POPULATION AND COMMUNITY ECOLOGY Status of Urban Bed Bug Infestations in Southern China: An Analysis of Pest Control Service Records in Shenzhen in 2012 and Dongguan in 2013 LEI WANG,1 XUQUAN CAI,2 AND YIJUAN XU1,3 J. Med. Entomol. 52(1): 76–80 (2015); DOI: 10.1093/jme/tju015 ABSTRACT The recent resurgence of bed bugs (Cimex spp.) in many developed countries has drawn increasing attention worldwide. The status of urban bed bug infestations were investigated in Shenzhen and Dongguan, two major cities in southern Guangdong Province of southern China, based on pest control service records from two different companies (one during 2012 and another during 2013). The results showed that Shenzhen and Dongguan have a severe problem with bed bug infestations: the control of bed bugs is a constant concern, except during the winter. In Shenzhen, a similar number of premises were treated for bed bugs in central business districts and suburban districts. However, in Dongguan, more premises were treated for bed bugs in suburban districts than in central business districts. The treatment rate for worker sleeping quarters, apartments, hotel, and private houses in Shenzhen was 53.8, 43.0, 1.9, and 1.3%, respectively. The percentage of treated rooms was 56.1% for worker sleeping quarters and 91.1% for apartments. In Dongguan, the treatment rate for worker sleeping quarters, apartments, hotel, and private houses was 90.0, 10.0, 0.0, and 0.0%, respectively. KEY WORDS Cimex spp., infestation, treatment record, seasonality Introduction Bed bugs are significant pests of humans with a history that dates back to ancient times (Romero et al. 2007). These insects include the bed bug, Cimex lectularius L., and the tropical bed bug, Cimex hemipterus F. (Usinger 1966). They are mainly active at night and feed on human blood. Biting by bed bugs can cause red itchy welts (Kolb et al. 2009) and severe iron deficiency anemia due to blood loss (Pritchard and Hwang 2009). Fortunately, there is no clear evidence to date that bed bugs can transmit disease-causing organisms (Delaunay et al. 2011). Bed bugs can also adversely affect mental health; bed bug infestations often are associated with sleep disturbance and symptoms of anxiety among humans (Susser et al. 2012). Bed bugs nearly disappeared in developed countries during the 1940s and 1950s principally because of the use of residual insecticides (Romero et al. 2007), but these pests made a comeback worldwide in the late 1990s (Doggett et al. 2004, Boase 2008). Bed bugs were found to have infested 30% of the homeless shelters in Toronto, ON, Canada, in 2003 (Hwang et al. 2005). The resurgence of bed bugs resulted in estimated economic losses of AUS$100 million in Australia (Doggett and Russell 2008). Insecticide resistance is 1 Department of Entomology, South China Agricultural University, 483 Wushan Rd., Guangzhou, 510642 China. Shenzhen Yili Pest Control Co. Ltd, 1279 Hongling Zhonglu, Shenzhen, 518022, China. 3 Corresponding author, e-mail: [email protected]. 2 the key trigger behind the resurgence of bed bugs, and the resistant bed bugs spread around the world through the increasing mobility of the human population and poor pest management practices (Davies 2012, Doggett et al. 2012). Knowledge on the ecology and biology of bed bugs is essential to devise ways to effectively control the species (Doggett et al. 2004, Reinhardt and Siva-Jothy 2007, Weeks et al. 2011, Khan and Rahman 2012, Saenz et al. 2012). There have been numerous reviews on pesticide efficacy and new management technologies to more effectively control bed bug infestations (Moore and Miller 2009, How and Lee 2011, Lehnert et al. 2011), and the development of industry standards that promote sound bed bug management practices for bed bug eradication (Madge 2012, Doggett 2013, the U.S. National Pest Management Association [NPMA] BMP Bed Bugs Best Management Practices 2011). The transcriptomics of C. lectularius have been studied to provide clues in identifying genes involved in pesticide resistance (Bai et al. 2011, Mamidala et al. 2012). Bed bugs became uncommon in Mainland China during the 1950s, and they currently are not a significant concern throughout China (Wang and Wen 2011). However, a survey in 2012 indicated that bed bugs had undergone a potential resurgence in China with bed bug infestations becoming common in the Pearl River Delta of southern China (Wang et al. 2013). A better understanding of the magnitude of the resurgence should be the first step to combat bed bugs (Doggett and Russell 2008). Compared with other countries, scientific reports relating to bed bugs are lacking in China. C The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. V All rights reserved. For Permissions, please email: [email protected] January 2015 WANG ET AL: STATUS OF URBAN BED BUG INFESTATIONS IN SOUTHERN CHINA Hunan Jiangxi 77 Fujian Guangxi Dongguan Guangzhou Macau Shenzhen Hongkong Guangdong province map Fig. 1. Geographic locations of Shenzhen and Dongguan. Shenzhen and Dongguan are two large cities of Guangdong Province in southern China. We surveyed bed bug treatment data from a pest control company in Shenzhen and another in Dongguan for 2012 and 2013, respectively. Shenzhen and Dongguan are two adjacent industrial cities in the Pearl River Delta, and their population is largely comprised of migrant workers from villages or small towns throughout China. The data were analyzed to document the extent of bed bug infestations in southern China. Materials and Methods Pest Control Service Records. Shenzhen and Dongguan are two large cities of Guangdong Province in southern China, geographic locations of the cities are shown in Fig. 1. There are 1,000 PCO companies in each of these two cities. According to our random preliminary survey of 11 PCO companies in Shenzhen and Dongguan, 35% of pest treatment services in these POC companies involved bed bug. The data used for analysis in this study were obtained from the Shenzhen Yili Pest Control Co. Ltd. (a medium-sized PCO company in Shenzhen) and Dongguan Xinxiwang Pest Control Co. Ltd. (one of the largest PCO companies in Dongguan). The data detailed information on the number of bed bug treatments, including the treatment date, structure type, and the number of infested rooms. Treated premises were categorized as 1) worker sleeping quarters (residences provided by industrialist for migrant workers; they consisted of a series of single rooms); 2) apartments (residences rented by tenants, and apartments that have more than one room and that only consisted of a bedroom and a living room); 3) hotels (hotels and motels); and 4) private houses (privately owned apartments or houses). Both pest control companies identified the bed bug to the genus Cimex in every treatment, but they did not collect and preserve the specimens in every bed bug incidences. Deng and Meng (1953) indicated C. hemipterus was the dominant species in Guangdong Province based on examined specimens. Because bed bug specimens were not available from every bed bug treatment, we did not know whether or not both C. lectularius and C. hemipterus were involved in these treatments, although all the specimens we checked are C. hemipterus. Thus, we use the genus Cimex in this article. Results In total, 373 sites were treated for pests in Shenzhen by Yili Pest Control Company in 2012, and 158 of these involved bed bugs. Of the 893 total sites treated for pests in Dongguan by Xinxiwang Pest Control Company in 2013, 261 sites involved bed bugs. In Shenzhen in 2012, no bed bug treatments were performed in January and February, with two treatments performed in March (Fig. 2A). The number of premises that needed bed bug control greatly increased thereafter and remained at a high level from June to October, and 78 JOURNAL OF MEDICAL ENTOMOLOGY Fig. 2. Vol. 52, no. 1 Number of bed bug treatments per month: (A) in Shenzhen in 2012 and (B) in Dongguan in 2013. then decreased from November to December. The largest number of treated premises (28) was in August. In Dongguan, in 2013, the number of premises that needed bed bug control showed a similar trend (Fig. 2B). No bed bug treatments were performed in January and only five premises were treated in February. Thereafter, the number of treated premises greatly increased, peaking in September. Treatments subsequently decreased and only five premises were treated for bed bugs in December. In Shenzhen, a similar number of premises were treated for bed bugs in central business districts (70 premises) and suburban districts (88 premises). However, in Dongguan, more premises were treated for bed bugs in suburban districts (219 premises) than in central business districts (42 premises). In Shenzhen, bed bug treatments were conducted in four types of residential structures, including worker sleeping quarters (53.8%), apartments (43.0%), hotels (1.9%), and private houses (1.3%). In contrast, in Dongguan, no bed bug treatments were conducted in hotels and private homes; instead, worker sleeping quarters accounted for most of the treatments (90.0%) and apartments were a minor component (10%). In Shenzhen, 91.1% of all rooms in those apartments treated were infested, and the room infestation rate in those January 2015 WANG ET AL: STATUS OF URBAN BED BUG INFESTATIONS IN SOUTHERN CHINA worker quarters treated was 56.1%. Similarly, in Dongguan, 83.7% of all rooms in those apartments treated were infested; 61.2% of all rooms in treated worker quarters were infested. Discussion This investigation indicates that bed bugs are a serious problem in Shenzhen and Dongguan, evidenced by two pest control companies reporting that 42.4 and 29.2% of their pest cases involved bed bugs in these two industrial cities, respectively. Bed bug treatments were conducted year-round, but were minimal in winter months. Bed bug treatment rates were similar between central business districts and suburban districts in Shenzhen, but more treatments were conducted in suburban districts than central business districts in Dongguan. Apartments and worker sleeping quarters had higher treatment rates than hotels and private homes. There was no difference in the number of bed bug treatments between worker sleeping quarters and apartments in Shenzhen. However, in Dongguan, more treatments were conducted in apartments than in worker sleeping quarters. In 2011, the population of Shenzhen was 10.46 million with a transient population comprising 74% (7.78 million; Statistical Communique on the 2011 National Economic and Social Development of the city of Shenzhen, Shenzhen Municipal Bureau of Statistics). In 2012, in Dongguan, the population was 8.29 million, with a transient population comprising 78% (6.42 million; Statistical Communique on the 2011 National Economic and Social Development of the city of Dongguan, Dongguan Municipal Bureau of Statistics). Approximately 9.72 million people left Shenzhen for the spring festival holiday from 8 January to 16 February 2012 (Shenzhen Evening Newspaper, 29 December 2011); in Dongguan, approximately 7.62 million people left for the spring festival holiday from 26 January to 26 March 2013 (Dongguan Daily Digital Newspaper, 9 March 2013). Most of these holiday travelers are migrant workers. Our survey showed that worker sleeping quarters and apartments were the two most common structures treated for bed bugs, and most residents of apartments and worker sleeping quarters are migrant workers. Thus, we speculate that migration of people might be related to the decline in the number of bed bug treatments during the winter in Shenzhen and Dongguan. Mabud et al. (2014) also mentioned that the yearly nadir in bed bug reports in December may occur because of increased travel during the holidays or because the Department of Public Health’s Vector Control Service is briefly closed during the holiday season. Private houses, apartments, hotels, and worker sleeping quarters in southern China are the most common places infested by bed bugs (Wang and Wen 2011). Similar phenomena also plague Toronto, ON, Canada (Hwang et al. 2005), Australia (Doggett and Russell 2008), and the United States (Potter et al. 2008). Notably, however, only 3.2 and 0.0% of bed bug treatment sites were private houses and hotels in Shenzhen and 79 Dongguan, respectively, whereas treatment rates reached 70.0% for private houses in single-family dwellings in Toronto, ON, Canada (Hwang et al. 2005). Possibly, prompt detection and treatment in southern China may have contributed to the observed phenomenon. Nevertheless, treatment rates in Shenzhen apartments and worker sleeping quarters were 43.0 and 53.8%, respectively. In Dongguan, apartments and worker sleeping quarters, the treatment rates were 10.0 and 90.0%, respectively. Increased urbanization and industrialization has produced a large transient population in China, which may facilitate the spread of bed bugs. Apartment tenants may conceal bed bug infestation information for fear of financial penalties or eviction (Moore and Miller 2009). Industrialists are often not willing to pay additional costs for pest control. These reasons may have contributed to high infestation rates in apartments and worker sleeping quarters in Shenzhen and Dongguan. This study suggests that the severe bed bug infestations in Shenzhen and Dongguan primarily afflict migrant workers from villages or small towns throughout China. Fortunately, bed bugs currently are not a significant concern in other places in China (Wang and Wen 2011). Based on our data, bed bug treatments in migrant worker sleeping quarters is very high; bed bugs are likely to spread into other areas as migrant workers travel (Wang and Wen 2011). Therefore, the local government of Guangdong Province needs to monitor this issue to prevent bed bugs from spreading and to ensure that infestations are properly managed. Effective methods following an integrated pest management approach and accepted industry management standards adopted in Europe, the United States, and Australia should be used to decrease bed bugs infestation rates in key areas, such as apartments and worker sleeping quarters. Educating residents on how to minimize the transmission of bed bugs is critical for reducing their spread. Adopting these measures would go a long way toward slowing the spread of bed bugs throughout the nation. Acknowledgments We thank Dr. Jian Chen from United States Department of Agriculture–Agricultural Research Services and Dr. Virna Saenz from North Carolina State University for critical reviews of an early version of the manuscript. We would like to thank two anonymous reviewers for many helpful comments on the manuscript. 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