REVIEW ARTICLE Insect Vectors and Rodents Arriving in China Aboard International Transport Mingchang Song, Baoling Wang, Jianzhong Liu, and Norman Gratz China has 360 seaports, airports and authorized land Rodents Found on Vessels Arriving from Abroad crossing points along its frontiers. Inspections have shown that the country is facing a serious problem with the Rodent infestations on vessels may result in the introduction of arthropod vectors and rodent reservoirs introduction of rodent-borne diseases into the country; of disease, as or even more serious than that of other species of rodents not previously found in the country countries. The surveys show that mosquitoes and other may be introduced and become established. The World insects are frequently imported aboard aircraft, whereas Health Organization International Health Regulations surveys of ships arriving in Chinese seaports show that require the control of rodents on vessels and in seaports, as much as a quarter of them have rodent infestations. and also require periodic inspections to determine and Surveys conducted in ports of the country show that the certify that ships engaged in international travel or trade proportions of incoming vessels carrying mosquitoes, flies are rodent-free.The extent of rodent infestations on vessels and cockroaches were 20%, 15%, and 50%, respectively. arriving in China has been found to be serious. An This article reviews the surveys and reports on introduced inspection by the Qingdao port CIQ on 9 September arthropods and rodents at airports and seaports and the 1988 found 266 rats on a single arriving ship. From magnitude of the problem. January 1990 to December 1998, the CIQ carried out a survey to determine the proportion of ships arriving at Surveillance of Introduced Vectors and Rodents Shanwei seaports infested with rodents; 270 of 1093 in China incoming ships (24.7%) were infested. Inasmuch as International Health Regulations require that vessels are The Government of China Import and Export periodically inspected and de-ratted if necessary, the Inspection and Quarantine Department Bureau (CIQ) percentage of rodent-infested vessels arriving at Chinese has the responsibility for both the surveillance of infectious seaports is very high. diseases and arthropod vectors and rodent reservoirs of disease in transport arriving from outside the country, Rodents Found on Other Incoming Transport and for the organization of control activities in seaports and airports. The data below are taken from surveys Aircraft, trains and cargo containers arriving in conducted by CIQ staff at international ports and airports. China have also been found to be rodent infested. Four aircraft, two trains and one container have been found with rodent infestations aboard them. The introduced rodent species included Rattus norvegicus, R. flavipectus, R. rattus alexandrinus, Mus musculus and Cricetulus triton. The four aircraft carrying rodents originated from Saudi Mingchang Song, MD, Baoling Wang, MD, and Jianzhong Arabia, Japan, Russia and Hong Kong (Table 1). Liu, MD: Department of Health, China Inspection and Quarantine, Beijing 100020, China; Norman Gratz, DSc: The presence of rodents aboard aircraft risks their 4 ch du Ruisseau, 1291 Commugny, Switzerland. introduction into the country but also poses a very serious risk to the safety of the aircraft and passengers; rodents The authors had no financial or other conflicts of interest to may gnaw at control cables, with possible disastrous results; disclose. generally, aircraft found with rodent infestation are Correspondence: Norman Gratz, DSc, 4 ch du Ruisseau, immediately grounded for inspection and control. Aircraft 1291 Commugny, Switzerland. in other parts of the world have been occasionally infested J Travel Med 2003; 10:241–244. by rodents but rarely reported in the scientific press; such 241 242 J o u r n a l o f Tr a v e l M e d i c i n e , Vo l u m e 1 0 , N u m b e r 4 Table 1 Rodent Infestations Found on Incoming Transport Date Port Species and Number From Conveyance 28 October 1984 Shanghai Rattus flavipectus 1 Japan Aircraft 1 January 1985 Shenyang Cricetulus triton 5 Japan Container ship R. norvegicus 23 January 1989 Erlian R. norvegicus 3 Mongolia Train 6 February 1990 Shanghai R. norvegicus 1 Russia Aircraft 6 December 1990 Beijing R. rattus 1 Saudi Arabia Aircraft 15 November 1994 Beijing Mus musculus 10 Russia Train 13 January 1995 Guangzhou R. norvegicus 1 Hong Kong Aircraft infestations are reported when passengers are present and with mosquitoes in Guangzhou port.5 Other instances may be the subject of newspaper reports. Thus these of mosquitoes aboard incoming transport are listed in findings are valuable in showing that rodents are more Table 2. commonly found aboard aircraft than generally known. Other countries in the region have also found To prevent such infestations occurring aboard transport, mosquitoes aboard arriving aircraft; in Japan, a survey it is essential that airports and seaports be kept rodent- showed that, of 928 aircraft arriving at Narita airport in free to reduce the possibility of their access to aircraft and Tokyo, live insects were found in no less than 400 vessels. Vessels should be regularly inspected for rodent (43.1%).6 A survey at Changi International airport in infestations, especially if they are coming from rodent- Singapore found that 57 (17.3%) of 330 incoming aircraft infested ports. harbored mosquitoes and other insects on board, and many of these were vector species.7 Mosquitoes Found Aboard Aircraft and “Airport malaria” is caused by the transmission of Vessels from Abroad malaria by infected Anopheles malaria vectors that have entered aircraft before their departure from endemic areas A recent review1 showed that mosquitoes are and which, after arrival, escape and transmit malaria in frequently introduced into countries aboard aircraft; a the country in which they have arrived, usually on the similar problem occurs in China. In 1993, a survey of grounds of the airport of arrival or in its vicinity.1 Diag- arriving aircraft for the presence of mosquitoes, or other nosis of cases of airport malaria is often delayed, as malaria insects, was carried out in Dalian airport by the CIQ; is rarely suspected as the cause of illness, especially if the 96 of 487 arriving aircraft were found to be carrying patient has not recently traveled to endemic countries. mosquitoes and/or flies (19.71%).2 In an earlier CIQ Cases of airport malaria have occurred in the Pacific survey of arriving aircraft in Guilin airport in 1987, 11 region in Australia8 and Japan.9 of 130 incoming aircraft inspected carried mosquitoes (8.5%).3 Cockroaches Found Aboard In 1990, the CIQ investigated 208 incoming cargo Incoming Transport and baggage containers arriving in Beijing from America, Japan and Iraq. The results showed that 53 of the con- Cockroaches are mechanical vectors of diarrheal tainers carried mosquitoes, some of which were potential diseases, as well as being unpleasant pests. Generally, both disease vectors; Culex pipiens pallens and Culex pipiens airline and shipping services contract with commercial quinquefasciatus were the most common species found. pest control operators to control or prevent infestations In 1996, the CIQ found that one incoming con- aboard aircraft or vessels. These ubiquitous insects are tainer in Shanghai seaport contained live Culex pipiens readily transported from one area to another unless control quinquefasciatus.4 In 1990, two containers were found measures are regularly applied. Table 2 Mosquitoes Found on Incoming Transport Date Port Species Conveyance 1 March 1987 Shenzen Culex pipiens pallens Truck Cx. pipiens fuscocephala Cx. nigropunctatus 24 February 1988 Guangzhou Cx pipiens pallens Aircraft 30 October 1989 Shanghai Cx. pipiens quinquefasciatus Aircraft Song et al., Insect vectors and rodents arriving in China on international transport 243 Ships are frequently heavily infested by cockroaches. was opened. The fleas were Ctenocephalides felis, a species In 1993, the CIQ surveyed 957 ships arriving in Dalian not previously found in the Nanjing area; the species is seaport; 511 of the ships (53.4%) carried cockroaches; the a vector of tapeworms and murine typhus. Other species majority of the infested vessels came from elsewhere in Asia found aboard arriving transport are listed in Table 5. and the Pacific. On 18 July 1989, 17 arriving aircraft at Guangzhou Baiyun Airport had to be disinsected by the Possible Consequences of the Introduction of Exotic Guangzhou Inspection and Quarantine Service because Vectors and Rodents cockroach infestations were found on them;13,262 cock- roaches were found in one aircraft.Other reports of arriving The introduction of potential vectors of disease may aircraft with cockroach infestations are listed in Table 3. result in the establishment of diseases not previously endemic in the country. The introduction by aircraft of Flies (Diptera) Found on Transport from Abroad several exotic Anopheles species into Guam resulted in malaria outbreaks in 1966 and 1969.10 The introduction On 8 April 1993, large numbers of flies were found of Aedes vigilax into Fiji in 1975 was related to an epidemic in three containers imported from Japan to Xiamen, of Ross River virus in 1979.11 Vector-borne infections China. After disinsection, 25.5 kg of various fly species are increasingly spreading from one country to another, were collected from the containers. Flies have also been usually through the medium of infected passengers. found in containers arriving in Beijing and Shenzhen However, spread can also occur by the introduction of ports (Table 4). infected reservoirs or vectors. The manner in which West Other Species of Vectors or Pests on Nile virus was introduced into the United States remains Arriving Transport uncertain, although its rapid spread is via indigenous mosquito species.12 In the late 1930s, the importation of In October 1993, living fleas were found in a the efficient African malaria vector, Anopheles gambiae, into container imported from Germany to Nanjing when it Brazil, apparently aboard a fast French naval vessel arriving from Dakar, West Africa, resulted in major outbreaks of Table 3 Blattella germanica Found Aboard Incoming malaria in the regions of Brazil that the vector had invaded Transport and the loss of many lives until the invading vector was eradicated. The pandemic of plague in China in the late Date Port Number Conveyance 19th century spread along shipping routes via rats on the 1 March 1992 Dongguan 100+ Ship vessels, and arrived in the United States in 1899. Although 18 July 1989 Guangzhou 13,262 Aircraft modern sanitation makes it unlikely that this will again 1 October 1988 Haikou 512 Ship 24 October 1987 Beijing 43 Aircraft occur, the large number of rats aboard vessels arriving in 28 October 1987 Beijing 32 Aircraft China gives cause for concern. 1 January 1986 Zhangjiagang 132 Ship 1 May 1985 Quanzhou 5,963 Ship Table 4 Diptera Found Aboard Arriving Transport Date Port Species Number From Conveyance 10 March 1997 Beijing Musca domestica 100+ Taiwan Container/Ship 16 October 1996 Beijing Muscina angustifrons 100+ South Africa Container/Aircraft 8 April 1993 Xiamen Calliphora lata 25.5 kg Japan Container/Ship Fucellia apicalis 1 March 1987 Shenzhen M. domestica 100+ Hong Kong Container/Ship Fannia canicularis Table 5 Other Species Found Aboard Incoming Vessels Date Port Species Number From Conveyance 24 August 1998 Shanghai Coptotermes formosanus N/A Taiwan Ship 2 October 1993 Nanjing Ctenocephalides felis N/A Germany Ship 1 March 1992 Dongguan Ants, Chilopoda sp. 1000+ Malaysia Ship 20 July 1990 Qingdao Dead dog 1 United States Ship 1 May 1987 Wuhan Parasitic bees 100+ United States Ship 1 June 1990 Shanghai Dead dog 1 United States Ship N/A=not available (too many to be counted). 244 J o u r n a l o f Tr a v e l M e d i c i n e , Vo l u m e 1 0 , N u m b e r 4 Health Measures Against Introduced different from the rat populations in the harbor. Of the Vectors in China rats captured aboard the ships and in the harbor, 12.8% of the R. norvegicus and 4.7% of the R. rattus were sero- Legislation positive for hantavirus.14 On 11 May 1979, China informed the WHO that The threat of introduction of diseases, vectors and China would adhere to the International Health Regu- rodents from one country to another would be reduced lations. In 1986, China enacted the Frontier Health if all seaports and airports were kept free of mosquito Quarantine Law of P.R. China. In 1989, Specific Rules breeding and rodent infestations, as required by the For Enforcing the Frontier Health Quarantine Law of International Health Regulations. The threat of imported P.R. China were issued. Subsequently, China issued a series diseases, vectors and rodents requires constant surveillance; of regulations specifically directed against the introduction China, therefore, maintains a large number of travel of vectors. medicine clinics as part of the State Administration for Entry-Exit Inspection and Quarantine; these clinics main- Health Quarantine Organization and Operations tain epidemiologic information on infectious diseases of China set up its first frontier heath quarantine service international significance; their entomologic laboratories in 1873. By 1949, there were 17 frontier heath quarantine identify the insects and rodents found on incoming services in the country. In 1988, the General Office of transport. China Health Quarantine was established, and the number of health quarantine stations was increased to 42 in that References year. In 1998, the State Administration for Entry-Exit Inspection and Quarantine of P.R. China was established, 1. Gratz NG, Steffen R, Cocksedge W. Why aircraft disinsection? and there are now 585 Frontier Inspection and Quarantine Bull World Health Organ 2000; 78:995–1004. Services.13 2. Xie JB, et al. An investigation on entry conveyance with vectors. J China Frontier Health Quarantine 1993; 6:353. Vector Control Laboratories 3. Jiang NY, et al. Entry aircraft with mosquitoes in Guilin To support the vector control program in the Airport. J China Frontier Heath Quarantine 1991; 1:29. quarantine stations, five Vector Control Laboratories have 4. Chen QG, et al. A survey on entry container with vectors in been established in Beijing,Shanghai,Nanjing,Guangzhou, Shanghai Port.J China Frontier Heath Quarantine 1996;3:276. and Shenzhen. In addition, a local vector control labora- 5. Fen SC, et al. Entry container sanitary situation in Guangzhou Port. J China Frontier Heath Quarantine 1991; 3:144. tory has been set up in each Frontier Inspection and 6. Takahashi S. Survey on accidental introductions of insects Quarantine Station; these are responsible for vector and entering Japan via aircraft. In: Laird M, ed. Commerce and rodent control in the ports and airports. the spread of pests and disease vectors. New York: Praeger, 1984:65–79. Information services 7. Goh KT, Ng SK, Kumarapathy S. Disease-bearing insects The Beijing Epidemic Situation Center was brought in by international aircraft into Singapore. Southeast established 20 years ago. The Center collects and publishes Asian J Trop Med Public Health 1985; 16:49–53. epidemiologic information. Details on the State Admini- 8. Infectious Agents Surveillance Report. Malaria in Japan. IASR stration for Entry-Exit Inspection and Quarantine are 2000; 18:110. available on an Epidemic Situation homepage (http:// 9. Jenkin GA, Ritchie SA, Hanna JN, Brown GV. Airport malaria www.aqsiq.gov.cn) . in Cairns. Med J Aust 1995; 166:307–308. 10. Nowell WT. Vector introduction and malaria infection on Discussion Guam. J Am Mosquito Control Assoc 1987; 3:259–265. 11. Self LS. Vector introductions associated with disease outbreaks Insect vectors, particularly mosquitoes, and rodent in the western Pacific Region. Dengue Newslett 1984; 10: reservoirs of disease are frequently found on incoming 50–51. transport arriving in China, creating a risk that vector and 12. Mafin AA, Gubler DJ. West Nile encephalitis: an emerging rodent reservoir species not previously found in China disease in the United States. Clin Infect Dis 2001; 33:1713– 1719. may be introduced and become established. It is likely 13. Yang S.One hundred twenty years of China’s health quarantine that insect vectors and rodents are also arriving at ports service. Zhong hua Yi Shi Za Zhi 1995; 25:77–82. and airports where no surveys have been carried out. 14. Suzuki S, Shinagawa M, Tamura T, Okuno Y, Hotta S, Lee Infectious agents not previously found in the country can HW. Seroepidemiological studies of Hantaan related virus in also be introduced if mosquitoes and rodents are infected. wild rodents captured at harbour area and in vessels of Port In nearby Japan, a survey In Port Shimizu captured 47 Shimizu, Japan, 1981–1986. In: Thongcharoen P, Kurstak E, rats aboard vessels arriving from Korea and Taiwan. eds. Virus diseases in Asia. Bangkok: Mahidol University 1988: Genetic studies of the ship rats showed that they were 238–242.
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