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Analysis of knowledge and attitudes related to parasitic infections among inhabitants of Ahvaz County, Khuzestan Province, Iran
Acta Tropica 193 (2019) 211–216
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Analysis of knowledge and attitudes related to parasitic infections among inhabitants of Ahvaz County, Khuzestan Province, Iran
T
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Raheleh Baghlaninezhada,b, Molouk Beiromvanda,b, , Mohammad Salehi Veisic a
Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran Department of Parasitology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran c Department of Statistics, Faculty of Basic Science, Behbahan Khatam Alanbia University of Technology, Behbahan, Iran b
A R T I C LE I N FO
A B S T R A C T
Keywords: Knowledge Attitudes Parasitic infections Khuzestan Province Iran
Parasitic diseases are among the major health problems of various societies, especially people in developing countries, causing high economic and mortality burdens. Many researchers have reported that awareness and knowledge of a disease are effective in preventing and controlling the disease. The aim of the present study was to assess the knowledge and attitudes on parasitic diseases of the population in Ahvaz County, southwestern Iran. This community-based cross-sectional study was carried out in 2017 on 3500 subjects above 15 years old of Ahvaz County. First, participants were provided the necessary information regarding the study, and then data were collected using a constructed questionnaire. Of the 3500 participants, 1732 (49.5%) were female and 1768 (50.5%) were male, 348 (9.9%) said that they had been infected with a parasitic disease at least once in their lifetime. Almost half of the participants (42.8%) knew malaria was a parasitic disease and 50.2%, 48.9%, and 41.5% were aware of the possible transmission of parasitic diseases through uncooked meat, dirty hands, and close contact with animals. Regarding clinical symptoms, 73.2% and 32.6% of the respondents knew diarrhea and abdominal pain respectively were clinical symptoms of intestinal parasitic diseases. However, only 31.3% were aware of the close contact with cats and the risk of human toxoplasmosis and possible abortion in pregnant women. The findings reveal that the attitude of most participants toward treatment was positive (93.9%), but only 47.5% of believed that disinfecting fruits and vegetables could prevent intestinal parasitic infections.
1. Introduction Parasitic diseases are one of the main problems of public health, especially among children, in low and middle-income countries (Erismann et al., 2016). These diseases are among the diseases that cause economic and mortality burdens globally (Isah et al., 2016). Among them, malaria, leishmaniasis, trypanosomiasis, schistosomiasis, echinococcosis, onchocerciasis, taeniasis/cysticercosis, and lymphatic filariasis affect millions of people causing thousands of deaths annually (Isah et al., 2016; WHO, 2017). In recent years, some protozoan and metazoan diseases such as leishmaniasis, human African trypanosomiasis, and schistosomiasis, as well as soil-transmitted helminths have been considered as neglected tropical diseases (NTDs). (Erismann et al., 2016; WHO, 2017). It is estimated that one-third of the three billion people who are living in developing regions of Asia, Sub-Saharan Africa, and the Americas suffer a group of protozoan and helminthic
infections belonging to the NTDs (Bhutta et al., 2014). The worst affected people are those who live in poverty; that is, the population living in areas with poor sanitation and being in close contact with infectious vectors, domestic animals as well as livestock (WHO, 2017). Parasitic infections may be influenced by various factors such as socioeconomic, behavioral, health, environmental, and biological agents. In addition, educational status, occupation, and monthly income can influence the risk of parasitic infection, transmission, and associated morbidity and mortality (Gelaw et al., 2013). In Iran, some parasitic diseases such as hookworms and ascariasis have declined significantly in recent years (Askarian et al., 2012); however, cutaneous and visceral leishmaniasis, malaria, giardiasis, hydatidosis, and fascioliasis are still considered some of the main public health problems (Askarian et al., 2012; Bahadori, 2016). Giardiasis, with a prevalence of 1%–60% (Hatam-Nahavandi et al., 2017), is the most common protozoan disease in Iran; hydatidosis with a prevalence
⁎ Corresponding author at: Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, P.O. Box 61357, 15794, Ahvaz, Iran. E-mail address: [email protected] (M. Beiromvand).
https://doi.org/10.1016/j.actatropica.2019.03.014 Received 27 July 2018; Received in revised form 22 February 2019; Accepted 10 March 2019 Available online 11 March 2019 0001-706X/ © 2019 Elsevier B.V. All rights reserved.
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of 1.18–3 per 100,000 in the human population and with an annual economic loss of USD 459,650 in ruminants, is one of the most costly infectious diseases (Fasihi Harandi et al., 2012). Many researchers believe that awareness and knowledge of a disease are important in preventing and controlling it (Khan et al., 2018). To achieve this awareness and behavioral changes, health education is needed (Acka et al., 2010). In recent years, many studies have focused on assessing people's awareness and attitudes about parasitic diseases globally (Acka et al., 2010; Altinoz Aytar et al., 2015; Elsafi et al., 2015; Elyana et al., 2016; Khan et al., 2018; Kungu et al., 2017; Li et al., 2015; Person et al., 2016; Yan-Li et al., 2017); however, in Iran, data on knowledge and awareness of people concerning parasitic diseases are insufficient and mainly focused on malaria (Fekri et al., 2014; Madani et al., 2017; Nejati et al., 2018; Soleimani-Ahmadi et al., 2014). Because the lack of knowledge and awareness of parasitic diseases, their transmission routes, treatment and prevention may increase the chances of infection, the current study was designed to assess the knowledge and attitudes on parasitic diseases of the people of Ahvaz County, southwest Iran.
Table 1 The variables studied in the current study. No.
Variable
No.
Variable
1 2 3 4 5
Gender Age Educational status Occupation Family size
6 7 8 9 10
Source of drinking water Hand washing Disinfecting vegetables Restaurant salads consumption Street food consumption
2.3. Study design and sample population This cross-sectional study was performed in 2017 using simple random sampling method. In total, 3500 participants above 15 years old from the different districts of the county enrolled in the study. The number of participants from each district was selected according to its population. The study objectives were explained to the participants in an interview in their two native languages (Persian and Arabic). Participants were asked to complete a questionnaire and those who were illiterate or had eyesight problems were assisted by one of their family members or a researcher. In the current study, we evaluated participants from different occupations and levels of education.
2. Methods 2.1. Ethical statements
2.4. Questionnaire
The ethics committee of Ahvaz Jundishapur University of Medical Sciences reviewed and approved the protocol (approval number: IR.AJUMS.REC.2018–701). Informed consent was obtained from the participants.
2.4.1. Socio-demographic questions The first part of the questionnaire related to socio-demographic data: gender, age, educational level, occupation, family size, type of drinking water, hand-washing before eating, disinfecting vegetables, consumption of restaurant salads, consumption of street food, and ways of obtaining information on parasitic diseases (Table 1).
2.2. Study area Ahvaz County, the capital of Khuzestan Province in southwestern Iran (31°19′ N 48°40′ E) lies at an altitude of approximately 17 m. The county has an area of 815 km2 and an estimated population of 1,136,989 persons. One of the country’s largest rivers and the only navigable river, the Karun, runs through the middle of Ahvaz County. Ahvaz weather is usually warm and dry, and occasionally humid in summer (Zarasvandi et al., 2011). In recent years, due to low rainfall and drought, the southwestern regions of Iran, particularly Ahvaz County, have faced dust storms, turning Ahvaz into the most polluted city in the world (Maleki et al., 2016). The dominant ethnicities of the city are Persians, Lurs and Arabs. Ahvaz County is divided into eight districts (Fig. 1) (Mohammadi Dehcheshmeh et al., 2018).
2.4.2. Knowledge and attitude questions The second part included questions on familiarity with parasitic diseases, transmission routes, clinical symptoms of intestinal parasitic diseases, prevention and control of parasitic diseases, and familiarity with parasites treatment.
2.5. Statistical analyses All statistical analyses were performed with SPSS Statistics 18 (SPSS Inc., Chicago, IL, USA).
Fig. 1. Map of Iran. Khuzestan Province, highlighted in yellow based on the map of Iran at (Beiromvand et al., 2013). Map of Ahvaz County with studied regions indicated by numbers (Mohammadi Dehcheshmeh et al., 2018). 212
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3. Results
Table 3 Knowing parasitic diseases ways among Ahvaz inhabitants (N = 3500) participated in the study.
3.1. Socio-demographic characteristics In this study, all 3500 participants completed the questionnaire; 1732 (49.5%) were female and 1768 (50.5%) were male. The maximum and minimum number of participants, 26.5% and 0.5% respectively, belonged to the age groups 15–25 and above 65 years old, respectively. On education levels, 49.7% had a degree and 2.5% were illiterate. The results showed that 88.4% of the participants used refined home water, 6.2% mineral water; only 5.4% drank tap water. With the family size, most participants (32.2%) were living in families with five members, 29.1% had six members, 28.4% had four members, 10.0% had three members or fewer, and 0.3% had seven or more members. Students with a frequency of 19.9% were the highest percentage, next were unemployed people (15.3%), housewives (12.3%), sellers (11.8%), workers (7.8%), drivers (5.9%), teachers (5.0), and 21.1% had jobs other than the jobs listed on the questionnaire. On washing hands before eating, 84.6% answered “yes” and 15.4% “no”; 54.8% said they disinfected raw fruits and vegetables with a disinfectant solution, 45.2% said they did not. Two questions concerned the consumption of restaurant salad and street foods: 49.9% and 17.0% answered “yes” and 50.1% and 82.1% answered “no”, respectively (Table 2). On how they get information on parasitic diseases, 21.6% of the participants selected the internet as an ideal source for obtaining information, 21.2% from television, 12.2% from friends and relatives, 6.9% from school and university, 1.4% from newspapers; the remaining 36.7% said they
Group
Frequency
%
Gender
Male Female 15-25 26-35 36-45 46-55 56-65 > 65 Illiteracy Primary school Middle school High school Academic Tap water Refined home Mineral water 2 3 4 5 6 ≥7 Unemployed Farmer Worker Teacher Housewife Student Driver Seller Others Yes No Yes No Yes No Yes No
1768 1732 927 845 829 473 410 16 86 209 305 1160 1740 188 3093 219 23 324 993 1130 1020 10 537 32 274 174 430 698 205 413 737 2960 540 1917 1583 1747 17.53 626 2874
50.5 49.5 26.5 24.1 23.7 13.5 11.7 0.5 2.5 6.0 8.7 33.1 49.7 5.4 88.4 6.2 0.7 9.3 28.4 32.2 29.1 0.3 15.3 0.9 7.8 5.0 12.3 19.9 5.9 11.8 21.1 84.6 15.4 54.8 45.2 49.9 50.1 17.9 82.1
Age groups (years)
Educational status
Drinking water source
Family size
Occupation
Hands washing before eating Disinfecting vegetables Restaurant salads consumption Street food consumption
Frequency
%
Internet Television School University Newspaper People More than one item Total
756 743 124 117 48 428 1284 3500
21.6 21.2 3.6 3.3 1.4 12.2 36.7 100.0
received the necessary information from more than one source (Table 3). 3.2. Knowledge of parasitic diseases Five questions were on knowledge of parasitic diseases. Of the 3500 participants, 348 (9.9%) had been infected with a parasitic disease at least once in their life. 1498 (42.8%) knew malaria was a parasitic disease; 1785 (50.2%), 1713 (48.9%), and 1452 (41.5%) were aware of the possible transmission of parasitic diseases through uncooked meat, dirty hands, and close contact with animals, respectively. Of the 348 participants who had been infected with a parasitic disease, 163 (46.8%) reported the heating of meat as a preventive way for some parasitic diseases, 273 (78.4%) had some information regarding the possible transmission of infection by dirty hands, and 248 (71.2%) were aware of the risk of infection by close contact with animals. On knowledge of soil contact and sexual transmission, participants believed that they might have a role in the transmission; 2561 (73.2%) and 1142 (32.6%) of the respondents knew diarrhea and abdominal pain were clinical symptoms of intestinal parasitic diseases, respectively. When asked about close contact with cats and the risk of infection and possible abortion in pregnant women, only 1049 (31.3%) were aware of that (Table 4).
Table 2 Socio-demographic information of Ahvaz inhabitants (N = 3500) participated in the study. Category
Category
3.3. Attitude toward treatment and prevention of parasitic diseases Two questions assessed participants’ attitude toward treatment and prevention of parasitic diseases. Most participants (3286, 93.9%) believe that if they suffer from a parasitic disease they will visit a doctor; however, 138 (3.9%) preferred self-medication and traditional medicine and the rest (2.2%) either did not take the infection seriously or did not know what to do. On the prevention of parasitic diseases, 47.5% believed that disinfecting fruits and vegetables could prevent intestinal parasitic infections. More details are shown in Table 5. 4. Discussion Parasitic diseases are among the most important infectious diseases, which have also been considered as such by Iranian ancient scientists. In the Avesta book, a disease with malaria-like symptoms is mentioned centuries BC. In addition, Abu Ali Sina (Avicenna), the Iranian philosopher and scientist, in the Canon of Medicine (the Law of Medicine) book discussed parasitic diseases, including cutaneous leishmaniasis, “Khayronieh”, and its treatment methods (Bahadori, 2016). Therefore, this fact can be accepted that Iran has been one of the most important foci of some parasitic diseases in the world in the past and present. Ascariasis was one of the most common parasitic diseases in Iran, in some parts of the country prevalence was 86.3% in 1961 but there was a dramatic decline in prevalence to 0.3% in 1995 (Askarian et al., 2012). Dracunculiasis, another helminthic infection, has not been reported in Iran since the 1970s (Askarian et al., 2012). On the other hand, in recent years we are witnessing emergent and re-emergent 213
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and Giardia duodenalis (9.09%). Therefore, it seems that the main cause of using refined water by 94.6% of the participants is their increased awareness regarding the risk of water-borne disease. Our data show that most households had 4–6 members (Table 2). Internet and television were the main sources of information for 21.6% and 21.2% of the participants, respectively. Interestingly, a small percentage of the participants mentioned school and university as their sources of information acquisition, while health educators have the role of health education in Iranian schools. A possible explanation for this might be that a large proportion of the students in the study may have been from non-medical sciences or their learned knowledge might be forgotten over time. Another notable finding was that 12.2% of the participants reported friends and relatives as suitable sources of information (Table 3). This result may be explained by the fact that the Internet and television can play an important role in increasing people’s information about parasitic diseases. Only 9.9% of the participants said that they had ever been infected with parasitic diseases at least once in their life. There are several possible explanations for this result. The first possibility is the infection with some parasites that might be asymptomatic. Another one is that the parasitic infection had not been detected. In addition, in some cases, parasitic disease might be diagnosed and treated; however, due to any reason, the patient forgot that once he was infected. Khuzestan Province was one of the foci of urinary schistosomiasis, hookworms, Trichostrongylus, and Trichuris in the last decades (Hamidinia et al., 2016; Massoud et al., 1980); however, in recent years, the prevalence of these parasites in the province has been decreasing or the parasites have been eradicated. Apart from climate changes (Hamidinia et al., 2016), it is likely that increased awareness of people about diseases has been effective. In this study, most participants (84.6%) said that they washed their hands before eating; 82.1% and 10% did not eat street food (Table 2). To evaluate the level of knowledge of the respondents, four diseases aids, malaria, brucellosis, and hepatitis were included in the questionnaire. More than a third (42.8%) said they knew malaria was a parasitic disease. The finding was higher than the reported 32.0%, 19.2% and 4.1% of knowledge about of schistosomiasis, malaria and STHs, respectively from Zimbabwe (Midzi et al., 2011) but lower than Li et al. study from China on cystic echinococcosis (Li et al., 2015). Malaria is an endemic disease in Iran and it was expected that a significant number of respondents would know about it. Probably, one of the main reasons for the decline in knowledge is because the disease has been controlled in recent years and its geographical distribution has been limited to the southern parts of the country (Askarian et al., 2012). Regarding transmission routes, approximately half of the participants were familiar with parasitic infections through contact with animals, dirty hands, soil contact, untreated water, and uncooked meat. Khuzestan Province is one of the endemic areas for some zoonotic and soiltransmitted parasitic infections, such as cystic echinococcosis, toxocariasis, and giardiasis (Alavi et al., 2011; Kasaei et al., 2018; Rokni, 2009). Thus, it can be concluded that one of the reasons for the decreasing occurrence of parasitic diseases in the province in recent years is the increasing knowledge and awareness of people on the transmission pathways of these diseases. Although trichomoniasis, one of the sexually transmitted infections, has been reported from Ahvaz County (Beiromvand and Daneshbakhtyar, 2016; Makvandi and Zargar Shoushtari, 2012), less than one fourth of the people knew about sexual transmission of the parasitic diseases. It appears that one of the main reasons for poor knowledge of this transmission route is that the risks of sexual transmission of the parasites may be considered negligible in Iranian schools, universities, or other public media. With regard to the clinical symptoms, most participants (73.2%) knew that diarrhea may be a clinical symptom of intestinal parasitic infections. Weight loss, abdominal pain and anemia, 35.6%, 32.6%, and 28.6%, respectively, were also known to be symptoms associated with parasitic diseases. It thus appears that the higher prevalence of intestinal parasitic infections
Table 4 Knowledge on parasitic diseases among Ahvaz inhabitants (N = 3500) participated in the study. Category Have you ever been infected with parasitic diseases? Do you know which disease is parasitic disease?
Do you know which may transfer parasitic diseases?
Which are the clinical symptoms of intestinal parasitic diseases?
Do you know that close contact with cats may cause human infection and increase the risk of abortion in pregnant women?
Yes No Aids Malaria Brucellosis Hepatitis Don't know Animal contact Soil contact Sexual contact Untreated water Dirty hands Uncooked meat Sweet foods Through sneezing All items Diarrhea Abdominal pain Anemia Weight loss Sore throat Yes No
Frequency
%
348 3152 215 1498 1030 81 676 1452 1273 810 1356
9.9 90.1 6.2 42.8 29.4 2.3 19.3 41.5 36.4 23.1 38.7
1713 1785
48.9 50.2
47 544
1.3 15.5
1500 2561 1142
42.9 73.2 32.6
1003 1247 68 1094 2406
28.6 35.6 1.9 31.3 68.7
Table 5 Attitude toward treatment and prevention of parasitic diseases among Ahvaz inhabitants (N = 3500) participated in the study. Category If you suffer from parasitic disease, which one to choose for treatment?
Which one prevents intestinal parasitic diseases?
Consult with a doctor Self-medication Traditional medicine Don't take seriously Don't know Disinfecting fruits and vegetables Cook meat Disinfecting fruits and vegetables/ Cook meat Wearing a face mask in public Don't know
Frequency
%
3286 42 96 52 24 1664
93.9 1.2 2.7 1.5 0.7 47.5
655 1064
18.7 30.4
46
1.3
71
2.1
parasitic disease such as microsporidiosis, cryptosporidiosis, and strongyloidosis in immunocompromised patients (Bahadori, 2016). Various factors contribute to reducing or increasing the incidence of these diseases. Among the factors effective in reducing incidence are improvement in sanitary conditions, access to clean water, and health education (Erismann et al., 2016). The current study assessed the participants’ knowledge and attitudes on parasitic diseases. Several variables such as age, gender, educational status, occupation, and family size were included in the study (Table 1). Demographic data showed that approximately half of the participants were in the group with university education and only 2.5% were illiterate. The water quality in Ahvaz County is low. In a study undertaken by Rahdar et al. (2014), 44 water samples collected from the Karun River, tap water, and refined home water in Ahvaz County were examined for the presence of intestinal parasites. The results revealed 63.6% intestinal parasitic infections, including Entamoeba spp. (50.0%), Cryptosporidium spp. (27.27%), Blastocystis spp. (13.63%),
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in Iran in the past decades, particularly of Ascaris lumbricoides, has changed the mentality of Iranian people toward diarrhea, that diarrhea may be due to intestinal parasitic infections. Another possible reason is the high frequency of intestinal protozoa, which cause diarrhea, such as Giardia duodenalis and Blastocystis hominis, in the province (Beiromvand et al., 2017; Kasaei et al., 2018; Rafiei et al., 2013; Salehi et al., 2017). In the current study, we also assessed participants’ knowledge of the risk of abortion caused by Toxoplasma gondii, due to close contact with cats. Most (68.7%) participants were not familiar with parasitic diseases transmitted by cats. Although Ahvaz County is an endemic area for toxoplasmosis (Saki et al., 2015), lack of enough knowledge about this disease can be a serious threat to high-risk persons (Table 4). On participants’ attitude to treatment of parasitic diseases, 93.9% said that if they were infected with a parasitic disease they preferred to consult with a doctor, while only a small percentage chose self-medication and traditional medicine as a suitable choice in treatment of parasitic infections. This finding is in line with a study from China on treatment of cystic echinococcosis (Li et al., 2015). One of the questions in the questionnaire was on prevention of intestinal parasites. Less than half of the participants (47.5%) claimed that disinfecting vegetables and fruits is one of the main ways of preventing intestinal parasitic infection, 18.7% said cooking meat, and 30.4% said disinfecting vegetables and fruits along with cooking meat. These results show that the people’s attitude on ways to prevent intestinal parasitic diseases is moderate and local health authorities should consider providing health education as a priority.
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5. Conclusion Despite the fact that malaria is endemic in Iran, there was moderate knowledge of it as a parasitic infection. The people’s knowledge of some transmission routes, such as soil and animal contact, dirty hands, untreated water, and uncooked meat, was favorable; however, knowledge of sexual transmission was low. Participants’ awareness was moderate regarding the possibility of increasing the risk of abortion through close contact with cats. Thus, it can be concluded that health authorities must be more concerned about the risk of sexually transmitted infections and should implement health education programs in schools and universities using public media to improve people's knowledge and awareness in order to increase the level of public health. Conflict of interest The authors have no conflict of interest. Funding source The present study was funded by grant (No. OG/96129) from Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, to Baghlaninezhad. Acknowledgments We thank all participants for helping us in collecting information for this study. References Acka, C.A., Raso, G., N’Goran, E.K., Tschannen, A.B., Bogoch, I.I., Seraphin, E., Tanner, M., Obrist, B., Utzinger, J., 2010. Parasitic worms: knowledge, attitudes, and practices in Western Cote d’Ivoire with implications for integrated control. PLoS Negl. Trop. Dis. 4, e910. https://doi.org/10.1371/journal.pntd.0000910. Alavi, S.M., Hosseini, S.A., Rahdar, M., Salmanzadeh, S.H., Nikkhuy, A.R., 2011. Determination of Seroprevalence Rate ofToxocara canis in 6-15 years Aged Rural and Urban School Children in Ahvaz, Iran. Jundishapur. J. Health. Sci 10, 240–248. Altinoz Aytar, A., Ozturk, E.C., Gocmen, S., Caliskan, E., Ozaras, F., Avcioglu, F., Yesildal
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Rokni, M.B., 2009. Echinococcosis/hydatidosis in Iran. Iran. J. Parasitol. 4, 1–16. Saki, J., Mohammadpour, N., Moramezi, F., Khademvatan, S., 2015. Seroprevalence ofToxoplasma gondii in Women Who Have Aborted in Comparison with the Women with Normal Delivery in Ahvaz, Southwest of Iran. Transfus. Apher. Sci. 2015, 764369. https://doi.org/10.1155/2015/764369. Salehi, R., Haghighi, A., Stensvold, C.R., Kheirandish, F., Azargashb, E., Raeghi, S., Kohansal, C., Bahrami, F., 2017. Prevalence and subtype identification of Blastocystis isolated from humans in Ahvaz, Southwestern Iran. Gastroenterol. Hepatol. Bed Benc 10, 235. Soleimani-Ahmadi, M., Vatandoost, H., Zare, M., Alizadeh, A., Salehi, M., 2014. Community knowledge and practices regarding malaria and long-lasting insecticidal nets during malaria elimination programme in an endemic area in Iran. Malar. J. 13, 511. https://doi.org/10.1186/1475-2875-13-511. WHO, 2017. Neglected Tropical Diseases. Accessed August 3, 2017. http://www.who. int/neglected_diseases/diseases/en/. Yan-Li, G., Yi-Qing, X., Yong-Gen, Z., Da-Cheng, X.U., Wen-Wei, X.U., Yang, D., MingXue, S., 2017. [Infection status of Toxoplasma gondii and its related knowledge and behavior among special population in Changzhou City]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 29, 498–501. https://doi.org/10.16250/j.32.1374.2016273. Zarasvandi, A., Carranza, E.J.M., Moore, F., Rastmanesh, F., 2011. Spatio-temporal occurrences and mineralogical–geochemical characteristics of airborne dusts in Khuzestan Province (southwestern Iran). J. Geochem. Explor. 111, 138–151. https:// doi.org/10.1016/j.gexplo.2011.04.004.
Massoud, J., Arfaa, F., Jalali, H., Keyvan, S., 1980. Prevalence of intestinal helminths in Khuzestan, Southwest Iran, 1977. Am. J. Trop. Med. Hyg. 29, 389–392. https://doi. org/10.4269/ajtmh.1980.29.389. Midzi, N., Mtapuri-Zinyowera, S., Mapingure, M.P., Paul, N.H., Sangweme, D., Hlerema, G., Mutsaka, M.J., Tongogara, F., Makware, G., Chadukura, V., Brouwer, K.C., Mutapi, F., Kumar, N., Mduluza, T., 2011. Knowledge attitudes and practices of grade three primary schoolchildren in relation to schistosomiasis, soil transmitted helminthiasis and malaria in Zimbabwe. BMC Infect. Dis. 11, 169. https://doi.org/10. 1186/1471-2334-11-169. Mohammadi Dehcheshmeh, M., Sajadian, N., Shojaeyan, A., Gheysari, N., 2018. Comparative study of leisure geography in Ahvaz metropolitan. J Geo Sci 18, 217–239 (in Persian). Nejati, J., Moosa-Kazemi, S.H., Saghafipour, A., Soofi, K., 2018. Knowledge, attitude and practice (KAP) on malaria, from high malaria burden rural communities, southeastern Iran. J. Parasit. Dis. 42, 62–67. https://doi.org/10.1007/s12639-017-0965-8. Person, B., Ali, S.M., A’Kadir, F.M., Ali, J.N., Mohammed, U.A., Mohammed, K.A., Rollinson, D., Knopp, S., 2016. Community knowledge, perceptions, and practices associated with urogenital schistosomiasis among school-aged children in Zanzibar, United Republic of Tanzania. PLoS Negl. Trop. Dis. 10, e0004814. https://doi.org/ 10.1371/journal.pntd.0004814. Rafiei, A., Roointan, E.S., Samarbafzadeh, A.R., Shayesteh, A.A., Shamsizadeh, A., Pourmahdi Borujeni, M., 2013. Investigation of possible correlation between Giardia duodenalis genotypes and clinical symptoms in southwest of Iran. Iran. J. Parasitol. 8, 389–395.
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Analysis of knowledge and attitudes related to parasitic infections among inhabitants of Ahvaz County, Khuzestan Province, Iran
T
⁎
Raheleh Baghlaninezhada,b, Molouk Beiromvanda,b, , Mohammad Salehi Veisic a
Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran Department of Parasitology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran c Department of Statistics, Faculty of Basic Science, Behbahan Khatam Alanbia University of Technology, Behbahan, Iran b
A R T I C LE I N FO
A B S T R A C T
Keywords: Knowledge Attitudes Parasitic infections Khuzestan Province Iran
Parasitic diseases are among the major health problems of various societies, especially people in developing countries, causing high economic and mortality burdens. Many researchers have reported that awareness and knowledge of a disease are effective in preventing and controlling the disease. The aim of the present study was to assess the knowledge and attitudes on parasitic diseases of the population in Ahvaz County, southwestern Iran. This community-based cross-sectional study was carried out in 2017 on 3500 subjects above 15 years old of Ahvaz County. First, participants were provided the necessary information regarding the study, and then data were collected using a constructed questionnaire. Of the 3500 participants, 1732 (49.5%) were female and 1768 (50.5%) were male, 348 (9.9%) said that they had been infected with a parasitic disease at least once in their lifetime. Almost half of the participants (42.8%) knew malaria was a parasitic disease and 50.2%, 48.9%, and 41.5% were aware of the possible transmission of parasitic diseases through uncooked meat, dirty hands, and close contact with animals. Regarding clinical symptoms, 73.2% and 32.6% of the respondents knew diarrhea and abdominal pain respectively were clinical symptoms of intestinal parasitic diseases. However, only 31.3% were aware of the close contact with cats and the risk of human toxoplasmosis and possible abortion in pregnant women. The findings reveal that the attitude of most participants toward treatment was positive (93.9%), but only 47.5% of believed that disinfecting fruits and vegetables could prevent intestinal parasitic infections.
1. Introduction Parasitic diseases are one of the main problems of public health, especially among children, in low and middle-income countries (Erismann et al., 2016). These diseases are among the diseases that cause economic and mortality burdens globally (Isah et al., 2016). Among them, malaria, leishmaniasis, trypanosomiasis, schistosomiasis, echinococcosis, onchocerciasis, taeniasis/cysticercosis, and lymphatic filariasis affect millions of people causing thousands of deaths annually (Isah et al., 2016; WHO, 2017). In recent years, some protozoan and metazoan diseases such as leishmaniasis, human African trypanosomiasis, and schistosomiasis, as well as soil-transmitted helminths have been considered as neglected tropical diseases (NTDs). (Erismann et al., 2016; WHO, 2017). It is estimated that one-third of the three billion people who are living in developing regions of Asia, Sub-Saharan Africa, and the Americas suffer a group of protozoan and helminthic
infections belonging to the NTDs (Bhutta et al., 2014). The worst affected people are those who live in poverty; that is, the population living in areas with poor sanitation and being in close contact with infectious vectors, domestic animals as well as livestock (WHO, 2017). Parasitic infections may be influenced by various factors such as socioeconomic, behavioral, health, environmental, and biological agents. In addition, educational status, occupation, and monthly income can influence the risk of parasitic infection, transmission, and associated morbidity and mortality (Gelaw et al., 2013). In Iran, some parasitic diseases such as hookworms and ascariasis have declined significantly in recent years (Askarian et al., 2012); however, cutaneous and visceral leishmaniasis, malaria, giardiasis, hydatidosis, and fascioliasis are still considered some of the main public health problems (Askarian et al., 2012; Bahadori, 2016). Giardiasis, with a prevalence of 1%–60% (Hatam-Nahavandi et al., 2017), is the most common protozoan disease in Iran; hydatidosis with a prevalence
⁎ Corresponding author at: Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, P.O. Box 61357, 15794, Ahvaz, Iran. E-mail address: [email protected] (M. Beiromvand).
https://doi.org/10.1016/j.actatropica.2019.03.014 Received 27 July 2018; Received in revised form 22 February 2019; Accepted 10 March 2019 Available online 11 March 2019 0001-706X/ © 2019 Elsevier B.V. All rights reserved.
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of 1.18–3 per 100,000 in the human population and with an annual economic loss of USD 459,650 in ruminants, is one of the most costly infectious diseases (Fasihi Harandi et al., 2012). Many researchers believe that awareness and knowledge of a disease are important in preventing and controlling it (Khan et al., 2018). To achieve this awareness and behavioral changes, health education is needed (Acka et al., 2010). In recent years, many studies have focused on assessing people's awareness and attitudes about parasitic diseases globally (Acka et al., 2010; Altinoz Aytar et al., 2015; Elsafi et al., 2015; Elyana et al., 2016; Khan et al., 2018; Kungu et al., 2017; Li et al., 2015; Person et al., 2016; Yan-Li et al., 2017); however, in Iran, data on knowledge and awareness of people concerning parasitic diseases are insufficient and mainly focused on malaria (Fekri et al., 2014; Madani et al., 2017; Nejati et al., 2018; Soleimani-Ahmadi et al., 2014). Because the lack of knowledge and awareness of parasitic diseases, their transmission routes, treatment and prevention may increase the chances of infection, the current study was designed to assess the knowledge and attitudes on parasitic diseases of the people of Ahvaz County, southwest Iran.
Table 1 The variables studied in the current study. No.
Variable
No.
Variable
1 2 3 4 5
Gender Age Educational status Occupation Family size
6 7 8 9 10
Source of drinking water Hand washing Disinfecting vegetables Restaurant salads consumption Street food consumption
2.3. Study design and sample population This cross-sectional study was performed in 2017 using simple random sampling method. In total, 3500 participants above 15 years old from the different districts of the county enrolled in the study. The number of participants from each district was selected according to its population. The study objectives were explained to the participants in an interview in their two native languages (Persian and Arabic). Participants were asked to complete a questionnaire and those who were illiterate or had eyesight problems were assisted by one of their family members or a researcher. In the current study, we evaluated participants from different occupations and levels of education.
2. Methods 2.1. Ethical statements
2.4. Questionnaire
The ethics committee of Ahvaz Jundishapur University of Medical Sciences reviewed and approved the protocol (approval number: IR.AJUMS.REC.2018–701). Informed consent was obtained from the participants.
2.4.1. Socio-demographic questions The first part of the questionnaire related to socio-demographic data: gender, age, educational level, occupation, family size, type of drinking water, hand-washing before eating, disinfecting vegetables, consumption of restaurant salads, consumption of street food, and ways of obtaining information on parasitic diseases (Table 1).
2.2. Study area Ahvaz County, the capital of Khuzestan Province in southwestern Iran (31°19′ N 48°40′ E) lies at an altitude of approximately 17 m. The county has an area of 815 km2 and an estimated population of 1,136,989 persons. One of the country’s largest rivers and the only navigable river, the Karun, runs through the middle of Ahvaz County. Ahvaz weather is usually warm and dry, and occasionally humid in summer (Zarasvandi et al., 2011). In recent years, due to low rainfall and drought, the southwestern regions of Iran, particularly Ahvaz County, have faced dust storms, turning Ahvaz into the most polluted city in the world (Maleki et al., 2016). The dominant ethnicities of the city are Persians, Lurs and Arabs. Ahvaz County is divided into eight districts (Fig. 1) (Mohammadi Dehcheshmeh et al., 2018).
2.4.2. Knowledge and attitude questions The second part included questions on familiarity with parasitic diseases, transmission routes, clinical symptoms of intestinal parasitic diseases, prevention and control of parasitic diseases, and familiarity with parasites treatment.
2.5. Statistical analyses All statistical analyses were performed with SPSS Statistics 18 (SPSS Inc., Chicago, IL, USA).
Fig. 1. Map of Iran. Khuzestan Province, highlighted in yellow based on the map of Iran at (Beiromvand et al., 2013). Map of Ahvaz County with studied regions indicated by numbers (Mohammadi Dehcheshmeh et al., 2018). 212
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3. Results
Table 3 Knowing parasitic diseases ways among Ahvaz inhabitants (N = 3500) participated in the study.
3.1. Socio-demographic characteristics In this study, all 3500 participants completed the questionnaire; 1732 (49.5%) were female and 1768 (50.5%) were male. The maximum and minimum number of participants, 26.5% and 0.5% respectively, belonged to the age groups 15–25 and above 65 years old, respectively. On education levels, 49.7% had a degree and 2.5% were illiterate. The results showed that 88.4% of the participants used refined home water, 6.2% mineral water; only 5.4% drank tap water. With the family size, most participants (32.2%) were living in families with five members, 29.1% had six members, 28.4% had four members, 10.0% had three members or fewer, and 0.3% had seven or more members. Students with a frequency of 19.9% were the highest percentage, next were unemployed people (15.3%), housewives (12.3%), sellers (11.8%), workers (7.8%), drivers (5.9%), teachers (5.0), and 21.1% had jobs other than the jobs listed on the questionnaire. On washing hands before eating, 84.6% answered “yes” and 15.4% “no”; 54.8% said they disinfected raw fruits and vegetables with a disinfectant solution, 45.2% said they did not. Two questions concerned the consumption of restaurant salad and street foods: 49.9% and 17.0% answered “yes” and 50.1% and 82.1% answered “no”, respectively (Table 2). On how they get information on parasitic diseases, 21.6% of the participants selected the internet as an ideal source for obtaining information, 21.2% from television, 12.2% from friends and relatives, 6.9% from school and university, 1.4% from newspapers; the remaining 36.7% said they
Group
Frequency
%
Gender
Male Female 15-25 26-35 36-45 46-55 56-65 > 65 Illiteracy Primary school Middle school High school Academic Tap water Refined home Mineral water 2 3 4 5 6 ≥7 Unemployed Farmer Worker Teacher Housewife Student Driver Seller Others Yes No Yes No Yes No Yes No
1768 1732 927 845 829 473 410 16 86 209 305 1160 1740 188 3093 219 23 324 993 1130 1020 10 537 32 274 174 430 698 205 413 737 2960 540 1917 1583 1747 17.53 626 2874
50.5 49.5 26.5 24.1 23.7 13.5 11.7 0.5 2.5 6.0 8.7 33.1 49.7 5.4 88.4 6.2 0.7 9.3 28.4 32.2 29.1 0.3 15.3 0.9 7.8 5.0 12.3 19.9 5.9 11.8 21.1 84.6 15.4 54.8 45.2 49.9 50.1 17.9 82.1
Age groups (years)
Educational status
Drinking water source
Family size
Occupation
Hands washing before eating Disinfecting vegetables Restaurant salads consumption Street food consumption
Frequency
%
Internet Television School University Newspaper People More than one item Total
756 743 124 117 48 428 1284 3500
21.6 21.2 3.6 3.3 1.4 12.2 36.7 100.0
received the necessary information from more than one source (Table 3). 3.2. Knowledge of parasitic diseases Five questions were on knowledge of parasitic diseases. Of the 3500 participants, 348 (9.9%) had been infected with a parasitic disease at least once in their life. 1498 (42.8%) knew malaria was a parasitic disease; 1785 (50.2%), 1713 (48.9%), and 1452 (41.5%) were aware of the possible transmission of parasitic diseases through uncooked meat, dirty hands, and close contact with animals, respectively. Of the 348 participants who had been infected with a parasitic disease, 163 (46.8%) reported the heating of meat as a preventive way for some parasitic diseases, 273 (78.4%) had some information regarding the possible transmission of infection by dirty hands, and 248 (71.2%) were aware of the risk of infection by close contact with animals. On knowledge of soil contact and sexual transmission, participants believed that they might have a role in the transmission; 2561 (73.2%) and 1142 (32.6%) of the respondents knew diarrhea and abdominal pain were clinical symptoms of intestinal parasitic diseases, respectively. When asked about close contact with cats and the risk of infection and possible abortion in pregnant women, only 1049 (31.3%) were aware of that (Table 4).
Table 2 Socio-demographic information of Ahvaz inhabitants (N = 3500) participated in the study. Category
Category
3.3. Attitude toward treatment and prevention of parasitic diseases Two questions assessed participants’ attitude toward treatment and prevention of parasitic diseases. Most participants (3286, 93.9%) believe that if they suffer from a parasitic disease they will visit a doctor; however, 138 (3.9%) preferred self-medication and traditional medicine and the rest (2.2%) either did not take the infection seriously or did not know what to do. On the prevention of parasitic diseases, 47.5% believed that disinfecting fruits and vegetables could prevent intestinal parasitic infections. More details are shown in Table 5. 4. Discussion Parasitic diseases are among the most important infectious diseases, which have also been considered as such by Iranian ancient scientists. In the Avesta book, a disease with malaria-like symptoms is mentioned centuries BC. In addition, Abu Ali Sina (Avicenna), the Iranian philosopher and scientist, in the Canon of Medicine (the Law of Medicine) book discussed parasitic diseases, including cutaneous leishmaniasis, “Khayronieh”, and its treatment methods (Bahadori, 2016). Therefore, this fact can be accepted that Iran has been one of the most important foci of some parasitic diseases in the world in the past and present. Ascariasis was one of the most common parasitic diseases in Iran, in some parts of the country prevalence was 86.3% in 1961 but there was a dramatic decline in prevalence to 0.3% in 1995 (Askarian et al., 2012). Dracunculiasis, another helminthic infection, has not been reported in Iran since the 1970s (Askarian et al., 2012). On the other hand, in recent years we are witnessing emergent and re-emergent 213
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and Giardia duodenalis (9.09%). Therefore, it seems that the main cause of using refined water by 94.6% of the participants is their increased awareness regarding the risk of water-borne disease. Our data show that most households had 4–6 members (Table 2). Internet and television were the main sources of information for 21.6% and 21.2% of the participants, respectively. Interestingly, a small percentage of the participants mentioned school and university as their sources of information acquisition, while health educators have the role of health education in Iranian schools. A possible explanation for this might be that a large proportion of the students in the study may have been from non-medical sciences or their learned knowledge might be forgotten over time. Another notable finding was that 12.2% of the participants reported friends and relatives as suitable sources of information (Table 3). This result may be explained by the fact that the Internet and television can play an important role in increasing people’s information about parasitic diseases. Only 9.9% of the participants said that they had ever been infected with parasitic diseases at least once in their life. There are several possible explanations for this result. The first possibility is the infection with some parasites that might be asymptomatic. Another one is that the parasitic infection had not been detected. In addition, in some cases, parasitic disease might be diagnosed and treated; however, due to any reason, the patient forgot that once he was infected. Khuzestan Province was one of the foci of urinary schistosomiasis, hookworms, Trichostrongylus, and Trichuris in the last decades (Hamidinia et al., 2016; Massoud et al., 1980); however, in recent years, the prevalence of these parasites in the province has been decreasing or the parasites have been eradicated. Apart from climate changes (Hamidinia et al., 2016), it is likely that increased awareness of people about diseases has been effective. In this study, most participants (84.6%) said that they washed their hands before eating; 82.1% and 10% did not eat street food (Table 2). To evaluate the level of knowledge of the respondents, four diseases aids, malaria, brucellosis, and hepatitis were included in the questionnaire. More than a third (42.8%) said they knew malaria was a parasitic disease. The finding was higher than the reported 32.0%, 19.2% and 4.1% of knowledge about of schistosomiasis, malaria and STHs, respectively from Zimbabwe (Midzi et al., 2011) but lower than Li et al. study from China on cystic echinococcosis (Li et al., 2015). Malaria is an endemic disease in Iran and it was expected that a significant number of respondents would know about it. Probably, one of the main reasons for the decline in knowledge is because the disease has been controlled in recent years and its geographical distribution has been limited to the southern parts of the country (Askarian et al., 2012). Regarding transmission routes, approximately half of the participants were familiar with parasitic infections through contact with animals, dirty hands, soil contact, untreated water, and uncooked meat. Khuzestan Province is one of the endemic areas for some zoonotic and soiltransmitted parasitic infections, such as cystic echinococcosis, toxocariasis, and giardiasis (Alavi et al., 2011; Kasaei et al., 2018; Rokni, 2009). Thus, it can be concluded that one of the reasons for the decreasing occurrence of parasitic diseases in the province in recent years is the increasing knowledge and awareness of people on the transmission pathways of these diseases. Although trichomoniasis, one of the sexually transmitted infections, has been reported from Ahvaz County (Beiromvand and Daneshbakhtyar, 2016; Makvandi and Zargar Shoushtari, 2012), less than one fourth of the people knew about sexual transmission of the parasitic diseases. It appears that one of the main reasons for poor knowledge of this transmission route is that the risks of sexual transmission of the parasites may be considered negligible in Iranian schools, universities, or other public media. With regard to the clinical symptoms, most participants (73.2%) knew that diarrhea may be a clinical symptom of intestinal parasitic infections. Weight loss, abdominal pain and anemia, 35.6%, 32.6%, and 28.6%, respectively, were also known to be symptoms associated with parasitic diseases. It thus appears that the higher prevalence of intestinal parasitic infections
Table 4 Knowledge on parasitic diseases among Ahvaz inhabitants (N = 3500) participated in the study. Category Have you ever been infected with parasitic diseases? Do you know which disease is parasitic disease?
Do you know which may transfer parasitic diseases?
Which are the clinical symptoms of intestinal parasitic diseases?
Do you know that close contact with cats may cause human infection and increase the risk of abortion in pregnant women?
Yes No Aids Malaria Brucellosis Hepatitis Don't know Animal contact Soil contact Sexual contact Untreated water Dirty hands Uncooked meat Sweet foods Through sneezing All items Diarrhea Abdominal pain Anemia Weight loss Sore throat Yes No
Frequency
%
348 3152 215 1498 1030 81 676 1452 1273 810 1356
9.9 90.1 6.2 42.8 29.4 2.3 19.3 41.5 36.4 23.1 38.7
1713 1785
48.9 50.2
47 544
1.3 15.5
1500 2561 1142
42.9 73.2 32.6
1003 1247 68 1094 2406
28.6 35.6 1.9 31.3 68.7
Table 5 Attitude toward treatment and prevention of parasitic diseases among Ahvaz inhabitants (N = 3500) participated in the study. Category If you suffer from parasitic disease, which one to choose for treatment?
Which one prevents intestinal parasitic diseases?
Consult with a doctor Self-medication Traditional medicine Don't take seriously Don't know Disinfecting fruits and vegetables Cook meat Disinfecting fruits and vegetables/ Cook meat Wearing a face mask in public Don't know
Frequency
%
3286 42 96 52 24 1664
93.9 1.2 2.7 1.5 0.7 47.5
655 1064
18.7 30.4
46
1.3
71
2.1
parasitic disease such as microsporidiosis, cryptosporidiosis, and strongyloidosis in immunocompromised patients (Bahadori, 2016). Various factors contribute to reducing or increasing the incidence of these diseases. Among the factors effective in reducing incidence are improvement in sanitary conditions, access to clean water, and health education (Erismann et al., 2016). The current study assessed the participants’ knowledge and attitudes on parasitic diseases. Several variables such as age, gender, educational status, occupation, and family size were included in the study (Table 1). Demographic data showed that approximately half of the participants were in the group with university education and only 2.5% were illiterate. The water quality in Ahvaz County is low. In a study undertaken by Rahdar et al. (2014), 44 water samples collected from the Karun River, tap water, and refined home water in Ahvaz County were examined for the presence of intestinal parasites. The results revealed 63.6% intestinal parasitic infections, including Entamoeba spp. (50.0%), Cryptosporidium spp. (27.27%), Blastocystis spp. (13.63%),
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in Iran in the past decades, particularly of Ascaris lumbricoides, has changed the mentality of Iranian people toward diarrhea, that diarrhea may be due to intestinal parasitic infections. Another possible reason is the high frequency of intestinal protozoa, which cause diarrhea, such as Giardia duodenalis and Blastocystis hominis, in the province (Beiromvand et al., 2017; Kasaei et al., 2018; Rafiei et al., 2013; Salehi et al., 2017). In the current study, we also assessed participants’ knowledge of the risk of abortion caused by Toxoplasma gondii, due to close contact with cats. Most (68.7%) participants were not familiar with parasitic diseases transmitted by cats. Although Ahvaz County is an endemic area for toxoplasmosis (Saki et al., 2015), lack of enough knowledge about this disease can be a serious threat to high-risk persons (Table 4). On participants’ attitude to treatment of parasitic diseases, 93.9% said that if they were infected with a parasitic disease they preferred to consult with a doctor, while only a small percentage chose self-medication and traditional medicine as a suitable choice in treatment of parasitic infections. This finding is in line with a study from China on treatment of cystic echinococcosis (Li et al., 2015). One of the questions in the questionnaire was on prevention of intestinal parasites. Less than half of the participants (47.5%) claimed that disinfecting vegetables and fruits is one of the main ways of preventing intestinal parasitic infection, 18.7% said cooking meat, and 30.4% said disinfecting vegetables and fruits along with cooking meat. These results show that the people’s attitude on ways to prevent intestinal parasitic diseases is moderate and local health authorities should consider providing health education as a priority.
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5. Conclusion Despite the fact that malaria is endemic in Iran, there was moderate knowledge of it as a parasitic infection. The people’s knowledge of some transmission routes, such as soil and animal contact, dirty hands, untreated water, and uncooked meat, was favorable; however, knowledge of sexual transmission was low. Participants’ awareness was moderate regarding the possibility of increasing the risk of abortion through close contact with cats. Thus, it can be concluded that health authorities must be more concerned about the risk of sexually transmitted infections and should implement health education programs in schools and universities using public media to improve people's knowledge and awareness in order to increase the level of public health. Conflict of interest The authors have no conflict of interest. Funding source The present study was funded by grant (No. OG/96129) from Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran, to Baghlaninezhad. Acknowledgments We thank all participants for helping us in collecting information for this study. References Acka, C.A., Raso, G., N’Goran, E.K., Tschannen, A.B., Bogoch, I.I., Seraphin, E., Tanner, M., Obrist, B., Utzinger, J., 2010. Parasitic worms: knowledge, attitudes, and practices in Western Cote d’Ivoire with implications for integrated control. PLoS Negl. Trop. Dis. 4, e910. https://doi.org/10.1371/journal.pntd.0000910. Alavi, S.M., Hosseini, S.A., Rahdar, M., Salmanzadeh, S.H., Nikkhuy, A.R., 2011. Determination of Seroprevalence Rate ofToxocara canis in 6-15 years Aged Rural and Urban School Children in Ahvaz, Iran. Jundishapur. J. Health. Sci 10, 240–248. Altinoz Aytar, A., Ozturk, E.C., Gocmen, S., Caliskan, E., Ozaras, F., Avcioglu, F., Yesildal
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