Prevalence and associated factors of bed bug infestations (Cimex lectularius) in lubaga division, Kampala capital city, Uganda

Background: There has been an increasing public health concern as a result of bed bug infestation, with devastating effects on health and quality of life in Uganda. This study provided the first community-based report on the situation of bed bugs in Lubaga division, Kampala Capital City, Uganda. Methods: This was a descriptive cross-sectional study design, in which data was collected using questionnaire, key informant interview guide and a data abstraction tools. Results: Out of the 356 respondents interviewed, 249(69.9%) had bed bugs in their homes. The study further revealed a significant statistical relationship between the variables of gender, sex, level of education, employment status. The health systems factors that include availability of professional personnel to control bed bugs, use of effective and recommended chemicals, availability of funds, and resistance of bed bugs to insecticides were all found to have an influence on the risk of bed bugs. Conclusion: The study has established the need to strengthen vector control programs in a city suburb. *Correspondence to: Ivan Mugisha Taremwa, Clarke International University, P.O Box 7782, Kampala, Uganda, Tel: +256774346368; Email: imugisha@ymail.com


Background
Bed bugs (Cimex lectularius) are blood-feeding insects that have plagued humans for thousands of years [1]. They have been a household pest issue for more than 3,300 years, dating back to ancient Egypt. During the latter half of the 20th century, this bloodfeeding species was almost extinct in many economically developed countries due to the widespread use of synthetic pesticides such as Dichlorodiphenyltrichloroethane (DDT) [2]. In recent years, however, there was a surge of reports of bed bug infestations among the developed countries [2][3][4]. Bed bugs belong to the Cimicidae family that feed exclusively on the blood of mammals, in particular human beings, or birds [2,5] and this affects the quality of life and is a mechanism of disease transmission and are common public health pests in many parts of Uganda.
Despite efforts to eliminate bed bugs by use of common pesticides and heat, there has been increasing public health problem as a result of bed bug increased infestation in Uganda. Infestation with Cimex lectularius is linked to a risk of transmitting Trypanosoma cruzi, the etiologic agent of Chagas disease [6]. With increased resistance to common pesticides such as chlorfenapyr, permethrin, and pyrethroids [7,8] it has become a critical challenge. Bed bug infestations can have adverse effects on health and quality of life as victims have been reported to suffer from loss of sleep, psychological distress, as well as allergic reactions [9]. Vigorous scratching and concomitant erosions predispose the skin to secondary bacterial infection, while chronic blood loss and iron-deficiency anemia have also been reported in people who have been continuously exposed to severe bed bug infestations. Bed bug infestations have been reported in places such as homesteads, schools, institutions, hotels, public transport, refugee camps and other places in Uganda. There is limited epidemiological data on bed bugs in Uganda. We report on the prevalence and risk factors for bed bug infestations in Lubaga division, Kampala capital city, Uganda.

Data collection and management
Data collection tools that were used included a questionnaire, key informant interview guide and a data abstraction tool for the quantitative component of the study.

Data tools
These included semi-structured researcher administered questionnaires. Respondents were asked questions in languages they understood properly.

Ethical consideration
Ethical approval was obtained from Clarke International University (Formerly, International Health Sciences University). In addition, permission was sought from Kampala Capital City Authority (KCCA), Ministry of Health (MOH), Local Councils (I, II and III). At an individual level, written informed consent was obtained from each participant.

Social factors influencing bedbug infestation
Three hundred and forty (N = 340, 95.5%) of the participant had knowledge about bed bugs and had varied skills to identify them. Only 43 (12.1%) used reddish brown spots on the mattresses and furniture to identify presence of bed bugs, 43 (12.1%) used presence of eggs in fabric seams, 33 (9.3%) of them were identified using a foul odor from oily secretions. 35 (9.8%) of the participants identified presence of bed bugs using fecal spots left around points of entry and exit to their hiding places, 84 (23.6%) used bite symptoms to identify presence of bed bugs, 49 (13.8%) used blood smears on sheet and clothes while 37 (10.4%) used moults and 72 (20.2%) identified presence of bed bugs using physical presence. The study finding also indicated that 154 (43.3%) of the participant agreed that visitors led in to bed bugs infestation in their homes, 68 (19.1%) revealed that it is transferred from school by children in to their homes, 75 (21.1%) agreed that buying second hand clothes leads in to manifestation of bed bugs in their homes. In addition to that, 43 (12.1%) of the respondents agreed that they carry bed bugs from taxis to their home while 115 (32.3%) revealed that it moves from their neighbors and 32 (9.0%) got them from hotels/guest houses. In regard to method used to control bed bugs, 144 (40.4%) of the respondent used application of chemicals, 76 (21.3%) used hot water to burn them, while 59 (16.6%) of the participant washed their clothes and bedding to control bed bug infestation in their homes. Out of 356 participants, almost a half 175 (49.2%) of them agreed that they used insecticides to control bed bugs while 181 (50.8%) did not use insecticides. The social characteristics were analyzed to determine their significant association with bed bugs infestation. The study established that bed bug infestation was significantly influenced by: having knowledge about bed bugs (X 2 8.388, p-value 0.004), identification with reddish brown spots (X 2 3.997, p-value 0.046), Bite symptoms(X 2 4.017, p-value 0.045), physical presence of bed bugs (X 2 10.828, p-value 0.001), visitors (X 2 8.218, p-value 0.004), neighbors (X 2 9.646, p-value0.002), burning with hot water (X 2 4.121, p-value 0.042) and employment of qualified personnel (X 2 6.159, p-value 0.013), these factors are presented in table 2.

Discussion
This study has found an overwhelming 70% prevalence of bed bugs in Lubaga division. Also, 249 (69.9%) had bed bugs in their homes. This is in agreement with a door to door study in a residential census tract of Philadelphia USA by Yage et al. [10]. According to that report, among the 596 respondents, 66 (11.1%) reported having bed bugs in their residence and were classified as reported positive. This also correlates with a study by Eliningaya et al. [11] which indicated that 1370 (51.3%) bed bugs were collected from houses with no bed nets and 980 (36.8%) bed bugs were collected from houses with torn bed nets, since this could be an indicator of the populations' financial capacity to buy and utilize intact bed nets. The high prevalence was attributed to both the individual and health systems factor because there was positive correlation between these factors and bed bug infestation. During the analysis, it was found that the very poor respondents and the economically-disadvantaged individuals had significant increased chances of being infected with bed bugs. There was a significant relationship found between the gender of the respondent (X 2 12.566 p-values .028) and bedbug infestation. This could be attributed to the different lifestyles. The females tend to have congested rooms due to an increased number of clothes which agrees with a publication by Pest management Consultancy in United Kingdom, (2008). This study reported that congested domestic premises make bed bug control difficult while the males could be attributed to the question of personal hygiene. The results indicated age categories of 26-35 participated more in the study, 96 (27.0%) were aged 26-30 years, 81 (22.8%) were between 31-35 years. These were all household heads or guardians with responsibility of the home. With the high prevalence of bed bugs in their homes, it implies that this age group is most at risk. This was confirmed by a significant causal relationship between age category 15-20 years (OR=3.133, 95% CI 1.011-9.703, p=.048) and bedbug infestation. The age group is believed to be that of a lower income status which proves the argument that bed bugs affect more of the poor people in communities. There was a correlation between level of education and bed bug infestation. The majority of participants had primary level of education which further indicated a causal relationship (OR 3.863, 95% CI 1.132-13.183, p=.031), and secondary level of education (OR 3.605, 95% CI 1.119-11.610, p= .032). Generally, there is an association of bed bug infestation with both low income levels and the education status. The confirmation that the low-income communities experienced high bed bug infestation trajectory agrees with earlier literature [12]. With low income levels, people cannot afford to employ professional personnel to help in controlling bed bugs from their homes; neither can they afford to buy the recommended insecticides to spray. The employment status (X 2 3.582 p-value .058) was also found to have a significant correlation. This could be attributed to the fact that both the employed and the unemployed are involved in the transmission of the bed bugs. The employed could acquire them from different work places while the unemployed could acquire them from home visitations. Therefore, this leaves both at a significant risk of being infested with bed bugs. The study confirmed that being employed (OR 2.4.093, 95% CI .759-22.078), was associated with bed bug infestation. The type of employment showed a positive correlation (X 2 17.528, p-value .000) with bedbug infestation. For example, being a civil servant (OR 4.292, 95% CI 2.204-8.384, p=.000) was associated with bedbug infestation. This is probably attributed to the large numbers of people they directly come into contact with and the unmatched low level of hygiene.
There was a positive correlation between bedbug infestation and knowledge (identification with reddish brown spots (X 2 3.997, p-value 0.046), bite symptoms (X 2 4.017, p-value 0.045), physical presence of bed bugs (X 2 10.828, p-value 0.001). This could be related to the multiple exposures of the communities, and thus have full recognition. This agrees with Goddard and deShazo [13], who indicated that bed bugs plague humans and Bonnefory et al. [2] who described the common bed bugs as having a light cream appearance, but progressively becoming reddish-brown in color. This proves that bed bugs are a serious problem in Lubaga division and many of them never hesitated to admit into their houses research assistants to see how badly off they are with hope that one day, they will be saved from this nuisance biter. Majority of respondents used bite symptoms to identify presence of bed bugs in their homes followed by the physical presence of bed bugs and blood smears on bed sheets (OR 3.593, 95% CI 1.859-6.944, p=.000). Bed bugs have very painful bites as indicated by a significant number of respondents who indicated that the biting symptoms (OR 2.251, 95% CI 1.172-4.322, p= .015) were used to identify these bed bugs. Sometimes one can develop red spots at the bite site due to body reactions. Bed bugs are shy to light and sound vibrations. It is therefore not very easy to observe physical presence of bed bugs unless when the infestation is considerably high. According to the study findings, majority of participants agreed that visitors to their homes (OR= 2.017, 95% CI 1.222-3.329, p=.006), were the leading source of bed bugs into their homes followed by the close neighborhoods, second hand clothes and schools where children. This is in line with findings from a report by the Pest management Consultancy in United Kingdom, (2008). This was also confirmed by respondents who indicated that the neighbors and friends were complaining about bed bugs (OR 7.549, 95% CI 4.086-13.945). In regard to methods used to control bed bugs, most respondents 144 (40.4%) used application of chemical to control them, while 76 (21.3%) used hot water for burning them. The use of hot water is probably due to lack of enough knowledge in bed bug control because eggs of the species Cimex lectularius are quite resistant to hot temperatures. In view of the above, out of 356 study participants, almost a half 175(49.2%) of them agreed that they used insecticides to control bed bugs while 181(50.8%) did not use insecticides. This implies that residents of Lubaga division believe that with effective chemicals, bed bugs can be eliminated. Nevertheless, majority of them did not use these insecticides probably because they are not available, affordable or accessible. With reference to type of insecticides used to control bed bugs, majority (N=313, 87.9%) did not know the type of the insecticides they could use to control bed bugs. This confirms a knowledge gap about the various insecticides in control of bed bugs. This calls for the relevant authorities to sensitize the community about the dangers of insecticides and the safest ways to administer pesticides. Most participants (N=331, 93.0%) disagreed that they had qualified people to help in control of bed bugs. This concurs with previous research [10], who maintained that inadequate training of pest control technicians contributes greatly to the resurgence and spread of bed bugs. The challenges faced in control of bed bugs according to the study indicated that 175(49.2%) of the respondents agreed that the bed bugs don't die, 167(46.9%) revealed that it comes back very fast and 14(3.9%) agreed that they don't have money to control them. This is probably because of the lack of knowledge in bed bug prevention and control and the ineffective chemicals. Further, poor techniques of chemical application and the equipment used was found wanting. Many respondents revealed that they could buy any unknown chemicals from street vendors and use bottles with punctures to apply the chemical to kill the bed bugs. One of the respondents said that "Bwetufuuyila nga tukozesa obukebe buno, ebiku tebifa. Ate abayitamu nga bafuuyila oyinza okulowooza nti babyoogedde bwongezi busuungu kutuluma. Bafuuyila mazzi meerere". Literally meaning that, "when we spray using the punctured bottles, bed bugs don't die. And it's as if the people who pass through our villages spraying only excite them to bite us the more. It seems they use water to spray bed bugs". There is a correlation between bed bug infestation and visitors (X 2 8.218, p-value 0.004) and neighbors (X 2 9.646, p-value 0.002) as they are carried by humans in seams of clothes. This agrees with the fact that bed bugs can rapidly spread to neighboring units and cause high infestation rates in multiunit dwellings [4,7]. These studies also asserted that in most cases, bed bugs are transported from infested areas to non-infested areas when they cling onto someone's clothing, or crawl into luggage, furniture or bedding that is then brought into homes. This justifies the relationship between the visitors, neighbors and bedbug infestation. The study found that the methods of bedbug control among the community was lacking. This was for example justified by the strong relationship between infestation of bedbug and use of burning with hot water (X 2 4.121, p-value 0.042) as a method of controlling bed bugs. This is attributed to the limited knowledge considering the fact that they were employing unqualified personnel (X 2 6.159, p-value 0.013) to control the bed bugs.

Conclusion
Based on these, bed bugs represent a very big challenge to public health in Lubaga division and Uganda at large as evidenced by the high prevalence (70%). The study has further established the need to strengthen vector control programs in a city suburb.