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Rabies is a viral zoonotic disease that causes progressive and fatal inflammation of the brain (1). China has been working on the control and elimination of human rabies. Since 1955, rabies became one of the notifiable infectious diseases in China. A total of 5,632 human rabies cases were reported comprising 4 epidemic peaks in Shandong Province from 1956 to 2020. In 2007, a total of 133 cases were reported and the number of cases reached the fourth peak in recent years (2). This study analyzed epidemiological characteristics and risk factors of human rabies in Shandong Province from 2010 to 2020. The data provided essential information and suggestions for adjustments to the rabies control policy in Shandong Province.
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Historical data of human rabies cases from 2010 to 2020 in Shandong Province were collected through China’s National Notifiable Disease Reporting System (NNDRS) from January 1, 2010 to December 31, 2020. The questionnaire about every case was filled out through a face-to-face interview with a family member of the patient by trained public health physicians at the county-level CDC and sent to the Shandong Provincial CDC. The questionnaire included patient information (gender, age, occupation), clinical manifestations, wounds caused by animals, and post-exposure prophylaxis (PEP) at the local clinics, etc. Reverse transcription-polymerase chain reaction (RT-PCR) and fluorescence quantitative PCR were carried out on patients’ saliva, urine, blood specimens and so on. Epidata (version 3.1, Epidata Association, Denmark) was used for data entering and ArcGIS (version 10.0, Esri Inc, California, USA) was used for making regional distribution graphics.
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A total of 414 human rabies cases were reported in Shandong Province from 2010 to 2020, and the incidence of human rabies decreased rapidly year over year, except for a small rebound in 2011 and 2015. The reported incidence rate decreased from 0.10/100,000 population in 2011 to 0/100,000 in 2020 with the mean incidence rate of 0.04/100,000 from 2010–2020. Overall, 74 and 91 cases were reported in 2010 and 2011, respectively, and the number of new cases reached 0 in 2020 (Figure 1). Only 15.22% (63/414) of specimens from cases were collected and confirmed in the lab. Among these 63 cases, 16 cases were laboratory-confirmed with a positivity rate of 25.40%. Also, 73.42% (304/414) of cases were recorded between March and October with a peak season in October. After 2015, rabies cases gradually reduced, and the peak season was not obvious.
Figure 1.The number of cases and incidence rate of human rabies in Shandong Province, China, 2010–2020.
These 414 human rabies cases were distributed widely in 16 municipal areas and 84 counties. Among the 414 human cases, 51 cases were reported from Heze, 48 cases from Linyi, 45 cases from Qingdao, 40 cases from Dezhou, 39 cases from Yantai, accounting for 53.86% of cases in 2010–2020 in Shandong Province. Pingdu City (16 cases), Cao County (14 cases), Laiyang City (12 cases), Junan County (12 cases), and Mudan District (12 cases) were the top five counties in the number of cases, accounting for 15.94% of the total cases in the whole province. All cases occurred in rural areas.
Overall, 71.01% (292/414) of cases were male, and 28.99% (122/414) cases were female. The gender ratio of cases was 2.39∶1. The average age was 52.30±17.04 years old, with a range from 2 to 89 years old. In total, 83.10% (344/414) cases were more than 40 years old. Most human rabies cases from 2010 to 2012 were among the age group from 40 to 49 (62/232, 26.72%), while most human rabies cases from 2013 to 2015 and 2016 to 2020 were among the age group from 50 to 59 (35/124, 28.23%) and from 60 to 69 (24/58, 41.38%), respectively (Table 1). The higher-risk population was born between 1954 and 1972. By occupation, 87.20% (361/414) of cases occurred in farmers, followed by 3.62% (15/414) in students, 3.14% (13/414) in homemakers and unemployed individuals, 2.17% (9/414) in preschool children, and 3.86% (16/414) others.
Age group (years) 2010–2012 2013–2015 2016–2020 Number of cases Proportion (%) Number of cases Proportion (%) Number of cases Proportion (%) 0– 4 1.72 2 1.61 0 0.00 5– 5 2.16 6 4.84 0 0.00 10– 6 2.59 0 0.00 2 3.45 20– 8 3.45 3 2.42 0 0.00 30– 26 11.21 5 4.03 3 5.17 40– 62 26.72 17 13.71 12 20.69 50– 53 22.84 35 28.23 10 17.24 60– 42 18.10 34 27.42 24 41.38 70– 22 9.48 18 14.52 6 10.34 80– 4 1.72 4 3.23 1 1.72 Table 1. Age distribution of human rabies cases in Shandong Province, 2010–2020.
The fatality rate was 100.00%. Overall, 407 questionnaires of human rabies cases were obtained and the response rate was 98.31% (407/414). The median course of disease was 4 days, ranging from 0 to 28 days; 91.40% (372/407) of patients died within one week. Most cases showed typical rabies symptoms such as agitation, hydrophobia, fearing of wind, convulsion, and photophobia, etc.
In the study, categories of exposure were recorded in 377 cases (92.63%); 265 (70.29%) of reported fatalities were category Ⅲ exposure. Location of exposure and exposure modes were recorded in 396 cases (97.30%). The wounds injured mostly occurred on the extremities, and the frequent exposure sites were hands (224 cases, 55.04%), followed by the lower limbs below the knee (78 cases, 19.16%). In 18 cases, there was more than one wound; 343 (86.62%) human cases that died from rabies were due to animal bites; 390 (95.82%) fatalities had reported wounding animal and animal origin; 139 cases (35.64%) were injured by stray animals; and 231 cases (59.23%) by domestic animals (belonging to the family of the case or a neighbor and raised in free range). Overall, 96.67% (377/390) of the cases were injured by dogs, and only 1.89% (4/212) of domestic dogs had been vaccinated against rabies (Table 2).
Exposure characteristics Number of human rabies cases Proportion (%) Age group (years) <20 24 5.90 20–39 42 10.32 40–59 189 46.44 ≥60 152 37.35 Gender Male 289 71.01 Female 118 28.99 Occupation Farmers 359 88.21 Students/preschool children 23 5.65 Others 25 6.14 Exposure level* Ⅰ 18 4.77 Ⅱ 94 24.93 Ⅲ 265 70.29 Exposure mode* Bite 343 86.62 Scratch 33 8.33 Others 20 5.05 Animal source* Domestic animal 231 59.23 Stray animal 139 35.64 Others 20 5.13 Animal vector* Dog 377 96.67 Cat 7 1.79 Others 6 1.54 Exposure reason* Active attack by the vector 211 56.42 Defensive attack by the vector 59 15.78 Playing with the vector 72 19.25 Other 32 8.56 Bite more than one person* Yes 59 15.69 No 317 84.31 Exposure site Head 33 8.11 Neck 4 0.98 Hand 224 55.04 Trunk 10 2.46 Arm 38 9.34 Lower limb above the knee 11 2.70 Below the knee 78 19.16 Wound treatment* Untreated 216 55.53 Self-treated 137 35.22 Treated in medical facilities 36 9.25 Rabies immunoglobulins administered Yes 4 0.98 No 403 99.02 Vaccination administered Yes 36 8.85 No 371 91.15 * Variables with missing values. Table 2. Characteristics of exposure history and post-exposure prophylaxis, according to data from case investigations, Shandong Province, 2010–2020.
Of the 389 (95.58%) cases with available PEP treatment, 216 (55.53%) cases had no wound treatment post exposure at all. Another 137 (35.22%) cases treated the wound by themselves. In total, there were 353 (86.73%) fatalities without proper wound treatment. Only 36 (9.25%) cases had their wounds treated in medical institutions, mostly in village clinics (21/36) (Table 2). Regarding the post-exposure vaccination, the rabies vaccine coverage rate was 8.85% (36/407), and 23 cases were vaccinated at village clinics or private clinics. Of the 11 cases who received the full vaccination, 10 cases classified as category Ⅲ exposure did not receive rabies immunoglobulin as recommended by the WHO guidelines. Among the 25 cases who were not fully vaccinated, 17 died before vaccination was completed.
Among the reported cases, 4 patients who were bitten by stray dogs came to county-level medical institutions for wound treatment and were injected with rabies vaccine and anti-rabies immunoglobulin within 12 hours. Among them, 2 cases were over 60 years old, and another 2 cases were pre-school children, all of whom were exposed as category Ⅲ and died before vaccination completed.
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Rabies is a vaccine-preventable disease. By taking measures to strengthen disease surveillance, conduct technical training, and standardize the clinic treatment for PEP (1,3), the number of human rabies cases in Shandong declined significantly from 2011 to 2020, which was consistent with the epidemic trend of human rabies in China (4–5). First, every reported human rabies case was investigated and the specimens were collected as soon as possible. The case survey rate was almost always 100%. Second, a special training class on rabies was conducted for staff from all over the whole province every year by Shandong CDC. Third, Shandong Province has gradually standardized the construction of PEP clinics since 2001. A series of documents such as construction standards of PEP clinics, were first issued in 2007. And now, there are more than 2,000 qualified rabies PEP clinics in Shandong Province, and they can provide timely services for people. Fourth, health education is indispensable for people.
The study indicated that people over 40 years old and farmers were still the main high-risk groups in Shandong in the past decade (5-7). Before 2013, the number of human rabies cases was the highest in the 40–49 age group, but in the following years, it gradually changed to the group of 50–69 years old. 11.52% (47/408) were young students and preschool children from 2003 to 2007 (2), declining to only 5.80% from 2010 to 2020.
This change indicated the elder people in rural areas need additional protection. Therefore, health education should be focused on the rural elderly. The main reasons for human rabies fatalities were failure to carry out timely and standardized wound treatment and immunization prevention after exposure. In the study, 353 (90.75%) cases died without proper wound treatment and 371 (91.15%) fatalities did not receive vaccination. The vaccination rate (8.85%) of the cases was lower than that in other studies (8). Most cases were treated with PEP in village clinics. These findings suggested that it is important to ensure the quality of PEP at village clinics and establish a transfer system to higher-level hospitals in case of complications. Since 2016, only 2 cases failed to complete the immune program, indicating that the standardized management of rabies vaccination has played an important role in the prevention and control of human rabies (3,8). A total of 4 cases received PEP due to category Ⅲ exposure on heads died before the vaccine procedure completion with an incubation period of 11 to 13 days. It is important for people to seek standardized PEP immediately after exposure, especially for wounds on the head. The physicians should also participate in training courses and pay more attention to serious wounds on the head and face (1).
The result showed that Shandong had a higher rate of dog-related injuries among the cases when compared with the national average level (96.67% vs. 91.46%) cases (5). The majority of attacking animals were domestic animals, with only 1.89% vaccinated for rabies, which was similar to a national study (5). These findings indicate that dog-related injuries are still a primary risk factor for human rabies in Shandong despite the sharp decline in the number of cases, and it is necessary to manage and vaccinate domestic dogs in rural areas as well as stray dogs.
This study was subject to some limitations. First, 7 of 414 human rabies cases have failed to carry out case investigation for missing data rate of 1.69% (7/414). Second, the survey response rate was not 100%, but still above 92.5%. Third, most human rabies cases were clinically diagnosed because no specimens were collected immediately and no laboratory results.
In conclusion, to achieve zero human deaths from rabies, management and vaccination of dogs in rural areas should be prioritized to reach the 70% vaccination target (9), as well as by improving the accessibility and quality of PEP in rural areas from the health departments in Shandong.
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Provincial, prefectural, and county-level CDC staff.
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No conflicts of interest.
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