Skip to main content
Download PDF

A large-scale study on the prevalence of intestinal parasites in patients referred to medical laboratories in Urmia, Northwest Iran

BMC Gastroenterology volume 23, Article number: 322 (2023) Cite this article

Abstract

Introduction

Intestinal parasitic infections (IPIs), caused by helminths and protozoans, are among the most prevalent infections in humans in developing countries. This study aimed to determine the prevalence of IPIs in patients referred to three educational and medical centers affiliated with Urmia University of Medical Sciences in Urmia.

Materials and methods

In this cross-sectional study, 2845 stool samples, including 2174 (76.4%) males and 671 (23.6%) females, were collected from patients referred to Imam Khomeini and Shahid Motahhari hospitals and Shahid Nikkhah Health Center in Urmia, Northwest Iran, from January 2020 to February 2022. The microscopic examination for IPIs was carried out using the wet mount method, and the hard-to-identify samples were stained by trichrome for accurate identification of protozoa. For diagnosis of infections by coccidian parasites modified Ziehl-Neelsen (mZN) staining was used.

Results

Based on the results, two hundred nine intestinal parasites were identified in 184 out of 2845 (6.5%) patients of which 136 out of 2174 males (6.3%) and 48 out of 671 females (7.2%) were positive. Some patients had tested positive for multiple protozoa. The observed intestinal protozoa are as follows: Blastocystis spp. 118 (4.1%), Endolimax Nana 42 (1.5%), Entamoeba coli 24 (0.8%), Giardia lamblia 13 (0.5%), Cryptosporidium spp. 6 (0.2%), Iodamoeba butschlii 3 (0.1%), Chilomastix mesnili 2 (0.1%), and an accidentally detected helminthic infection Enterobius vermicularis 1 (0.05%).

Conclusion

According to the results, the most prevalent IPIs in West Azerbaijan Province are caused by Blastocystis spp., and Giardia lamblia. Most intestinal protozoa observed in the study were nonpathogenic and commensal, which shows water or food contamination in the area. Thus, medical technologists in the parasitology section must be trained and aware of IPIs in medical laboratories.

Peer Review reports

Introduction

Intestinal parasite infections are a major public health concern, especially in low- and middle-income countries [1]. Intestinal parasitic infections (IPIs) morbidities differ among individuals, depending on parasite factors such as the type, load, and intensity of intestinal parasites [2,3,4] and host factors especially age and nutritional status [4]. Intestinal parasites are common among school-aged children [2,3,4,5]. Lack of soap for handwashing [4], safe water, and sanitation are thought to be important risk factors for acquiring IPIs [2].

Intestinal parasites are abundant and infect millions of people all around the globe in the tropics and developing countries. However the potential transmission of intestinal parasites in developed countries and temperate zones has recently become problematic, especially among immigrants, returning travelers, and humans with immune system disorders [1].

Currently, on a global scale, age-specific mortality has gradually improved over the past 35 years; this pattern of overall development has been sustained in the past decade [6]. IPIs also declined dramatically during recent decades, mostly because of increased hygienic status, health education, and sanitation [7], even in African developing countries the decline in parasitic infections is noticeable [8].

One of the very important complications regarding intestinal parasites, especially intestinal helminths, is the nutritional effect, and growth retardation in children. These effects depend on the species of parasite, coinfection with multiple parasites, the duration of infection, and the load of worms. The influence of infections on different individuals also depends on the nutritional status of the host. Treating helminthic infections can lead to improvements in nutritional status and consequently in growth [2]. Based on what was discussed formerly, the diagnosis of IPIs is crucial and it is prerequired for treatment. On the other hand, because of the declining trend of most parasitic infections, having new updates on the prevalence of these infections in every region will help physicians and healthcare authorities to be aware of the situation in their region. Thus, the present study aimed to determine the prevalence of IPIs in a large group of patients referred to three healthcare facilities in Urmia, Northwest Iran.

Materials and methods

Samples collection

In this cross-sectional study, 2845 stool samples were collected from patients referred from different regions of West Azerbaijan Province to Imam Khomeini and Shahid Motahhari hospitals and Shahid Nikkhah Health Center in Urmia, Northwest Iran, from January 2020 to February 2022. Patients were informed about the study and a questionnaire of demographic variables was cpmpleted by interviewing every patient. The collected stool samples were transferred to the parasitology laboratory in the Department of Parasitology and Mycology, School of Medicine, Urmia University of Medical Sciences, Urmia, Iran, for further laboratory workouts.

COVID-19 pandemic

Two months after the initiation of sampling, COVID-19 quarantine began in Iran, thus 649 samples were collected before the COVID-19 pandemic quarantine and 2196 samples were collected during the pandemic quarantine.

Samples preparation

Stool samples were divided into two parts in a suitable stool container, one preserved by 4% formalin to be used for wet mount and modified cold Ziehl–Neelsen staining (mZN), and the other preserved in polyvinyl alcohol (PVA) to be used for trichrome staining when needed [9].

Microscopic examination

Samples were examined microscopically by the wet mount method with normal saline or Lugol’s iodine stain using 10X and 40X objectives. The identification was solely based on the morphological features of the parasites and those with unidentifiable organisms by the wet mount, were then stained with the trichrome staining method and investigated under the 100X objective [10]. For the diagnosis of coccidian parasites, mZN was used and studied with the 100X objective [11].

Limitations of the study

Stool samples were studied by the direct wet mount, trichrome, and mZN staining methods without formalin-ethyl-acetate concentration, and other species-specific methods, such as adhesive cellophane tape for detecting Enterobius vermicularis eggs or agar plate culture for Strongyloides stercoralis, could not be performed. Thus, we studied and reported the prevalence of intestinal infections/colonizations that the parasite could be detected by wet mount, trichrome staining, and mZN on stool specimens.

Data analyses

Data of findings from the microscopic examination and variables in the questionnaires were analyzed by IBM SPSS Statistics for Windows, version 23 (IBM Corp., Armonk, N.Y., USA) using chi-square, Mann-Whitney, t-, and logistic regression tests depending on the variable tested. Throughout the manuscript, we used infection when referring to a pathogenic parasite, colonization when referring to a nonpathogenic organism, and infection/colonization when referring to pathogenic and nonpathogenic organisms together.

Results

Over two years, 2845 stool samples were collected, including 2174 (76.4%) males and 671 (23.6%) females with an age range of 1–87 years and a mean age of 32.86 years. Stool examination (wet mount with saline and Lugol’s iodine, trichrome, and mZN) resulted in 209 infections/colonizations in 184 out of 2845 humans (6.5%), among whom 136 out of 2174 males (6.3%), and 48 out of 671 females (7.2%) were positive (p = 0.409).

Total IPIs/C was more prevalent in patients aged 40–49 and 50–59 years than in patients aged 0–9 years, with odds ratios of 2.369 (p = 0.021) and 3.218 (p = 0.002), respectively. The seasonal prevalence showed the highest rates in winter, and the prevalence was significantly lower in summer and fall than in winter, with the odds ratio of 0.528 and 0.564, respectively (P = 0.02). The prevalence of IPIs/Cs was higher in diarrheic patients than in those with normal stool (OR = 3.613; P = 0.002) (Table 1).

Table 1 Odds ratios estimated for total IPIs/Cs among sexes, age groups, habitat, season, COVID-19 pandemic period, and stool consistency. The odds ratio is calculated for being positive
Full size table

The observed intestinal protozoa in order from highest to lowest frequency are as follows: Blastocystis spp. 118 (4.1%), Endolimax nana 42 (1.5%), Entamoeba coli 24 (0.8%), Giardia lamblia 13 (0.5%), Cryptosporidium spp. 6 (0.2%), Iodamoeba butschlii 3 (0.1%), Chilomastix mesnili 2 (0.1%), and an accidentally detected helminth Enterobius vermicularis 1 (0.05%). No other parasitic elements other than the mentioned ones were detected (Table 2).

Table 2 Odds ratio estimated for being positive in different observed intestinal protozoa among sexes, age groups, habitats, and seasons. The chi-square test was performed on 2 × 2 tables yet for the variables with more than two variants, a binary logistic regression test was used to estimate the P value
Full size table

Cryptosporidiosis was observed only in patients with diarrhea and loose stool. No statistically significant difference was observed solely for other observed protozoa with the consistency of stool specimens (Table 3).

Table 3 Odds ratio estimated for stool consistency among different IPIs/Cs using binary logistic regression test
Full size table

A fraction of samples were collected before the quarantine during the COVID-19 pandemic, 649 out of 2845 samples (22.8%). The prevalence of intestinal protozoa was not significantly different in the pre- and post-COVID-19 periods, yet E. nana was more prevalent in the post-COVID-19 period than in the pre-COVID-19 period (OR = 16.66; P = 0.005) (Table 4).

Table 4 Odds ratios and P values estimated for different IPIs/Cs in the pre- and post-COVID-19 periods. The odds ratios were calculated for being negative for each infection and can be inversed by 1 ÷ OR
Full size table

Considering coinfections, 21 out of 184 patients (11.41%) had mixed infections/colonizations with two (81%) or three (19%) protozoa. There was no patient coinfected by Cryptosporidium with other parasites and all six patients had a single infection. The most frequent coinfections/colonizations in order from the highest to lowest were as follows: E. coli-Blastocystis spp., Blastocystis spp.-G. lamblia, E. nana-E. coli, E. nana-E. coli-Blastocystis spp., and E. nana-Blastocystis spp. (Table 5).

Table 5 The observed mixed infections among the 2845 studied humans
Full size table

The mean age of the patients with IPIs/C (35.75 years) was significantly higher (p = 0.005) than that of the noninfected patients (32.67 years) when tested by a nonparametric Mann-Whitney test.

Discussion

In the present study, a considerable fraction (6.5%) of humans referred to health care facilities of Urmia University of Medical Sciences, in Urmia had IPIs/Cs, however; some of the observed organisms were pathogenic, and some were nonpathogenic. The patients were referred from different regions of West Azerbaijan Province. The observed IPIs/Cs in order from highest to lowest were Blastocystis spp., Endolimax nana, Entamoeba coli, Giardia lamblia, Cryptosporidium spp., Iodamoeba butschlii, Chilomastix mesnili, and Enterobius vermicularis. As is obvious, intestinal helminthic infections were not observed except for one accidental case of E. vermicularis in stool, which is regularly analyzed either from adhesive cellophane tape or swab samples [12] that were not performed in this study. All other observed ones were protozoa, which are mostly transmitted by the fecal-oral route. Some of the observed infections are known to be associated with diarrhea such as giardiasis and cryptosporidiosis [13]. Other important parasites, such as Entamoeba histolytica, intestinal soil-transmitted helminths, intestinal tapeworms, and hepatic and intestinal trematodes were not observed in the patients using stool examination, which is very promising because in past decades, intestinal parasitic infections were highly prevalent in Iran [14,15,16] and in Urmia [17, 18]. However; in the present study direct stool samples were not concentrated by any method. Considering that the concentration method increases the sensitivity of detecting some parasitic infections, there may be a probability that some IPIs were underreported by the wet mount technique [19].

Hazrati-Tapeh et al. (2010) studied the prevalence of intestinal parasitic infections among mentally disabled children and adults in Urmia, the same region as the present study, but in a different population and by a more sensitive formalin-ether concentration method. They reported the overall prevalence of the infection as 20.4% among which 17.3% had protozoal infection and 3.1% had Enterobius vermicularis eggs. Their reported protozoa were as follows: Entamoeba coli 9.7%, Giardia lamblia 6.2%, Iodamoeba butschlii 5.7%, Blastocystis 4%, and Entamoeba histolytica/dispar 0.4%. Their reported protozoa are also reported in the present study, except E. histolytica/dispar [17]. However, their reported prevalences in most of the parasites (except Blastocystis) are considerably higher than in the present study with different studied populations. This dramatic decline in the prevalence of intestinal parasites is likely the result of the recent improvement in hygienic status, sanitation, and health education in society. The recent decline in the prevalence of intestinal parasites has also occurred in other parts of the country that parasitic infections were prevalent in the past [14,15,16,17,18]. This reduction is also true for Cryptosporidium spp. infection, as Nuri et al. (1991) reported 7.66% in patients with diarrhea [18], and Hazrati-Tapeh et al. (1970) reported 11.5% in renal transplant recipients and 3.88% in hemodialysis patients [20], which are noticeably higher than our findings, however in a different studied population.

Blastocystis is classified in phylum stramenopile and is the most common enteric protozoa in the human intestinal tract [21]. Currently, it is genetically classified into at least 34 subtypes (STs) [22]. ST1–9 and 12 are reported in humans and more than 90% of human infections are caused by ST1–4 [21]. Despite the high prevalence, the public health significance and pathogenicity remain uncertain. Blastocystis has been reported frequently in healthy individuals. It is also reported to decrease the population of gut microbiota e.g. Bifidobacterium and Lactobacillus [21, 23]. The zoonotic aspect of Blastocystis is also hypothesized and may contribute to some infections [21]. Blastocystis is also reported to be a neglected cause of urticaria and some skin disorders and is suggested to be treated in patients with urticaria or skin disorders who are infected by the parasite [24]. In the present study, similar to other reports [7, 25, 26] Blastocystis was the most prevalent parasite in the studied population, yet there was no relationship to abnormal stool consistency. However, in our previous study from Isfahan, the infection rate was significantly higher in patients with loose stool [25]. Additionally, in the present study, Blastocystis was more prevalent in winter than in the other seasons.

Endolimax nana is considered a nonpathogenic and commensal protozoon of the human colon that remains largely unexplored in terms of morphology, genetic diversity, taxonomy, host specificity, and epidemiology [27]. However, E. nana is rarely reported to be responsible for cases of diarrhea [27, 28], abdominal pain, polyarthritis [27], and urticaria [29, 30] in some individuals. Some reports considered Blastocystis and E. nana to be associated with diarrhea in children when they occur at a high prevalence and intensity [28]. In the present study, E. nana infection was ranked second in terms of prevalence, yet there was no association with diarrhea. The prevalence was significantly high during winter.

Entamoeba coli is also considered a nonpathogenic organism of the gastrointestinal tract of humans [31]. In 1991, E. coli was reported in 10 patients with diarrhea, which was resolved after treating the E. coli infection [32]. In the present study, E. coli infection was in the third rank in terms of prevalence, yet there was no association with diarrhea.

Giardiasis is caused by G. lamblia which is an intestinal protozoan flagellate that infects the upper small intestine and causes acute watery diarrhea, yet some infections may be asymptomatic. It is suggested that infection with Giardia can be protective against other diarrheal diseases. G. lamblia may also result in irritable bowel syndrome (IBS) and food allergies after clearance [33]. In the present study, giardiasis was the fourth most prevalent protozoan (0.5%), prevalent in summer and winter. The observed prevalence is either close to some other recent reports from Iran, for instance, Shiraz [7], or lower than the report from Roudehen in Tehran Province [34].

Cryptosporidium is a protozoan that is well known for its resistance to chlorination during water treatment. It is transmitted by the fecal-oral route through contaminated food or water, man-to-man or animal-to-man contact, and environmental exposure and resides in the small intestine of hosts. Acute gastrointestinal symptoms are usually self-limiting, but they could be problematic in immune deficiencies [35]. In the present study, all cases with cryptosporidiosis had loose (50%) or watery stool (50%), and no coinfection was observed with Cryptosporidium. The observed prevalence in Urmia is considerably lower than most of the previous reports from different regions of the country [36, 37] and Urmia [20, 38].

Enterobius vermicularis, or pinworm, is among the most prevalent nematode infections worldwide. Humans are the only natural host for E. vermicularis, and it is spread among people living in crowded environments directly through egg ingestion. The diagnosis of enterobiasis can be achieved by cellophane tape or pinworm paddle tests, in which adhesive tape is placed on the perianal area and then examined under a microscope to detect eggs. Stool examination is not recommended for the diagnosis of enterobiasis, yet eggs are rarely detectable in stool [39]. In the present study, an accidental case of enterobiasis was diagnosed by observation of eggs in the stool examination.

Salehi et al. (2020) carried out research on IPIs in 52 children with cancer in Ahvaz, Southwest Iran. They reported that 38.38% of their studied population was infected/colonized by a variety of intestinal parasites/commensals. Similar to the present study they reported Blastocystis (23%), Endolimax nana (7.7%), Entamoeba coli (1.92%), and Chilomastix mesnili (1.92%) as the most prevalent protozoa. However, they also reported Strongyloides stercoralis (3.84%) which was not detected in the present study. They concluded that Blastocystis and Endolimax nana are the most prevalent in individuals admitted to Baqaei2 Hospital of Ahvaz, Iran [26]. Comparing their reported prevalence with the present study shows that IPIs/Cs in Ahvaz in children with cancer are considerably higher than our results in Urmia.

Abbaszadeh et al. (2021) in a meta-analysis studied intestinal parasites among intellectually disabled individuals in Iran. They reported an overall pooled prevalence of 41% with a range of 21–68% across subgroups. The most prevalent reported parasites were Entamoeba coli (16.2%), Blastocystis spp. (12.2%), Giardia duodenalis (11.9%), and Enterobius vermicularis (11.3%) followed by Strongyloides stercoralis (10.9%) and Hymenolepis nana (2.8%) [40]. Based on the results of their study, IPIs are highly prevalent in intellectually disabled humans compared to our studied population (6.5%).

Teimouri et al. (2020) studied the prevalence of intestinal parasites among food handlers in Iran in a meta-analysis. Their findings showed the overall pooled prevalence of IPs as 19.3%. They reported a significantly higher prevalence of protozoan parasites (20%) compared to helminthic parasites (1.6%). The reported parasites were Giardia lamblia (5.2%), Entamoeba coli (5.0%), Blastocystis spp. (4.4%), Ascaris lumbricoides (1.4%), Enterobius vermicularis (0.9%), and Hymenolepis nana (0.5%). Additionally, food handlers with lower education were 20% more exposed to IPIs [41]. Based on their report, the prevalence of IPIs among food handlers in Iran is considerably high, approximately three times higher than that in our study population, which is a risk factor for spreading directly transmitted parasites in society.

Conclusion

According to the results, the most prevalent IPIs in West Azerbaijan Province are caused by Blastocystis spp., and Giardia lamblia; however, most intestinal protozoa observed in the study were nonpathogenic and commensal, which shows water or food contamination in the area. In terms of helminthic infections, no helminths were detected except for one accidental case of enterobiasis; thus, West Azerbaijan is in a decent condition compared to past studies in Urmia and other regions of the country. Furthermore, medical technologists in the parasitology section of medical laboratories and physicians must be trained and aware of the presence of intestinal parasites.

Data Availability

Results data (raw or analyzed) will be available and presented by contacting the corresponding author.

References

  1. Jong E. Intestinal parasites. Prim Care. 2002;29(4):857–77.

    Article  PubMed  Google Scholar 

  2. Hall A, Hewitt G, Tuffrey V, de Silva N. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr. 2008;4(Suppl 1):118–236.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sayasone S, Utzinger J, Akkhavong K, Odermatt P. Multiparasitism and intensity of helminth infections in relation to symptoms and nutritional status among children: a cross-sectional study in southern Lao People’s Democratic Republic. Acta Trop. 2015;141(Pt B):322–31.

    Article  PubMed  Google Scholar 

  4. Shrestha A, Schindler C, Odermatt P, Gerold J, Erismann S, Sharma S, Koju R, Utzinger J, Cissé G. Intestinal parasite infections and associated risk factors among schoolchildren in Dolakha and Ramechhap districts, Nepal: a cross-sectional study. Parasit Vectors. 2018;11(1):532.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Njenga D, Mbugua AK, Okoyo C, Njenga SM. Intestinal parasite infections and Associated Risk factors among Pre-School aged children in Kibera Informal Settlement, Nairobi, Kenya. East Afr Health Res J. 2022;6(1):86–97.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Global regional. National life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the global burden of Disease Study 2015. Lancet. 2016;388(10053):1459–544.

    Article  Google Scholar 

  7. Teimouri A, Alimi R, Farsi S, Mikaeili F. Intestinal parasitic infections among patients referred to hospitals affiliated to Shiraz University of Medical Sciences, southern Iran: a retrospective study in pre- and post-COVID-19 pandemic. Environ Sci Pollut Res Int. 2022;29(24):36911–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Aliyo A, Geleto A. Trends of intestinal parasites among the patients attended at Yabelo General Hospital, Borena Zone, Southern Ethiopia. SAGE Open Med. 2022;10:20503121221143644.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Garcia LS. Collection, Preservation, and shipment of fecal specimens. Diagnostic Medical Parasitology. 6 ed.: Wiley; 2015.

  10. Garcia LS. Macroscopic and microscopic examination of fecal specimens. Diagnostic Medical Parasitology. 6 ed. Wiley; 2015.

  11. Smith H. Diagnostics. In: Cryptosporidium and Cryptosporidiosis 2nd edn. Edited by Fayer R, Xiao L. United States of America: CRC press; 2008: 187–188.

  12. Garcia LS. Examination of other specimens from the intestinal tract and the Urogenital System. Diagnostic Medical Parasitology. 6 edn.: Wiley; 2015.

  13. Haque R. Human intestinal parasites. J Health Popul Nutr. 2007;25(4):387–91.

    PubMed  PubMed Central  Google Scholar 

  14. Sayyari AA, Imanzadeh F, Bagheri Yazdi SA, Karami H, Yaghoobi M. Prevalence of intestinal parasitic infections in the Islamic Republic of Iran. East Mediterr Health J. 2005;11(3):377–83.

    CAS  PubMed  Google Scholar 

  15. Arfaa F, Ghadirian E. Epidemiology and mass-treatment of ascariasis in six rural communities in central Iran. Am J Trop Med Hyg. 1977;26(5 Pt 1):866–71.

    Article  CAS  PubMed  Google Scholar 

  16. Mohammad K, Zalie MR, Sirous S, Masjedi MR. Intestinal Parasites in Iran. Iran J Public Health. 1970;24(3–4):9–26.

    Google Scholar 

  17. Tappeh Kh H, Mohammadzadeh H, Rahim RN, Barazesh A, Khashaveh S, Taherkhani H. Prevalence of intestinal parasitic infections among mentally disabled children and adults of Urmia, Iran. Iran J Parasitol. 2010;5(2):60–4.

    PubMed  PubMed Central  Google Scholar 

  18. Nouri M, Moghadam A, Haghighatnia H. Cryptosporidium infection in human diarrhoea patients in West Azerbaijan, Iran. Med J Islamic Repub Iran. 1991;5(1):35–8.

    Google Scholar 

  19. Demeke G, Fenta A, Dilnessa T. Evaluation of Wet Mount and Concentration techniques of Stool Examination for Intestinal Parasites Identification at Debre Markos Comprehensive Specialized Hospital, Ethiopia. Infect Drug Resist. 2021;14:1357–62.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Tappeh KHH, Gharavi MJ, Makhdoumi K, Rahbar M, Taghizadeh A. Prevalence of Cryptosporidium spp. Infection in renal transplant and hemodialysis patients. Iran J Public Health 1970, 35(3).

  21. Stensvold CR, Tan KSW, Clark CG, Blastocystis. Trends Parasitol. 2020;36(3):315–6.

    Article  PubMed  Google Scholar 

  22. Jiménez P, Muñoz M, Ramírez JD. An update on the distribution of Blastocystis subtypes in the Americas. Heliyon. 2022;8(12):e12592.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Deng L, Wojciech L, Gascoigne NRJ, Peng G, Tan KSW. New insights into the interactions between Blastocystis, the gut microbiota, and host immunity. PLoS Pathog. 2021;17(2):e1009253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bahrami F, Babaei E, Badirzadeh A, Riabi TR, Abdoli A. Blastocystis, urticaria, and skin disorders: review of the current evidences. Eur J Clin Microbiol Infect Dis. 2020;39(6):1027–42.

    Article  PubMed  Google Scholar 

  25. Jafari R, Sharifi F, Bagherpour B, Safari M. Prevalence of intestinal parasites in Isfahan city, central Iran, 2014. J Parasit Dis. 2016;40(3):679–82.

    Article  PubMed  Google Scholar 

  26. Salehi Kahyesh R, Alghasi A, Haddadi S, Sharhani A. Intestinal Parasites Infection in Children with Cancer in Ahvaz, Southwest Iran. Interdiscip Perspect Infect Dis 2020, 2020:8839740.

  27. Poulsen CS, Stensvold CR. Systematic review on Endolimax nana: a less well studied intestinal ameba. Trop Parasitol. 2016;6(1):8–29.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Graczyk TK, Shiff CK, Tamang L, Munsaka F, Beitin AM, Moss WJ. The association of Blastocystis hominis and Endolimax nana with diarrheal stools in zambian school-age children. Parasitol Res. 2005;98(1):38–43.

    Article  PubMed  Google Scholar 

  29. Veraldi S, Angileri L, Rossi LC, Nazzaro G. Endolimax nana and urticaria. J Infect Dev Ctries. 2020;14(3):321–2.

    Article  PubMed  Google Scholar 

  30. Veraldi S, Schianchi-Veraldi R, Gasparini G. Urticaria probably caused by Endolimax nana. Int J Dermatol. 1991;30(5):376.

    Article  CAS  PubMed  Google Scholar 

  31. Stensvold CR, Ascuña-Durand K, Chihi A, Belkessa S, Kurt Ö, El-Badry A, van der Giezen M, Clark CG. Further insight into the genetic diversity of Entamoeba coli and Entamoeba hartmanni. J Eukaryot Microbiol. 2023;70(2):e12949.

    Article  CAS  PubMed  Google Scholar 

  32. Wahlgren M. Entamoeba coli as cause of diarrhoea? Lancet. 1991;337(8742):675.

    Article  CAS  PubMed  Google Scholar 

  33. Einarsson E, Ma’ayeh S, Svärd SG. An up-date on Giardia and giardiasis. Curr Opin Microbiol. 2016;34:47–52.

    Article  PubMed  Google Scholar 

  34. 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(3):364–73.

    PubMed  PubMed Central  Google Scholar 

  35. Chalmers RM, Davies AP, Tyler K. Cryptosporidium. Microbiol (Reading). 2019;165(5):500–2.

    Article  CAS  Google Scholar 

  36. Mirzaei M. Prevalence of Cryptosporidium sp. infection in diarrheic and non-diarrheic humans in Iran. Korean J Parasitol. 2007;45(2):133–7.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Berahmat R, Spotin A, Ahmadpour E, Mahami-Oskouei M, Rezamand A, Aminisani N, Ghojazadeh M, Ghoyounchi R, Mikaeili-Galeh T. Human cryptosporidiosis in Iran: a systematic review and meta-analysis. Parasitol Res. 2017;116(4):1111–28.

    Article  PubMed  Google Scholar 

  38. Hazrati Tappeh K, Rahbar M, Hejazi S, Mostaghim M. Cryptosporidium in Children referred to Oncology Center of Urmia, Imam Khomeini Hospital, 2001 [Persian]. J Ardabil Univ Med Sci. 2005;5(4):327–32.

    Google Scholar 

  39. Rawla P. Enterobius Vermicularis. In: StatPearls [Internet] edn. Edited by Sharma S. Treasure Island (FL): StatPearls Publishing. Copyright © 2023, StatPearls Publishing LLC.; 2023.

  40. Abbaszadeh Afshar MJ, Mohebali M, Mohtasebi S, Teimouri A, Sedaghat B, Saberi R. Intestinal parasites among intellectually disabled individuals in Iran: a systematic review and meta-analysis. Gut Pathog. 2021;13(1):28.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Teimouri A, Keshavarz H, Mohtasebi S, Goudarzi F, Mikaeili F, Borjian A, Allahmoradi M, Yimam Y, Abbaszadeh Afshar MJ. Intestinal parasites among food handlers in Iran: a systematic review and meta-analysis. Food Microbiol. 2021;95:103703.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the Vice-Chancellor of Research and Technology of Urmia University of Medical Sciences, Urmia, Iran, for approval and financial support (Research no: 2683, ethical code: IR.UMSU.REC.1398.533) of this study and to Imam Khomeini and Shahid Motahhari hospitals, and Shahid Nikkhah Health Center for their help and contribution.

Funding

The present study was approved and financially supported by the Vice-Chancellor of Research and Technology of Urmia University of Medical Sciences, Urmia, Iran, under Research no 2683.

Author information

Authors and Affiliations

  1. Student Research Committee, Urmia University of Medical Sciences, Urmia, Iran

    Shiva Zeinali

  2. Department of Parasitology and Mycology, School of Medicine, Urmia University of Medical Sciences, Urmia, Iran

    Shiva Zeinali, Mahsa Rezgi, Morteza Gholinejad & Rasool Jafari

  3. Cellular and Molecular Research Center, Cellular and Molecular Medicine Research Institute, Urmia University of Medical Sciences, Urmia, Iran

    Rasool Jafari

Authors
  1. Shiva Zeinali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahsa Rezgi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Morteza Gholinejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rasool Jafari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.Z., M.R, and M.G collected samples, filled questionnaires, and conducted laboratory work. R.J. supervised the study, confirmed the diagnoses, analyzed the data, and prepared the manuscript.

Corresponding author

Correspondence to Rasool Jafari.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

All methods in the present study were carried out in accordance with relevant guidelines and regulations of the Iran National Committee for Ethics in Biomedical Research. Additionally, the study was approved by the ethical committee of Urmia University of Medical Sciences under the ethical code of IR.UMSU.REC.1398.533. All participants in the study provided their informed consent and were also informed about the study. The questionnaires were completed about the demographic variables of the participants by interview. Only stool samples were used and studied and patients gave their permission to use their samples. No sample was taken solely for the present study and we used the same sample that the patients delivered to the laboratories for their other laboratory tests requested by their physicians.

Consent for publication

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeinali, S., Rezgi, M., Gholinejad, M. et al. A large-scale study on the prevalence of intestinal parasites in patients referred to medical laboratories in Urmia, Northwest Iran. BMC Gastroenterol 23, 322 (2023). https://doi.org/10.1186/s12876-023-02947-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12876-023-02947-5

Keywords

BMC Gastroenterology

ISSN: 1471-230X

Contact us