculated by the model, including the annual percent change (APC) and average annual percent change (AAPC), with AAPC being calculated as geometric weighting average of various APC. In this study, we used joinpoint regression analysis to assess the magnitude of temporal trends in rabies ASIR, ASMR, and ASDR during 1990–2019. Increasing trend in ASIR, ASMR, and ASDR of rabies was defined as APC or AAPC > 0 and p value < 0.05, and decreasing trend was defined as APC or AAPC < 0 and p value < 0.05, and stable trend was defined as the 95% CI containing 0 and p value ≥ 0.05. We used the Joinpoint Regression Program (version 4.9.1.0) from the Surveillance Research Program of the US National Cancer Institute to conduct the joinpoint regression analysis.
2.3.2. Age-period-cohort analysis
In this study, we used APC model to assess the age, period, and cohort effects on the incidence and mortality of rabies. This method specifically focuses on determining the contributions of age-associated biological factors as well as technological and social factors to disease trends [19]. The APC model is capable of not only determining the net drift and local drift of rabies incidence rate and mortality rate over time, which represent the overall temporal trend and the temporal trend within each age group, respectively, but also estimating the independent effects of age, period, and cohort [20]. This approach has been adopted in the epidemiological studies of diseases, including tuberculosis, congenital heart disease, and musculoskeletal disorders [19,21].
In the APC model, the net drift is an estimate of the overall trend of rabies incidence rates and mortality rates, expressed as annual percentage changes of the rates. The local drift indicates the temporal trend of incidence rates and mortality rates within each age group, expressed as the annual percentage changes of age-specific rates. The age effects are represented by fitted longitudinal age-specific rates in reference cohort adjusting for period deviations. The period (or cohort) effects are represented by the ratio of age-specific rates in each period (or cohort) relative to reference period (or cohort). In a typical APC model, the age and period interval should be equal. Therefore, we converted the data into consecutive 5-year age groups (from 0–4 years old to 90–94 years old) and successive 5-year periods (from 1990–1994 to 2015–2019). Birth cohorts could be calculated by periods minus ages, so birth cohorts were divided into 1900–1904 to 2015–2019. We used the APC Web Tool designed by the US National Cancer Institute to estimate the parameters for APC model [22].
The Wald chi-squared test was used to examine the significance of parameters and functions. The slops of the period rate ratio (RR) and the cohort RR were tested by a general linear model. All statistical tests were two sided and p < 0.05 was considered as statistical significance.
2.3.3. Association between ratio of animals vaccinated against rabies and age-standardized incidence rate of rabies
We extracted the number of animals vaccinated against rabies, and the population of countries and territories reporting relevant data in WAHIS. Then we divided the number of animals vaccinated against rabies by the population of corresponding countries and territories to obtain the ratio of vaccinated animals from 2005 to 2019 (per 10 000 000 population), and explored the association between the ratio of animals vaccinated against rabies and age-standardized incidence rates of rabies.
3. Results
3.1. Long-term spatio-temporal trends in rabies burden
At global level, the number of rabies incident cases, deaths, and DALYs decreased by 43.12%, 47.20%, and 54.59% during 1990–2019, respectively (Table 1, Table S1-S2).
Table 1.
The incident cases, ASIR and corresponding percentage change of rabies by gender, SDI regions and GBD regions in 1990 and 2019.
| Number (95% UI) |
Percentage change of number (%, 95% UI) |
ASIR per 10 000 000 population (95% UI) |
Percentage change of ASIR (%, 95% UI) |
|||
|---|---|---|---|---|---|---|
| Characteristics | In 1990 | In 2019 | From 1990 to 2019 | In 1990 | In 2019 | From 1990 to 2019 |
| Global | 24744.66 (9201.76, 40728.99) | 14075.51 (6124.33, 21618.11) | −43.12 (−64.04, −20.13) | 45.99 (17.74, 75.23) | 18.45 (7.89, 28.18) | −59.89 (−74.46, −45.31) |
| Gender | ||||||
| Female | 9633.26 (2796.03, 15201.68) | 4425.27 (1303.27, 7130.31) | −54.06 (−65.31 to − 34.77) | 36.37 (11.04, 57.78) | 11.47 (3.38, 18.30) | −68.46 (−75.89, −55.88) |
| Male | 15111.40 (4101.96, 31868.52) | 9650.23 (3370.02, 15554.67) | −36.14 (−66.92 to 3.36) | 55.63 (15.26, 114.68) | 25.29 (8.85, 40.44) | −54.53 (−75.60, −28.73) |
| SDI regions | ||||||
| High SDI | 15.26 (9.86, 23.71) | 18.08 (8.70, 26.55) | 18.46 (−24.11, 72.96) | 0.17 (0.12, 0.27) | 0.14 (0.07, 0.19) | −22.21 (−49.05, 11.51) |
| High-middle SDI | 876.21 (416.99, 1353.27) | 526.27 (241.38, 803.66) | −40.11 (−56.73, −19.68) | 7.92 (3.79, 12.32) | 3.37 (1.45, 5.15) | −57.62 (−70.00, −42.46) |
| Middle SDI | 4210.12 (1534.77, 5785.54) | 2174.88 (859.81, 2939.93) | −50.33 (−63.51, −36.87) | 26.82 (10.36, 38.53) | 9.05 (3.55, 12.26) | −67.53 (−75.77, −60.20) |
| Low-middle SDI | 12869.88 (4481.01, 19336.64) | 6074.70 (2726.70, 9755.16) | −54.18 (−74.75, −32.33) | 119.27 (45.28, 184.66) | 36.52 (16.66, 60.12) | −70.26 (−83.73, −57.26) |
| Low SDI | 6766.78 (2841.41, 15981.13) | 5278.04 (2251.79, 9237.14) | −29.60 (−58.38, 11.14) | 126.93 (53.86, 279.41) | 48.70 (22.06, 85.80) | −64.91 (−79.10, −49.54) |
| GBD regions | ||||||
| Central Asia | 62.08 (43.60, 87.58) | 72.44 (43.99, 120.12) | 16.69 (−34.22, 118.38) | 12.33 (8.51, 18.31) | 10.29 (5.99, 17.76) | −16.52 (−57.42, 68.12) |
| Central Europe | 6.51 (5.09, 8.08) | 2.39 (1.51, 3.91) | −63.23 (−77.81, −36.93) | 0.60 (0.49, 0.72) | 0.12 (0.08, 0.20) | −79.42 (−87.21, −65.33) |
| Eastern Europe | 30.26 (22.58, 44.87) | 26.60 (18.89, 37.89) | −12.10 (−47.06, 42.51) | 1.32 (0.97, 1.96) | 0.91 (0.66, 1.28) | −31.08 (−55.95, 11.49) |
| Australasia | 0.02 (0.02, 0.03) | 0.06 (0.04, 0.08) | 161.93 (60.14, 309.50) | 0.01 (0.01, 0.02) | 0.02 (0.01, 0.03) | 31.57 (−20.10, 112.98) |
| High-income Asia Pacific | 2.57 (1.05, 3.58) | 0.72 (0.51, 0.93) | −71.77 (−81.18, −33.82) | 0.17 (0.09, 0.22) | 0.02 (0.01, 0.02) | −91.00 (−93.39, −84.89) |
| High-income North America | 2.21 (1.99, 2.82) | 3.48 (3.01, 4.36) | 57.10 (19.81, 98.67) | 0.08 (0.07, 0.10) | 0.09 (0.08, 0.11) | 10.89 (−12.61, 38.02) |
| Southern Latin America | 1.52 (0.97, 2.38) | 0.59 (0.27, 1.29) | −61.54 (−84.28, −5.90) | 0.33 (0.21, 0.51) | 0.07 (0.03, 0.16) | −77.25 (−90.74, −44.48) |
| Western Europe | 2.72 (2.09, 3.69) | 2.02 (1.63, 2.81) | −25.61 (−48.75, 9.44) | 0.06 (0.05, 0.08) | 0.03 (0.02, 0.04) | −52.51 (−67.40, −30.03) |
| Andean Latin America | 30.51 (6.19, 39.19) | 5.19 (2.49, 20.51) | −82.99 (−92.67, 2.84) | 9.29 (2.45, 11.86) | 0.88 (0.43, 3.43) | −90.52 (−95.79, −56.83) |
| Caribbean | 4.13 (1.29, 7.36) | 5.41 (0.88, 9.08) | 31.12 (−43.03, 136.54) | 1.17 (0.36, 2.01) | 1.15 (0.19, 1.95) | −1.47 (−54.83, 72.16) |
| Central Latin America | 72.34 (64.28, 79.84) | 3.93 (2.09, 5.95) | −94.57 (−96.92, −91.73) | 4.53 (4.06, 4.94) | 0.16 (0.08, 0.24) | −96.50 (−98.01, −94.74) |
| Tropical Latin America | 85.25 (62.51, 133.34) | 1.56 (1.33, 2.06) | −98.17 (−98.88, −97.14) | 5.36 (4.05, 8.01) | 0.07 (0.06, 0.09) | −98.68 (−99.16, −98.01) |
| North Africa and Middle East | 169.31 (51.84, 243.49) | 75.51 (22.31, 115.87) | −55.40 (−72.01, −34.03) | 5.59 (1.81, 7.82) | 1.40 (0.43, 2.06) | −74.87 (−83.59, −64.12) |
| South Asia | 15139.39 (5621.07, 23976.88) | 7287.84 (3560.98, 12760.99) | −51.86 (−72.32, −24.64) | 149.76 (59.06, 233.50) | 43.41 (21.15, 75.94) | −71.01 (−83.53, −54.95) |
| East Asia | 1391.00 (935.27, 3395.93) | 771.23 (277.95, 1021.39) | −44.56 (−76.95, −18.27) | 12.32 (8.36, 30.73) | 4.58 (1.69, 6.15) | −62.83 (−84.35, −45.82) |
| Oceania | 0.87 (0.14, 1.90) | 1.58 (0.22, 3.04) | 81.56 (3.49, 205.53) | 4.02 (0.56, 11.75) | 2.74 (0.40, 6.08) | −31.96 (−65.94, 23.80) |
| Southeast Asia | 3385.34 (702.47, 4810.38) | 1291.56 (441.00, 1949.45) | −61.85 (−75.45, −26.13) | 72.83 (18.46, 100.20) | 20.13 (7.14, 30.25) | −72.35 (−81.97, −55.36) |
| Central Sub-Saharan Africa | 56.24 (20.69, 209.39) | 37.75 (15.21, 162.06) | −32.88 (−68.57, 29.88) | 9.51 (4.32, 33.71) | 3.56 (1.46, 13.55) | −62.61 (−79.83, −40.32) |
| Eastern Sub-Saharan Africa | 2091.14 (688.12, 9359.35) | 1853.33 (662.37, 4341.83) | −11.37 (−59.39, 92.74) | 98.72 (35.19, 423.10) | 43.16 (17.39, 100.33) | −56.28 (−78.76, −14.74) |
| Southern Sub-Saharan Africa | 45.76 (18.59, 81.09) | 39.34 (18.87, 75.28) | −14.02 (−49.45, 41.81) | 8.40 (3.32, 15.00) | 5.21 (2.48, 9.95) | −38.05 (−63.18, −1.04) |
| Western Sub-Saharan Africa | 2165.48 (764.27, 3729.82) | 2592.96 (761.58, 4266.32) | 19.74 (−27.48, 94.29) | 106.46 (35.73, 199.07) | 56.97 (16.28, 92.62) | −46.48 (−67.07, −20.55) |
Abbreviations: ASIR, age-standardized incidence rate; SDI, socio-demographic index; GBD, Global Burden of Disease Study; UI, uncertainty interval.
From 1990 to 2019, the ASIR, ASMR, and ASDR of rabies had decreased trends, with AAPC − 3.08 (95% CI: −3.24, −2.91) in ASIR, AAPC − 3.38 (95% CI: −3.69, −3.06) in ASMR, and AAPC − 3.55 (95% CI: −3.87, −3.23) in ASDR, respectively (Table 2).
Table 2.
The annual percent change and average annual percent change of rabies ASIR, ASMR, and ASDR at global level from 1990 to 2019.
| ASIR |
ASMR |
ASDR |
|||||||
|---|---|---|---|---|---|---|---|---|---|
| Characteristics | Period | APC (95% CI) | AAPC (95% CI) | Period | APC (95% CI) | AAPC (95% CI) | Period | APC (95% CI) | AAPC (95% CI) |
| Segment | |||||||||
| Trend1 | 1990–2003 | −1.85 (−1.91, −1.80)* | – | 1990–2000 | −2.17 (−2.33, −2.01)* | – | 1990–2000 | −2.30 (−2.48, −2.13)* | – |
| Trend2 | 2003–2006 | −2.74 (−3.68, −1.80)* | – | 2000–2003 | −3.23 (−5.09, −1.33)* | – | 2000–2003 | −3.66 (−5.70, −1.58)* | – |
| Trend3 | 2006–2009 | −7.00 (−7.91, −6.08)* | – | 2003–2006 | −1.32 (−3.2, 0.59) | – | 2003–2006 | −1.41 (−3.45, 0.68) | – |
| Trend4 | 2009–2014 | −4.64 (−4.92, −4.35)* | – | 2006–2011 | −6.72 (−7.24, −6.2)* | – | 2006–2011 | −6.83 (−7.40, −6.25)* | – |
| Trend5 | 2014–2017 | −2.84 (−3.72, −1.95)* | – | 2011–2014 | −5.24 (−6.8, −3.65)* | – | 2011–2015 | −4.91 (−5.78, −4.03)* | – |
| Trend6 | 2017–2019 | −1.90 (−2.78, −1.01)* | – | 2014–2019 | −2.53 (−2.89, −2.18)* | – | 2015–2019 | −2.59 (−3.14, −2.04)* | – |
| AAPC | 1990–2019 | – | −3.08 (−3.24, −2.91)* | 1990–2019 | – | −3.38 (−3.69, −3.06)* | 1990–2019 | – | −3.55 (−3.87, −3.23)* |
Abbreviations: ASIR, age-standardized incidence rate; ASMR, age-standardized mortality rate; ASDR, age-standardized DALYs rate; DALYs, disability-adjusted life-years; APC, annual percentage change; AAPC, average annual percentage change; CI, confidence interval; *p < 0.05.
At regional level of SDI, low-middle region had the most rabies incident cases and deaths, whereas low SDI region had the most DALYs and the highest age-standardized rates (ASRs) in 2019 (Table 1, Table S1-S2). From 1990 to 2019, the ASRs declined in all SDI regions and the maximum decline was in the low-middle SDI region (Figure 1, Figure S1). At regional level of GBD in 2019, South Asia had the most rabies incident cases, deaths, and DALYs, while Western Sub-Saharan Africa had the highest ASRs (Table 1, Table S1-S2). From 1990 to 2019, rabies ASRs showed declining or stable trend in most GBD regions, while Australasia and High-income North America exhibited increasing trend in ASIR (Figure 1).
Figure 1.
Trends in age-standardized rates of incidence, mortality, and DALYs of rabies at global and regional levels from 1990 to 2019.
At national level, in 2019, India had the highest number of rabies cases, deaths, and DALYs, followed by Nigeria and Pakistan (Table S3-S5). In 2019, ASIR of rabies exceeded the global average in 44 countries and territories. The top three countries with the highest ASIR were Nepal, Myanmar, and Niger (Figure 2(b)). From 1990 to 2019, the trends in ASIR of rabies varied significantly across 204 countries and territories. Specifically, the ASIR increased in 28 countries and territories, decreased in 167 countries and territories, and remained stable in 9 countries and territories (Figure 2(d)). The Netherlands had the largest increase in rabies ASIR, followed by Puerto Rico and Greece. Conversely, Mexico had the largest decrease in rabies ASIR, followed by Costa Rica and Brazil (Table S3).
Figure 2.
The ASIR of rabies across 204 countries and territories in 1990 (a) and in 2019 (b), the AAPC of ASIR during 1990-2019 (c), and the trend in ASIR during 1990-2019 (d). ASIR, age-standardized incidence rate; AAPC, average annual percentage change.
The ASMR of rabies exhibited an increasing trend in 17 countries and territories, a decreasing trend in 146 countries and territories, and remained stable in 41 countries and territories (Figure S2). The largest increases in rabies ASMR were observed in the Netherlands, Puerto Rico, and Greece, while the largest decreases were seen in Mexico, Costa Rica, and Brazil (Table S4).
Similarly, the ASDR of rabies increased in 19 countries and territories, decreased in 149 countries and territories, and remained stable in 36 countries and territories (Figure S3). The largest increases in rabies ASDR were observed in Puerto Rico, the Netherlands, and Suriname, while the largest decreases were seen in Mexico, Brazil, and Guatemala (Table S5).
Regarding demographics, in 2019, the number of rabies incident cases, deaths, and DALYs peaked at the age of 0–4 year in females and at the age of 5–9 years in males (Figure S4A, 4C and 4E). In 2019, the age-specific incidence rates for both females and males peaked at 75–79 years, while mortality rates peaked at 95+ years for females and 75–79 years for males. DALYs rates were the highest for females aged 0–4 and males aged 5–9 (Figures S4B, S4D, and S4F). Overall, the rabies incident cases, deaths, DALYs, and corresponding ASRs of males were higher than females during 1990–2019 (Figure S5).
3.2. Age, period, and birth cohort effects on rabies burden
Globally, declines were observed in rabies incidence and mortality, with a net drift of −3.11% per year for incidence rates and −3.16% per year for mortality rates (Table S6-S7). The local drifts for both incidence rates and mortality rates were below zero for all age groups (Figure 3(a), Figure S6A).
Figure 3.
Estimated parameters of rabies incidence rates of age, period, and cohort effects from 1990 to 2019. (a) Local drifts for rabies incidence. (b) Fitted longitudinal age curves of rabies incidence. (c) Rate ratios of rabies incidence due to period effects. (d) Rate ratios of rabies incidence due to birth cohort effects.
The rabies incidence rates and mortality rates peaked at the age of 0–9 years, then decreased with age (Figure 3(b), Figure S6B). The highest incidence rate and mortality rate occurred at the age of 5–9 years and 0–4 years, respectively (Table S8). The period effects exhibited a downward trend in both rabies incidence rates and mortality rates from 1990 to 2019 (Figure 3(c), Figure S6C). Specifically, the highest RR of incidence (RR = 1.21) and mortality (RR = 1.25) occurred during 1990–1994 for whole population (Table S9). The lowest RR of rabies incidence (RR = 0.56) and mortality (RR = 0.57) occurred during 2015–2019 (Table S9).
Overall, the cohort effects showed a decreasing trend in rabies incidence rates and mortality rates (Figure 3(d), Figure S6D). Compared with individuals in the reference 1955–1959 cohort, individuals in the 1900–1904 birth cohort had the highest RR of incidence (RR = 7.50) and mortality (RR = 6.95) (Table S10). Individuals born in the 2015–2019 cohort had the lowest RR of incidence (RR = 0.15) and mortality (RR = 0.12) (Table S10).
3.3. Association between ratio of vaccinated animals and age-standardized incidence rates of rabies from 2005 to 2019
From 2005 to 2019, a notable observation was that countries and territories with high rabies ASIR generally had low ratios of vaccinated animals (Figure 4, Figure S7). From 2005 to 2013, countries with high ratio of vaccinated animals experienced a relatively low ASIR. Yet during 2014 to 2015, a shift, i.e. a disproportionately high ASIR of rabies, was observed in Malawi, Vietnam and Uzbekistan, despite having high ratios of vaccinated animals. A similar trend was observed in the Philippines and Laos between 2016 and 2019.
Figure 4.
Association between ratio of vaccinated animals and age-standardized incidence rates of rabies by country from 2011 to 2019. (a) 2011, (b) 2012, (c) 2013, (d) 2014, (e) 2015, (f) 2016, (g) 2017, (h) 2018, and (i) 2019.
In 2019, a total of 69 countries and territories reported the number of animals vaccinated against rabies. Among the countries and territories reporting data to WAHIS, Nepal had the highest ASIR (121.18 per 10 000 000 population), followed by Niger (92.49 per 10 000 000 population), Ghana (77.58 per 10 000 000 population), Chad (75.41 per 10 000 000 population), and Mali (72.11 per 10 000 000 population). The ratio of vaccinated animals was 3345.57 per 10 000 000 population in Nepal, 127.79 per 10 000 000 population in Ghana, whereas none rabies vaccination was delivered to animals in Niger, Chad, and Mali (Table S11).
4. Discussion
The global rabies incident cases, deaths, DALYs, and corresponding age-standardized rates decreased significantly during 1990–2019. Rabies ASIR, ASMR, and ASDR decreased in all SDI regions, while these indicators consistently remained the highest in low SDI region and the lowest in high SDI region. The burden of rabies was higher in males than that in females. Age-specific incidence and mortality rates peaked among children aged 0–9 years. Globally, RR of rabies incidence and mortality continued to decline from 1990 to 2019. Individuals in recent birth cohorts exhibited lower RR of rabies incidence and mortality than previous birth cohorts. From 2005 to 2019, countries and territories with high rabies ASIR had low ratio of vaccinated animals.
The ASRs of rabies decreased across all SDI regions during 1990–2019, while low SDI region still had the highest ASRs. Human rabies is primarily caused by bites or scratches from infected animals, and prompt post-exposure prophylaxis (PEP) significantly reduces the risk of death in patients [9]. Poor accessibility and inefficient use of rabies medical resources would pose severe health threats to vulnerable population, leading to high rabies burden. In resource-limited countries and territories, the lack of effective rabies surveillance systems and the shortage of human rabies vaccines may exacerbate rabies burden [7].
We observed the largest reductions of rabies burden in Tropical Latin America (including Brazil and Paraguay). In 1983, with technical cooperation from the Pan American Health Organization (PAHO), countries in the Americas have pledged to eliminate human rabies transmitted by dogs. Since then, there has been a strong political mandate and international commitment in the Americas to eliminate human rabies transmitted by dogs [23]. Due to national efforts and regional collaboration under the Regional Program for the Elimination of Rabies, human rabies cases have dropped significantly in the Americas [23]. These achievements have been facilitated by the strengthening of capacities for regular mass dog vaccination, timely post-exposure prophylaxis, and improved public health surveillance [24].
In contrast, we found a rise of rabies ASIR in Australasia (including Australia and New Zealand) and High-income North America (including Canada, Greenland, and United States of America). Rabies in Australia was exotic, while the spread of rabies in eastern Indonesia posed an increasing risk to northern Australia [25,26]. In New Zealand, a survey revealed that New Zealanders traveling abroad were largely unaware of the risk of contracting rabies, and 79.7% of the survey population remained at risk of contracting rabies [27]. In countries dog-mediated rabies is effectively controlled, vigilance is still needed for rabies caused by wildlife. Canada and United States of America had eliminated canine rabies, while elimination of specific wildlife virus variants remained a goal for both countries [28]. The increase in the ASIR of rabies may partly be due to the risks posed by external introductions and transmission from wildlife.
Globally, males had higher rabies burden than females, consistent with previous studies [9,29]. Previous studies revealed that males were at high risk of exposure to rabies at work, and middle-age male were less likely to seek for PEP compared to younger age group [29,30]. After adjusting for period deviations, rabies incidence and mortality rates peaked in children aged 0–9 years old, and then decreased with age. It could be attributed to that children were afraid of guardians’ scolding, i.e. being bitten by dogs, and they missed timely treatment [9]. Additionally, children lack the ability to distinguish if dogs are infected, and struggle to resist dogs’ attacks, making them susceptible to serious injuries from rabies [31,32].
The risks of rabies incidence and mortality decreased gradually over time. This indicates that significant progress has been made in the diagnosis, treatment, and management of rabies over the past decades. The intergovernmental tripartite, non-governmental organization and regional cooperation made numerous efforts to strengthen rabies prevention and control [7,33]. For instance, the emergence of the Rabies in West Africa (RIWA) forum has addressed the issue of the lack of reliable rabies data in West African countries such as Liberia, Nigeria, and Sierra Leone. This is crucial for assessing the rabies burden and informing the implementation of control measures [7]. Incidence and mortality risks from rabies were lower in recent birth cohorts compared to previous ones. One possible reason is that recent cohorts had more access to health education and improved health literacy [12,34]. This may also relate to the strong rabies-related health policies implemented by the government to reduce dog bite exposure and ensure adequate provision of human rabies vaccines [35].
Ratios of vaccinated animals varied across countries and territories. From 2005 to 2019, countries and territories with high ASIR generally have low ratios of vaccinated animals. Experience from countries with successful rabies control demonstrates that mass vaccination of dogs is an effective approach to prevent and control rabies [36]. Thus, inadequate animal rabies vaccination may be one of the reasons for the high ASIR in these countries and territories. Findings also imply that controlling rabies requires a scientifically integrated management approach, with animal rabies vaccination being the most effective method [4].
In 2019, Philippines had the highest ratio of vaccinated animals, while the ASIR of rabies in Philippines was not as low as expected. Despite efforts to expand Animal Bite Treatment Centers (ABTCs) nationwide and provide free rabies PEP, studies have shown that the number of human rabies cases in the Philippines did not significantly decrease between 2008 and 2018 [37]. This may be attributable to the failure of rabies patients to access PEP in time. A retrospective study found that, from 2006 to 2015, among the 437 patients with a history of animal exposure admitted to a referral hospital in Metro Manila, Philippines, only 42 patients (9.6%) received at least one dose of rabies vaccine, which may be attributed to considerations of time or cost [29]. Having no time was the most common reasons for not completing PEP series [38].
Although free PEP policies are crucial for preventing deaths caused by rabies, they are unable to eliminate rabies at its source or reduce the risk of exposure [39]. Mass canine vaccination campaigns are one of the most important actions for controlling rabies. A study in Tanzania showed that after two consecutive vaccination campaigns, canine rabies decreased by 70% and 97%, respectively, resulting in a significant reduction in the demand for PEP in cases of human exposure [40]. It is commonly assumed that at least 70% of dogs must be vaccinated to eliminate rabies transmission among dogs, and thereby eliminate rabies transmission to humans [41]. Therefore, accurate estimation of the dog population is crucial. However, current animal surveillance systems in the Philippines do not adequately reflect the burden of rabies in the canine population, resulting in insufficient vaccination coverage for dogs [39]. These factors offer a partial elucidation of the phenomenon whereby, in the Philippines, despite the high ratios of animals vaccinated against rabies, the ASIR does not exhibit a low value.
The WHO, the Food and Agriculture Organization (FAO), and the WOAH advocate the use of the One Health approach to eliminate rabies. The essence of the One Health approach is the collaboration of multiple disciplines, including human public health and animal health institutions, to achieve common goals [4]. A One Health approach to rabies control would encompass several key strategies: implementing mass dog vaccination campaigns, enhancing accessibility to PEP for humans, managing infections at the interface of humans, domestic animals, and wildlife, and raising rabies awareness within local communities [35]. Moreover, efficient surveillance systems are essential for the control of rabies [39]. Rabies is highly prevalent in developing countries. However, most of these countries have limited resources and weak rabies surveillance systems, which lead to significant issues of under-reporting and under-vaccination. The limited and potentially unreliable rabies data available further contribute to the insufficient prioritization of rabies prevention on public health agendas and pose challenges in advocating for sustainable control programs [6].
WHO and global partners recommend Integrated Bite Case Management (IBCM) as a gold standard method to strengthen rabies surveillance in low- and middle-income countries. IBCM directly and formally links staff from public health and veterinary departments to assess the risk of rabies in both animal-bite victims and the biting animals, respectively. By enhancing surveillance, IBCM has the potential to provide more accurate estimates of the rabies burden and to inform the implementation of control and prevention measures, including facilitating management decisions to reduce unnecessary use of PEP and assessing the progress of elimination programs [42].
KwaZulu-Natal, the United Republic of Tanzania, and Bangladesh have significantly reduced the burden of rabies through comprehensive strategies encompassing data collection, surveillance, and diagnostics; dog vaccination and management; human vaccine provision and bite management; education and training; and the development of long-term rabies elimination and sustainable surveillance strategies. These successful cases demonstrate the feasibility of controlling and eliminating human rabies in low-income countries by targeting canine rabies, thereby promoting evidence-based strategies [43].
There are several limitations in this study. First, the rabies burden in GBD 2019 is based on detected cases, not actual incidence. In countries with poor surveillance infrastructure, under-reporting of both animal vaccination and rabies cases may occur. Second, due to lack of dog rabies vaccine coverage data, we used the number of animals vaccinated per 10 000 000 population as a proxy. Data availability also limited the analysis of animal vaccination and rabies incidence period to 2005–2019. Third, we could not explore rabies risk factors due to the lack of related data in GBD 2019. Finally, using community as the analysis unit may introduce ecological fallacy, and individuals over 95 years old were excluded from the APC analysis, because they did not meet the requirements of APC tool.
5. Conclusions
Overall, global rabies incidence, deaths, DALYs, and relevant age-standardized rates declined from 1990 to 2019, yet disparities in rabies burden regarding gender, age, period, cohort and SDI region existed. Low SDI region continued to experience the highest rabies burden. We observed declined period and cohort effects on rabies incidence and mortality, with the highest risk of rabies incidence and mortality in children aged 0–9 years old. In addition, countries with high ASIR of rabies generally had low ratios of vaccinated animals. To globally eliminate rabies, one-health strategies and measures against rabies should be prioritized, including increasing rabies vaccination coverage in animals, enhancing accessibility to PEP for high-risk populations, optimizing surveillance systems, and raising public awareness of rabies, particularly in low SDI regions and rabies-endemic areas.
Supplementary Material
Funding Statement
This work was supported by the China Medical Board under Grant [numbers 14–202 and 19–307].
Author contributions
XYT and ZZQ conceptualized the study and designed the analysis plan. Material preparation, data collection and analysis were performed by ZZQ, XHM, and ZYM. ZZQ wrote the first draft of manuscript. ZZQ, HJQ, XXH and RW accessed and verified the data used in the study. All authors made significant contributions to the revision of the manuscript. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication.
Availability of data and materials
The data used and analyzed during the current study will be shared with researchers from the corresponding author on reasonable request.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Ethical statement
Ethical approval and consent were not required as this study was based on publicly available data. No individual-level data were used in this study.
Supplementary material
Supplemental data for this article can be accessed online at https://doi.org/10.1080/20477724.2025.2502904
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Associated Data
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Supplementary Materials
Data Availability Statement
The data used and analyzed during the current study will be shared with researchers from the corresponding author on reasonable request.