Tropical Biomedicine 36(1): 103–113 (2019)

Prevalence and time-trend analysis of intestinal parasitic infections in north-central , 2012-2016

Karimazar, M.1, Rezaeian, S.2, Ebrahimipour, M.3*, Ranjbarpour, A.4, Madanipour, H.4, Javan, S.4 and Najjari, M.5 1Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran 2Research Center for Environmental Determinants of Health (RCEDH), School of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran 3Research Center for Hydatid Disease in Iran, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran 4Nazarabad Health Network, Alborz University of Medical Sciences, Alborz, Iran 5Department of Parasitology and Mycology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran *Corresponding author e-mail: [email protected] Received 15 January 2018; received in revised form 14 August 2018; accepted 25 August 2018

Abstract. Intestinal parasitic infections are still considered as health challenges, predominately in the areas with low sanitation and socioeconomic conditions. Owing to the socioeconomic impact, these infections are considered as important Neglected Tropical Diseases in developing countries, including Iran. This study aimed to evaluate the prevalence and time-trend of intestinal parasitic infections in Nazarabad, north-central Iran. In a cross-sectional study, medical records of 4427 suspected cases of intestinal parasites, referred to the Nazarabad health network, from 2012 to 2016 were reviewed. Bio-data, as well as laboratory data, were extracted after obtaining ethics approval. The descriptive and time-trend analyses were applied to the data. Linear regression analysis was used for the time-trend analysis. The results indicated that 18.0% of the cases to have at least one parasite in their intestine. A total of 4.5% (36/798) of positive cases has mixed infection. The median age was 31 with a range from 4 to 84 years. There are 12 different parasites detected. Blastocystis (9.2%) and Giardia (7.4%) were more prevalent parasites in the cases. Time-trend analysis showed a decreasing trend of the infection from 2012 to 2016. The most prevalent infection was found in the spring months. These infections are still among the health challenges in north-central Iran. More investigations are needed to determinate the main sources of these parasites in this area. More effective control programs are needed to combat these infections, especially in the spring and summer months.

INTRODUCTION clinical manifestations (Rokni, 2008; Bdir & Adwan, 2010). Owing to the socio- Intestinal parasitic infections (IPIs) are economic impact, IPIs are considered as still considered as health challenges, important neglected tropical diseases in predominately in the areas with low developing countries, including Iran sanitation and socioeconomic conditions (Sayyari et al., 2005). (Abu-Madi et al., 2016; Archer et al., 2017; Due to some progress in the control Alanazi, 2017; Dib et al., 2015). According of parasitic diseases, distinct decreases to the World Health Organization, these have been achieved in Iran. This is parasites infect about 3.5 billion people obvious, especially in helminthic infections globally, of which 450 million cases have (Motazedian et al., 2015; Sadeghi et al.,

103 2015). However, the high prevalence rate of 1997; Jaran, 2017; Martins-Melo et al., 2016). IPIs, especially protozoans, remains as a Many IPIs are reported in spring and nationwide dilemma for the health system summer months when the high temperature in the country (Sarkari et al., 2016; Bdir and moisture is suitable for transmission of & Adwan, 2010; Campbell et al., 2016; these parasites. More focus on the control Sabzikarian et al., 2016). programs in these periods could be more Transmission of most intestinal effective in the management of IPIs organisms is through the oral-faecal route (Huffman et al., 1997; Jaran, 2017). (Efstratiou et al., 2017; Tulu et al., 2016). Time-trend analysis of IPIs has less Contaminated food and water with human consideration in Iran. The transmission and animal faeces are the most important rate of these parasites in the different sources for human societies (Lim & seasons of the year is not exactly known Nissapatorn, 2017; Dubey, 2015; Rokni, in the country. This study’s aim was to 2008). Among IPIs, infections with Ascaris evaluate the prevalence and time-trend of lumbricoides, Trichuris trichiura, hook IPIs in north-central Iran. worms, Taenia saginata, and Strongyloides stercoralis show clear decreases in Iran (Afrakhteh et al., 2016). Hymenolepis nana MATERIALS AND METHODS and Enterobious vermicularis are two other more common helminthic parasites Patients and study site in the country (Amiri et al., 2016; Daryani In a cross-sectional study, medical records et al., 2017; Turki et al., 2016). Enterobiosis of 4427 suspected cases of infections is reported more in the preschool and with intestinal parasites, referred to the school children, especially in the rural Nazarabad health network, from 2012 to areas (Barkhori Mahni et al., 2016; Turki 2016 were reviewed. Bio-data (sex and age), et al., 2016; Wang et al., 2017). as well as laboratory reports of the cases, Giardia and Blastocystis, as pathogenic were extracted and inserted in a prepared and Entamoeba coli as nonpathogenic form. The prevalence of intestinal parasites protozoans are more prevalent in human was calculated as a number of infected infections and reported throughout the cases divided by a total number of subjects country (Barkhori Mahni et al., 2016; Jafari in each year or in each month. Nazarabad, et al., 2016; Kia et al., 2008; Nasiri et al., located in north-central Iran has a temperate 2009; Abera et al., 2016; MacKenzie et al., weather with 301 mm annual precipitation 1995). The high frequency of nonpathogenic (I.R. of Iran Meteorological Organization). parasites could be considered as an index Water distribution network is well deve- for the measure of the level of sanitation loped in this area; however, more attention and health in each region (MacKenzie et is needed especially in the rural areas. al., 1995). Prevalence of IPIs is more in the rural areas, and are strongly dependent on Statistical analyses the low level of hygiene and environmental Descriptive analyses were used to calculate conditions (Campbell et al., 2016; Kia et frequencies, percentages, means, and al., 2008; Kuzehkanani et al., 2011; Sinniah standard deviation (SD). To compare the et al., 2014). variables according to the health status of For evidence-based management of the subjects, chi-square, t-test, and analysis each disease, different aspects of epide- of variance were conducted, as appropriate. miology should be investigated in the Linear regression analysis was used for the endemic regions (Huffman et al., 1997). time-trend analysis. Statistical analysis was Determination of transmission patterns and performed at a significance level of 0.05 timelines of IPIs are very important for the using STATA version 12. The figures were control of these diseases (Huffman et al., plotted by Sigmaplot software version 12.

104 RESULTS IPIs by seasons. A significant difference was found in the prevalence rate between Between 2012 and 2016, a total of 4427 summer, fall and winter with spring. cases were referred to the Nazarabad There was no significant difference in Health network. Overall, the prevalence of the total prevalence of IPIs between intestinal infections was 18.0% and most male (19.89±8.3) and female (17.37±6.4) of them (98.0%) were due to protozoans. (P=0.064). However, time-trend analysis of More than half of these cases were males the prevalence by sex indicated a declining (58.6%) and the mean age was 31.8 (SD trend in males and females with a significant 12.5). The most number of infected cases trend in males (P=0.007) (Fig. 3). were in 21-50 year age groups with 67.5% Analysis of monthly trend prevalence of positive cases (Table 1). Blastocystis in the different age groups revealed a and Giardia were the most prevalent declining trend in 0-20 (P=0.244) and 21- parasites with 9.2% and 7.4% infections, 50 (P=0.007) groups. The upward trend in respectively. Mixed infections were the age group 51 and over was observed observed in 4.5% (n=36/798) of positive but was non-significant (regression cases. coefficient=0.02, P=0.846) (Fig. 4). Table 2 shows the overall prevalence of protozoan and helminthic parasites by different seasonal and age groups. DISCUSSION Figure 1 depicts a declining trend in the prevalence of IPIs with a regression In spite of massive progress in the global coefficient of -0.071 (P=0.075) and the control of IPIs, these infections still remain higher prevalence was recorded in April as a health challenge, especially in the low 2013. During this time, the prevalence of socioeconomic areas (Emile et al., 2013). IPIs declined from 22.4% in 2012 to 16.3% As with developing countries, IPIs caused in 2016 (Fig. 1). The trend of the monthly by anthroponotic and zoonotic parasites, prevalence of IPIs showed the most in impose a health threat in Iran (Sayyari et April 2012 (38.03%) and March 2012 al., 2005; Bahmani et al., 2017; Balarak et (26.83%), whereas the lowest prevalence al., 2016; Ramos et al., 2014). was in December 2016 (7.41%) (Fig. 1). In As with previous studies, in the current addition, the time-trend analysis indicated study, a high prevalence (18.0%) of IPIs was declining in the prevalence of IPIs from indicated in Iran. Other studies in Iran 2012 (22.4%) to 2016 (16.3%). have reported the prevalence to range from A significant downward trend was 4.7-56% throughout the country (Bahmani found according to the seasons with a more et al., 2017; Balarak et al., 2016; Barkhori prevalent trend in spring (Fig. 2). Fig. 2 Mahni et al., 2016; Kuzehkanani et al., 2011; shows the comparison of prevalence of Masoumeh et al., 2012; Nasiri et al., 2009;

Table 1. Characteristics of the cases referred to Nazarabad Health network by healthy status

Variable Subgroup Intestinal infection No. (%) Healthy No. (%) P-value

Sex Female 446 (55.9) 2147 (59.2) 0.089 Male 352 (44.1) 1482 (40.8) Age groups 0-20 211 (26.4) 474 (13.1) <0.001 21-50 539 (67.5) 2847 (78.4) 51 and over 48 (6.1) 308 (8.5) Season Spring 257 (32.2) 856 (23.6) <0.001 Summer 187 (23.4) 904 (24.9) Fall 182 (22.8) 967 (26.6) Winter 172 (21.6) 902 (24.9)

105 Total No. (%) 0 (0.0)(30.8) 685 stercoralis Oxyur S. 0 (0.0) 0 (0.0)(13.5) 356 trichura t seasonal and age groups Helminthic parasites No. (%) (0.0) 0 (0.0) 7 (1.0) saginata H. nana T. 1 (0.1) 1 (0.1) 0 (0.0) 0 (0.0) 1 (0.1) 1091 (17.1) 1 (0.1) 0 (0.0) 1 (0.1) 4 (0.4) 0 (0.0) 1074 (16.0) (0.1) 1 (0.1) 1 (0.1) 1 (0.1) 2 (0.2) 0 (0.0) 1149 (15.8) (0.0) 0 (0.0) 0 (0.0) 0 (0.0) (0.1) 3 (0.1) 3 (0.1) 2 (0.1) 0 (0.0) 1 (0.03) 3386 (15.9) E. colihominis T. T. (0.2) 1 (0.1) 0 (0.0) 0 (0.0) 1 (0.1) 0 (0.0) 1 (0.1) 0 (0.0) 1113 (23.1) 1 (0.2) 3 (0.4) 1 (0.2) 0 (0.0) 0 dispar E. histolytica/ butschlii Protozoan parasite No. (%) nana I. Blastocystis E. (7.3) 94 (8.6) 5 (0.5) 0 (0.0) 2 (0.2) 3 (0.3) 0 (0.0) (3.9) 106 (9.9) 1 (0.1) 3 (0.3) 4 (0.4) 8 (0.7) 2 (0.2) Giardia 178 (5.3) 314 (9.3) 9 (0.3) 6 (0.2) 9 (0.3) 12 (0.4) 2 140 (12.6) 107 (9.6) 4 (0.4) 1 (0.1) 2 Fall 65 (5.7) 100 (8.7) 1 (0.1) 5 (0.4) 2 (0.2) 3 (0.3) 1 Summer 80 >51 16 (4.5) 31 (8.7) 0 (0.0)Winter 1 (0.3) 42 0 (0.0) 0 (0.0) 0 Spring <20 133 (19.4) 62 (9.1) 2 (0.3) 2 (0.3) 21-50 Table 2. Overall prevalence of protozoan and helminthic parasites in the cases referred to Nazarabad Health network by differen Table of Type parasite Season Age groups (in years)

106 Figure 1. Trend of monthly prevalence of IPIs in the cases referred to Nazarabad Health network.

Figure 2. Prevalence of intestinal parasitic infections by season in the cases referred to Nazarabad Health network, figures shows the P-value of comparison.

107 Figure 3. Trend of monthly prevalence of IPIs by sex in the cases referred to Nazarabad Health network.

Figure 4. Trend of monthly prevalence of IPIs by age groups in the cases referred to Nazarabad Health network.

108 Pestehchian et al., 2015; Daryani et al., 2017; patients with immune diseases (Dhital et Sarkari et al., 2016; Rasti et al., 2017). One al., 2016; Ashtiani et al., 2011; Kiani et al., study in Boyer-Ahmad District, South- 2016; Kyambikwa Bisangamo et al., 2017; western Iran, showed that more than 30% Mukhiya et al., 2012; Nanthavong et al., of rural areas have individuals with at least 2017; Najjari et al., 2016). Food-handlers one parasite in their intestine (Sarkari et al., being the most important guild in preparing 2016). All previous studies in Iran indicated and distributing foods amongst societies a noticeable decrease in the prevalence of were emphasised in several studies to be human helminthic parasites, whereas the source of infection as studies have infections with intestinal protozoans remain shown high prevalence of IPIs amongst them quite high especially in the rural regions (Abu-Madi et al., 2008; Balarak et al., 2016; (Arani et al., 2008; Kia et al., 2008; Rasti et Kheirandish et al., 2014; Zaglool et al., 2011; al., 2017). Sharif et al., 2015; Heydari-Hengami et al., In this study, infection with intestinal 2018). parasite was more in males (58.6%) and it Previous researchers have tended to concurs with previous studies in Iran and focus more on the prevalence of IPIs only, other countries (Kuzehkanani et al., 2011; which led to ignoring the other important Rasti et al., 2017; Alanazi, 2017). However, patterns of IPIs epidemiology. Time-trend some studies showed more infections in analysis of IPIs helps health authorities females (Barkhori Mahni et al., 2016; to implement the control programs at the Motazedian et al., 2015; Pestehchian et al., proper time with the best outcome in 2015). One study in Shiraz, Iran, indicated combating these infections (Huffman et al., more infections in females with a significant 1997; Jaran, 2017; Ahmad et al., 2014). statistical difference that showed the In the current study, a significant presence of women like men in the distri- association was found between IPIs and bution of foods amongst societies as time. Transmission of intestinal parasites food-handlers (Motazedian et al., 2015). was significantly (P<0.001) more in the As with previous studies, in the recent spring months. Owing to warmer and higher study, IPIs caused by Blastocystis and humidity in the spring and summer months, Giardia parasites was more prevalent the weather is suitable for reproduction throughout the world (Arani et al., 2008; and transmission of intestinal parasites. Jafari et al., 2016; Masoumeh et al., 2012; Contamination of water supplies and foods MacKenzie et al., 1995; Soriano et al., 2011). with cyst and eggs of these parasites could While not medically threatening, it is result in parasitic infections in each area important to evaluate these non-pathogenic (Efstratiou et al., 2017). parasites, as well as the pathogenic ones Although Nazarabad County has access due to the similar transmission route of to urban water supply, sanitation and other these parasites. High prevalence of non- services are much needed, especially in the pathogenic parasites like E. coli act as rural areas. Evaluation of contaminated indicators that reveal the contamination of foods and water supply, the two important water supplies and low level of sanitation sources for IPIs, should be done more in indices (Bopda et al., 2016; MacKenzie et this area. al., 1995; Sianturi et al., 2016; Dib et al., 2015). Due to the transmission patterns of CONCLUSION IPIs, it could occur in the different age and sex groups (Bopda et al., 2016). However, Despite some progress in the control of infections in children and immuno- IPIs, a high prevalence of IPIs is observed compromised patients must be given more in Nazarabad County in north-central Iran. consideration. These infections cause mal- More investigation is needed to determinate nutrition, mental and behavioural disorders the main sources of these parasites in the in children and could be even fatal in the mentioned area. More effective control and

109 management programs are needed to Alanazi, A.D. (2017). The prevalence of combat these infections, especially in the intestinal parasitic protozoan among spring and summer months when the patients in Ad-Dawadimi General prevalence of infection is high. Hospital, Saudi Arabia (Article). Tropical Biomedicine 34: 453-460. Acknowledgments. The authors would like Amiri, S.A., Rahimi, M.T., Mahdavi, S.A., to express their gratitude to the personnel Moosazadeh, M., Ramzani, O., Koshk, of Nazarabad Health Network in Alborz A.F., Rosbehan, R. & Siyadatpanah, Province for their useful collaboration. S.A. (2016). Prevalence of Enterobius vermicularis infection among preschool Conflict of Interest children, Babol, North of Iran. Journal The authors declare that they do not have of Parasitic Diseases 40: 1558-1562. conflicts of interest. Arani, A.S., Alaghehbandan, R., Akhlaghi, L., Shahi, M. & Lari, A.R. (2008). Prevalence of intestinal parasites in a population REFERENCES in south of Tehran, Iran. Revista do Instituto de Medicina Tropical de Sao Abera, B., Yitayew, G. & Amare, H. (2016). Paulo 50: 145-9. Salmonella serotypeTyphi, Shigella, Archer, C.E., Appleton, C.C., Mukaratirwa, and intestinal parasites among food S., Lamb, J. & Corrie Schoeman, M. handlers at Bahir Dar University, (2017). Endo-parasites of public-health Ethiopia. Journal of Infection in importance recovered from rodents in Developing Countries 10: 121-6. the Durban metropolitan area, South Abu-Madi, M.A., Behnke, J.M., Boughattas, Africa. Southern African Journal of S., Al-Thani, A. & Doiphode, S.H. (2016). Infectious Diseases 1-10. A decade of intestinal protozoan epide- Ashtiani, M.T., Monajemzadeh, M., Saghi, miology among settled immigrants in B., Shams, S., Mortazavi, S.H., Khaki, S., Qatar. BMC Infectious Diseases 16: 370. Mohseni, N., Kashi, L. & Nikmanesh, B. Abu-Madi, M.A., Behnke, J.M. & Ismail, A. (2011). Prevalence of intestinal para- (2008). Patterns of infection with sites among children referred to intestinal parasites in Qatar among Children’s Medical Center during 18 food handlers and housemaids from years (1991-2008), Tehran, Iran. Annals different geographical regions of of Tropical Medicine and Parasitology origin. Acta Tropica 106: 213-20. 105: 507-12. Afrakhteh, N., Marhaba, Z., Mahdavi, S.A., Bahmani, P., Maleki, A., Sadeghi, S., Garoosian, S., Mirnezhad, R., Vakili, M.E., Shahmoradi, B. & Ghahremani, E. Shahraj, H.A., Javadian, B., Rezaei, R. (2017). Prevalence of intestinal pro- & Moosazadeh, M. (2016). Prevalence tozoa infections and associated risk of Enterobius vermicularis amongst factors among schoolchildren in kindergartens and preschool children Sanandaj City, Iran (Article). Inter- in Mazandaran Province, North of Iran. national Journal for Parasitology 12: Journal of Parasitic Diseases 40: 1332- 108-116. 1336. Balarak, D., Modrek, M.J., Bazrafshan, E., Ahmad, A.F., Ngui, R., Muhammad Aidil, R., Ansari, H. & Kord Mostafapour, F. Lim, Y.A. & Rohela, M. (2014). Current (2016). Prevalence of Intestinal Para- status of parasitic infections among sitic Infection among Food Handlers Pangkor Island community in Peninsular in Northwest Iran. Journal of Para- Malaysia (Article). Tropical Bio- sitology Research 2016: 8461965. medicine 31: 836-843.

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