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LETTERS

Human Rabies in The compiled data also showed 1960s, coinciding with pet reduction substantially more rabies cases in the policy. The second major epidemic China summer and autumn than in the spring peaked in the late 1970s and early To the Editor: Rabies has occurred and winter. Similar seasonality was 1980s, when economic reforms were in China for >2,000 years and was first reported in animals (2), indicating the initiated in China and the dog popula- described in ≈556 BC (1). Since 1950, pattern of transmission from animals tion increased dramatically. Popu- human rabies has been a class II noti- to humans. Rabies patients range in lation immunity may also play a role fiable disease in China, and the annual age from infancy to >65 years of age. in these cyclic epidemics. However, number and distribution of human The ratio of male to female victims is neither the dramatic decline of rabies rabies cases have been archived. We 68 to 32. Although human rabies has cases in the early part of 1990s nor examined the archived data from 1950 been reported in almost all provinces, the initiation of the third epidemic to 2004 and analyzed epidemiologic 15 provinces have had >1,000 cumu- around the turn of the millennium characteristics. lative cases each. These provinces are could be explained simply by dog During the 55-year period, Hunan, Guangdong, Sichuan, population dynamics. Other factors 108,412 human rabies cases were , , Hubei, , may include untimely and inappropri- recorded in China. The Figure shows , , Anhui, Jiangsu, ate postexposure treatment (3,4) and the number of annual cases from 1950 Hebei, Fujian, Yunnan, and Liaoning. the existence of healthy carrier dogs to 2004; 3 major epidemics of human These 15 provinces account for >93% (5–7). Wounds of 118 of 178 patients rabies in China are apparent. In the of the total cases. Four provinces were not treated; 60 of the patients early 1950s, only a few cases (Hunan, Guangdong, Sichuan, and washed the wounds with soap and occurred; the first peak occurred from Guangxi) have had >7,000 cumulative water. A total of 129 (72%) patients 1956 to 1957 with ≈2,000 cases each cases each. did not receive vaccine. Of the year. Then the number of cases Most of the human patients were remaining 49 (28%) patients, 35 declined during subsequent years and infected with rabies by dog bites. The received vaccination in a timely man- was relatively constant throughout the number of dogs has increased gradu- ner. Two of the 178 patients received 1960s. By 1969, the number of cases ally in China since the late 1970s. antirabies serum intramuscularly. ≈ increased again to ≈2,000. This Now 70% of households in Guangxi, Among the 49 patients who received ascending phase continued through- Guizhou, and Jiangsu, and Hunan, postexposure vaccination, 30 did not out the 1970s and 1980s. The second where the most cases were recorded in complete the immunization require- epidemic peaked in the early 1980s. recent years, have >1 dog (data not ments. Healthy carriers have been In 1981, 7,037 cases were recorded, shown). However, the rate of dog vac- detected, and rabies virus antigen was ≈ the largest number of cases in a single cination remains 3%. found in 25 (10%) of 248 brain spec- year during the 55-year period. The rabies epidemics in China imens from healthy dogs collected During the 1980s, 55,367 cases were since 1950 may be partially explained from Guangxi, Guizhou, and Jiangsu reported (>5,000 cases annually), rep- by dog population dynamics. The first (data not shown) in 1 study. Further resenting >50% of the 108,412 cases major epidemic subsided at the end of investigation is needed to confirm seen during the entire period. In the the 1950s and the beginning of the these findings. early 1990s, the number of In summary, rabies remains human cases decreased a public health problem in dramatically from 3,520 in China. Strategies to control and 1990 to 159 in 1996. prevent human rabies include However, this downward public education and aware- trend reversed its course in ness about rabies, pet vaccina- 1998, and annual cases tion programs, elimination of have increased gradually stray animals, and enhanced since then. In 2004, a total postexposure management. In of 2,651 cases were report- addition, the large number of ed, an increase of >16 fold rabies cases should encourage when compared with the rabies prophylaxis for foreign numbers in 1996. This travelers before they visit third rabies epidemic China, particularly those who apparently has not yet might travel to rural areas. Figure. Annual rabies cases reported in China from 1950 to 2004 peaked.

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005 1983 LETTERS

Yong-Zhen Zhang,* Cheng-Long Resistant fur, cephalothin, nalidixic acid, and Xiong,* Dong- Xiao,* tetracycline and with reduced suscep- Ren-Jie Jiang,† -Xiao Wang,‡ Salmonella tibility to ciprofloxacin (MICs >0.125 Ling-Zhu Zhang,§ and Zhen F. Fu¶ Virchow in Quail µg/mL) (3). Polymerase chain reac- *Chinese Center for Disease Control and Products tion detection and sequencing (4) Prevention, Beijing, China; †Yancheng showed that the β-lactam resistance Municipal Center for Disease Control and To the Editor: Salmonella spp. was mediated by blaCTX-M-9. Pulsed- Prevention, Yanchen, China; ‡Guizhou resistant to multiple antimicrobial Center for Disease Control and Prevention, field gel electrophoresis was per- Guiyang, China; §Guangxi Center for agents have emerged worldwide in formed by using XbaI and BlnI as Disease Control and Prevention, Nanning, recent years, but clinical relevance restriction enzymes according to the China; and ¶University of Georgia, Athens, varies with the agent to which resist- PulseNet protocol (5), and all 3 iso- Georgia, USA ance evolves. Fluoroquinolones are lates had the same profile. often the drug of choice to treat gas- On October 23, the importer was References trointestinal infections in humans, and informed of the laboratory’s findings 1. Wang XJ, Huang JT. Epidemiology. In: Yu resistance to this class of antimicro- and the increased risk associated with YX, editor. Rabies and rabies vaccine. bial agents is associated with salmonella isolates simultaneously Beijing: Chinese Medicine Technology increased illness and death (1). resistant to quinolones and Press; 2001. p. 127–44. 2. Gylys L, Chomel BB, Gardner IA. Resistance to fluoroquinolones has cephalosporins. Based on this infor- Epidemiological surveillance of rabies in emerged worldwide during the last mation, the importer withdrew the Lithuania from 1986 to 1996. Rev Sci Tech. decade. Salmonella isolates resistant product from the supermarkets on 1998;17:691–8. to oxyiminocephalosporins because October 24. Recently, S. enterica 3. Centers for Disease Control and β Prevention. Human rabies prevention— they produce extended-spectrum - Virchow with blaCTX-M-9 has also been United States, 1999; recommendations of lactamases (ESBLs) have emerged reported in poultry, poultry products, the Advisory Committee on Immunization worldwide since 1992. This emer- and humans in France (6), as well as Practice (ACIP). MMWR Recomm Rep. gence has caused concern since humans in Spain (7) and the United 1999;48(RR-1):1–21. 4. Chhabra M, Ichhpujani RL, Tewari KN, Lal cephalosporins are drugs of choice to Kingdom (8). The isolates from S. Human rabies in Delhi. Indian J Pediatr. treat salmonellosis in children, to France were also resistant to nalidixic 2004;71:217–20. whom fluoroquinolones must not be acid; the isolates we have obtained 5. Hu JY, Xu TQ, Wu ZM, Y, Zhao LL, administered because of toxicity from fresh quails imported from Shen RH, et al. A study on the epidemiolog- ical characteristics and the preventive issues. In Denmark, the first ESBL- France are possibly related to these measures of rabies in [article in producing isolate of animal origin isolates. Chinese]. Chin J Epidemiol. 2001;22: from a Salmonella enterica serovar The global food-products trade is 11–13. Heidelberg isolated from a boar expected to increase in the future. 6. Du F, Huang MT, Liang FP, Luo HM, Wen JH, Chen DR, et al. Investigation on rabies imported from Canada in 2003 was Thus, attempts to improve food safety virus in dogs in Guangdong [article in reported (2), but such isolates have must emphasize detection of antimi- Chinese]. Chin J Zoonoses. 1992;8:39–41. not previously been reported in food crobial drug–resistant bacteria in 7. Fekadu M, Shaddock JH, Chandler FW, products. imported food products. Furthermore, Baer GM. Rabies virus in the tonsils of a carrier dog. Arch Virol. 1983;78:37–47. On October 15, 2003, the Danish international agreements that limit Institute for Veterinary Research, the contamination with drug-resistant Address for correspondence: Yong-Zhen national reference laboratory, bacteria and resistance genes at the Zhang, Institute for Infectious Disease Control received 3 Salmonella isolates found primary production site are necessary and Prevention, Chinese CDC, Liuzi 5, in quails imported from France. to ensure consumer safety (9). Changping 102206, Beijing, 102206, China; Salmonella isolates found at any International agreements must be fax: 86-10-61739457; email: yongzhenzhang@ importer’s laboratory in Denmark are based on antimicrobial-resistance data sohu.com submitted to the reference laboratory and early reports of emerging prob- for further analyses. The quails were lems. Recently, the World Health in the importer’s storage room at the Organization (WHO) launched the time of sampling; sampling was per- Global Salm Surv program (10) to formed routinely by the importer’s isolate and identify antimicrobial own laboratory. At the reference labo- resistance to Salmonella globally. ratory, the isolates were serotyped as Many national and international S. enterica serovar Virchow and rules, as well as marketing and con- found resistant to ampicillin, ceftio- sumer factors, regulate the interna-

1984 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 12, December 2005