The transmission of intestinal parasites among a population is dependent firstly on the presence of infected individuals, and then for species that employ the fecal-oral route, on poor sanitation. Socioeconomic and behavioral factors in the population are also crucially important. In our study, we found that the prevalence of combined protozoan infections in the newly arrived immigrant workers to Qatar was significantly higher (12.1%) than that among immigrant workers who had previously visited Qatar (6.6%) and mostly had lived and worked in the city. The overall prevalence of helminth infections was lower than that of protozoan parasitic infections but the trend was in the same direction with 7.2% for the newly arrived and 4.9% for individuals who had previously visited Qatar. Analysis by univariate statistical models of the questionnaire completed by all subjects in the study revealed that personal and familial characteristics including religion, education, number of siblings and parent’s educational background, and environmental factors such as number of rooms in the house, type of floor and toilet facility, and household contents index, all played some role in influencing the prevalence of combined protozoan infection. Our data revealed also that only the mother’s educational level and the household contents index had a significant effect on the prevalence of enteric helminth infections, although no clear directional trend correlating with increasing or decreasing values of the index was identified. However, fitting univariate models does not allow the influence of confounding factors and their interactions to be identified, so in the second phase of our analysis, we fitted all the significant effects from phase 1 into multifactorial models and combined these with age class and region of origin, which had been shown in our earlier paper to have had an influence on parasitic infections in these same individuals [14]. This showed that many of the factors identified by univariate analysis are likely to have arisen through confounding interactions between the initially fitted factors. The resulting minimum sufficient models showed that the prevalence of combined helminth infections was influenced only by the host age class and the mother’s educational level. The prevalence of combined protozoan infections in contrast was affected by five factors that retained significance (age class, floor of the house, household contents index, father’s education, and the number of siblings).
An earlier study conducted in the Emirate of Sharjah was focused on intestinal protozoan infection rates among both immigrant workers and locals, and the infection rate here was reported as 7.7% [17]. The prevalence of protozoan infections in our study was higher at 11.7%. However, the prevalence of helminth infections in our study was marginally lower at 7.0%, and lower also compared to similar studies in the region [8, 18,19,20]. In addition, 17.8% of the study population carried at least one of the species (helminths + protozoa combined) that were identified.
Soil-transmitted helminth (STH) infections continue to plague large parts of the world with India known to be a significant contributor to the burden of disease [21]. STH infections are a significant health problem in Qatar given the huge number of immigrants from India and Nepal. In our earlier analyses of the prevalence of parasitic infections and their temporal trends among settled immigrants in Qatar [13], immigrants from western Asia were observed to harbor the highest prevalence of helminth infections whereas immigrants from most other regions lost their helminth burdens almost completely after acquiring residency permits. Most importantly, the prevalence of helminth infections in the period from 2005 to 2008, and then in subsequent years (2009–2011) showed a clear trend of declining prevalence in Qatar. In the current study, the lowest prevalence was observed for helminth infections among immigrants who had visited previously (4.9%). This trend of declining prevalence of intestinal parasitic infections has been reported previously as evidence of the success of Qatar’s policies [22], which demand that newcomers wishing to work and live in Qatar must undergo mandatory checks of their health in order to receive a Work Residence Permit. In addition, the efforts to introduce the usage of efficient latrines instead of open defecation, mass deworming programs, and improvements in water quality and sanitation in countries, where intestinal parasitic infections are endemic and which are the sources of the immigrant labour force in Qatar, have led to a reduction in the prevalence of these infections, as for example in India. A conducive climate for helminth transmission, rapid and unplanned urbanization, social practices of open defecation, and lack of community education and sanitation are some of the factors, which have impeded control of parasitic infections in India in the past [23]. However, India has undertaken two massive deworming programs, one starting in the year 2000 where a single dose of Albendazole and DEC was administered to communities in the filarial-endemic regions and another in 2015 covering 241 million children for the treatment of STH infections [24, 25]. These have been very successful in reducing the prevalence of helminth infections in the country [24, 25].
In the present study, a relatively high prevalence of protozoan parasitic infections (15%) was initially found in univariate models to be associated with the Hindu religion, but the influence of religion was not retained in models that took into account other factors and is likely therefore to be a consequence of the confounding effect of other markers that reflect the subjects living conditions in their country of origin. Our finding might be due to the fact that the Hindu community are composed of Indian and Nepalese nationals [26], among whom protozoan infections are highly endemic. On the other hand, no significant difference in the prevalence of helminth infections was observed between subjects practicing different religions, which may be due to massive deworming programs conducted in endemic countries.
In our study, we observed that the individual’s educational level and that of their parents also had an important influence on the prevalence of protozoan infections. Prevalence was highest among uneducated subjects (15.2%) and also among those whose parents were illiterate (14.6% in both cases) and this was a highly significant finding. There was also a trend of decreasing prevalence with increasing level of education. Other studies have shown also that a mother's literacy is an important socio-economic factor influencing parasite prevalence [27,28,29,30]. Another study has reported similar results to our study [31], with increasing parent’s educational level correlating with the declining prevalence of protozoan infections. We found a similar trend when examining the parents’ occupational levels, the prevalence of protozoan infections declining consistently with increasing father’s occupational level from no occupation (12.6%), blue collar workers (11.9%), and then white collar workers (5.3%). A similar continuous reduction in prevalence was observed also with the mother’s occupational level from no occupation (12.1%) to white collar workers (4.2%). In contrast, our analysis found no significant effects of occupational level on the prevalence of helminth infections, although there was a somewhat surprising finding in relation to the mother’s educational level, but this did not change consistently with increasing level of education. The highest prevalence of helminth infections was among the offspring of graduates.
In our analysis of the influence of environmental factors in the country of origin on protozoan and helminth infections, we observed that in general large families were more prone to infection. Although across the seven levels of house occupants detailed in Table 1, there were no significant differences, it is nevertheless interesting to note that helminth and protozoan infections were least prevalent among people living alone or in couples. Notably, the prevalence of protozoan infections increased from just 3.4% among people living alone or in couples, to over 10% in all other cases and a maximum of 13.7% in the case of 5 occupants in a household. Our results are consistent with Halpenny et al. [32] who found that the large families (with more than three children) were more likely to experience a high prevalence of intestinal parasitic infections and higher co-infection patterns with multiple species, and these are likely to be attributable to overcrowding conditions in households [32]. In addition, we found the highest prevalence of protozoan infections among people who lived in houses with only soil as the floor (18.9%). Considering other possible household deficiencies that may enhance transmission of parasites between household inhabitants, and hence lead to higher prevalence, water and sanitization are two such key components. Access to clean water and efficient sanitary facilities within or in proximity to the household are essential to prevent deleterious effects on the health of inhabitants. In our study, the prevalence of protozoan infections was highest among individuals whose only supply of drinking water was directly from a local river (16.7%), or who exploited water from an uncovered well (13.4%). However, perhaps unexpectedly, even those who had access to a tap indoors, were also subject to a relatively high risk of protozoan infection, in this case being 13.6%, which indicates perhaps that the water supplies in these countries are contaminated. Interestingly, those who relied primarily on bottled water and/or used a covered well were less likely to be infected. The prevalence of helminth infections was also relatively high among individuals drinking river water (9.3%).
The prevalence and control of STH and protozoan infections are inextricably linked to water quality, sanitation, hygiene practices and the socio-economic status of communities in regions where these parasites are endemic [33]. Studies have shown that improved water quality, efficient sanitary facilities, and good hygiene practice, all contribute significantly to preventing diarrhea, morbidity, and mortality caused by protozoa and soil transmitted helminth in low- and middle-income countries [34]. Therefore, household access to clean tap water, safe disposal of excreta (for example use of flushing toilets instead of open defecation) and education about good hygiene practice are crucially important for targeted interventions aimed at reducing the incidence of intestinal parasitic infections [33, 35, 36]. The vulnerability of drinking water supply systems to contamination by pathogens and the consequent increase of risk of waterborne diseases have been highlighted in several studies [37, 38]. In addition, the protection of drinking water from these protozoa is a serious problem for water supply organizations around the world. Cryptosporidium and Giardia remain the two most important water pathogens that could not be eradicated until relatively recently [34]. Giardia is an anaerobic flagellated protozoa capable of encysting through a complex process of cyst wall formation [39], with this infective form being resistant to common disinfection controls such as chlorine and chloramines [40].
Since the intestinal helminths and protozoa studied in the current work are all dependent on fecal-oral transmission, the proper, safe and efficient management of feces and its disposal are key issues. When the surrounding environment is contaminated with feces, the magnitude of the problem may seem overwhelming [41,42,43,44]. Pit latrines are often recommended as an important step away from open defecation in the bush, but in our study, we observed that 13.9% of individuals who use pit latrines in their home country suffered from protozoan infection, a figure that is significantly higher than the prevalence among those using flushing toilets, and even open defecation. Throughout the world, there is considerable variation in the use of different types of toilets. Approximately 1.77 billion people around the world use pit latrines as the primary means of sanitation. Pit latrines are the simplest and most inexpensive form of improved sanitation, but they have to be maintained carefully to avoid infections. Pit latrines usually lack a physical barrier, such as concrete, between stored excrement and soil and/or groundwater [45]. In some countries where pit latrines are common, more than two billion people use groundwater as a source of drinking water [45]. Therefore, contaminants from pit latrines can also enter groundwater and create a threat to human health.
Our study is the first comprehensive study to address the issue of parasitic prevalence in an apparently healthy immigrant population in Qatar. However, our study suffered from certain limitations. First, laboratory diagnosis of intestinal parasitic infection (IPI) was based on a single stool examination, which could have underestimated the prevalence, as optimal laboratory diagnosis of IPIs requires the examination of at least three stool specimens collected over several days [46], but clearly this was just not possible in our study. However, more recent studies have suggested that one or two stool samples will detect up to 90% of the protozoa present [47, 48].