Distribution of Parasites Detected in Stool Samples of Patients in Le Dantec University Hospital of Dakar, Senegal, from 2011 to 2015

To identify the parasites responsible for intestinal parasitic infections diagnosed at Le Dantec University Hospital of Dakar, distribution of parasites detected in stool samples of patients was studied. From 2011 to 2015, 2578 patients were included in the study. A direct examination and Ritchie technique were performed as parasite search techniques. In total, 408 samples were positive showing 440 intestinal parasites; this corresponds to prevalence of 15.8%. Parasites were detected in monoparasitism (85.7%) and multiparasitism (14.3%). The most common species found in monoparasitism were Entamoeba coli (38.9%), E. histolytica/dispar (12.7%), Giardia intestinalis (8%), and Ascaris lumbricoides (7.3%). The most common associations were A. lumbricoides-Trichuris trichiura (3.6%) and E. coli-G. intestinalis (2.7%). Nonhospitalized patients were significantly more affected with 65.4% compared to hospitalized counterparts; and also there were more men (50.7%) than women. With 67.4%, adults were the most affected age group, while the elderly were less affected with only 7% (p = 0.5). This study shows increasing prevalence of intestinal parasitic infections over the years. So health education should be promoted in addition to the already begun mass treatment program. This would help to limit or even halt the spread of these diseases.


Introduction
Intestinal parasitic infections are recognized as neglected tropical diseases [1]. They are a global health problem causing morbidity in 450 million people [2]. These infestations are particularly prevalent in disadvantaged communities, particularly in tropical and subtropical areas, because of their hot and humid climate and also because health conditions are often faulty and/or access to drinking water is more difficult [1,3]. Their prevalence depends on not only the geographical location but also various socioeconomic factors such as climate, hygiene, and age [4].
The objective of this study is to identify the parasite species responsible for intestinal parasitic infections diagnosed at Le Dantec University Hospital of Dakar, Senegal.

Patients and Methods
We carried out a retrospective and descriptive study at the parasitology and mycology laboratory of Le Dantec University Hospital of Dakar. Between 2011 and 2015, all patients received in the laboratory were included in the study for parasitological examination of stools with symptoms suggestive of intestinal parasitic infections.
The main collection tool was the bench registries specially designed for parasitological examination of stools. These registries collected information on age, sex, hospitalized or nonhospitalized status of the patients, and the year and the results of the examinations. The age was defined in four categories: children (below 15 years), young adults (15-30 years), elder adults (31-60 years), and elderly (over 60 years). Stool specimens were sent to the laboratory promptly after collection, in a plastic jar, for hospitalized patients; they were collected, in the laboratory itself, for the nonhospitalized patients. The stool was treated by two techniques: For statistical analysis, the data were saved with Microsoft Excel 2007 software and transferred to Epi Info 7 where they were processed. The significance level of statistical calculations was set at 5% ( value < 0.05).
The following formulas have made it possible to calculate the parasitic indices: (i) Simple parasitic index (SPI), which corresponds to the prevalence here, is equal to the percentage of parasitized subjects relative to the total parasitological examinations of stools carried out. (ii) Corrected parasitic index (CPI) is equal to the ratio of the number of parasites recorded on the number of total examinations multiplied by 100.

Characteristics of the Study Population.
A total of 2578 patients were included in the study with a sex ratio of 1.1. Patients' age ranged from 11 days to 91 years with a mean age of 28.56 years. The distribution of patients by age group was as follows: children, 723 (28%); young adults, 768 (29.8%); elder adults, 907 (35.2%); and elderly, 180 (7%).

Parasitic Indices and Evolution of Prevalence according to Years of Study.
Of the 2578 stool samples examined, 408 showed the presence of intestinal parasites in monoparasitism, biparasitism, or triparasitism, corresponding to a SPI or prevalence of 15.8%. Of these confirmed intestinal parasitic infections, 440 strains belonging to sixteen species of intestinal parasites, including seven protozoa and nine helminths, were counted as a CPI of 17%. The evolution of prevalence over the years showed a significantly increasing trend (p < 0.001) from 7.5% in 2011 to 29.2% in 2015. However, between 2012 and 2013, it decreased from 19.8 to 11.7% ( Figure 1).  With 67.4% of confirmed intestinal parasitic infections, adults (15-60 years) were the most affected age group with more elder adults (39%) than young adults (28.4%), while the elderly were less affected with only 6.1% ( Figure 2). However, this distribution according to age group was not significant ( = 0.96).
In biparasitism (13.6%), 60 parasites were identified with, first, associations between protozoa dominated by E. coli-G. intestinalis with 6 cases and E. coli-E. histolytica/dispar with 4 cases and then between helminths in which the only recovered association was that between A. lumbricoides and T. trichiura found 8 times; and finally for associations between protozoa and helminths, the most representative of which was that between A. lumbricoides and E. coli found 4 times (Table 2(b)).

Discussion
Intestinal parasitic infections are a global health problem because of their morbid nature. They are due to different species of parasites varying with period and geographical region. It is in this context that this study was carried out within the laboratory of parasitology and mycology of Le Journal of Tropical Medicine 3  [5] but also that found in a study of slaughterhouse workers in Dakar with 49.56% even if the latter may be classified among subjects at risk [6].
Elsewhere, but still in West Africa, a study among schoolchildren in three regions of Mauritania found 33.4% prevalence of intestinal parasitic infections [7].
In the Maghreb, prevalence of 68.1% was found in rural areas among schoolchildren in Morocco in 2009 [8].
These values, especially the last one, are very high above ours. However, these differences could be put into perspective, given that these cross-sectional studies had been carried out in a population aged between 5 and 15 years, where hygiene conditions remained much more precarious, especially with promiscuity.
This same trend was also observed in the South American intertropical area, with prevalence of 70.7% which was found in Brazil in 2005 [9].
On the contrary, in Turkey, the prevalence found (3.7%) by a study carried out between 2012 and 2014 was four times lower than ours [10]. This low prevalence may be justified by the fact that intestinal parasitic infections are more frequent in developing countries (30 to 60%) than in developed ones (≤2%) [11]. However, taking into account the distribution of prevalence by years, we note that, in 2011, with 3.7%, our result was exactly equal to that found in Turkey.
We found intestinal parasitic infections higher in women (50.7%) than in men (49.3%) but without significant difference ( = 0.96). An opposite trend with similar proportions was found in Malaysia in a study on intestinal protozoa with 51% of men versus 49% of women [12]. This undoubtedly shows that gender does not necessarily influence infestation by intestinal parasites.
Regarding hospitalized or nonhospitalized status, intestinal parasitic infections were significantly more frequent in nonhospitalized patients with 65.4% than in hospitalized patients with 34.6%. This same observation was made studying the epidemiological aspects of intestinal parasitic infections diagnosed at the Fann hospital in Dakar [5]. This observation can be explained on one hand by the fact that very often patients considered nonhospitalized (outpatients) are, for the majority, hospitalized in other structures without a laboratory of parasitology. So they are actually hospitalized patients. On the other hand, the aim of the parasitological examination in outpatients, in general, is to confirm intestinal parasitic infection before treatment unlike in hospitalized patients (inpatients) in whom, very often, the parasitological examination of stools could aim to rule out the hypothesis of intestinal parasitic infection.
The distribution of infestation according to age group was not significant in our series with a higher frequency of infestation in adults with 67.4% and lower frequency in the elderly with 6.1%; between the two groups were the children with 26.5%.
This same trend was observed for intestinal parasitic infections diagnosed at the Fann University Hospital in Dakar between 2006 and 2010 [5]. On the other hand, this distribution of intestinal parasitic infections according to age is contrary to what has been reported in Morocco, where patients under the age of 18 years were the most infected with 80%, while patients over 18 years were the least affected with only 20% [13].
The species found in our studies remain with a few exceptions, the same found throughout the world, although the specific species' prevalence may vary over time and from one region to another [13]. E. coli (38.9%), E. histolytica/dispar (12.7%), G. intestinalis (8%), and A. lumbricoides (7.3%) were the most found species in our series.
These same species have already been found among the predominant species by El Guamri et al. and Baba et al., respectively, in Morocco in 2009 and Mauritania in 2012 [7,13]. However, the order of distribution could be different.
E. coli was the most frequent parasite found with 38.9%. This may be justified by the commensal nature of this amoeba considered to be little or not pathogenic [14]. E. histolytica and G. intestinalis, both pathogenic, followed with 12.7% and 8%, respectively. They were found with similar proportions in Man in Côte d'Ivoire during a study of the prevalence of protozoa in students [14]. There, they were also found in association with a rate of 1.9% contrary to our study where they were not found together. The associations of protozoa which we found were dominated by E. coli-G. intestinalis (2.7%) and E. coli-E. histolytica (1.8%). Dhital et al. observed the latter association, with 1.7% in 2016 in Nepal [4].
Concerning helminths, a single association between helminths was found at 3.6% with A. lumbricoides associated with T. trichiura and especially associations between helminths and protozoa. The latter were also reported in Nepal in 2016 with 2 cases by Dhital et al. [4] who also found a triparasitism associating protozoa, while our study also found a triparasitism but with two helminths (A. lumbricoides and T. Trichiura) and a protozoan (E. histolytica/dispar).
The associations found in our study showed very often the species considered as little or not pathogenic as E. coli or T. intestinalis, which confirms the opportunistic and frequent character of these protozoan species which, in the presence of favorable factors, can increase in number and determine digestive disorders.

Conclusion
Intestinal parasitic infections are found in Dakar (Senegal) with low prevalence compared to those of the subregion but they have an increasing trend. The parasites responsible are both protozoa and helminths but with predominance of the first. They are found in monoparasitism, biparasitism, or triparasitism. The protozoa species remain dominated by E. coli considered as little or not pathogenic species followed by E. histolytica/dispar, whereas the most frequent helminths were A. lumbricoides and T. trichiura. So health education needs to be promoted in addition to the mass treatment program that has already begun. This would help to limit or even halt the spread of these diseases, which remain a burden in developing countries.

Conflicts of Interest
The authors declare that there are no conflicts of interest regarding the publication of this paper.