Abstract
Background:
Nowadays, intestinal parasitic infections (IPIs) are one of the most common and serious public health problems, which affected 3.5 billion people worldwide, especially in developing countries. During the time of distribution, the pattern of disease may alter as a result of changing the life style of residents.Objectives:
The current study was aimed to determine the prevalence of IPIs in the town of Haftkel, southwest Iran.Methods:
In this descriptive cross-sectional study, 13698 stool specimens were collected during 2010 - 2013. For all samples, both direct smear and formalin ether concentration methods were done. Finally data analysis was performed using SPSS version 11.0.1 (SPSS Inc., Chicago, IL, USA).Results:
658 (4.8%) out of 13698 specimens were positive for IPIs and Giardia lamblia was detected in 433 (3.16%) samples as the commonest parasite. Other parasites were included: Entamoeba histolytica/dispar (0.7%), E. coli (0.56%), E. hartmanni (0.21%), Blastocystis hominis (0.1%), Hymenolepis nana (0.04%), Taenia spp (0.014%), and Enterobius vermicularis (0.007%). A decreasing trend was observed in the prevalence of intestinal parasites in which the frequency was 281 (6.42%) cases in 2010 and declined to 114 (3.83) in 2013. The maximum and minimum infection was seen in the summer season (34.35%) and winter (15.35%), respectively. Furthermore, the number of infected men was significantly higher than women (64.5% against 35.5%). Interestingly, no hookworm, Ascaris lumbricoides, and Trichuris trichiura eggs were seen in the current study.Conclusions:
Based on the current findings, IPIs particularly helminthic cases have been declined during the past decades. Therefore, health education and improving facilities environmental especially in rural and semi-urban areas can be helpful.Keywords
1. Background
Intestinal parasites are considered as a major public health problem worldwide especially in developing countries. An estimated 3.5 billion people are affected and approximately 450 million individuals currently suffer from these infections, which most of them constitute children. Protozoa and helminthes are 2 categories of pathogenic and non-pathogenic parasites that cause gastrointestinal tract ailments (1). Intestinal parasitic infections (IPIs) is commonly transmitted by both indirect and direct routes via oral-fecal, ingestion of contaminated food, vegetables, and drinking water (2-5). In addition some flies might have a role as mechanical vectors for some intestinal parasites such as Ascaris lumbricoides, Hymenolepis nana, Entamoeba histolytica/dispar, and Giardia lamblia (6). Despite great efforts and improving the hygiene status in order to eliminate the intestinal parasites, these infectious agents are still common in many areas throughout the world. Pathogenesis, morbidity, and mortality of intestinal parasites are depending upon species, climate, age, gender, immune system condition, nutritional status of the host, and differ from person to person (1). IPIs in the majority of cases are asymptomatic; however, it can cause a wide spectrum of clinical symptoms such as: chronic diarrhea, watery diarrhea or mucoidal, nausea, vomiting, dehydration, abdominal pain, fever, iron deficiency anemia, malnutrition, and vitamin deficiencies that may lead to malabsorption syndrome, growth retardation in children, mental, and physical health disorders (1, 5, 7) after a long period. In immunocompromised individuals symptoms are more severe and may cause irreparable consequences (8).
Numerous investigations in various parts of the world have confirmed a direct correlation among the high rate of parasitic infections and lower socioeconomic status of the area. Furthermore, poor sanitary and environmental statuses are other critical epidemiological factors relevant with the prevalence of these infectious agents (1, 9, 10). Recently, many studies throughout the country of Iran have been performed and demonstrated a significant reduction in human helminthic disease compared with previous studies, although intestinal protozoan infection like Entamoeba spp., G. lamblia, and Blastocystis hominis are still prevalent (11-13). High rate of parasitic infections, especially in small towns and rural areas justified with a low hygienic status, illiteracy, social and economic poverty, defects in healthcare system, as well as a lack of safe drinking water filtration system (1, 9).
From intestinal protozoan infections, G. lamblia is the common infection with a prevalence ranging from 20% - 30% in developing countries and 2% - 5% in developed countries that affected about 200 million individuals throughout the world (14). In addition, E. histolytica, agent of amoebiasis, is another IPIs that affects about 180 million indiviuals worldwide and responsible for 40000 - 110000 mortality annually. E. histolytica and E. dispar are absolutely similar and cannot be distinguished by conventional microscopic examination. The first is a potential pathogen, while latter is a non-pathogen protozoa (15). Among helminthic infections, A. lumbricoides is still one of the most prevalent IPIs with 807 - 1221 million cases worldwide especially in sub-Saharan Africa and East Asia. In addition hookworm and whipworm (Trichuris trichiura) are liable for 576 - 740 million and 604 - 795 infections, respectively (16). Prevalence of intestinal parasites in different parts of Iran is varied from 9.1% in Mazandaran province (North Iran) (17), 21.2% in Tehran city (North Iran) (11), 7.6% in Kashan city (Central Iran) (18), and 35.1% in Hamadan city (12). It is noteworthy that climatic conditions are a key factor for prevalence of IPIs all around Iran (9).
2. Objectives
During the time, distribution patterns and prevalence of intestinal parasitic diseases fluctuate as a result of changing in behavior and life style of society population. Hence, periodic epidemiological surveys, in order to determine the exact burden of infection in region and adopting suitable strategies, is required and should be continued. Thus the aim of the current survey was to describe the prevalence of IPIs in individuals referred to central health center in Haftkel district, located at southwest of Iran.
3. Methods
3.1. Study Area
Haftkel County is located in southwest Iran (east of Khuzestan province) (Figure 1). Based on the 2011 census, the county’s population estimated 22391 people in 5399 families included both rural (7514 people) and urban (14,77 people) areas. The climate of Haftkel is generally hot and occasionally humid, while winters are much more pleasant and dry. Summertime temperatures routinely exceed 50°C and in the winter, it can drop below freezing point. The annual average rainfall is about 380 mm.
Location of Haftkel County in Iran (http://en.wikipedia.org/wiki/Haftkel)
3.2. Study Population
This descriptive cross-sectional study was carried out in the laboratory of the central health center of Haftkel County during 4 r consecutive years (2010 - 2013). The study population included all individuals who were referred to laboratory the for s parasitology stool exam request.
3.3. Stool Examination
Stool specimens (1 - 4 g) were taken in labeled plastic containers without any preservatives and less than 1.5 hours after collecting underwent examination. For all samples, both direct smear and formalin ether concentration methods were done. Direct wet-mount smear was carried out to detect parasites motility using saline and lugol’s iodine solution. The formalin ether concentration technique was performed. Briefly, a piece of stool (0.5 - 1.5 g) was mixed with 4 g formol saline. Mixture passed through filter and then diethyl ether was added and mixed again. Mixture centrifuged by 3000 rpm for 2 minutes. Finally sediments after staining with 0.85% iodine, was placed on a clean slide, and were examined by a light microscope (× 100 magnification) in order to parasite detection. The diagnosis of helminth and protozoa was based on microscopic morphological features such as trophozoite size, cyst, and ova shape.
3.4. Statistical Analysis
Data analysis was done using SPSS version 11.0.1 (SPSS Inc., Chicago, IL, USA) software and Chi-square statistical test.
4. Results
Out of 13698 stool specimens, 658 positive cases (424 male and 234 female) were diagnosed for IPIs and the overall prevalence was calculated 4.8% (Table 1). Between these number, 649 (4.73%) and 9 (0.07%) belonged to protozoan and helminth infections, respectively (Table 2). Among infected men and women significant differences were seen (Table 1). Our findings indicated a decreasing trend in rate of infection so that the prevalence from 6.42% in 2010 fell down to 3.83% in 2013 (Table 1). Also maximum infection was observed in summer season (34.35%) and autumn (27.96%) placed in second rank (Figure 2). The most common protozoa and worm belonged to G. lamblia (3.16%) and H. nana (0.04%), respectively (Table 2). Prevalence of other parasites are summarized in Table 2. No positive cases with A. lumbricoides, hookworm, T. trichiura and Strongyloides stercoralis were reported.
Seasonal Prevalence of IPIs in Haftkel County, Iran (2010 - 2013)
Prevalence of IPIs Based on Year and Gender in Haftkel County, Iran (2010 - 2013)
| Year | Number of Referred, No. (%) | Positive Cases, No. (%) | Female, No. (%) | Male, No. (%) |
|---|---|---|---|---|
| 2010 | 4375 (31.94) | 281 (6.42) | 101 (36) | 180 (64) |
| 2011 | 3373 (24.63) | 136 (4.03) | 51 (37.5) | 85 (62.5) |
| 2012 | 2981 (21.76) | 127 (4.26) | 50 (39.4) | 77 (60.6) |
| 2013 | 2969 (21.67) | 114 (3.83) | 32 (28) | 82 (72) |
| Total, No. (%) | 13698 (100) | 658 (4.8) | 234 (35.5) | 424 (64.5) |
Frequency of IPIs in Haftkel County Population During 2010 - 2013
| Parasite Species | Frequency, No. | Percentage, % |
|---|---|---|
| No. of people examined (N = 13698) | ||
| E. histolytica/dispar | 96 | 0.7 |
| E. coli | 77 | 0.56 |
| E. hartmanni | 29 | 0.21 |
| G. lamblia | 433 | 3.16 |
| B. hominis | 14 | 0.1 |
| H. nana | 6 | 0.04 |
| E. vermicularis | 1 | 0.007 |
| Taenia spp. | 2 | 0.014 |
| Total | 658 | 4.8 |
5. Discussion
Globally helminth and protozoan parasites are one of the most serious public health concerns with a widely distribution pattern in many countries and territories particularly in tropical and subtropical developing countries and seen mainly in children (1, 7, 9, 19-26). Prevalence of intestinal parasitic diseases in each society considered as an indices of health condition of region. Some personal (immunity condition, nutrition status, hygiene, literacy, cultural habits, and etc.) and environmental factors like climate, geographical position, poverty and socioeconomic status, poor sanitary conditions, and high density of population may contribute to IPIs prevalence (1). In recent years numerous investigations have been done throughout the country of Iran and all of them demonstrated a dramatical slump in the frequency of IPIs, particularly in helminthic infections (13, 27, 28) in comparison with past decades (29). This sharp decrease may be due to improving the sanitation status, hygienic level, and knowledge of majority of people.
Based on our findings, a continual decline was seen in the rate of infection. The overall prevalence of IPIs was 4.8% (Table 1), which is consistent with studies such as Nasiri et al. (27) in the city of Karaj (4.7%), and, Sadeghi and Borji (28) in Qazvin city (5.8%), while higher prevalence of IPIs was reported from the Mazandaran province (9.1%) (30), Isfahan city (10.42%) (31) as well as Hamadan city (35.1%) (12). At Sayyari et al., in the study in the general population of Islamic Republic of Iran, which was done during 1999 - 2000, IPIs infection were reported 19.3% and G. lamblia with 10.9% placed at first rank that is consistent with our study. Furthermore, proportion of other parasites were as follows: E. histolytica 1%, A. lumbricoides 1.5%, E. vermicularis 0.5%, Taenia saginata 0.2%, Trichostrongylus colubriformis 0.2%, T. trichiura 0.1%, Ancylostoma duodenale 0.1% and, others 5.1% (9).
Current findings showed that the rate of infection caused by protozoa is dramatically higher than helminthic cases (4.73% and 0.07%, respectively) (Table 2). One reason for this fact is that protozoa could transmit easier than larvae and ova of helminths. From protozoan, G. lamblia was diagnosed as the most frequent parasite with 3.16%, which is similar to studies such as Yemen (17.7%) (10), Karaj city (3.8%) (27), Kashan city (2.7%) (18), and Ghaemshahr town (32), while in some researches E. coli (12, 28), E. histolytica/dispar (33) or B. hominis (11, 31) were most common. Giardia is found in food, soil, and any surface that was contaminated with infected feces (2). Additionally, polluted water supplies could be a potential factor for amebiasis and giardiasis. Many intestinal parasite outbreaks, due to contamination of municipal water resources, have been reported during the past decades (34). Based on a systematic review and meta-analysis study done by Karambaigi et al., in Iran during 1988 - 2009, from 234570 individuals who were examined, the prevalence of E. histolytica/dispar was reported as 1.3% (2.5% and 0.8% in rural and urban regions, respectively) (35). In the present survey, only 96 (0.7%) E. histolytica/dispar cases were detected, which is lower than the average prevalence of Karambaigi study.
In our study, among helminthic infections, H. nana with 0.04% was the most common detected worm that is in agreement with Akhlaghi et al. (11) in Tehran city (0.2%), Hooshyar et al. (18) in Kashan city (0.02%), and Sedeghi and Borji (28) in Qazvin city (0.1%), while in the Shobha et al. study in India, A. lumbricoides (2.04%) was reported as a major infection (36). Previous conducted studies in the province of Khuzestan have demonstrated the potential presence of intestinal parasites in food handlers, soils, water resources, and vegetables that indicated the establishment and persistence of IPIs in all parts of the region (2, 3, 13, 37-39). In a 10-year retrospective study, performed by Saki et al., in the province of Khuzestan, among food handlers, 62007 stools were examined and 7.78% of total population were identified positive for pathogenic IPIs. Frequency of G. lamblia, H. nana, E. histolytica/dispar and, A. lumbricoides was 4.52%, 1.29%, 1.39%, and 0.57%, respectively (37).
In the present study, the prevalence of IPIs in males with 64.5% was significantly higher than females. This issue could be explained by the number of study population and cultural habit such as working women in agricultural farms. Overall, the differences between our results and other studies may be attributed to the sample size, type of sampling, methodology, cultural habits of the region, occupations, geographical location, sanitary status, and many other factors.
5.1. Conclusion
According to the current paper, the trend of IPIs in samples that be received to the central health laboratory of Haftkel county was decreased and the prevalence from 6.42% in 2010 dropped to 3.83% in 2013. Health education and improving facilities environmental, especially in rural and semi-urban areas can be helpful. Along with those epidemiological studies done for screening, determining the severity of infection and early treatment of patients in order to adopting prevention program is necessary. Furthermore it is highly recommended to choose a specific staining including Trichrome for better discrimination of amoeba in the future study.
Acknowledgements
References
-
1.
Alum A, Rubino JR, Ijaz MK. The global war against intestinal parasites--should we use a holistic approach? Int J Infect Dis. 2010;14(9):e732-8. [PubMed ID: 20399129]. https://doi.org/10.1016/j.ijid.2009.11.036.
-
2.
Saki J, Asadpoori R, Khademvatan S. Prevalence of intestinal parasites in vegetables consumed in Ahvaz, South West of Iran. J Med Sci. 2013;13(6):488-92.
-
3.
Rafiei A, Rahdar M, Valipour Nourozi R. Isolation and identification of parasitic protozoa in sampled water from the southwest of Iran. Jundishapur J Health Sci. 2014;6(4). https://doi.org/10.5812/jjhs.23462.
-
4.
Saki J, Foroutan-Rad M, Asadpouri R. Molecular Characterization of Cryptosporidium spp. in Wild Rodents of Southwestern Iran Using 18s rRNA Gene Nested-PCR-RFLP and Sequencing Techniques. J Trop Med. 2016;2016:6834206. [PubMed ID: 27956905]. https://doi.org/10.1155/2016/6834206.
-
5.
Javaherizadeh H, Khademvatan S, Soltani S, Torabizadeh M, Yousefi E. Distribution of haematological indices among subjects with Blastocystis hominis infection compared to controls. Prz Gastroenterol. 2014;9(1):38-42. [PubMed ID: 24868297]. https://doi.org/10.5114/pg.2014.40849.
-
6.
Getachew S, Gebre-Michael T, Erko B, Balkew M, Medhin G. Non-biting cyclorrhaphan flies (Diptera) as carriers of intestinal human parasites in slum areas of Addis Ababa, Ethiopia. Acta Trop. 2007;103(3):186-94. [PubMed ID: 17658447]. https://doi.org/10.1016/j.actatropica.2007.06.005.
-
7.
Miller SA, Rosario CL, Rojas E, Scorza JV. Intestinal parasitic infection and associated symptoms in children attending day care centres in Trujillo, Venezuela. Trop Med Int Health. 2003;8(4):342-7. [PubMed ID: 12667154]. https://doi.org/10.1046/j.1365-3156.2003.01011.x.
-
8.
Bottieau E. Tropical parasitic diseases and immunosuppression. Clin Microbiol Infect. 2014;20(4):277. [PubMed ID: 24529256]. https://doi.org/10.1111/1469-0691.12590.
-
9.
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. [PubMed ID: 16602457].
-
10.
Alyousefi NA, Mahdy MA, Mahmud R, Lim YA. Factors associated with high prevalence of intestinal protozoan infections among patients in Sana'a City, Yemen. PLoS One. 2011;6(7). e22044. [PubMed ID: 21789210]. https://doi.org/10.1371/journal.pone.0022044.
-
11.
Akhlaghi L, Shamseddin J, Meamar AR, Razmjou E, Oormazdi H. Frequency of intestinal parasites in Tehran. Iran J Parasitol. 2009;4(2):44-7.
-
12.
Jafari R, Fallah M, Yousofi Darani H, 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(2). https://doi.org/10.17795/ajcmi-21445.
-
13.
Safi M, Tavalla M, Mardani M, Afrisham R. Prevalence of intestinal parasitic infections among applicants for health cards attending Ahvaz East Health Center during 2012–2013. Asian Pac J Trop Dis. 2016;6(2):151-4. https://doi.org/10.1016/s2222-1808(15)61002-7.
-
14.
Fletcher SM, Stark D, Harkness J, Ellis J. Enteric protozoa in the developed world: a public health perspective. Clin Microbiol Rev. 2012;25(3):420-49. [PubMed ID: 22763633]. https://doi.org/10.1128/CMR.05038-11.
-
15.
Shahrul Anuar T, M. Al-Mekhlafi H, Abdul Ghani MK, Osman E, Mohd Yasin A, Nordin A, et al. Prevalence and risk factors associated with Entamoeba histolytica/dispar/moshkovskii infection among three Orang Asli ethnic groups in Malaysia. PLoS One. 2012;7(10). e48165. [PubMed ID: 23133561]. https://doi.org/10.1371/journal.pone.0048165.
-
16.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521-32. [PubMed ID: 16679166]. https://doi.org/10.1016/S0140-6736(06)68653-4.
-
17.
Vahedi M, Gohardehi S, Sharif M, Daryani A. Prevalence of parasites in patients with gastroenteritis at East of Mazandaran Province, Northern Iran. Trop Biomed. 2012;29(4):568-74. [PubMed ID: 23202601].
-
18.
Hooshyar H, Bagherian T, Baghbani F. Prevalence of intestinal parasitic infections among patients referred to Kashan reference laboratory in 2007-2011. Jundishapur Sci Med J. 2013;5(1):18-22.
-
19.
Khademvatan S, Salmanzadeh S, Foroutan-Rad M, Ghomeshi M. Elimination of urogenital schistosomiasis in Iran: past history and the current situation. Parasitology. 2016;143(11):1390-6. [PubMed ID: 27279000]. https://doi.org/10.1017/S0031182016000883.
-
20.
Khademvatan S, Yousefi E, Rafiei A, Rahdar M, Saki J. Molecular characterization of livestock and human isolates of Echinococcus granulosus from south-west Iran. J Helminthol. 2013;87(2):240-4. [PubMed ID: 22691442]. https://doi.org/10.1017/S0022149X12000296.
-
21.
Akinbo FO, Ikedje A, Okaka CE. Intestinal parasitic infections among artisans in Benin city, Nigeria. Nigeria J Basic Clin Sci. 2013;10(2):66-9. https://doi.org/10.4103/0331-8540.122761.
-
22.
Ngui R, Ishak S, Chuen CS, Mahmud R, Lim YA. Prevalence and risk factors of intestinal parasitism in rural and remote West Malaysia. PLoS Negl Trop Dis. 2011;5(3). e974. [PubMed ID: 21390157]. https://doi.org/10.1371/journal.pntd.0000974.
-
23.
Altaif KI. RETRACTED: Prevalence of intestinal parasitic infestation in Ma'an governorate, Jordan. Asian Pac J Trop Dis. 2011;1(2):110-2. https://doi.org/10.1016/s2222-1808(11)60047-9.
-
24.
Dagci H, Kurt O, Demirel M, Ostan I, Azizi NR, Mandiracioglu A, et al. The prevalence of intestinal parasites in the province of Izmir, Turkey. Parasitol Res. 2008;103(4):839-45. [PubMed ID: 18604653]. https://doi.org/10.1007/s00436-008-1065-6.
-
25.
Saab BR, Musharrafieh U, Nassar NT, Khogali M, Araj GF. Intestinal parasites among presumably healthy individuals in Lebanon. Saudi Med J. 2004;25(1):34-7. [PubMed ID: 14758375].
-
26.
Phiri K, Whitty CJ, Graham SM, Ssembatya-Lule G. Urban/rural differences in prevalence and risk factors for intestinal helminth infection in southern Malawi. Ann Trop Med Parasitol. 2000;94(4):381-7. [PubMed ID: 10945048].
-
27.
Nasiri V, Esmailnia K, Karim G, Nasir M, Akhavan O. Intestinal parasitic infections among inhabitants of Karaj City, Tehran province, Iran in 2006-2008. Korean J Parasitol. 2009;47(3):265-8. [PubMed ID: 19724700]. https://doi.org/10.3347/kjp.2009.47.3.265.
-
28.
Sadeghi H, Borji H. A survey of intestinal parasites in a population in Qazvin, north of Iran. Asian Pac J Trop Dis. 2015;5(3):231-3. https://doi.org/10.1016/s2222-1808(14)60659-9.
-
29.
Mohammad K, Zalie MR, Sirous S, Masjedi MR. Intestinal parasites in Iran. Iran J Public Health. 1995;24(3-4):9-26.
-
30.
Rahimi EB, Gholami SH, Ghorbani PKA, Pour HBM, Hasannia H, Shaban R, et al. The prevalence of intestinal parasitic infections among the people living in the central areas of Mazandaran province (2009-2010). Med Lab J. 2013;7(2):37-41.
-
31.
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. [PubMed ID: 27605766]. https://doi.org/10.1007/s12639-014-0557-9.
-
32.
Ranjbar-Bahadori S, Dastorian AR, Heidari B. Prevalence of intestinal parasites in Ghaemshahr in 2004. Medical science journal of Islamic Azad Univesity-Tehran Medical Branch {In Persian]. 2005;15(3):151-5.
-
33.
Koohsar F, Amini A, Ayatollahi AA, Niknejad F, Abbasi Nejat Z. The prevalence of intestinal worms and amebiasis in Gorgan (2005-2011) [In Persian]. Med Lab J. 2013;7(3):54-60.
-
34.
Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res. 2011;45(20):6603-14. [PubMed ID: 22048017]. https://doi.org/10.1016/j.watres.2011.10.013.
-
35.
Karambaigi F, Abdi J, Sayehmiri K. Prevalence of Entamoeba histolytica in Iran during 1988 to 2009: Systematic review and meta-analyses. Afr J Microbiol Res. 2012;6(17):3944-7. https://doi.org/10.5897/AJMR12.314.
-
36.
Shobha M, Bithika D, Bhavesh S. The prevalence of intestinal parasitic infections in the urban slums of a city in Western India. J Infect Public Health. 2013;6(2):142-9. [PubMed ID: 23537828]. https://doi.org/10.1016/j.jiph.2012.11.004.
-
37.
Saki J, Khademvatan S, Masoumi K, Chafghani M. Prevalence of intestinal parasitic infections among food handlers in Khuzestan, Southwest of Iran: a 10 year retrospective study. Afr J Microbiol Res. 2010;6:2475-80. https://doi.org/10.5897/ajmr11.1533.
-
38.
Khademvatan S, Abdizadeh R, Rahim F, Hashemitabar M, Tavalla M. Stray cats gastrointestinal parasites and its association with public health in Ahvaz city, South Western of Iran. Jundishapur J Microbiol. 2014;7(7). https://doi.org/10.5812/jjm.11079.
-
39.
Khoshnood S, Saki J, Rafiei A, Alizadeh K. Prevalence of intestinal parasitic infections among people in Baghmalek during 2013 ‒ 2014. Jentashapir J Health Res. 2015;6(2). https://doi.org/10.5812/jjhr.6(2)2015.24792.