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Rabies is a zoonoses infectious disease caused by the rabies virus and its mortality rate is nearly 100%. Each year, about 55000 people die of rabies worldwide, which is estimated to cause 1.74 million annual losses for a disability-adjusted lifetime[12]. Rabies is widely distributed throughout the world and China is one of countries that experience the most serious impact from the disease[13]. In 1980s, the epidemic situation of rabies in China reached a peak, in 1981, 7037 cases were reported but since then the number of cases decreased until 1996 when a minimum of 196 cases were recorded[20]. Since this time however, there has been a gradual reemergence of the disease, and cases once again increased on a yearly bases until 2007 when 3300 human rabies cases were recorded. Subsequently, the number of cases has slowly decreased; in 2011 there were 1918 cases, but the epidemic situation remains serious. To identify and understand the possible reasons behind the reduction of cases since 2007 and to endeavor to providing a scientific basis for further controlling the rabies epidemic in China, in this paper we carry out a retrospective epidemiological analysis of the rabies surveillance data of collected in recent years.
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For countrywide reported human rabies cases from 2007 to 2011, there were 3300, 2466, 2213, 2048 and 1918 cases, respectively. Annual reduction rate of reported cases from 2007 to 2011 were respectively 25.27%, 10.26%, 7.46% and 6.35%, and total number of disease cases reduced year by year. Over this five year period, there were a total of 11714 deaths, with a mortality rate of 98.07%, with the possible reason of case reporting not in time.
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Time distribution: monthly cases for each year are shown in Fig. 1. Cases occurred throughout the whole year; the percentages of spring, summer, autumn and winter cases for the whole period were 21.17%, 30.00%, 29.01% and 19.82% respectively. Notably more cases occurred in the spring and summer months (41.11%); in contrast, there were fewest cases in February and March.
Regional distribution and characteristics of the epidemic: Nationally overall, the distribution of cases show no obvious change in the time period considered. In 2007, there were 984 counties and districts reporting an epidemic of rabies. In 2008, 2009, 2010 and 2011, the number of rabies-epidemic counties or districts were 858, 892, 817 and 862 respectively. However, the variation in number of cases for each county and district showed that the epidemic was consistently diffused between counties and districts in the same province and ultimately from high-incidence provinces to low-incidence provinces (Fig. 2). In some low-incidence provinces, the incidence of human rabies rose significantly. For example, the number of counties and districts reporting rabies cases in Shanxi increased from 2 in 2007 to 48 in 2011, and the number of counties and regions reporting rabies cases in Shaanxi increased from 1 in 2007 to 19 in 2011.
From 2007 to 2011, the five provinces with the highest number of rabies cases nationwide were Guangxi (1778 cases), Guangdong (1485 cases), Guizhou (1427 cases), Hunan (1075 cases) and Sichuan (803 cases), and the total cases in these five provinces accounted for 54.99% of all reported cases. In this five year period, with the exception of three provinces (Tibet, Qinghai and Heilongjiang) there were reported cases in every other province. For some of these provinces, there were only isolated cases, indicating that the virus circulation has not yet been established in these regions. These include one case in Gansu in 2009; 1 and 2 cases in Xinjiang in 2008 and 2011 respectively; one case in Jilin in 2007; 2 cases in Liaoning in 2011; and 2 cases in Ningxia in 2011. For other 23 provinces and municipalities the changes are more marked, these are summarized in Fig. 3. The epidemic situation in rabies in Beijing, Tianjin, Shanghai and Inner Mongolia appears to be sporadic, but the number of cases in these regions was significantly less than other provinces or municipalities. For other provinces where rabies epidemic appeared to be well established at the beginning of the study (more than 100 cases recorded in 2007), the number of annual cases gradually decreased over the study period (Hebei, Jiangsu, Jiangxi, Shangdong, Henan, Hunan, Guangxi, Chongqing, Sichuan and Guizhou) although the magnitude of the decrease varied. The most notable reduction occurred in Sichuan with a 79.84% decrease in cases over the five year period. However, for Yunnan, Jiangsu, Shaanxi and Shanxi provinces, the number of cases appears to have increased over this period, particularly for Shaanxi and Shanxi, indicating the virus circulation began to establish itself in these regions over this period. In Shaanxi, before 2009, cases were sporadic but increased to 26 in 2009, 25 of which occurred in Hanzhong city; similarly Weinan city reported 5 cases in 2010 and 29 cases in 2011. For Shanxi province the number of cases rose continuously from 3 cases in 2007 to 88 cases in 2011. For Yunnan and Jiangsu provinces the pattern was less pronounced, but the number of cases has been gradually increasing.
Distribution of Occupations: Most cases from 2007 to 2011 were farmers, students and pre-school children. These three kinds of populations respectively accounted for 68.27% of cases (annual percentage over 5 years were respectively 66.27%, 68.13%, 69.32%, 69.14% and 69.76%), 12.47%(annual percentages 14.82%, 13.26%, 10.57%, 11.67% and 10.38%) and 6.32% (annual percentages 6.27%, 5.96%, 7.37%, 6.20% and 6.00%). Overall, these three populations together accounted for 87.10% of all cases (annual percentages 87.36%, 87.35%, 87.26%, 7.01%, and 86.13%). The percentage of farmer cases increased slowly, while the number of student cases reduced slowly, and the number of pre-school children cases was relatively unchanged over this period.
Gender and age distributions: The ratio of male cases to female cases was 2.32:1. Cases were primarily concentrated to ages 5-15 years and 35-70 years (Fig. 4 and 5). With the exception of the 45-50 year old male group which saw a gradual increase, the 45-50, 80-85, 85-year old female groups, along with the 60-65, 70-75, 80-85, 85-year old male group, remained relatively unstable, and Showed an overall increasing tendency. The number of cases in other age groups gradually decreased from 2007 to 2011. The largest decrease occurred 5-15 years old and 50-55 year old groups for both male and female, which had all previously been high-incidence groups.
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The active surveillance program reported 2346 rabies deaths from 2007 to 2010. Diagnosis of rabies cases complied with the national Diagnostic Criteria for Rabies (WS281-2008)[9], and a summary of PEP of all investigated human rabies cases is shown in Table 1. Over 50% cases were category Ⅲ exposure, the wound treatment rates of received in medical institutions were low, and there was no difference between the various years (χ2 test p > 0.05). For other prophylaxis procedures, there were significant differences between various years (χ2 test p < 0.05); generally, the situations in 2007 and 2009 were better than those in 2008 and 2010. In 4 years, only 66 cases (2.81%) from 2346 rabies deaths completed the PEP rabies deaths, no timely and standard PEP was carried out.
Table 1. Post-exposure prophylaxis of human rabies cases in China, 2007-2010
Incubation period of 72.21% cases was within half a year, and distributions of specific incubation time are shown in Table 2. After the incubation time, most cases presented typical rabies symptoms, such as anxiety, hydrophobia, anemophobia, salivation and dysphasia.
Table 2. Estimated incubation period of rabies cases reported in China, 2007-2010
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The general situation of PEP of people after bitten by dog at surveillance points from 2007 to 2010 is shown in Table 3; the exposure was mainly category Ⅱ or Ⅲ. The rate of wounds treatment in medical institution of Guangxi was lowest and for whole-course vaccination rate of Shandong was lowest. Generally, injection rate of rabies immunoglobulin (RIG) or rabies anti-serum was not high, but on the whole, the rate of people who received PEP, vaccination and injection of RIG or rabies anti-serum for category Ⅲ exposure were significantly higher than those for fatal rabies cases, suggesting that timely and standardization of PEP could greatly reduce incidence risk.
Table 3. Post-exposure prophylaxis for people bitten by dog in clinics of national surveillance sites in China, 2007-2010
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From 2007 to 2010, 88.53% of identified cases were exposure to canines, followed by cats (5.20%); the majority of incidents were bites. Other reported cases included rats, horses, squirrels, pigs, bats, monkeys and raccoons. Canine density and canine immunization rate were estimated in two ways. In the first method information was retrieved from local farming and public security departments (Ecological investigation); in the second method information was collected by performing household surveys at a local level, i.e. one village or town was considered a unit(Household investigation)[5]. From 2007 to 2010, the goal was to collect 60 estimated (15 surveillance points over 4 years), of which 51 were completed; of these, 33 estimates used the public records and 18 were based on household surveys. The results are shown in table 4. It was found that estimates of canine density obtained by the ecological investigation method were consistently less than that obtained by the household surveys, whereas estimates of canine immunization rate was consistently greater when estimated from public records. Due to the limited investigation range, an estimate of these quantities at a national level was not possible. Several years of continuous survey showed that canine density and immunization rate in our investigation were in variable trends: from 2008 to 2010, canine density obtained by the household investigation method reduced year by year, and canine immunization rate was in an overall increasing trend.
Table 4. The surveillance of host animal in monitor point in China, 2007-2010(median)
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Economic situation and medical treatment: Number of rabies cases and distribution were significantly associated with social factors. According to an estimation by the WHO, over 99% of human rabies cases occur in developing countries, and rural areas were more affected than cities. Similarly, overall reduction of epidemic situations in China in recent years was closely related to social economic improvement. From 2007 to 2010, average per capita annual net incomes of towns and rural residents respectively increased by 2041.60 Yuan and 592.87 Yuan (t=9.58, p < 0.01) and average per capita annual medical care expenditures of towns and rural residents respectively increased by 57.56 Yuan and 38.23 Yuan (t=11.50, p < 0.01). It was found that the bearing capacity for disease burden of towns was far higher than that of rural areas and it requires further investigation to determine whether this is directly associated with cost of rabies PEP treatment in rural populations. Annual governmental health expenditure and the accounted ratio increased year by year. Also, rural health facilities were constantly enhanced with a consequent improvement in health care. These findings are summarized in Table 5.
Table 5. Economic and health care changes in China, 2007-2010
High-incidence rabies regions such as Guangdong and Hunan have included rabies PEP expenditures into the new rural cooperative medical reimbursement coverage, including vaccine cost and the whole PEP treatment. This has greatly improved the PEP situations of peasants and thus increased treatment rate of PEP. The state is trying to further expand the scope of medical insurance for rabies PEP treatment to cover the entire rabies epidemic region.
Development of rabies vaccine for human use in China: The quality of rabies vaccine for human use has been increasing on a yearly basis. In 2001, it was forbidden to use concentrated rabies vaccines in China, but it was permitted to use refined purified vaccine .[8]From August 1, 2005, a trial rabies vaccine was approved for human use with the goal of supervising and improving rabies vaccine quality in China. This is reflected in a comparison of relative efficacy of the treatments available in 2005 and 2010.The protein content in the 2010 vaccine was reduced from 120 µg/dose to 80 µg/dose, DNA residual content was no more than 100 pg/dose, bacterial endotoxin was reduced to 1/4 of the 2005 standard content and preservative thiomersal content reduced from 100 µg/mL to 50 µg/mL[6]. All of these improvements have helped to reduce side effects of vaccination and increase patient tolerance.