The Prevalence of Intestinal Parasites and Associated Risk Factors Among Students of Jahrom University of Medical Sciences

1Department of Parasitology, Jahrom University of Medical Sciences, Jahrom, Iran 2Student Research Committee, School of Medicine, Jahrom University of Medical Sciences, Jahrom, Iran 3Department of Parasitology, School of Medicine, Jahrom University of Medical Sciences, Jahrom, Iran 4Department of Immunology and Microbiology, School of Medicine, Jahrom University of Medical Sciences, Jahrom, Iran Int J Enteric Pathog. 2017 November;5(4):121-126

an infection cycle where malnutrition and repeated infections lead to excess morbidity that can continue for several generations. 9People of all ages may be affected by the prevalence of parasitic infections; therefore, these infections are not specific to special periods.Interestingly, transmission possibilities of intestinal parasites increase in areas with high population density, such as garrisons and schools.Multiple intestinal parasites cause gastric symptoms.For instance, Giardia intestinalis, the former Giardia lamblia, is considered as the most prevalent protozoan parasite across the world which has affected almost 200 000 000 people currently. 10,11Another usual enteric protozoan is Blastocystis hominis whose parasitic traits are still controversial. 7It is believed that over 2 000 000 000 people (nearly one-third of the human population) are infected with intestinal parasites. 12,13lthough, the mortality associated with IPIs is low, the global number of related deaths is considerable, because of the extent of the complications. 14

Objectives
Consequently, determining the prevalence of the IPIs in crowded populations, such as university students that are in potential conditions for the transmission of infection to each other is critical.Given that there is no information on the prevalence of the intestinal parasites among the students of universities in the south of Iran, this study aimed to determine the prevalence and risk factors of infection among students of Jahrom University of Medical Sciences.

Sample Collection
This cross-sectional, population-based survey was conducted from September 2013 to February 2014.The study population consisted of 431 students of Jahrom University of Medical Sciences, an institute in the southern part of Iran.Simple random sampling method was used to select the students.We randomly selected 431 male and female students.After getting official permission from the university administration, consent forms were given to all the study students.Then, a questionnaire based on sociodemographic data (sex, age, education and socioeconomic level of parents, field of education, and living place) was designed.After interviewing, 3 stool samples were collected from each student in alternate days.

Parasitological Examination
The samples were immediately transported to a diagnostic laboratory.Then, the samples were examined for gastrointestinal parasites.Initially, the slides were prepared directly from each sample based on the wet mount method using saline as well as iodine, and slides were microscopically examined.Furthermore, all of the samples were examined using the formol-ether method.
Briefly, 5 g of each sample was diluted in 7 mL of 5% formaline and 3 mL ether, followed by centrifugation for 10 minutes.

Statistical Analysis
All analyses were done using SPSS for windows version 16.0 (SPSS, Chicago, IL, USA).Statistical difference for each independent variable was identified using the chisquare or student's t test.The variables (risk factors) and the prevalence of parasitic infection were compared using logistic regression analysis with an odds ratio and a confidence interval of 95%.A P value less than 0.05 were regarded as statistically significant.

Descriptive Characteristics
Demographic and socioeconomic data are shown in Table 1.A total of 1293 stool specimens were examined from 431 students in college (3 stool samples from each student in alternate days).The age range was 19-24 years for all students and the mean age was 21.62 ± 2.34 years.The students were classified based on age, and the results showed that the distribution was 107 for students aged <20 years (24.8%),217 for those aged 20-22 years (50.4%), and 107 for those aged ≥23 years (24.8%).

Prevalence of Intestinal Parasitic Infections
Our findings showed a 29% gastrointestinal parasitic infection among 431 students.Overall, the prevalence of infection with only 1 parasite species was 22.03%, the prevalence of infection with 2 parasites was 2.73%, and the prevalence of infection with 3 parasite species was 0.46%.In general, 4 distinct intestinal parasite species were observed.As it is shown in The prevalence of intestinal parasitism in individuals living in the dormitory was significantly higher than that in students living in a personal house (odds ratio [OR] = 1.6; 95% CI: 1.8; 2.6, P = 0.01).The prevalence of intestinal infections in individuals, whose fathers had elementary level of education, was higher than that in students, whose fathers had higher educational level, and this prevalence was statically significant (OR = 0.5; 95% CI: 0.3; 1.1, P = 0.02).Moreover, the rate of intestinal infections in males was significantly higher than that in females (OR = 1.5; 95% CI: 1.1; 2.1, P = 0.01).

Discussion
In this study, we investigated the overall rate of IPIs and the risk factors associated with IPIs among a number of students of Jahrom University of Medical Sciences, a medical institute in the southern part of Fars province, Iran.The prevalence of intestinal parasites was estimated to be 29%, from which the prevalence of helminth and protozoan infections were 0.7% and 28.3%, respectively.
Various studies have consistently demonstrated the widespread distribution of intestinal parasites in Iran [15][16][17][18][19] and other countries among different populations, 20,21 varying among different races and communities.Differences in the rate of infection in various studies could be due to the differences in target populations and the years in which these surveys were performed.
Comparing our findings with those recently reported for other populations of Iran, a slightly similar rate of IPI was revealed.Based on data collected in studies carried out in different parts of Iran, a 0%-5.8%prevalence of intestinal helminth parasite infections 15,22,23 was reported that indicated contradictory result with the findings of the present experiment on students (0.7%), which was lower than other studies on students in other institutes of Iran 24 and other countries. 25However, the current study was of further importance in comparison with other similar studies, because students of Jahrom University of Medical Sciences were studying in interrelated fields with direct correlations with universal health and this provided them with higher awareness compared to other groups; therefore, usual monitoring was found to be more critical.When there are multiple intestinal infections such as common IPIs (e.g.infections with B. hominis and G. lamblia), we can hypothesize the fact that many species of protozoa have probably the same route of transmission.For example, human can be infected with G. lamblia by water and possibly food, and like majority of prevalent parasites, person-to-person transmission is believed to be the primary mechanism of infection distribution in the community of students.Moreover, due to poor personal hygiene, some students may inadvertently be infected through food sources. 26On the other hand, the relatively high prevalence in these individuals could be explained by poor sanitary conditions, contaminated water supplies, and high density that in a recent study may be explained as the result of low awareness among the students regarding personal hygienic behaviors.
Our results also showed that gender of the students, living area and parents' level of education were significantly correlated with IPI.In our study, the prevalence was slightly higher in males (34.9%) than in females (24.4%), that was statistically a significant difference (P = 0.01).Several studies have reported a higher prevalence of infection in males than females, 17,19,27 whereas other studies have indicated the opposite findings. 15,18,28In the present study, infection was more common in the 20-22-year-old age group and was lower in the 20-yearold age group, but these data were not significant.Interestingly, age is an important risk factor for IPIs; our finding was similar to that reported in some previous surveys 24,29 and contradictory to some other reports. 9,15,16hese differences could be explained by considering the developed sanitary conditions and behaviors among students, who were acquainted with proper hygienic practices in their living places.Several other risk factors were significantly associated with IPIs.It was stated that parents' level of education was positively associated with the prevalence of pediatric infection, which the present report confirmed it (P=0.02).However, some studies reported a negative association in this regard. 302][33] This indicated that the level of awareness of parents is directly intertwined with raising the healthy students that were educated with educational intervention as an effective means in reducing parasitic prevalence.
The higher infection rate reported among students living in dormitory showed a statistically significant relationship, compared to those living in personal houses and rental properties (P = 0.01).This finding was not in line with that reported in previous surveys. 24,34This study also indicated that the high population density increased the possibility of IPIs.However, our observation did not suggest a statistically significant relationship between parasitic infection and either the students' field of education (P = 0.39) or mothers' educational level (P = 0.09).Furthermore, the present study showed low rates of helminths and relatively high rates of potentially pathogenic protozoan infections, such as G. lamblia among students.

Conclusion
As a matter of fact, pathogenic IPIs among students of medical universities should be frequently monitored because of their direct relationship to the health of the community; however, there has been little investigations done on this group.Therefore, it is suggested that these students take a set of personal hygienic programs and behaviors.And in doing so, there exists a need to promote the mass scale health conditions to raise awareness about health and hygiene.However, further prospective studies should be conducted before coming to any conclusion.

Table 1 .
Demographic Characteristics of Participants in the Project at Jahrom University of Medical Sciences, Southern Iran, 2013-2014

Table 2
Probable Relationship of Independent Variables With Intestinal Parasitic InfectionsAs it is declared in Table3, there were several factors related to intestinal parasitism including parents' educational level, place of residence, gender, and other risk factors.

Table 2 .
Prevalence of Single Parasitism and Polyparasitism Among 431 Participants in the Project at Jahrom University of Medical Sciences, Southern Iran, 2013-2014

Table 3 .
Univariate Analysis of Factors Associated With Intestinal Parasitic Infection Among Participants in the Project at Jahrom University of Medical Sciences, Southern Iran, 2013-2014