J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 68 http://jad.tums.ac.ir Published Online: March 31, 2020 Original Article Effects of Resident Education and Self-Implementation of Integrated Pest Man- agement Strategy for Eliminating Bed Bug Infestation in Ahvaz City, South- western Iran Ismaeil Alizadeh1,2; Elham Jahanifard1,3; *Mona Sharififard1,3; Mohammad Ebrahim Azemi4 1 Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 2 Department of Biology and Vector Control, School of Public Health, Kerman University of Medical Sciences, Kerman, Iran 3 Department of Medical Entomology and Vector Control, School of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 4 Department of Pharmacognosy, Medicinal Plant and Natural Product, Research Center, School of Pharmacy, Jundishapur University of Medical Sciences, Ahvaz, Iran (Received 01 Aug 2018; accepted 12 Mar 2020) Abstract Background: Bed bugs as blood-sucking insects have become a public health problem in urban communities through- out the world. The objective of this study was to determine the effects of resident education and self-implementation of Integrated Pest Management (IPM) strategy for eliminating bed bug infestation in infected apartments in Ahvaz City, Iran. Methods: This interventional study was conducted in seventy apartments infested with bed bug (Cimex lectularius) in Ahvaz City, southwest Iran, during a 6-month period. The bed bug infestations reported to Health centers were inspected visually and confirmed by medical entomology experts. Then, the heads of the households were received techniques/ tools of the IPM program and trained by medical entomology experts before self-implementation of control methods. Finally, the infected apartments were inspected by the experts at 1, 3, and 6 months after intervention and data were rec- orded in a checklist. Results: From the seventy infected apartments, 57%, 28% and 15% were considered as low, moderate, and high level infestation respectively. The bed bug infestation was eliminated from 53 apartments (76%) after one month and it reached to 62 apartments (88%) by the end of third month. Finally, after six months of applying IPM program, bed bugs infesta- tion was eliminated from all infected apartments (100%). Residents expressed their 100% satisfaction with applying the bed bug IPM strategy. Conclusion: Training residents to implement the IPM program can reduce pest control costs, the volume of pesticides consumed, and human exposure to chemical pesticides, resulting in increased human and environmental health and safety. Keywords: Bed bug; Urban pest; Integrated pest management; Strategy Introduction The bed bugs (Cimex lectularius and C. he- mipterus) as blood-sucking insects have become a serious pest and public health problem in ur- ban communities throughout the world. They af- fected human health through blood feeding that can lead to pain, itching, secondary infections, loss of sleep, psychological distress and other allergic responses to humans (1-8). These urban pests have adapted to live in close to indoor human environments including hous- es, hotels, dormitories, sports, workplace environ- ments, and transport systems all over the world during the past decade (1, 2, 5, 9). Generally, increased international travels, insecticide re- sistance, climate changes, lack of awareness, lack of effective monitoring and management tools and the decreased use of broad-spectrum insec- ticides in human dwellings can be outlined as *Corresponding author: Dr Mona Sharififard, E- mail: sharififard-m@ajums.ac.ir http://jad.tums.ac.ir/ mailto:sharififard-m@ajums.ac.ir J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 69 http://jad.tums.ac.ir Published Online: March 31, 2020 leading reasons involve with the bed bug emerg- ing (2, 5, 9–11). Also social interactions between residents, home visits, or exchange of infested furniture are revealed to cause bed bug distri- bution in recent studies (5, 12, 13). Elimination of bed bug infestation is costly and time-consuming because of activity and noc- turnal blood feeding, habit of hiding, spreading around the house (5, 14, 15). They are providing to be one of the most challenging urban pests. Most people prefer to use chemical insecticides for removing the bed bug infestation due to more convenient application of chemical method com- pared with other control tools. Even if relatively proper insecticides are used, the challenges with pesticide resistance can occur. Also, using chem- ical insecticides directly on furnishings in hu- man dwellings increases the risk of human ex- posing to pesticides (1, 5). Integrated pest management (IPM) approach is considered as a promising, comprehensive and safe strategy for humans and environment re- cently. It exploits cooperation between residents and professional pest experts to use both chem- ical and non-chemical tools and technics simul- taneously to eliminate of pest infestation (13). Non-chemical techniques include heat treatment, vacuuming, mattress encasements, laundering, freezing and heat steam (3, 5, 14, 16, 17). In or- der to effectively eliminate bed bug infestations, recognition, management, and eradication are the components of successful control program (13). Bed bug infestation is increasing in Ahvaz City, south west of Iran based on health services reports, as well as resident’s reports to Depart- ment of Medical Entomology. The average cost of bed bug control is about $ 0.78 per m2 for chemical control based on pest control services reports in Ahvaz City in 2019. While the bed bug infestation usually occurs in low-income communities, control by those companies is not cost-effective and the people prefer to apply some conventional control methods by them- selves. Little studies have been documented the use- fulness of IPM strategy for control bed bugs (5, 13, 18, 19). But there are no studies on resident education and self-implementation of IPM strat- egy for control of bed bug infestation. The ob- jective of this study was to determine the ef- fects of resident training to apply IPM strategy for eliminating bed bug infestation in infected apartments. Materials and Methods Design of Interventional study This interventional study was one arm pre- post study conducted in 70 apartments with bed bug infestation in Ahvaz City, southwest Iran during a 6-month period from May 2015 to Oc- tober 2016. Ahvaz City is one of the metropol- itan cities in the southwestern of Iran, with a pop- ulation of 1.3 million. It is located in a dry area of Iran with subtropical hot desert climate. The infected apartments were located in different parts of the city both in west and east of the Karun River (Fig. 1). All the apartments were in- cluding bedroom, living room, kitchen, and bath- room. At first, a list of the apartments with reported bed bug infestation was prepared from the health centers and Department of Medical Entomol- ogy of Ahvaz Jundishapur University of Med- ical Sciences in Ahvaz City. Inspection of the infected site is the first step of each IPM program (Fig. 2). The houses were inspected visually by medical entomology ex- perts to confirm the bed bug infestation (Fig. 3). From the reported infected houses, 70 houses were selected randomly for the study. Residents of infected apartments were informed about the objectives and procedures of the investigation. All the heads of households signed written con- sent prior to implementation of the program. A self-administered checklist was used to evaluate the bed bugs infestations level. The bed bug infestation was assessed through the visu- al observation of live and dead bed bugs, fecal spots, cast skins, and eggs and categorized to three levels of low, medium and high infestation (Low: 1–10 live or dead bed bugs, few fecal http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 70 http://jad.tums.ac.ir Published Online: March 31, 2020 spots and few cast skins; medium: 11–50 live and dead bed bugs, fecal spots and cast skins, high: > 50 live or dead bed bugs, lots of fecal spots and cast skins). Bed bugs were collected and preserved in 75% ethanol and sent to the laboratory of Medical Entomology and Vector Control for identification. Training of residents After inspection, identification of the infes- tation, signing the consent form, the head of the households were trained by medical entomol- ogy experts to control the bed bug infestation by self-applying of IPM strategy. They also pro- vided guidelines to improve the prevention and control programs based on IPM approach. Eight techniques/tools and six steps were considered in the bed bug management program are ex- plained in (Figs. 4 and 5). Totally two hours was spent to train the head of each house in this sur- vey. The steps of T1, T3, T7 and T8 were per- formed only once by residents in the first week but the use of other steps includes laundering, vacuuming, steam cleaner and wipes were con- tinued several times until bed bug elimination (Fig. 4). Entomological experts were on-call with the residents until complete bed bug elimination. Data Collection The infected apartments were inspected by the entomological experts at 1, 3, and 6 months after intervention. The bed bug infestations in each home were recorded in self-administered checklist based on visual inspection. Also, after one, three and six months, the residents were in- terviewed for three questions: (1) Do you still have bed bug infestation in your apartment? (2) How effective do you think this program is? (3) How worried you are about bed bug infestation? A total of 241 residents from seventy infected apartments were interviewed. Data Analysis The data were collected to determine the overall effectiveness of IPM strategy in infected apartments. Excel Version 2013 software was used to analysis the frequency and descriptive variables. Results Evaluation of the self-implementation Inte- grated Pest Management program Totally, 70 infected apartments were inspect- ed during this survey. The levels of infestation were recognized as low, moderate and high in 57%, 29% and 15% of infected houses based on initial inspection. The collected specimens were identified as common bed bug (C. lectu- larius). During the home inspection phase, it was found that the infestations rate of bedrooms and living rooms were 73% and 27%, respectively. Also in 38%, 32%, 18% and 14% of the in- fected houses, the bed bug harborages were crack and cervices, bedding, wooden furniture and wallpaper and Belka, respectively (Fig. 8). Residents of all apartments attended to the in- tegrated bed bug control program in this study (Fig. 5). The bed bugs infestations from 53 apart- ments (76%) were eliminated after one month. In this time 100%, 90% and 30% of apartments with low, moderate and high level of infesta- tions were cleaned from bed bug infestations, respectively. The bed bug infestation was elim- inated from apartments with low infestations without using pesticide. Then, the bed bug elim- ination from 62 apartments (88%) was occurred after three months of self-implementation of IPM strategy. In this time 100% and 70% of apart- ments with moderate and high levels of infes- tation were cleaned, respectively. Finally, after six months of applying IPM strategy by resi- dents, the bed bug infestation was eliminated from all infected apartments (100%) (Fig. 6). All residents have high cooperation in this study. In total, all residents expressed their 100% satis- faction with applying the IPM strategy. As shown in (Fig. 6), elimination of bed bugs from apartments with low and moderate level of in- festation occurred faster than those with high bed bugs infestations. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 71 http://jad.tums.ac.ir Published Online: March 31, 2020 Resident’s interview During this survey, 286 people were lived in the infested apartments. From them, 241 people with the age of > 16 years were inter- viewed. All of them were satisfied with IPM strategy as an effective approach for bed bug elimination. Bed bug bite signs were observed in 23% of the residents. Among the inter- viewed resident, 82% were very concerned, experienced sleep loss, and psychological dis- tress, 10% of them had a somewhat concern and 8% showed no concern. Fig. 1. Study areas in Ahvaz City, southwestern Iran Fig. 2. Different steps of running an Integrated Pest Management program http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 72 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 3. (A) and (B) Infested living room, (C) Common Bed bug colony over the bed, (D) Bed bug infestation under wallpapers (F) Visual inspection by medical entomology expert Fig. 4. Techniques/tools of the integrated bed bug control program http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 73 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 5. Flowchart of applying the IPM Program in bed bug infested houses in Ahvaz City, southwest Iran Fig. 6. (A) Vacuuming, (B) Infested Belka in living room, (C) Vacuum airless bag, (D) Sealing wall cracks and crev- ices, (E) Discarded wooden furniture, photo by Ismaeil Alizadeh http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 74 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 7. Bed bugs infestations rate in different sources of the infected apartments Fig. 8. Effect of Integrated Pest Managaemnt (IPM) on bed bug eliminating rate with low, moderate and high level of infestation Discussion The role of education in raising knowledge of the public and consequently reducing the prevalence rate of vectors and vector-borne dis- eases is completely clear. A study by Alizadeh et al. (2018) in Ahvaz City reported residents' knowledge about transmission of bed bug, med- ical importance, habitat, infestation control, pre- vention of bed bug were 36.7%, 13.3%, 35%, 75% and 66.7% respectively (20). Most peo- ple get their necessary information by searching the internet, but they are not practically familiar with pest control techniques. Our study is the first documented practically application of self- implementation IPM strategy in order to elim- inating bed bug infestation in Iran. The purpose of this study was to examine the overall effec- tiveness of IPM approach to removing bed bug infestation, not to evaluate specific techniques/ tools. The IPM program was attributed to five practices including: A) Inspection of infected apartments, B) Identification of insect species, (C) Monitoring the infestation level, D) Action http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 75 http://jad.tums.ac.ir Published Online: March 31, 2020 including training residents to apply the IPM techniques/tools according to protocol, (E) Eval- uation the effectiveness of control program. Education of residents regarding biology, be- havior, medical importance of bed bug, and what actions should be to take for infestation remov- ing is an important component of any IPM ef- fort in multifamily housing (13). Bed bug infestation was eliminated complete- ly (100%) using non-chemical techniques/tools in houses with low infestation in our study. This finding is confirmed by Wang et al. 2016, Cooper et al. 2.16. They also reported that residents training, non-chemical techniques/tools, and pe- riodic monitoring of bed bug can effectively remove light bed bug infestations (5, 13). Alt- hough the IPM strategy is time consuming, re- ducing the use of pesticides and exposing them to humans are two of the main goals of an IPM program that can offset the time delay. Generally, integrated pest management strat- egy which uses various non-chemical techniques/ tools before chemicals becomes more prevalence and promising in last decades. Furthermore, IPM considered as practical strategy in urban envi- ronment where bed bug control is challenging in low-income communities and multiunit hous- ing building (18). Due to the high cost of bed bug elimination (about $ 0.78 per m2) by pest control services, residents in low-income com- munities prefer to control the infestation them- selves. Therefore, the role of education of res- idents and their involvement in the implemen- tation of the pest control program can reduce their costs (1). A few studies have documented the effectiveness of IPM strategy for reducing or eliminating of bed bug infestation around the world (1, 5, 9, 13, 19). Ongoing education and commitment of the housing residents will play an important role in program success and elimination of bed bug in- festation (13). We continued our inspection and training weekly until complete clean-up of the houses. These actions resulted in complete re- moving of bed bug infestation after one, three and six months in 76%, 88% and 100% of the houses, respectively. In the study of Cooper et al. (2015), bed bug infestation was eliminated from 52 apartments out of 62 treated apartments using IPM strategy and the mean bed bug counts was reduced to 96% after 6 month of inspec- tion treated apartments. Moreover, the infesta- tion rate was decreased from 15 to 2.2% after 12 months (13). The effectiveness of IPM strategy for de- leting bed bug infestation was reported by all the residents. The results of our study are also consistent with Wang et al. (2019) which report- ed IPM program as a much more effective ap- proach for building-wide control of bed bugs than conventional pest control service(19). Generally, the failure of IPM program and the prolonged infestation are probably related to not completely follow-up the control instruction, lack of resident cooperation (5, 10, 13, 21) or bed bug re-infestation of the houses. Additionally, phys- ical disabilities, financial problems, no concern about bed bug infestation and resident`s distrust to non-chemical methods can be the reasons of lack cooperation of residents (9). Continuous monitoring and evaluation of control operations are two key factors in assessing the effective- ness of every IPM program (19). Close supervision of medical entomology ex- perts until the full bed bug elimination have been the strengths of this study in addition to high level of resident’s cooperation. Residents' home attendance during weekly monitoring was one of the drawbacks of the program, making it dif- ficult to accurately estimate the infestation lev- el and quality of the program execution. Also, the reduction in bed bug infestation during the implementation of the program was not quanti- tatively estimated. Conclusion The present study provides first evidence for using IPM strategy in control bed bugs infes- tation in Iran. This study was focused on training the residents of infected apartments to eliminate http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 76 http://jad.tums.ac.ir Published Online: March 31, 2020 the bed bug infestation using IPM strategy. In addition, this present research provided a good model that is effective for self-implementation in infected apartments suffering from bed bug infestations in Ahvaz City. In conclusion, to get rid of the bed bugs infestations, residents must have high motivation and cooperation in this model. The use of sticky trap and dusts (silica gel or diatomaceous earth± pyrethrum and PBO) (17) in combination with the IPM strategy is sug- gested in future studies. We also recommend that residents who involve in controlling this urban pest can be trained by mobile health application (22) to improve knowledge and awareness of IPM strategy and arrive to successful bed bug control. Acknowledgement This article is a part of Ismaeil Alizadeh MSPH thesis and it was financially supported by Ahvaz Jundishapur University of Medical Sciences (AJUMS). (Project No. OG-95102) and Ethical Number: IR.AJUMS.REC.1394.709. The authors are grateful to Dr Changlu Wang, De- partment of Entomology, Rutgers University, New Brunswick, NJ, USA, for his helpful com- ments on an earlier draft and reviewing the man- uscript. We would like to thank all the residents who participated in our study and help us to complete the study. References 1. Wang C, Cooper R, Dhang P (2011) Envi- ronmentally sound bed bug manage- ment solutions. In book: Urban Pest Man- agement: An environmental perspective Chapter: Four Publisher: CAB Interna- tional Editors: Partho Dhang. 18: 44–63 2. Bennett GW, Gondhalekar AD, Wang C, Buczkowski G, Gibb TJ (2016) Using research and education to implement prac- tical bed bug control programs in multi- family housing. Pest Manag Sci. 72 (1): 8–14. 3. Stedfast ML, Miller DM (2014) Development and evaluation of a proactive bed bug (He- miptera: Cimicidae) suppression program for low-income multi-unit housing facil- ities. J Integr Pest Manag. 5(3): E1–E7. 4. Wang C, Singh N, Cooper R (2015) Field study of the comparative efficacy of three pyrethroid/ neonicotinoid mixture products for the control of the common bed bug, Cimex lectularius. Insects. 6(1): 197–205. 5. Wang C, Singh N, Zha C, Cooper R (2016) Bed bugs: Prevalence in low-income communities, resident’s reactions, and im- plementation of a low-cost inspection protocol. J Med Entomol. 53(3): 639–46. 6. Sharififard M, Alizadeh I, Jahanifard E, Wang C, Azemi ME (2018) Chemical Compo- sition and Repellency of Origanum vul- gare Essential Oil against Cimex lectular- ius under Laboratory Conditions. J Ar- thropod Borne Dis. 12(4): 387–397. 7. Alizadeh I, Sharififard M, Jahanifard E, Rajaei F, Mousavian G, Mehraghaei M (2018) Identification, Knowledge, and Awareness of People Regarding Public Health Nuisance Insect (Cimex lectular- ius) in Southwest of Iran. Jundishapur J Health Sci. 10(3): 1–7. 8. Alizadeh I, Sharififard M, Jahanifard E (2017) Allergic reactions and dermatitis to com- mon bed bug bites: A case report from Ahvaz, southwest of Iran. Iran J Derma- tol. 20: 65–67. 9. Wang C, Saltzmann K, Bennett G, Gibb T (2012) Comparison of three bed bug man- agement strategies in a low-income apart- ment building. Insects. 3(2): 402–409. 10. Romero A, Potter MF, Potter DA, Haynes KF (2007) Insecticide resistance in the bed bug: a factor in the pest’s sudden re- surgence? J Med Entomol. 44 (2): 175– 178. 11. Zhu F, Wigginton J, Romero A, Moore A, Ferguson K, Palli R, Potter MF, Haynes http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 68–77 I Alizadeh et al.: Effects of Resident … 77 http://jad.tums.ac.ir Published Online: March 31, 2020 KF, Palli SR (2010) Widespread distri- bution of knockdown resistance muta- tions in the bed bug, Cimex lectularius (Hemiptera: Cimicidae), populations in the United States. Arch Insect Biochem Physiol. 73(4): 245–257. 12. Wang C, Saltzmann K, Chin E, Bennett GW, Gibb T (2010) Characteristics of Cimex lectularius (Hemiptera: Cimicidae), infes- tation and dispersal in a high-rise apart- ment building. J Econ Entomol. 103(1): 172–177. 13. Cooper RA, Wang C, Singh N (2016) Eval- uation of a model community‐wide bed bug management program in affordable housing. Pest Manag Sci. 72(1): 45–56. 14. Wang C, Gibb T, Bennett GW (2009) Eval- uation of two least toxic integrated pest management programs for managing bed bugs (Heteroptera: Cimicidae) with dis- cussion of a bed bug intercepting device. J Med Entomol. 46(3): 566–571. 15. Potter MF, Haynes KF (2014) Bed bug na- tion: Is the United States making any progress. Proceedings of the 8th Interna- tional Conference on Urban Pests, 20– 23 July 2014, Zurich, Switzerland, pp. 51–58. 16. Doggett SL, Orton CJ, Lilly DG, Russell RC (2011) Bed bugs: the Australian re- sponse. Insects. 2(2): 96–111. 17. Davies TG, Field LM, Williamson MS (2012) The re-emergence of the bed bug as a nui- sance pest: implications of resistance to the pyrethroid insecticides. Med Vet En- tomol. 26(3): 241–254. 18. Romero A, Sutherland A, Gouge D, Spaf- ford H, Nair S, Lewis V, Choe DH, Li S, Young D (2017) Pest management strategies for bed bugs (Hemiptera: Cimi- cidae) in multiunit housing: a literature re- view on field studies. J Integr Pest Manag. 8(1): 1–10. 19. Wang C, Eiden A, Cooper R, Zha C, Wang D (2019) Effectiveness of Building-Wide Integrated Pest Management Programs for German Cockroach and Bed Bug in a High-Rise Apartment Building. J Integr Pest Manag. 10(1): 33–38. 20. Alizadeh I, Sharififard M, Jahanifard E, Ra- jaei F, Mousavian G, Mehraghaei M (2018) Identification, knowledge, and awareness of people regarding public health nuisance insect (Cimex lectulari- us) in southwest of Iran. Jundishapur J Health Sci. 10(3): 1–7. 21. Wang C, Singh N, Cooper R, Liu C, Bucz- kowski G (2013) Evaluation of an insec- ticide dust band treatment method for controlling bed bugs. J Econ Entomol. 106(1): 347–352. 22. Alizadeh I, Gorouhi MA, Aghaei Afshar A, Hayati R, Mirr I (2019) Satisfaction of Mobile Users with mobile Application" Identification, Prevention, and Control of Bed Bugs": Designing and Developing Mobile Health Application. J Health Bio- med Info. 6(1): 24–31. http://jad.tums.ac.ir/ javascript:; javascript:; javascript:;