Abstract
Aim:
This study aimed to determine the distribution of enteric parasitic infections and related risk factors among rural communities of Guilan province, Northern Iran, and to compare the results with the situation in the past.
Background:
Intestinal parasitic infections are still considered as a major public health concern, particularly in human communities with poor economy and sanitation.
Methods:
This cross-sectional study was performed in rural areas of Masal and Shanderman district from February to December 2020. A total of 917 stool samples were collected and examined for presence of intestinal helminthes and protozoa using direct, formalin-ether and Kato-Katz techniques.
Results:
A total of 156 (17%) out of 917 examined individuals were infected with intestinal parasites. The overall prevalence of protozoa, helminths and mixed infections were 11.8% (108/917), 4.5% (41/917) and 0.8% (7/917), respectively. Blastocystis was the most prevalent intestinal protozoa (9.6%) followed by Giardia lamblia (1.9%), Endolimax nana (1.1%), E. coli (0.8%) and Entamoeba hartmani (0.1%). The highest prevalence of intestinal helminths belonged to Trichostongylus spp. (3.5%) and Strongyloides stercoralis (1.3%). Statistical analysis showed significant association between giardiasis and sex (P<0.03). On the other hand, prevalence of enteric helminths was influenced by close contact with livestock, keeping herbivorous animals at home, job, education, and consumption of uncooked vegetables (P<0.05).
Conclusion:
The findings indicate a decreasing trend in the prevalence of intestinal parasitic infections in Guilan province in comparison to the past few decades. Hookworm infections, which was very prevalent in the area, are now rare, while trichostrongylosis showed a high prevalence in rural residents of the study area.
Key Words: Intestinal parasites, Trichostrongyliasis, Risk factors, Guilan, Iran
Introduction
Parasites are responsible for hundred thousand of mortality in human populations, particularly those living in tropical and subtropical regions of the world (1). Intestinal parasitic infections (IPIs) are considered as a substantial globally public health problem, especially in underdeveloped and developing countries. About 1.45 billion people have been estimated to be infected with soil-transmitted helminths, resulting in 4.98 million years lived with disability (YLDs) and 5.18 million disability-adjusted life years (DALYs). The number of cases infected with Ascaris lumbricoides, Trichuris trichiura and hookworms (Necator americanus and Ancylostoma duodenale) in 2010 was reported as 819 million, 464.6 million and 438.9 million, respectively (2). The annual number of death has also been estimated as 10,500 for A. lumbricoides and 65,000 for hookworms (1). The global burden reported for soil transmitted helminthes in 2017 has been estimated at 1.9 million disability-adjusted life years (DALYs) (3).
Intestinal parasites are mainly prevalent among rural population of equatorial regions with warm and humid climate, where proper sanitation facilities are lacking. In such a situation, children are more influenced by the parasites compared to general population (1, 4, 5). Iron deficiency anemia, malnutrition, poor cognitive functions and learning ability, stunting of growth, malabsorption, and weight loss are among the most important consequences of intestinal parasitic infections, particularly in children (6-8).
Untreated drinking water, low socioeconomic status, poverty, poor sanitation, close proximity with animals, ignorance, eating unwashed vegetables, and contact with contaminated soil are major risk factors predisposing rural communities to intestinal parasitic infections (4, 5, 9-11).
During past decades, intestinal helminthic infections, soil-transmitted helminths in particular, have been reported with very high prevalence from different parts of Iran. Recent epidemiological studies indicate a very sharp decrease in prevalence of IPIs in the country with prevalence rate of less than 1% for most of them (12-15). Although the prevalence of most of intestinal helminthic infections such as hookworms, T. trichiura and A. lumbricoides has significantly decreased in recent decades, but Trichostrongylus species and Strongyloides stercoralis have been frequently reported in northern provinces of Iran (13, 14). Indeed, some protozoan parasites such as Giardia lamblia are still a major public health problem in the country (14).
Since, few studies have been conducted on the prevalence of IPIs in northern Iran, the present study aimed to determine the prevalence of IPIs and their risk factors in the rural residents of Masal and Shanderman district, located in Guilan province, northern Iran, to obtain a clear picture from the current status of parasitic infections in this area.
Methods
Ethics approval
This study was approved by the ethics committee of GUMS (IR.GUMS.REC.1396.270). Only the subjects with a signed consent form were included in the present study. In case of children the approval was obtained from their parents or legal guardians.
Study area
This cross-sectional study was performed from February 2018 to January 2019 in the rural community of Masal and Shanderman district (37º15′N to 37º29′N, 48º43′E to 49º11′E) (Figure 1). This district covers an area of 622 km2 and is located in western part of Guilan province. The study area constitutes of forested mountainous, foothill and plain areas with humid climate in the plain and semi-humid in mountainous regions.
Figure 1.
The study area. Masal is located in western part of Guilan province in northern Iran.
A total of 52000 people are estimated to live in this district, of which 25000 (48.1%) inhabitants reside in rural regions. Agriculture, mainly rice planting, is the main source of employment for people in plain areas and animal husbandry for those living in the mountainous regions. Mean annual temperature and rainfall of the study area are 16.1 C (-11 C to 35 C) and 1241 mm, respectively (https://en.climate-data.org/asia/iran/gilan/masal-51910/#climate-graph).
Study population
The sample size was calculated using the statistical formula, n=z2p(1-p)/d2, where n is the sample size, p is the estimated prevalence of intestinal parasites in the area, z is the standard score at a 95% confidence interval and d is the allowed relative error. The minimum sample size calculated for this study was 850 individuals. In order to compensate the anticipated loses during follow-up, the samples size was increased by 8% to final number of 917.
The rural population of Masal and Shanderman live in 7234 households in 86 villages (about 3.5 individuals per household), so for collecting the determined samples 262 households were randomly selected.
Samples collection and processing
Following coordination with the authorities of health center of study area, we referred to the villager’s houses and the protocol of the study and procedure of sample collection were clearly explained to the participants. A written consent form was provided to each person, to the parents in case of the children, and a predesigned questionnaire was administered to each participant to obtain demographic data (age, gender, occupation and level of education) and potential and personal risk factors such as eating raw vegetables, drinking untreated water, contact with contaminated soil, close proximity to domestic animals, washing hand before meals and after using toilets.
Thereafter, a pre-labeled screw capped plastic container was provided to each person and on the second day the stool samples were collected and confirmed by the participant name and number and immediately transferred to the parasitology laboratory of School of Medicine of Guilan University of Medical Sciences (GUMS). The stool samples were examined using formalin-ether concentration and Kato-Katz techniques. Direct wet smear was also used in the case of watery stool samples. One Kato-Katz smear and two 22 22 mm slides from formalin-ether concentrate were examined for each participant.
Statistical analysis
Statistical Package for Social Sciences (SPSS) version 22.0 was used for analyzing the collected data. The chi-square ( 2) test was used to determine whether demographic data, type of drinking water, close contact with livestock, eating raw vegetables, hygiene status, contact with contaminated soil, livestock raised at home and prevalence of pathogenic parasites were significant risk factors for intestinal parasitic infections. The differences were considered as significant when the P value was less than 0.05.
Results
A total of 917 individuals, aged 1-85 years (35.919.9) participated in this study, of which 45.3% (415.917) and 54.7% (502.917) were male and female, respectively. The study population was categorized in four age groups (<20, 20-39, 40-59 and >60-year-old). The numbers of participants in the age groups were 240 (26.2%), 271 (29.5%), 277 (30.2%) and 129 (14.1%) respectively. The highest prevalence rate of 27.1% (35.129) was seen in participants aged ≥60 and the lowest rate 9.7% (24.240) in individuals aged <20 years. A statistically significant difference was found between the infection with IPs and age groups of the individuals (P<0.0001)
The overall prevalence of IPIs was 17% (156.917) of which 4.5% (41.917), 11.8% (108.917) and 0.7% (7.917) belonged to helminthic, protozoan, and mixed infections, respectively. The prevalence rate was 18.1% (81/502) in females and 16.2% (75.415) in males. No statistically significant difference was found between IPIs and gender (P<0.43) (Table 1).
Table 1.
Prevalence of intestinal parasitic infections in rural areas of Guilan province, northern Iran, by demographic factors.
| Variables | Positive N (%) | Negative N (%) | P-value |
|---|---|---|---|
| Age group (yr) | 0.001 | ||
| <20 | 24 (9.7) | 216 (90.3) | |
| 20-39 | 43 (16.3) | 228 (84.1) | |
| 40-59 | 54 (19.5) | 223 (80.5) | |
| ≥60 | 35 (27.1) | 94 (72.9) | |
| Gender | 0.437 | ||
| Male | 75 (18.1) | 340 (81.9) | |
| Female | 81 (16.1) | 421 (83.9) | |
| Educational status | 0.059 | ||
| Illiterate | 64 (21.3) | 237 (78.7) | |
| Under diploma | 56 (15.8) | 298 (84.2) | |
| diploma | 26 (12.4) | 183 (87.6) | |
| postgraduate | 10 (18.9) | 43 (81.1) | |
| Occupation | 0.120 | ||
| Farmer and Shepherd | 16 (25) | 48 (75) | |
| Housekeeper | 59 (18.2) | 266 (81.8) | |
| Other | 81 (15.3) | 447 (84.7) | |
| Raw vegetable consumption | 0.882 | ||
| Daily | 32 (18) | 146 (82) | |
| Sometimes | 115 (16.9) | 565 (83.1) | |
| Never | 9 (16.3) | 50 (84.7) | |
| Water supply status | 0.153 | ||
| Untreated (well, mineral spring) | 18 (22.8) | 61 (77.2) | |
| Treated pipe water | 138 (16.5) | 700 (83.5) | |
| Livestock proximity | 0.043 | ||
| No | 51(13.9) | 315(86.1) | |
| Yes | 105(19.1) | 446(80.9) |
Considering the occupation, IPIs were most prevalent in farmers and ranchers with prevalence rate of 25% (16.64) followed by housewives 18.2% (59.325) and other occupations 15.3% (81/528). The difference between occupation and the infection rate of IPIs was not statistically significant (P<0.120).
According to the educational status, illiterate individuals had the higher prevalence rate at 21.3% (64.301) when compared to participants with higher educational level but this difference was not statistically significant (P<0.059).
By close proximity to livestock and/or livestock raised at home, the prevalence of intestinal infections was more frequent among participants with livestock contact at 19.1% (105.551) in comparison with those who denied livestock contact 13.9% (51.366). Statistical analysis verified the relationship between livestock contact and/or livestock raised at home with IPIs (P<0.043)
Concerning the type of drinking water, a higher prevalence of intestinal parasites was observed in people who drink untreated water from wells, springs and streams at 22.8% (18.79) compare to those who drink pipe water 16.5% (138.838). This difference was not statistically significant (P<0.153). Considering raw vegetable consumption, no significant differences were seen in relationship with IPIs (P<0.882) (Table 1).
Trichostrongylus spp. was the most frequently detected helminth with infection rate of 3.5% (32.917) in study population, followed by S. stercoralis at 1.3% (12.917). We also found 4 cases (0.4%) of Enterobius vermicularis and 1 case (0.1%) of Taenia saginata. The most prevalent protozoa were identified as Blastocystis 9.6% (88.917) and G. lamblia 1.9% (17.917). Three species of non-pathogenic protozoa were also identified including Endolimax nana 1.1% (10.917), Entamoeba coli 0.9% (8.917) and Entamoeba hartmani 0.1% (1.917) (Table 2).
Table 2.
Prevalence of different species of intestinal parasites in 917 inhabitants of rural areas of Guilan province, northern Iran.
| Parasite | Number | Percentage (%) |
|---|---|---|
| Giardia lamblia | 17 | 1.9 |
| Entamoeba coli | 8 | 0.9 |
| Entamoeba hartmani | 1 | 0.1 |
| Endolimax nana | 10 | 1.1 |
| Blastocystis sp | 88 | 9.6 |
| Trichostrongylus spp | 32 | 3.5 |
| Strongyloides stercoralis | 12 | 1.3 |
| Enterobius vermicularis | 4 | 0.4 |
| Taenia sp. | 1 | 0.1 |
| Total | 173 | 18.9 |
Risk factors associated with intestinal helminthic infections
Trichostrongyliasis
Thirty-two among 917 participants (3.5%) were found to be infected with Trichostrongylus spp. As far as we know this is the highest rate of infection in recent two decades in the country. Bivariate (chi-square) statistical analysis indicated that the demographic variables, age and gender were significantly associated with trichostrongylosis (P<0.002 and P<0.02, respectively). Close proximity with livestock and/or raising livestock at home was also significantly associated with Trichostrongylus infection (P<0.01). No statistically significant associations were observed between trichostrongylosis and eating fresh vegetables and education (Table 3).
Table 3.
Prevalence of infection with Trichostrongylus spp. in rural areas of Guilan province, northern Iran by demographic factors.
| Variables | Positive N (%) | Negative N (%) | P-value |
|---|---|---|---|
| Age group (yr) | 0.002 | ||
| <20 | 0 (0) | 248 (100) | |
| 20-39 | 13 (4.9) | 258 (95.1) | |
| 40-59 | 10 (3.6) | 267 (96.4) | |
| ≥60 | 9 (7) | 120 (93) | |
| Gender | 0.020 | ||
| Male | 11 (2.7) | 404(97.3) | |
| Female | 21 (4.2) | 481 (95.8) | |
| Occupation | 0.211 | ||
| Farmer and Shepherd | 2 (3.1) | 62 (96.9) | |
| Housekeeper | 16 (4.9) | 309 (95.1) | |
| Other | 14 (2.7) | 514 (97.3) | |
| Raw vegetable consumption | 0.135 | ||
| Yes | 32 (3.7) | 827 (96.3) | |
| No | 0 (0) | 58 (100) | |
| Livestock close contact | 0.013 | ||
| No | 6 (1.6) | 360 (98.4) | |
| Yes | 26 (4.7) | 525 (95.3) |
Strongyloidiasis
S. stercoralis was the second prevalent intestinal helminth among study population (1.3%; 12.917). Age, gender and occupation were identified as risk factors associated with strongyloidiasis using bivariate (chi-square) statistical analysis (P<0.0001, P<0.03 and P<0.04 respectively). No significant association was observed between S. stercoralis infection and education, source of drinking water, eating fresh vegetables, and close contact with livestock (Table 4).
Table 4.
Prevalence of infection with Strongyloides stercoralis in rural areas of Guilan province, northern Iran, according to the demographic factors.
| Variables | Positive N (%) | Negative N (%) | P-value |
|---|---|---|---|
| Age group (yr) | 0.001 | ||
| <20 | 0 (0) | 248 (100) | |
| 20-39 | 2 (0.7) | 269 (99.3) | |
| 40-59 | 1 (0.4) | 276 (99.6) | |
| ≥60 | 9 (7) | 120 (93) | |
| Gender | 0.037 | ||
| Male | 9 (2.2) | 406 (97.8) | |
| Female | 3 (0.6) | 499 (99.4) | |
| Occupation | 0.046 | ||
| Farmer and Shepherd | 3 (4.7) | 61 (95.3) | |
| Housekeeper | 3 (0.9) | 322 (99.1) | |
| Other | 6 (1.1) | 522 (98.9) | |
| Educational status | 0.050 | ||
| Illiterate | 8 (2.7) | 293 (97.3) | |
| Under diploma | 4 (1.9 | 358 (98.9) | |
| diploma | 0 (0.0) | 209 (100) | |
| postgraduate | 0 (0.0) | 53 (100) |
Risk factors associated with intestinal protozoan infections
Giardiasis
G. lamblia infection was the second intestinal protozoan infection (1.9%; 17.917) next to B. hominis (9.6%; 88.917). Among demographic variables sex was the only risk factor associated with giardiasis by using chi-square statistical analysis (P<0.03). No statistically significant associations were observed between giardiasis and age, source of drinking water, eating fresh vegetables, personal hygiene and, close proximity to livestock (Table 5).
Table 5.
Prevalence of infection with Giardia lamblia in rural areas of Guilan province, northern Iran by demographic factors.
| Variables | Positive N (%) | Negative N (%) | P-value |
|---|---|---|---|
| Age group (yr) | 0.235 | ||
| <20 | 5 (2.0) | 243 (98.0) | |
| 20-39 | 4 (1.5) | 259 (98.5) | |
| 40-59 | 8 (2.9) | 269 (97.1) | |
| >60 | 0 (0) | 129 (100) | |
| Gender | 0.034 | ||
| Male | 12 (2.9) | 403 (97.1) | |
| Female | 5 (1) | 497 (99) | |
| Occupation | 0.493 | ||
| Farmer and Shepherd | 2 (3.1) | 62 (96.9) | |
| Housekeeper | 4 (1.2) | 321 (98.8) | |
| Other | 11 (2.1) | 517 (97.9) | |
| Raw vegetable consumption | 0.940 | ||
| Yes | 16 (1.9) | 843 (98.1) | |
| No | 1 (1.7) | 57 (98.3) | |
| Water supply status | 0.180 | ||
| Untreated (well, mineral spring) | 3 (3.8) | 76 (96.2) | |
| Treated pipe water | 14 (1.7) | 824 (98.3) |
Discussion
It has been estimated that 1.45 billion people were globally infected only with soil-transmitted helminthes in 2010. Despite the significant reduction in the number of people infected with intestinal parasitic infections, in particular infections caused by soil-transmitted helminthes, the prevalence of these infections has remained highly endemic in tropical and subtropical areas of the world (2, 3). This reflects the fact that IPIs still have significant public health effects on human populations, so it is important to monitor the situation of these infections in order to determine the predisposing factors and implement the control strategies in endemic regions.
In recent decades a sharp decline was observed in the prevalence of intestinal parasitic infections particularly soil-transmitted helminthes in Iran (Table 6). This reduction is mainly due to the considerable improvement in economic and living conditions, health facilities, and personal hygiene, access to safe drinking water and health services and significant increase in the level of education of the Iranian people.
Table 6.
Comparative prevalence (%) of some intestinal helminthes in different provinces of Iran based on community-based studies in 1970s, 2005 and 2020s.
| Province | Intestinal helminthes | Refs | |||||
|---|---|---|---|---|---|---|---|
| Ascaris | Hookworms | Trichuris | Strongyloides | Trichostrongylus | Hymenolepis | ||
| 1970s | |||||||
| Azerbaijan | 56-93 | - | 10-76 | - | - | 0-17 | (62) |
| Khorasan Khorasan |
23-95 | - | 0-57 | - | - | 0-22 | (62) |
| 15-74 | - | 2-12 | - | - | 4-8 | (63) | |
| Isfahan | 62-98 | 5 | 29-32 | - | 69.5 | 4 | (63) |
| Khuzestan | 27-76 | 25-75 | 9-13 | - | 59-69 | 7-13 | (63) |
| Mazandaran | 14-58 | 2-76 | 6-78 | - | 2-7.5 | 3-13 | (63) |
| Kermanshah | 59-86 | - | 32-80 | - | 2-5 | - | (64) |
| Guilan | 4-38 | 29-63 | 19-57 | 5-9 | 3-20 | - | (65) |
| 2005 | |||||||
| Iran | 1.5 | <0.1 | 0.1 | - | 0.2 | - | (66) |
| 2020s | |||||||
| Khorasan | 0.55 | - | - | - | - | 6.7 | (67) |
| Golestan | 0.5 | 0.4 | - | - | - | 1.5 | (68) |
| Mazandaran Mazandaran |
- | - | - | 1.6 | 2.1 | - | (16) |
| - | 1.7 | 0.1 | 1.1 | 2.6 | 0.6 | (69) | |
| Kerman | 0.2 | - | - | - | 0.1 | 1.1 | (40) |
| Azerbaijan | 0.09 | - | - | - | ND | 0.03 | (70) |
| Guilan | - | 0.07 | 0.07 | 1.5 | 3.13 | - | (14) |
| Khuzestan | - | 0.1 | - | - | 0.5 | 0.4 | (71) |
| Hamadan | - | - | 0.4 | - | - | 0.9 | (72) |
According to the results of the present work 17% of the study populations were infected with intestinal parasites of which 4.5% belonged to helminthic, 11.8% to protozoan and 0.7% to mixed infections. In comparison to the past decades, the prevalence of some IPIs including ascariasis, trichuriasis and hook worm infections has sharply decreased in Guilan province, so that these infections are very rarely encountered. However, S. stercoralis and Trichostrongylus spp. are still prevalent in northern part of the country particularly in the study area (13, 14). It appears that the reduction in the prevalence of A. lumbricoides, T. trichiura and hook worms is related to the facts that (i) these parasites are mainly anthroponotic and animals have no critical role in their transmission (ii) mechanization of agriculture has decreased the human contact with soil (iii) chemical fertilizers are more attractive for villagers than night soil which was frequently used in the past (iv) whole rural population have access to health services (v) the majority of the villagers have a higher level of education, personal hygiene, economic condition and life facilities.
Despite the significant decrease in the prevalence of ascariasis, trichuriasis and hookworms, trichostrongyliasis and strongyloidiasis are still prevalent in Guilan province. Thirty-two among 917 participants (3.5%) were found to be infected with Trichostrongylus spp. and twelve (1.3%) with S. stercoralis. The prevalence of trichostrongyliasis in present study was the highest rate in Iran in last two decades. Based on literature, the highest rate of infection (2.1% and 2.6%) reported from other provinces before our study belonged to neighboring province of Mazandaran, located at eastern part of Guilan (16). The prevalence rate of the present study is also higher than those reported from Brazil (1.2%) (17) and southern Sudan (2.5%) (18), while significantly lower than that of Laos (36.9%) (19).
Up to the moment ten valid species of Trichostrongylus have been reported from livestock all over the country, nine of which have also been reported from humans (13, 20). Recent studies have indicated the zoonotic transmission of T. colubriformis, T. vitrinus, T. axei and T. longispicularis in Guilan province (13, 21). The high prevalence of trichostrongyliasis in the study area might be due to the close proximity of rural residents to their livestock and the potential for zoonotic transmission of Trichostrongylus spp. Bivariate (chi-square) statistical analysis identified a positive association between close proximity to livestock and trichostrongyliasis (P<0.003).
Both northern provinces of Iran (Guilan and Mazandaran), located at the southern littoral of Caspian Sea, are well recognized endemic regions for S. stercoralis in Iran. This dangerous parasite was the second most prevalent helminth in the study area (1.3%). This rate of infection is higher than the rate reported from Khuzestan province (0.47%) (22) and lower than that of Mazandaran province (1.6%) (16). Comparing to other parts of the world, the rate of infection in present study was higher than those reported from rural areas of Brazil (0.7%) (23); Cuba (0.7%) (24); Kenya (0.5%) (25) and Southern Thailand (0.9%) (26), while lower than the rates reported from Combodia (21%) (27), (44.7) (28), (48.6%) (29); China (11.7%) (30); Thailand (5%) (31); Brazil (5%) (32) and Ethiopia (20.7%) (33).
The auto-infection phenomena and presence of free-living cycle are considered as the main factors which lead to the survival of the parasite in human populations. This accompanied with soil contact, mainly through agricultural activities, expose local population to the infection caused by this pathogenic helminth. In addition, the zoonotic aspect of strongyloidiasis has recently been documented and transmission of S. stercoralis from dogs to humans been indicated using molecular genetic analyses (34, 35). On the other hand, dogs might be considered as a reservoir for human infection by S. stercoralis and this might be another factor for parasite survival in the nature. Bivariate statistical analysis indicated occupation and personal hygiene as the risk factors associated with strongyloidiasis (P<0.04 and P<0.002 respectively). Accordingly, the farmers have a higher risk for S. stercoralis infection through contact with contaminated soil.
As already mentioned, 12.5% of the studied population were infected by pathogenic and none pathogenic intestinal protozoa. B. hominis (9.6%) and G. lamblia (1.9%) were the most prevalent protozoa in the study area. The prevalence rate of G. lamblia in this study was higher than those reported in Ilam (0.5%) (36); Tehran (1.2%) (37) and Qazvin (1.6%) (38) Provinces and lower than the rates reported from Mazandaran (10.6%) (16); Chaharmahal & Bakhtiari (28.2%) (39); Kerman (7.8%) (40); Kordistan (4.1%) (41); Hamadan (10.9%) (42); Khuzestan (7.7%) (22) and Kohgiluyeh & Boyer-Ahmad (17.5%) (43) Provinces. The prevalence of this pathogenic protozoa in other countries, neighboring countries in particular, was very higher than that reported in the present study; Iraq (37%) (44), (30.9%) (45), (26.1%) (46); Turkey (18.1%) (47), (47.9%) (48); Pakistan (28.9%) (49); Afghanistan (41.9%) (50); Yemen (16.1%) (51), Saudi Arabia (11.5%) (52), India (14.4%) (53); Tajikestan (26.4%) (54); Brazil (11%) (55); Argentina (46.4%) (56); Peru (15.1%) (57); Ethiopia (13.2%) (58); Kenya (6%) (59); Sudan (9.7%) (60); and South Africa (9.9%) (61).
Conclusion
It appears that the current status of intestinal parasitic infections in Iran is quite different in comparison to the past. While the prevalence of soil-transmitted helminthes and intestinal protozoan infections has sharply decreased in almost all areas, human fascioliasis, strongyloidosis, and trichostrongylosis are frequently reporting from northern provinces of Guilan and Mazandaran. It appears that the significant reduction in the prevalence of intestinal parasitic infections in Iran might be associated with improvement in health facilities, personal hygiene, economic and living conditions, people access to safe drinking water and health services, using chemical fertilizer instead of night soil, presence of appropriate waste disposal systems, agricultural mechanization, significant increase in the level of education of the Iranian people and increasing public health awareness.
Conflict of interests
The authors report no conflicts of interest in this work.
References
- 1.Brooker S. Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers–a review. Int J Parasitol. 2010;40:1137–1144. doi: 10.1016/j.ijpara.2010.04.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasite Vectors . 2014;7:1–19. doi: 10.1186/1756-3305-7-37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.GBD 2017 DALYs, HALE Collaborators. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392:1859–1922. doi: 10.1016/S0140-6736(18)32335-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Hailegebriel T. Prevalence of intestinal parasitic infections and associated risk factors among students at Dona Berber primary school, Bahir Dar, Ethiopia. BMC Infect Dis. 2017;17:1–8. doi: 10.1186/s12879-017-2466-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.da Silva JV, Fontes G, Dos Santos CD, Dos Santos RV, da Rocha EM. Factors associated with gastrointestinal parasitic infections among young population in Northeast Brazil. Can J Infect Dis Med Microbiol. 2016;2016:6239434. doi: 10.1155/2016/6239434. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Lim Y, Romano N, Colin N, Chow S, Smith H. Intestinal parasitic infections amongst Orang Asli (indigenous) in Malaysia: has socioeconomic development alleviated the problem? Trop Biomed. 2009;26:110–122. [PubMed] [Google Scholar]
- 7.Oberhelman RA, Guerrero ES, Fernandez ML, Silio M, Mercado D, Comiskey N, Ihenacho G, Mera R. Correlations between intestinal parasitosis, physical growth, and psychomotor development among infants and children from rural Nicaragua. Am J Trop Med Hyg. 1998;58:470–475. doi: 10.4269/ajtmh.1998.58.470. [DOI] [PubMed] [Google Scholar]
- 8.Patel J, Gupta D, Rathi C, Parikh P, Ingle M, Sawant P. Uncommon presentation of Strongyloidiasis: chronic malabsorption, multiple small bowel strictures and appendicitis in HTLV-1 positive patient. Trop Gastroenterol. 2015;36:212–215. doi: 10.7869/tg.293. [DOI] [PubMed] [Google Scholar]
- 9.Liao CW, Chiu KC, Chiang IC, Cheng PC, Chuang TW, Kuo JH, et al. Prevalence and risk factors for intestinal parasitic infection in schoolchildren in Battambang, Cambodia. Am J Trop Med Hyg. 2017;96:583–588. doi: 10.4269/ajtmh.16-0681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Gyang VP, Chuang TW, Liao CW, Lee YL, Akinwale OP, Orok A, et al. Intestinal parasitic infections: current status and associated risk factors among school aged children in an archetypal African urban slum in Nigeria. J Microbiol Immunol Infect. 2019;52:106–113. doi: 10.1016/j.jmii.2016.09.005. [DOI] [PubMed] [Google Scholar]
- 11.Forson AO, Arthur I, Olu-Taiwo M, Glover KK, Pappoe-Ashong PJ, Ayeh-Kumi PF. Intestinal parasitic infections and risk factors: a cross-sectional survey of some school children in a suburb in Accra, Ghana. BMC Res Note. 2017;10:1–5. doi: 10.1186/s13104-017-2802-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Rokni M. The present status of human helminthic diseases in Iran. Annal Trop Med Parasitol. 2008;102:283–295. doi: 10.1179/136485908X300805. [DOI] [PubMed] [Google Scholar]
- 13.Sharifdini M, Derakhshani S, Alizadeh SA, Ghanbarzadeh L, Mirjalali H, Mobedi I, Saraei M. Molecular identification and phylogenetic analysis of human Trichostrongylus species from an endemic area of Iran. Act Trop. 2017;176:293–299. doi: 10.1016/j.actatropica.2017.07.001. [DOI] [PubMed] [Google Scholar]
- 14.Sharifdini M, Ghanbarzadeh L, Barikani A, Saraei M. Prevalence of intestinal parasites among rural inhabitants of Fouman, Guilan Province, Northern Iran with emphasis on Strongyloides stercoralis. Iran J Parasitol. 2020;15:91–100. [PMC free article] [PubMed] [Google Scholar]
- 15.Sharifdini M, Ghanbarzadeh L, Kouhestani-Maklavani N, Mirjalali H, Saraei M. Prevalence and molecular aspects of human hookworms in Guilan province, northern Iran. Iran J Parasitol. 2017;12:374. [PMC free article] [PubMed] [Google Scholar]
- 16.Daryani A, Sharif M, Nasrolahei M, Khalilian A, Mohammadi A, Barzegar G. Epidemiological survey of the prevalence of intestinal parasites among schoolchildren in Sari, northern Iran. Trans Royal Soc Trop Med Hyg. 2012;106:455–459. doi: 10.1016/j.trstmh.2012.05.010. [DOI] [PubMed] [Google Scholar]
- 17.Souza RP, Souza JN, Menezes JF, Alcântara LM, Soares NM, Aquino Teixeira MC. Human infection by Trichostrongylus spp in residents of urban areas of Salvador city, Bahia, Brazil. Biomédica. 2013;33:439–445. doi: 10.7705/biomedica.v33i3.770. [DOI] [PubMed] [Google Scholar]
- 18.Magambo J, Zeyhle E, Wachira T. Prevalence of intestinal parasites among children in southern Sudan. East African Med J. 1998;75:288–290. [PubMed] [Google Scholar]
- 19.Watthanakulpanich D, Pongvongsa T, Sanguankiat S, Nuamtanong S, Maipanich W, Yoonuan T, et al. Prevalence and clinical aspects of human Trichostrongylus colubriformis infection in Lao PDR. Act Trop. 2013;126:37–42. doi: 10.1016/j.actatropica.2013.01.002. [DOI] [PubMed] [Google Scholar]
- 20.Ghadirian E, Arfaa F. Present status of trichostrongyliasis in Iran. Am J Trop Med Hyg. 1975;24:935–941. doi: 10.4269/ajtmh.1975.24.935. [DOI] [PubMed] [Google Scholar]
- 21.Ashrafi K, Tahbaz A, Sharifdini M, Mas-Coma S. Familial Trichostrongylus infection misdiagnosed as acute fascioliasis. Emerg Infect Dis. 2015;21:1869. doi: 10.3201/eid2110.141392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Mowlavi G, MirAhmadi H, Rezaeian M, Kia E, Rokni M, Golestan B, et al. Prevalence of intestinal parasites in tribal parts of Khuzestan Province during 2005-07. Govaresh. 2008;12:219–228. [Google Scholar]
- 23.Barbosa CV, Barreto MM, Andrade RdJ, Sodré F, d’Avila-Levy CM, Peralta JM, et al. Intestinal parasite infections in a rural community of Rio de Janeiro (Brazil): prevalence and genetic diversity of Blastocystis subtypes. PLoS One. 2018;13:0193860. doi: 10.1371/journal.pone.0193860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Santos AP, Fernández FN, Sánchez RM, Cañete ID, Rodríguez M, Puebla LJ, et al. Prevalence and risk factors for intestinal parasitic infections in a rural community in “Consolación del Sur” municipality, Cuba. West Indian Med J. 2014;63:333. doi: 10.7727/wimj.2013.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Rop DC, Nyanchongi BO, Nyangeri J, Orucho VO. Risk factors associated with intestinal parasitic infections among inmates of Kisii prison, Kisii county, Kenya. BMC Res Note. 2016;9:1–10. doi: 10.1186/s13104-016-2191-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Punsawad C, Phasuk N, Bunratsami S, Thongtup K, Siripakonuaong N, Nongnaul S. Prevalence of intestinal parasitic infection and associated risk factors among village health volunteers in rural communities of southern Thailand. BMC Public Health. 2017;17:1–9. doi: 10.1186/s12889-017-4486-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Khieu V, Schär F, Marti H, Bless PJ, Char MC, Muth S, et al. Prevalence and risk factors of Strongyloides stercoralis in Takeo province, Cambodia. Parasite Vectors. 2014;7:1–8. doi: 10.1186/1756-3305-7-221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Khieu V, Schär F, Forrer A, Hattendorf J, Marti H, Duong S, et al. High prevalence and spatial distribution of Strongyloides stercoralis in rural Cambodia. PLoS Negl Trop Dis. 2014;8:2854. doi: 10.1371/journal.pntd.0002854. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Forrer A, Khieu V, Schär F, Vounatsou P, Chammartin F, Marti H, et al. Strongyloides stercoralis and hookworm co-infection: spatial distribution and determinants in Preah Vihear province, Cambodia. Parasite Vectors. 2018;11:1–13. doi: 10.1186/s13071-017-2604-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Steinmann P, Zhou XN, Du ZW, Jiang JY, Wang LB, Wang XZ, et al. Occurrence of Strongyloides stercoralis in Yunnan Province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis. 2007;1:75. doi: 10.1371/journal.pntd.0000075. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Suntaravitun P, Dokmaikaw A. Prevalence of intestinal parasites and associated risk factors for infection among rural communities of Chachoengsao Province, Thailand. Korean J Parasitol. 2018;56:33. doi: 10.3347/kjp.2018.56.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Naves MM, Costa-Cruz JM. High prevalence of Strongyloides stercoralis infection among the elderly in Brazil. Rev Instit Med Trop São Paulo. 2013;55:309–313. doi: 10.1590/S0036-46652013000500003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Amor A, Rodriguez E, Saugar JM, Arroyo A, López-Quintana B, Abera B, et al. High prevalence of Strongyloides stercoralis in school-aged children in a rural highland of north-western Ethiopia: the role of intensive diagnostic work-up. Parasite Vectors. 2016;9:1–8. doi: 10.1186/s13071-016-1912-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Jaleta TG, Zhou S, Bemm FM, Schär F, Khieu V, Muth S, et al. Different but overlapping populations of Strongyloides stercoralis in dogs and humans—Dogs as a possible source for zoonotic strongyloidiasis. PLoS Negl Trop Dis. 2017;11:0005752. doi: 10.1371/journal.pntd.0005752. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Nagayasu E, Aung MPPTHH, Hortiwakul T, Hino A, Tanaka T, Higashiarakawa M, et al. A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Sci Rep. 2017;7:4844. doi: 10.1038/s41598-017-05049-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Viesy S, Abdi J, Rezaei Z. What are hidden facts behind intestinal parasitic infections in Ilam city? Infect Disord Drug Targets. 2019;19:284–287. doi: 10.2174/1871526518666180508125418. [DOI] [PubMed] [Google Scholar]
- 37.Hemmati N, Razmjou E, Hashemi-Hafshejani S, Motevalian A, Akhlaghi L, Meamar AR. Prevalence and risk factors of human intestinal parasites in Roudehen, Tehran province, Iran. Iran J Parasitol. 2017;12:364. [PMC free article] [PubMed] [Google Scholar]
- 38.Sadeghi H, Borji H. A survey of intestinal parasites in a population in Qazvin, north of Iran. Asian Pac J Trop Dis. 2015;5:231–233. [Google Scholar]
- 39.Pestehchian N, Nazari M, Haghighi A, Salehi M, Yosefi HA, Khosravi N. Prevalence of intestinal parasitic infection among inhabitants and tribes of Chelgerd, Iran, 2008-2009. J Clin Diag Res. 2015;9:1–4. doi: 10.7860/JCDR/2015/11580.5879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Mahni MB, Rezaeian M, Kia EB, Raeisi A, Khanaliha K, Tarighi F, et al. Prevalence of intestinal parasitic infections in Jiroft, Kerman Province, Iran. Iran J Parasitol. 2016;11:232. [PMC free article] [PubMed] [Google Scholar]
- 41.Shahnazi M, Abdollahpour H, Alipour M, Sadeghi M, Saraei M, Hajialilo E, et al. Prevalence of intestinal parasites in food handlers of the city of Saqqez in 2016. J Parasit Dis. 2019;43:113–119. doi: 10.1007/s12639-018-1065-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Sedighi I, Asadi M, Olfat M, Maghsood AH. Prevalence and risk factors of Giardia lamblia and Blastocystis hominis infections in children under ten years old, Hamadan, Iran. Avicenna J Clin Microbiol Infect. 2015;2:22713–22713. [Google Scholar]
- 43.Sarkari B, Hosseini G, Motazedian MH, Fararouei M, Moshfe A. Prevalence and risk factors of intestinal protozoan infections: a population-based study in rural areas of Boyer-Ahmad district, Southwestern Iran. BMC Infect Dis. 2016;16:1–5. doi: 10.1186/s12879-016-2047-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Al-Naemy BS, Al-Kalak S, Rahemo ZI. The intestinal parasites of Bashiqa district, Nineveh governorate, Iraq. Int J Mol Zool. 2012:2. [Google Scholar]
- 45.Jarallah HM. Intestinal parasitic infections among rural villages in Basrah marshes regions. J Basrah Res Sci. 2012;38:40–43. [Google Scholar]
- 46.Al-Hamairy AK, Al-Mosaui AM, Al-Rubaea AH. Prevalence of parasitic infection and relationship with anemia in Al-Doullab village, Babylon province, Iraq. Egy J Exp Biol. 2013;1:300–309. [Google Scholar]
- 47.Ak M, Keleş E, Karacasu F, Pektaş B, Akkafa F, Özgür S, et al. The distribution of the intestinal parasitic diseases in the Southeast Anatolian (GAP=SEAP) region of Turkey. Parasitol Res. 2006;99:146–152. doi: 10.1007/s00436-006-0138-7. [DOI] [PubMed] [Google Scholar]
- 48.Doni NY, Gurses G, Simsek Z, Zeyrek FY. Prevalence and associated risk factors of intestial parasites among children of farm workers in the southeastern Anatolian region of Turkey. Annal Agricult Environ Med. 2015;22.:438–42. doi: 10.5604/12321966.1167709. [DOI] [PubMed] [Google Scholar]
- 49.Mehraj V, Hatcher J, Akhtar S, Rafique G, Beg MA. Prevalence and factors associated with intestinal parasitic infection among children in an urban slum of Karachi. PloS One. 2008;3:3680. doi: 10.1371/journal.pone.0003680. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Korzeniewski K, Augustynowicz A, Smoleń A, Lass A. Epidemiology of intestinal parasitic infections in school children in Ghazni province, eastern Afghanistan. Pakistan J Med Sci. 2015;31:1421. doi: 10.12669/pjms.316.8889. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Al-Mekhlafi AM, Abdul-Ghani R, Al-Eryani SM, Saif-Ali R, Mahdy MA. School-based prevalence of intestinal parasitic infections and associated risk factors in rural communities of Sana'a, Yemen. Act Trop. 2016;163:135–141. doi: 10.1016/j.actatropica.2016.08.009. [DOI] [PubMed] [Google Scholar]
- 52.Amer OH, Ashankyty IM, Haouas NAS. Prevalence of intestinal parasite infections among patients in local public hospitals of Hail, Northwestern Saudi Arabia. Asian Pac J Trop Med. 2016;9:44–48. doi: 10.1016/j.apjtm.2015.12.009. [DOI] [PubMed] [Google Scholar]
- 53.Dhanabal J, Selvadoss PP, Muthuswamy K. Comparative study of the prevalence of intestinal parasites in low socioeconomic areas from South Chennai, India. J Parasitol Res. 2014;2014:630968. doi: 10.1155/2014/630968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Matthys B, Bobieva M, Karimova G, Mengliboeva Z, Jean-Richard V, Hoimnazarova M, et al. Prevalence and risk factors of helminths and intestinal protozoa infections among children from primary schools in western Tajikistan. Parasite Vectors. 2011;4:1–13. doi: 10.1186/1756-3305-4-195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Seguí R, Muñoz-Antoli C, Klisiowicz DR, Oishi CY, Köster PC, de Lucio A, et al. Prevalence of intestinal parasites, with emphasis on the molecular epidemiology of Giardia duodenalis and Blastocystis sp in the Paranaguá Ba , Brazil: a community survey. Parasite Vectors. 2018;11:1–19. doi: 10.1186/s13071-018-3054-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Molina N, Pezzani B, Ciarmela M, Orden A, Rosa D, Apezteguía M, et al. Intestinal parasites and genotypes of Giardia intestinalis in school children from Berisso, Argentina. J Infect Develop Countr. 2011;5:527–534. doi: 10.3855/jidc.1660. [DOI] [PubMed] [Google Scholar]
- 57.Choi B, Kim B. Prevalence and risk factors of intestinal parasite infection among schoolchildren in the peripheral highland regions of Huanuco, Peru. Osong Public Health Res Perspectives. 2017;8:302. doi: 10.24171/j.phrp.2017.8.5.03. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Derso A, Nibret E, Munshea A. Prevalence of intestinal parasitic infections and associated risk factors among pregnant women attending antenatal care center at Felege Hiwot Referral Hospital, northwest Ethiopia. BMC Infect Dis. 2016;16:1–7. doi: 10.1186/s12879-016-1859-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Mbae CK, Nokes DJ, Mulinge E, Nyambura J, Waruru A, Kariuki S. Intestinal parasitic infections in children presenting with diarrhoea in outpatient and inpatient settings in an informal settlement of Nairobi, Kenya. BMC Infect Dis. 2013;13:1–11. doi: 10.1186/1471-2334-13-243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60.Babiker M, Ali bS, Ahmed E. Frequency of intestinal parasites among food-handlers in Khartoum, Sudan. EMHJ-East Mediterranean Health J. 2009;15:1098–1104. [PubMed] [Google Scholar]
- 61.Nxasana N, Baba K, Bhat V, Vasaikar S. Prevalence of intestinal parasites in primary school children of Mthatha, Eastern Cape province, South Africa. Annals Med Health Sci Res. 2013;3:511–516. doi: 10.4103/2141-9248.122064. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Sabbaghian H, Arfaa F. Prevalence and intensity of intestinal helminthiases in northwest and northeast of Iran. Act Med Iran. 1970;1:11–18. [Google Scholar]
- 63.Arfaa F. Present status of human helminthiasis in Iran. Trop Geographic Med. 1972;24:353–362. [PubMed] [Google Scholar]
- 64.Ghadirian E, Arfaa F, Missaghian G, Bahrani H. Prevalence of intestinal helminthiasis in Kermanshah City and some villages in the province. Iran J Public Health. 1973;2:90–101. [Google Scholar]
- 65.Alemi A, Arfaa F. Prevalence of intestinal helminthiasis in the rural area of gilan province (caspian littoral) Iran J Public Health. 1978;7:25–34. [Google Scholar]
- 66.Sayyari A, Imanzadeh F, Bagheri Yazdi S, Karami H, Yaghoobi M. Prevalence of intestinal parasitic infections in the Islamic Republic of Iran. EMHJ-East Mediterranean Health J. 2005;11:377–383. [PubMed] [Google Scholar]
- 67.Taheri F, Namakin K, Zarban A, Sharifzadeh G. Intestinal parasitic infection among school children in South Khorasan province, Iran. J Res Health Sci. 2011;11:45–50. [PubMed] [Google Scholar]
- 68.Masoumeh R, Farideh T, Mitra S, Heshmatollah T. Intestinal parasitic infection among school children in Golestan province, Iran. Pak J Biol Sci. 2012;15:1119–1125. doi: 10.3923/pjbs.2012.1119.1125. [DOI] [PubMed] [Google Scholar]
- 69.Gholipoor Z, Khazan H, Azargashb E, Youssefi MR, Rostami A. Prevalence and risk factors of intestinal parasite infections in Mazandaran province, North of Iran. Clin Epidemiol Global Health. 2020;8:17–20. [Google Scholar]
- 70.Kazemi E, Rostamkhani P, Hooshyar H. A survey on prevalence of intestinal parasites infections in patients referred to the public hospital in Khoy, West Azarbaijan province, Iran, 2014-2016. Avicenna J Clin Microbiol Infect. 2017;4:56114–56114. [Google Scholar]
- 71.Beiromvand M, Panabad E, Rafiei A. Status of intestinal parasitic infections among rural and urban populations, southwestern Iran. Asian Pacific J Trop Med. 2019;12:130. [Google Scholar]
- 72.Jafari R, Fallah M, Darani HY, Yousefi HA, Mohaghegh MA, Latifi M, et al. Prevalence of intestinal parasitic infections among rural inhabitants of Hamadan city, Iran, 2012. Avicenna J Clin Microbiol Infect. 2014;1:21445–21445. [Google Scholar]

