Insect Vectors and Rodents Arriving in China Aboard International by xdu18397



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;
                                                                       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

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
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