Abstract

This study was to determine risk assessment associated with bed bugs (Insecta: Hemiptera: Cimicidae) using participatory epidemiological tools in the selected public hospitals of district Faisalabad, Punjab, Pakistan. Bed bugs were collected and morphologically identified through a standard taxonomic key. A descriptive cross-sectional survey of patients using a pre-designed questionnaire containing open-ended and closed-ended questions was conducted for six months between January 2023 and June 2023. Of the 384 participants, 113 (29.43%) had experienced itching or skin irritation presumably from the bed bug feeding activity. The study further revealed patients above age 40 (35.43%) and males (30.57%) experienced greater skin irritation responses compared to other participants. Among administrative divisions (tehsils) in the city of Faisalabad, Tehsil Sadar had the highest number of participants with itching or skin irritation (35.48%), while Tehsil Chak Jhumra had the lowest number (24.62%). Most observations of bed bugs by patients were in their beds (10.42%), with chairs (3.91%) being the second most reported location. However, we found bed bugs from only 17 (4.42%) beds and 5 (1.30%) from chairs. A majority of patients (60.9%) reported daily change of bedding; however, a significant proportion (29.9%) reported infrequent changes. About 25.5% of the patients shared beds with others and about 77.1% of patients brought their own bedding or clothing to the hospitals. The current study concluded that the bed bug infestation is a problem in the public hospitals of Faisalabad, Punjab, Pakistan. Risk factors such as sharing a bed, infrequent change of bedding, and bringing personal bedding to hospital while having medical treatment pose a concern.

Introduction

Bed bugs (Insecta: Hemiptera: Cimicidae) are hematophagous temporary ectoparasites of public health concern affecting human life globally [2]. The prevalence of bed bug infestations in functioning residential buildings appears to be increasing in USA, Canada, Europe, and other locations [12]. Bed bugs have been closely associated with humans for several hundred thousand years, adapting to human environments over time. Central heating which was introduced in the early 1900鈥檚, contributed to the widespread prevalence of bed bugs in the United States and other western industrialized nations making them a serious health and economic pest. Following the rediscovery of Dichlorodiphenyltrichloroethane (DDT) in the 1930鈥檚 which proved to be a very effective treatment against the insect during the 1940鈥檚 and early 1950鈥檚, they were basically extirpated from wealthy western nations. Reservoir populations remained though in third world economies, and these became the source for resurgent bed bug infestations in the west during the late 1990鈥檚 early 2,000鈥檚 brought on by high-speed international trade [9, 24].

The most prevalent and commonly found bed bugs in Pakistan are the common bed bug, Cimex (C.) lectularius L., and the tropical bed bug C. hemipterus (F). They have a life expectancy of around 6鈥�12 months [1]. They can survive in temperatures that range from 40掳C down to 鈭�10掳C [12]. They host seek by picking up on body warmth, odour, and exhaled carbon dioxide [4]. Bed bugs can disperse through two means. By actively walking from one space to another or by being accidentally transported in luggage, on clothing, or other objects [5, 8].

Those who have been fed on by bed bugs report suffering from psychological distress, including anxiety, depression, and loss of sleep. They also can experience clinical symptoms such as skin rashes, itchiness, dermatitis, asthma, and allergic reactions. Although human disease causing pathogens have been identified in bed bug systems; however, they are incompetent vectors of these pathogens and in that capacity are considered medically harmless [8]. One study showed bed bugs were found positive for 45 human disease causing pathogens in laboratory trials, but not in the field [6], yet speculation still remains that they are associated with certain particular medical diseases such as epidemic cerebrospinal meningitis, blood loss, influenza, malaria, sleeping sickness, epidemic typhus, beriberi, pellagra, respiratory issues, tuberculosis, and redness of ears [30].

Despite the economic impact of this urban pest, Cimex spp., has been hardly studied in Pakistan. Hussain et al. [11] published a study that indicated 70.14% of patients in public healthcare facilities in Karachi had bed bugs. There is a common public belief that bed bugs are an issue in seaport cities. Karachi is a densely populated seaport city. It is located on the northeast coast of the Arabian sea and has moderate to high temperatures and high levels of humidity (personal observation). Trade, a dense human population, and a favourable climate likely conspire to promote bed bug populations in the city and the belief that seaport cities have higher than average bed bug populations. Wider knowledge of the pest prevalence and risk factors is needed in a densely populated country such as Pakistan. In view of high populations of the insect being present in many communities it is important to determine the magnitude of abundance of the bed bug infestations in healthcare centers. With a hypothesis of 鈥淧ublic hospitals of metropolitan Faisalabad are under threat of bed bug infestations鈥�, the current study is a maiden attempt to determine the prevalence and distribution of bed bugs and their associated risk factors in the public hospitals of the Faisalabad district of Pakistan.

Materials and methods

Study area

The city of Faisalabad stands on the rolling flat plains of northeast Punjab at 31.45掳N latitude and 73.14掳E longitude with an elevation of 184听m (604 feet) above sea level. The average population of the city of Faisalabad is 7,874,790, and is divided up into five administrative divisions (Tehsils), Sadar Faisalabad, Samundari, Chak Jhumra, Jaranwala, and Tandlianwala. The five tehsils (administrative divisions) of the Faisalabad district possess distinct economies. Sadar Faisalabad is an urban commercial center with an active textile industry, trades and services. Samundari has an agrarian economy with a particular focus on wheat, sugarcane and dairy. Chak Jhumra has light industry, expanding residential market and some agriculture; Jaranwala has active agro-based industries around wheat, rice, and sugarcane; and Tandlianwala has an agricultural industry based on sugarcane production. The average annual temperature of Faisalabad is 24.8掳C and humidity is 59鈥�66%. There is a monsoon season between July and September when high rainfall e.g., 526听mm or 20.7 inches. The physical map of Faisalabad with selected public hospitals is shown in Fig.听1.

Fig. 1

Map of the city of Faisalabad, Punjab, Pakistan divided into administrative divisions.听A Map of Pakistan.听B听Map of Punjab with highlighted area of the city of Faisalabad.听C听Map of the city of Faisalabad showing the administrative divisions of Sadar (Allied hospital 31.45掳N; 73.08掳 E), Jaranwala (Civil Hospital 31.34掳 N; 73.43掳 E), Samundari (Tehsil Head Quarter 31.03掳 N; 73.13掳 E), Chak Jhumra (Tehsil Head Quarter 31.57掳 N; 73.18掳 E), and听Tandlianwala (Tehsil Head Quarter 31.03掳 N; 73.13掳)

Study design & sample size

A descriptive cross-sectional active surveillance was designed to determine the prevalence and awareness of associated risk factors of bed bugs. Samples were collected through complete random sampling. The sample size (n鈥�=鈥�384) was conveniently collected through the sentinel surveillance method (non-probability sampling), and participants were patients in the hospitals selected from particular public hospitals of several administrative divisions in the city of Faisalabad. Informed written consent was obtained from each patient prior to interviews. Research was approved by the Research Ethics Committee, Faculty of Veterinary Science, University of Agriculture, Faisalabad, Pakistan vide letter No. MPL 637/11鈥�22. No human subjects were sampled during this investigation and only questing bed bugs were collected in the study.

Questionnaire-based participatory epidemiology

Development of questionnaire

Both open and close-ended (multiple-choice) questions were used in the study questionnaire (S Table听1). The survey was based on following aspects regarding bed bugs: prevalence of bed bugs, awareness, and knowledge regarding bed bug infestations, risk factors associated with bed bugs, and history of bed bug infestations. It was observed to keep the categories mutually inclusive and exhaustive.

Selection of hospitals and respondents

Each administrative division (Tehsil) of the district has one public hospital, known as the Tehsil Headquarter Hospital (THQ). In the present study, we selected the THQs from each administrative division. For passive surveillance, non-probability sampling method was used and THQ hospitals were considered as sentinels for investigation. The data was collected from the following hospitals: Allied hospital; Sadar Faisalabad, Civil hospital; Jaranwala, Tehsil Head Quarter (THQ) hospital;听Samundari, THQ hospital;听Tandlianwala, and THQ hospital;听Chak Jhumra of Faisalabad district, Punjab, Pakistan (Fig.听1). The participants were divided into 3 age groups e.g., 0鈥�20, >鈥�21鈥�40, and >鈥�41. Primary data collection was comprised of two phases: individual interviews and electronic communications. Before the start of the survey, meetings with community health professionals and leaders were conducted to respect cultural norms. A written consent was obtained from each participant before the start of their interviews, and they were informed they could withdraw from the study at any point, if they felt uncomfortable.

To prevent bias, the questionnaire was prepared in English and translated into local languages of the region for participant convenience [10]. The responses to the questions were received in the local languages and translated back to English. The team did not know the respondents to avoid the personal bias. Each answer option was given a code number to avoid bias. The selection of the THQs hospitals听irrespective of its location avoided spatial bias. Similarly, gender bias was absent, because the study was open to any gender respondent. However, the six (6) month period for the investigation was constrained due to available resources, time, and physiological needs of the insects e.g., optimum temperatures and humidity.

Collection, preservation, transportation, and examination of bed bug specimens

Specimens of bed bugs were collected from different collection sites, including beds, chairs, side tables, etc. of the selected public hospitals (Allied hospital; Sadar听Faisalabad, Civil hospital; Jaranwala, THQ听hospital; Samundari, THQ hospital;听Tandlianwala, and THQ hospital;听Chak Jhumra) in Faisalabad district, Punjab, Pakistan using the standard entomological procedures over a period of six months, mostly during early morning. The collected samples were preserved in 70% ethanol for identification [15] and sent to the Molecular Parasitology and One Health Laboratory, Department of Parasitology, University of Agriculture, Faisalabad, Pakistan for taxonomic identification using the standard taxonomic keys [25].

Data management and statistical analysis

Questionnaire responses were recorded in Microsoft Excel spreadsheet. Descriptive statistics was used to analyze the prevalence using Statistical Analysis System (SAS) 2010, while a Chi-Square test was used to determine association and significant differences between parameters tested at p鈥夆墹鈥�0.05.

Results

Only one species, Cimex lectularius L. was identified. Cimex lectularius is small, reddish-brown with an oval flat segmented body. It is considered a wingless insect, though it possesses reduced hemelytral pads. Adults are approximately 4鈥�6听mm long and 1.5鈥�3听mm wide with a distinct head, thorax, and abdomen. Short, golden-colored hairs cover the body, giving it a banded appearance. Male abdomens are posteriorly while female are round.

Of the 384 participants, 113 (29.43%) were positive with skin irritation while 271 (70.57%) were negative. A non-significant association (P鈥�>鈥�0.05) of skin irritation experienced by patients in public hospitals in Faisalabad was recorded. The highest rate of skin irritation was found in the public hospital of administrative division Sadar Faisalabad (35.48%) followed in order by the administrative divisions Sumundary, Jaranwala, Tandlianwala, and Chak Jhumra. Gender showed a non-significant association with skin irritation (P鈥�>鈥�0.05); however, the prevalence of skin irritation was higher in males than females. Similarly, age groups also exhibited a non-significant association with skin irritation (P鈥�>鈥�0.05), with the highest prevalence observed in patients older than 41 years. The descriptive epidemiology skin irritation experienced by patients in public hospitals in Faisalabad is given in Table听1.

Table 1 Descriptive epidemiology of skin irritation experienced by patients in public hospitals in the city of Faisalabad, Punjab, Pakistan

According to the data collected from patients, 19.01% reported observing bed bugs in and around their beds. Specifically, of 73 patients, 40 (10.41%) had seen bed bugs on the bed, 15 (3.90%) had seen them on chairs, 10 (2.60%) on clothing, and 8 (2.08%) on other objects (Table听2). After completing each patient鈥檚 interview, we carefully examined the bed and surrounding area and found bed bugs on 17 beds (4.42%) and 5 chairs (1.30%). The overall prevalence of bed bugs in the public hospitals of Faisalabad was 5.73%.

Table 2 Patient responses to the bed bug infestation survey in public hospitals in the five administrative divisions of the city of Faisalabad, Punjab, Pakistan

A majority of the patients (58.9%) were aware of the bed bugs. A smaller portion of patients (21.1%) reported noticing bed bug feeding sites. Most observations or experiences of bed bugs occurred on the bed (10.42%), with the chair being the second most reported location. About 25.5% of the patients shared their beds with others and a majority of patients (60.9%) reported daily change of their beddings; however, a significant portion (29.9%) reported infrequent change of beddings. A majority of the patients (77.1%) brought their own beddings or clothing鈥檚 from their homes to the hospitals. A small percentage of patients (15.6%) had a history of bed bug infestations at home. The descriptive statistics and the risk factors positively or negatively associated with the bed beg infestations in public health hospitals of Faisalabad, Punjab, Pakistan is provided in Fig.听2.

Fig. 2

Risk factors associated with the Cimex lectularius infestations in public health hospitals in the city of Faisalabad, Punjab, Pakistan

Discussion

In Pakistan, bed bug infestations of homes and healthcare centers is one of the most neglected, under-reported as well as under-studied health care concerns. This study is the first of its kind on bed bug infestations in the city of Faisalabad. It revealed a provenance of the bugs in the public hospitals. Underreporting is common due to cultural acceptance, lack of awareness, or the social stigma associated with the insect [16]. As no previous work was done on the frequency distribution of bed bugs in Faisalabad, the design of the current research to evaluate the probable risk factors attributable to their abundance in public hospitals of Faisalabad city, Punjab, Pakistan is justified. Cimex lectularius was identified as the species associated with these selected hospitals. This has also been reported elsewhere [3, 19, 20].

Bed bugs infestations have been increasingly reported during the last two decades worldwide [23, 29]. In the 2,000鈥檚 the resurgence of bed bugs was observed both in high-income western industrialized nations [14] and low-income economies of Africa and Asia [17]. The distribution of bed bugs has been driven by factors such as rapid urbanization, increased international trade, poor economic conditions, overcrowding, poverty, and lack of awareness. Additional contributors include poor hygiene practices, low-quality housing, rising humidity and temperatures, insecticide resistance, and insufficient knowledge about bed bug prevention and control, all of which are linked to a higher prevalence of infestations [7, 18, 22]. Climate change due to global warming has been postulated as a factor in the boom of bed bug infestations [18]. Most of the hospitals in developing countries are overburdened due to high patient numbers and turn over which favors bed bugs [26].

Bed bugs are considered an important indoor pest with public health implications [9]. The results of the present study showed a 5.73% prevalence of bed bug infestations in public hospitals in the city of Faisalabad. This is fewer than those of the Karunamoorthi et al. [13] study which revealed 72.7% of participants were infested with bed bugs in Ethiopia. The reason for this was public over-crowding, elevated humidity, and lack of hygiene. In another study conducted by Senabulya et al. [19], 69.9% of homes in Kampala Capital City, Uganda were infested. A door-to-door survey in the United States revealed 11.1% C. lectularius infestations in homes [28]. Other descriptive cross-sectional studies revealed 9.61% prevalence in Ahviz city, Southwest of Iran [21], and 21.8% prevalence in Nigeria [10]. In Karachi, Pakistan 70.14% prevalence of bed bug infestations in primary care hospitals were reported [11].

Bed bug infestations are common in resource-limited situations [27]. There was a greater incidence of male participation over female participation. The differences may have been due to the types of wards and facilities men and women were admitted too as well as shared bed linens, furniture, and proximity to other patients. This agreed with the study by Sheele et al. [23]. Additionally, infestation rates were elevated in high patient turnover wards and facilities [21]. These infestations in public medical facilities lead to higher medical community concerns because of the insects鈥� physical presence and psychological impact on patients [2].

The data indicated that while a majority of patients were aware of bed bugs, infestation reporting was lacking. This suggested toleration and a lack of education about the insects [16]. The identification of beds as the most common site for bed bug sightings further underscored the need for targeted intervention strategies in areas where patients spend most of their time. Additionally, the correlation between reported bed bug bites and dermal symptoms highlighted the importance of prompt identification and treatment to prevent discomfort and potential secondary infection among patients [13].

Furthermore, the frequency of bedding changes appears to be a critical factor in managing infestations, with a significant minority of patients reporting infrequent bedding changes. The practice of bed-sharing, although not widespread, also poses a risk for the movement of bed bugs between patients [9]. The finding that a significant portion of patients brought their own bedding and clothing to hospital, coupled with a small percentage with a history of infestation at home, suggests external factors may play a role in the introduction and proliferation the insects in hospitals. This pointed to the necessity of a comprehensive approach to bed bug management that includes both in-hospital practices and patient education on minimizing risk of introduction [23].

This study had some limitations viz., the study was dependent on patients鈥� self-reporting which was vulnerable to patient bias, toleration of the insect, and memory. Additionally, the data was collected from only public hospitals in the Faisalabad area limiting the applicability of the findings to the Punjab region. Private hospitals were not included in this study. These generally serve more affluent patient and may have offered an interesting comparison. Physical examination for bed bugs was also limited to the immediate vicinity of patients鈥� beds and chairs excluding waiting rooms, corridors and other public spaces. Finally, even though the study evaluated the frequency of bed bugs it did not consider prevention and treatment measures used by hospitals or patients which might have influenced the observed bed bug populations in this study.

Conclusions

The research showed significant infestations of the common bed bug C. lectularius in public hospitals in Faisalabad. The percentage of patients claimed to have seen bed bugs in hospitals was much higher than the overall observed prevalence of bed bugs in the public hospitals. Although nearly 29.43% of participants reported skin irritations a link to bed bug activity was inconclusive. However, it was noted that patient over the age of 41 were more prone to complaining about dermal irritation due to what they think might be bed bug feeding. More than 50% of patients had some prior knowledge of bed bugs, however management of the insects such as changing the bed linens or avoiding shared bedding was limited. To conclude issues raised by the study point to a need for improved surveillance and education of patients to avoid the introduction of bedding and other personal items from home when be admitted into hospital. On the basis of current study, it is recommended that future studies should include both public and private hospitals across different districts. They should assess bed bugs in all hospital areas and evaluate prevention and treatment measures. Reducing patient bias through objective data collection is also recommended.