In the present study, a prevalence of papular urticaria of 20.3% was observed in children between 1 and 6 years of age. This prevalence is high in comparison to the prevalence reported in previous studies, and it could be due to several of those reports included children with a higher average age [13,14,15], and it has been reported a reduction in the immunological reaction to insect bite after the seventh year of life [2, 19].
Even though there are few published studies about the risk factors associated with papular urticaria, having pets at home has been proved a predisposing factor for insect bite dermatitis; another risk factor has been residing in an area of heavy insect infestation, warm weather, spring and the use of perfumes and colognes [20]. In contrast, 32.1% of the households confirmed the presence of at least one pet, but, pets at home were not a risk factor. In general, pets and rodents have been also considered a risk factor [21], especially on the Rattus norvegicus, Rattus rattus, Mus musculus, dogs, and cats have been collected species of Pulex irritans, Ctenocephalides catis, Ct. Cannis and Xenopsylla cheopis; highlighting the possibility the interchange of fleas in the hosts around the houses. However, surprisingly in our study, the rodents behaved as a protective factor in the in the bivariate analysis and it was discarded from the multivariate analysis. To our knowledge, this is the first study with the objective of identifying risk factors for papular urticaria caused by flea bite. We found that having a soil /earth floor in the main bedroom is a risk factor for the disease and it has been reported that dirty floors are a risk factor associated with FBPU due to the close association between these conditions and the presence of immature fleas feeding and continuing its metamorphosis under favorable environmental parameters [22].
A history of atopic dermatitis in siblings was found as other risk factors for FBPU; however, in the tropics, it is difficult to clearly diagnose atopic dermatitis [23], and also, it could be limited by recall as well a diagnostic bias. Others risk factors were the use of public transport for transportation of the children, the use of mattresses without springs or foam lining, and the detection of fleas inside the accommodation (Table 2). Among the risk factors, we would highlight the presence of fleas in view of the fact that patients attending the Pediatric Dermatology and Allergy division of the Fundación Santa Fe de Bogotá D.C. have showed papular urticaria immune and histopathological reactions when exposed to flea antigens [3, 16, 19]. These results support that fleas can be involved in those reactions of papular urticaria frequently diagnosed in this dermatological practice all year round.
Mosquitoes and bedbugs are other insects associated worldwide with papular urticaria [1], but only Culex quinquefasciatus has been reported in Bogotá D.C. [24]. The differentiation between mosquitoes and fleas bite is not totally accurate but just suggested by clinical identification of corporal distribution of the bites. However, in our study, we were able to discriminate between the skin reactions caused by bites insects and fleas, by assessing the clinical manifestations of the reactions, the presence of the papules in body areas where clothing fits snugly, such as the trunk and limbs. In only a few patients were exposed areas of the body extremities also affected. For flying insects such as mosquitoes, the usual sites of bite are the exposed areas of skin, with single lesions tending to be the majority of the cases [25]. On the contrary, the trunk may be involved in the case of bedbug bites and they may leave single or double bite marks [25]. Bedbug bites are usually multiple, painless and linear in configuration [1]. A row of three bedbug bites is sometimes referred to as the ‘breakfast, lunch, dinner’ sign [1, 26, 27]. Also a predilection for the eyelid has been reported in the case of bedbugs, perhaps because this area is the only one exposed when a child is sleeping [28]. Flea bite can sometimes also cause papules in groups of three [29], but in these reported cases the presence of papular urticaria due to flea bite was associated with the presence of pets [29,30,31]. As a limitation in the present study, information about the presence of mosquitoes or bedbugs inside the houses was not asked. Even though, household fleas and papular urticaria associated with their bites have been reported previously [29,30,31,32], this study reports for the first time the relationship between the presence of fleas in households and the clinical diagnosis of the disease demonstrated in Bogotá D.C. Fleas are highly adaptable to different environmental domiciliary conditions and a favorable weather conditions in Bogotá D.C., could make possible flea reproduction and growth in this region [33], as has been previously shown [16].
Our results also showed an association between public transportation and FBPU in Bogotá D.C. Different studies have reported the presence of fleas and other insects on board ships and aircraft [34, 35]. No literature has been published on fleas in public transportation in Bogotá D.C.; however, the presence of fleas in buses and other services has been well known. The continual flow of people in the available infrastructure will certainly favor the spread of fleas [36,37,38]. The presence of fleas associated with the type of flooring material (especially soil /earth floor) is consistent with difficulty maintaining hygienic conditions [38, 39]. In most cases, immature stages of fleas are found entirely off-host and feeding on organic matter that can be found on the soil floor of the burrow and/or the nest of the host [40]. These conditions provide immatures with the environmental conditions necessary for their postembryonic development [40]. In this study, housing with soil floors was associated with FBPU in Bogotá D.C., although the CI of 95% was wide because households presenting this characteristic were not very frequent. The negative phototactic responses as a positive geotropism characteristic of the larvae may help to explain the association between fleas and the material of mattresses. Protective and environmental conditions sought by the larvae can be found in the deepest part of rugs, mattresses and stuffed furniture [41, 42]. In 2005, Bogotá D.C. had 9.2% of the population with unsatisfied basic needs [43], and 24.8% of the population lived in conditions below the poverty line; besides, the city showed great contrasts between economic strata, ethnic-cultural groups and geographical areas [44]. Housing occupied by the poorest populations possesses dirt floors, indicating that poverty is strong enough to be selected as a risk factor associated with FBPU, as has been shown by Naafs 2006 in the case of urticaria papular associated with insect bites in the tropics [22]. Something similar is observed in Colombia between lack of sewerage and poverty [45, 46].
Atopic dermatitis in siblings was another factor associated with FBPU in our study (Table 2). Family history has always been considered an important risk factor for the development of allergic diseases such as asthma, allergic rhinitis and atopic dermatitis [47]. However, this study found no association between the presence of asthma and allergic rhinitis in children and their families with FBPU. As in other studies, atopic dermatitis may or may not be associated with asthma and/or allergic rhinitis [48]. On the other hand, other related arthropods with urticaria papular has been associated with allergic diseases such as mosquitoes and caddisflies [49]. Future studies might focus on the relationship between atopic dermatitis and FBPU. In accordance with the bivariate analysis results, the occurrence of the highest prevalence of papular urticaria in socioeconomic strata (one to three) in children living in households with soil floors in the main areas, and in those households had presence of fleas suggest a possible relationship of FBPU with adverse socioeconomic conditions. Multivariate analysis confirmed the strong statistical significance of the presence of fleas in housing and the mattress material, and also there was a high OR for soil floor in the main bedroom, although the CI was very wide (Table 4).
Together, these findings raise the possibility of a strong association between socioeconomic status in Bogotá D.C. and FBPU (Table 2). To confirm this association a rigorous socioeconomic stratification and housing typology should be prioritized in future studies. Although, in the field of dermatoses in Colombia, this is the first population-based, cross-sectional study carried out in this age group, some limitations of the study can be highlighted. For instance, it was not possible to establish a change over time for the risk factors, nor to include children in this age group who are not attending educational institutions. Finally, in our study, the protective factors for FBUP were Sewerage system, wooden floor, adjacent house and private transportation. It was found that the protective factors for insect bite dermatitis are the use of full sleeve clothes and keeping the doors and windows closed at night [43].
It is important to implement strategies in order to prevent and control the presence of fleas in housing, educational institutions and public transportation, as recommended by the World Health Organization [39]. Papular urticaria is a preventable disease and it is strongly recommended that school teachers, school nurses and family members are trained to recognize the symptoms of the disease, to carry out cleaning activities and to ask for control campaigns against fleas in schools and homes. At the level of policy makers, it is highly recommended to include in public health policies the control of fleas in public schools and public transportation in order to prevent the exposure of the children to fleas. In addition, all efforts carried out to reduce the level of poverty in the city and improve in living conditions of the citizens (sewerage and appropriate social housing) will be conducive to a decrease in the prevalence of papular urticaria in Bogotá D.C. as it has been reported in other countries [5, 14, 50]. An increase in skin diseases as a consequence of the deterioration in socioeconomic conditions has also been reported [51]. A reduction of fleas in Bogotá D.C. could have an effect on the prevalence of FBPU, as well as on the costs imposed on the health system as a consequence of the repeated treatments needed, as well as indirect costs caused by the absence from work of parents or caregivers.