Background The incidence of fractures in rural populations is lower than in urban populations, although the reason for this difference is unclear. This cross-sectional study was designed to examine the difference in bone mineral density (BMD), a primary predictor of fracture risk, between urban and rural Thai populations.
Background
The incidence of fractures in rural populations is lower than in urban populations, although the reason for this difference is unclear. This cross-sectional study was designed to examine the difference in bone mineral density (BMD), a primary predictor of fracture risk, between urban and rural Thai populations.Methods Femoral neck and lumbar spine BMD was measured by dual-energy X-ray absorptiometry (GE Lunar, Madison, WI) in 411 urban and 436 rural subjects (340 men and 507 women), aged between 20 and 84 years. Body mass index (BMI) was calculated from weight and height.
Methods
Femoral neck and lumbar spine BMD was measured by dual-energy X-ray absorptiometry (GE Lunar, Madison, WI) in 411 urban and 436 rural subjects (340 men and 507 women), aged between 20 and 84 years. Body mass index (BMI) was calculated from weight and height.Results After adjusting for age and body weight in an analysis of covariance model, femoral neck BMD in rural men and women was significantly higher than those in urban men and women ( P  < 0.001), but the difference was not observed at the lumbar spine. After stratifying by sex, age group, and BMI category, the urban-rural difference in femoral neck BMD became more pronounced in men and women aged <50 years and with BMI ≥ 25 kg/m 2 .
Results
After adjusting for age and body weight in an analysis of covariance model, femoral neck BMD in rural men and women was significantly higher than those in urban men and women ( P  < 0.001), but the difference was not observed at the lumbar spine. After stratifying by sex, age group, and BMI category, the urban-rural difference in femoral neck BMD became more pronounced in men and women aged <50 years and with BMI ≥ 25 kg/m 2 .PConclusions These data suggest that femoral neck BMD in rural men and women was higher than their counterparts in urban areas. This difference could potentially explain part of the urban-rural difference in fracture incidence.
Conclusions
These data suggest that femoral neck BMD in rural men and women was higher than their counterparts in urban areas. This difference could potentially explain part of the urban-rural difference in fracture incidence.

Background Osteoporosis and its ultimate consequence of low traumatic fracture pose a major public health problem, because it incurs significant costs and increased risk of mortality [ 1 - 3 ]. Osteoporosis is sometimes considered a "consequence" of modernization, because the incidence of fractures in urban regions is often higher than in rural regions [ 4 - 10 ], although the underlying reason for this trend is largely unknown. Measurement of bone mineral density (BMD) is considered the primary predictor of fracture risk [ 11 ]. Therefore, it could be hypothesized that the urban-rural difference in fracture incidence is partly explained by the urban-rural difference in BMD. However, such a difference has not been well documented due to limited data available [ 12 - 14 ]. Some previous studies reported that rural subjects had higher BMD or bone mineral content (BMC) than those urban subjects [ 12 , 13 ], but another study found no such difference [ 14 ]. The pace of urbanization in developing countries is more pronounced than in developed countries. Therefore, developing countries are ideal settings for studying the urban-rural difference in BMD. The aim of this study was to examine the difference in BMD between an urban population and a rural population in Thailand.
Background
Osteoporosis and its ultimate consequence of low traumatic fracture pose a major public health problem, because it incurs significant costs and increased risk of mortality [ 1 - 3 ]. Osteoporosis is sometimes considered a "consequence" of modernization, because the incidence of fractures in urban regions is often higher than in rural regions [ 4 - 10 ], although the underlying reason for this trend is largely unknown.Measurement of bone mineral density (BMD) is considered the primary predictor of fracture risk [ 11 ]. Therefore, it could be hypothesized that the urban-rural difference in fracture incidence is partly explained by the urban-rural difference in BMD. However, such a difference has not been well documented due to limited data available [ 12 - 14 ]. Some previous studies reported that rural subjects had higher BMD or bone mineral content (BMC) than those urban subjects [ 12 , 13 ], but another study found no such difference [ 14 ].The pace of urbanization in developing countries is more pronounced than in developed countries. Therefore, developing countries are ideal settings for studying the urban-rural difference in BMD. The aim of this study was to examine the difference in BMD between an urban population and a rural population in Thailand.Methods Setting and subjects The present study was designed as a cross-sectional, population-based investigation. The setting was Bangkok city and Khon Kaen province in Thailand. Bangkok is the capital city with a population of 5.7 million and Khon Kaen is a rural province, located 445 km northeast of Bangkok with a population of 1.8 million and is largely an agricultural community. Further details of this study have been described elsewhere [ 15 ] The study included 872 Thai men and women, aged between 20 and 84 years, of whom 422 subjects were from Bangkok and 450 subjects from Khon Kaen. In Khon Kaen, subjects were recruited from 2 villages in the Muang district. There were 14 hamlets in the two villages. In each hamlet, a full list of subjects was obtained, from which 40 subjects were randomly selected by the village's administrator. The selected subjects were then sent a letter of invitation to participating in the study. The response rate was 80.3%. In Bangkok, subjects were recruited via a media campaign, and the sampling technique was similar to the scheme used in Khon Kaen, where subjects were randomly selected from 5 districts within the city of Bangkok. All Khon Kaen subjects were farmers, while Bangkok subjects were office workers, factory workers or house workers. Twenty-one subjects were excluded from analysis because of bone disorders, chronic diseases, history of taking medications that are deemed to affect calcium and bone metabolism, such as the use of steroids or thyroid hormone; and 4 women were excluded on the basis of pregnancy, lactation, delivery or abortion within the previous 3 months, previous history of oophorectomy and premature menopause. The study was conducted in accordance with the Helsinski Declaration in 1975 and as revised in 1983 and was approved by the Ethics Committee of Faculty of Medicine Ramathibodi Hospital Mahidol University (Bangkok) and Khon Kaen University (Khon Kaen), and written informed consent was obtained from all subjects. Measurements BMD at the femoral neck and lumbar spine (L2-4) in g/cm 2 , was measured by dual-energy X-ray absorptiometry with a Lunar DXP-IQ densitometer (GE Lunar Radiation Corp, Madison, WI, USA). The two study sites (Bangkok and Khon Kaen) used the same model of the DXA machine and the same protocol of measurements. The radiation dose with this method is < 0.1  μ Gy. The coefficient of variation of BMD for normal subjects is 0.96 and 0.98 at proximal femur and lumbar spine, respectively. Body weight (including light indoor clothing) was measured using an electronic balance (accuracy 0.1 kg) and standing height (without shoes) with a standiometer (nearest 0.1 cm). Body mass index (BMI) was calculated as ratio of weight (in kg) over height (in meter squared). Statistical analyses Descriptive statistics were computed for each residential region and sex separately. In order to test for difference between urban and rural regions, an analysis of covariance (ANCOVA) model was performed. In this model, BMD was treated as outcome variables; age and weight (or BMI) were treated as covariates; and residence (urban or rural) was the factor. Interactions between age and BMI or age and residence variable were also considered in the model. Estimates of the model parameters were based on the least square method via the SPSS version 9.0 (SPSS, Inc, Chicago).
Methods
Setting and subjects The present study was designed as a cross-sectional, population-based investigation. The setting was Bangkok city and Khon Kaen province in Thailand. Bangkok is the capital city with a population of 5.7 million and Khon Kaen is a rural province, located 445 km northeast of Bangkok with a population of 1.8 million and is largely an agricultural community. Further details of this study have been described elsewhere [ 15 ] The study included 872 Thai men and women, aged between 20 and 84 years, of whom 422 subjects were from Bangkok and 450 subjects from Khon Kaen. In Khon Kaen, subjects were recruited from 2 villages in the Muang district. There were 14 hamlets in the two villages. In each hamlet, a full list of subjects was obtained, from which 40 subjects were randomly selected by the village's administrator. The selected subjects were then sent a letter of invitation to participating in the study. The response rate was 80.3%. In Bangkok, subjects were recruited via a media campaign, and the sampling technique was similar to the scheme used in Khon Kaen, where subjects were randomly selected from 5 districts within the city of Bangkok. All Khon Kaen subjects were farmers, while Bangkok subjects were office workers, factory workers or house workers. Twenty-one subjects were excluded from analysis because of bone disorders, chronic diseases, history of taking medications that are deemed to affect calcium and bone metabolism, such as the use of steroids or thyroid hormone; and 4 women were excluded on the basis of pregnancy, lactation, delivery or abortion within the previous 3 months, previous history of oophorectomy and premature menopause. The study was conducted in accordance with the Helsinski Declaration in 1975 and as revised in 1983 and was approved by the Ethics Committee of Faculty of Medicine Ramathibodi Hospital Mahidol University (Bangkok) and Khon Kaen University (Khon Kaen), and written informed consent was obtained from all subjects.
Setting and subjects
The present study was designed as a cross-sectional, population-based investigation. The setting was Bangkok city and Khon Kaen province in Thailand. Bangkok is the capital city with a population of 5.7 million and Khon Kaen is a rural province, located 445 km northeast of Bangkok with a population of 1.8 million and is largely an agricultural community. Further details of this study have been described elsewhere [ 15 ]The study included 872 Thai men and women, aged between 20 and 84 years, of whom 422 subjects were from Bangkok and 450 subjects from Khon Kaen. In Khon Kaen, subjects were recruited from 2 villages in the Muang district. There were 14 hamlets in the two villages. In each hamlet, a full list of subjects was obtained, from which 40 subjects were randomly selected by the village's administrator. The selected subjects were then sent a letter of invitation to participating in the study. The response rate was 80.3%. In Bangkok, subjects were recruited via a media campaign, and the sampling technique was similar to the scheme used in Khon Kaen, where subjects were randomly selected from 5 districts within the city of Bangkok.All Khon Kaen subjects were farmers, while Bangkok subjects were office workers, factory workers or house workers. Twenty-one subjects were excluded from analysis because of bone disorders, chronic diseases, history of taking medications that are deemed to affect calcium and bone metabolism, such as the use of steroids or thyroid hormone; and 4 women were excluded on the basis of pregnancy, lactation, delivery or abortion within the previous 3 months, previous history of oophorectomy and premature menopause. The study was conducted in accordance with the Helsinski Declaration in 1975 and as revised in 1983 and was approved by the Ethics Committee of Faculty of Medicine Ramathibodi Hospital Mahidol University (Bangkok) and Khon Kaen University (Khon Kaen), and written informed consent was obtained from all subjects.Measurements BMD at the femoral neck and lumbar spine (L2-4) in g/cm 2 , was measured by dual-energy X-ray absorptiometry with a Lunar DXP-IQ densitometer (GE Lunar Radiation Corp, Madison, WI, USA). The two study sites (Bangkok and Khon Kaen) used the same model of the DXA machine and the same protocol of measurements. The radiation dose with this method is < 0.1  μ Gy. The coefficient of variation of BMD for normal subjects is 0.96 and 0.98 at proximal femur and lumbar spine, respectively. Body weight (including light indoor clothing) was measured using an electronic balance (accuracy 0.1 kg) and standing height (without shoes) with a standiometer (nearest 0.1 cm). Body mass index (BMI) was calculated as ratio of weight (in kg) over height (in meter squared).
Measurements
BMD at the femoral neck and lumbar spine (L2-4) in g/cm 2 , was measured by dual-energy X-ray absorptiometry with a Lunar DXP-IQ densitometer (GE Lunar Radiation Corp, Madison, WI, USA). The two study sites (Bangkok and Khon Kaen) used the same model of the DXA machine and the same protocol of measurements. The radiation dose with this method is < 0.1  μ Gy. The coefficient of variation of BMD for normal subjects is 0.96 and 0.98 at proximal femur and lumbar spine, respectively.μBody weight (including light indoor clothing) was measured using an electronic balance (accuracy 0.1 kg) and standing height (without shoes) with a standiometer (nearest 0.1 cm). Body mass index (BMI) was calculated as ratio of weight (in kg) over height (in meter squared).Statistical analyses Descriptive statistics were computed for each residential region and sex separately. In order to test for difference between urban and rural regions, an analysis of covariance (ANCOVA) model was performed. In this model, BMD was treated as outcome variables; age and weight (or BMI) were treated as covariates; and residence (urban or rural) was the factor. Interactions between age and BMI or age and residence variable were also considered in the model. Estimates of the model parameters were based on the least square method via the SPSS version 9.0 (SPSS, Inc, Chicago).
Statistical analyses
Descriptive statistics were computed for each residential region and sex separately. In order to test for difference between urban and rural regions, an analysis of covariance (ANCOVA) model was performed. In this model, BMD was treated as outcome variables; age and weight (or BMI) were treated as covariates; and residence (urban or rural) was the factor. Interactions between age and BMI or age and residence variable were also considered in the model. Estimates of the model parameters were based on the least square method via the SPSS version 9.0 (SPSS, Inc, Chicago).Results Demographic characteristics After excluding 25 subjects, data from 847 subjects (340 men and 507 women) were analysed. There was no significant difference between urban and rural subjects with respect to age or sex distribution. The mean age was 49 and 50 years old in men and women, respectively. However, urban men had higher weight and greater height than rural men ( P  < 0.001), whereas urban women had a greater height ( P  < 0.001) but equivalent weight ( P  = 0.72) compared with rural women (Table  1 ). Table 1 Characteristics of study subjects Urban (Bangkok) Rural (Khon Kean) Mean Difference (95% CI) P  value Men Number of Subjects 159 181 Age (years) 49.6 ± 17.5 49.1 ± 17.1 0.5 (-3.2, 4.2) 0.800 Body weight (kg) 64.3 ± 11.1 58.2 ± 8.8 6.1 (3.0, 8.1) <0.001 Height (cm) 165.5 ± 6.3 161.2 ± 5.9 4.3 (3.0, 5.6) <0.001 Body Mass Index (kg/m 2 ) 23.4 ± 3.6 22.4 ± 2.8 1.0 (0.3, 1.7) 0.003 Bone Mineral Density (g/cm 2 )  Femoral neck 0.87 ± 0.16 0.96 ± 0.18 -0.09 (-0.13, 0.05) <0.001  Lumbar spine 1.12 ± 0.17 1.11 ± 0.16 0.01 (-0.03, 0.04) 0.64 Women Number of Subjects 252 255 Age (years) 50.4 ± 15.1 50.6 ± 15.9 -0.2 (-2.9, 2.4) 0.853 Body weight (kg) 55.5 ± 8.9 55.9 ± 10.5 -0.4 (-2.0, 1.4) 0.718 Height (cm) 154.7 ± 5.4 152.1 ± 5.2 2.6 (1.6, 3.5) <0.001 Body Mass Index (kg/m 2 ) 23.2 ± 3.8 24.1 ± 4.0 -0.9 (-1.5, -0.1) 0.017 Bone Mineral Density (g/cm 2 )  Femoral neck 0.79 ± 0.13 0.87 ± 0.19 -0.08 (-0.11, -0.05) <0.001  Lumbar spine 1.05 ± 0.18 1.01 ± 0.21 0.04 (-0.11, 0.08) 0.16 All values are shown in mean ± standard deviation (SD). In the entire sample, higher weight was associated with higher BMD in men ( r  = 0.13,  P  = 0.017 for femoral neck, and  r  = 0.37,  P  < 0.001 for lumbar spine) and in women ( r  = 0.33,  P  < 0.001 for femoral neck, and  r  = 0.33,  P  < 0.001 for lumbar spine). On the other hand, advancing age was associated with a significant reduced BMD in men ( r  = -0.53,  P  < 0.001 for femoral neck, and  r  = -0.15,  P  = 0.007 for lumbar spine) and women ( r  = -0.63,  P  < 0.001 for femoral neck, and  r  = -0.60,  P  < 0.001 for lumbar spine). However, the strength of relationship between age and BMD in urban subjects was less pronounced than in rural subjects, such that rural women had a higher cross-sectional "rate of bone loss" than urban women, particularly at the femoral neck. For example, in women, each 5-year increase in age was estimated to associate with a 2.1% and 1.2% decrease in femoral neck BMD for rural and urban group, respectively; in men, the respective rate of decrease was 1.3% and 0.8%. As a result, among those aged 50 +  years, BMD in rural subjects tended to be lower than (or converged to) BMD in urban subjects (Figure). Figure 1 Interaction effects of age and residence variable on bone mineral density at the femoral neck in men (A) and women (C), and at the lumbar spine in men (B) and women (D). Urban-rural difference in BMD In both sexes, after adjusting for age and weight, BMD in rural individuals was significantly higher than in urban individuals. For instance, femoral neck BMD in rural men and women was 0.22 and 0.23 g/cm 2  significantly higher ( P  < 0.001) than in urban men and women, respectively; but the difference was lower for the lumbar spine BMD (0.12 g/cm 2  in men,  P  = 0.017 and 0.05 g/cm 2  in women,  P  = 0.293). The statistical significance of the age-by-residence interaction term in the ANCOVA model suggested that the urban-rural difference in BMD decreased with advancing age (Table  2 ). Table 2 Effects of age, weight and residence on bone mineral density: estimates of parameters of the analysis of covariance stratified by sex and BMD site Effect Estimate ± SE P  value Men Femoral neck BMD  Age (+5 yr) -0.020 ± 0.003 <0.001  Weight (+5 kg) 0.015 ± 0.004 <0.001  Residence (Rural) 0.222 ± 0.046 <0.001  Age × Residence (Rural) -0.012 ± 0.004 0.008 Lumbar spine BMD  Age (+5 yr) -0.001 ± 0.003 0.874  Weight (+5 kg) 0.030 ± 0.004 <0.001  Residence (Rural) 0.122 ± 0.051 0.017  Age × Residence (Rural) -0.010 ± 0.004 0.048 Women Femoral neck BMD  Age (+5 yr) -0.026 ± 0.002 <0.001  Weight (+5 kg) 0.026 ± 0.003 <0.001  Residence (Rural) 0.233 ± 0.034 <0.001  Age × Residence (Rural) -0.015 ± 0.003 <0.001 Lumbar spine BMD  Age (+5 yr) -0.033 ± 0.003 <0.001  Weight (+5 kg) 0.031 ± 0.003 <0.001  Residence (Rural) 0.047 ± 0.045 0.293  Age × Residence (Rural) -0.009 ± 0.004 0.036 SE, Standard Error. Notes: Since height was not a significant factor in the analysis of covariance model, it was removed from the final model with no significant change of the results. Further analyses stratified by sex, age group, and BMI category indicated that the urban-rural difference in femoral neck BMD was more pronounced in the younger age group (< 50 years old) and higher BMI (≥ 25 kg/m 2 ). This trend was consistent for men and women. However, for lumbar spine BMD, no significant urban-rural difference was observed in most subgroups, with the exception of women aged ≥ 50 years and BMI < 25 kg/m 2  in whom BMD was lower in the rural group compared to the urban group (Table  3 ). Table 3 Bone mineral density in urban and rural men and women by age group and body mass index (a) Lumbar spine BMD Sex Age (years) BMI (kg/m 2 ) Bone mineral density (g/cm 2 ) Urban Rural Mean difference and 95% CI Men < 50 < 25 0.94 ± 0.16 1.05 ± 0.16 -0.11 a  (-0.16, -0.06) ≥ 25 0.89 ± 0.12 1.04 ± 0.17 -0.15 b  (-0.26, -0.03) ≥ 50 <25 0.80 ± 0.15 0.86 ± 0.15 -0.06 b  (-0.12, -0.01) ≥ 25 0.83 ± 0.11 0.92 ± 0.15 -0.09 b  (-0.17, -0.01) Women < 50 < 25 0.85 ± 0.11 0.97 ± 0.13 -0.12 a  (-0.16, -0.09) ≥ 25 0.92 ± 0.11 1.04 ± 0.13 -0.12 b  (-0.20, -0.05) ≥ 50 <25 0.70 ± 0.11 0.71 ± 0.15 -0.01 (-0.05, 0.03) ≥ 25 0.76 ± 0.11 0.82 ± 0.15 -0.06 b  (-0.11, -0.01) (b) Femoral neck BMD Sex Age (years) BMI (kg/m 2 ) Bone mineral density (g/cm 2 ) Urban Rural Mean difference and 95% CI Men < 50 < 25 1.12 ± 0.14 1.13 ± 0.15 -0.01 (-0.06, 0.04) ≥ 25 1.11 ± 0.09 1.14 ± 0.16 -0.03 (-0.13, 0.08) ≥ 50 < 25 1.05 ± 0.18 1.06 ± 0.16 -0.01 (-0.07, 0.05) ≥ 25 1.21 ± 0.19 1.19 ± 0.20 0.02 (-0.11, 0.14) Women < 50 < 25 1.14 ± 0.13 1.13 ± 0.14 0.01 (-0.04, 0.04) ≥ 25 1.21 ± 0.15 1.15 ± 0.13 0.06 (-0.02, 0.15) ≥ 50 < 25 0.92 ± 0.14 0.83 ± 0.19 0.09 b  (0.03, 0.14) ≥ 25 1.02 ± 0.17 0.97 ± 0.21 0.05 (-0.01, 0.13) Statistical significance at  a P  < 0.001 and  b P  < 0.05. Statistical significance is indicated by bold-faced letters.
Results
Demographic characteristics After excluding 25 subjects, data from 847 subjects (340 men and 507 women) were analysed. There was no significant difference between urban and rural subjects with respect to age or sex distribution. The mean age was 49 and 50 years old in men and women, respectively. However, urban men had higher weight and greater height than rural men ( P  < 0.001), whereas urban women had a greater height ( P  < 0.001) but equivalent weight ( P  = 0.72) compared with rural women (Table  1 ). Table 1 Characteristics of study subjects Urban (Bangkok) Rural (Khon Kean) Mean Difference (95% CI) P  value Men Number of Subjects 159 181 Age (years) 49.6 ± 17.5 49.1 ± 17.1 0.5 (-3.2, 4.2) 0.800 Body weight (kg) 64.3 ± 11.1 58.2 ± 8.8 6.1 (3.0, 8.1) <0.001 Height (cm) 165.5 ± 6.3 161.2 ± 5.9 4.3 (3.0, 5.6) <0.001 Body Mass Index (kg/m 2 ) 23.4 ± 3.6 22.4 ± 2.8 1.0 (0.3, 1.7) 0.003 Bone Mineral Density (g/cm 2 )  Femoral neck 0.87 ± 0.16 0.96 ± 0.18 -0.09 (-0.13, 0.05) <0.001  Lumbar spine 1.12 ± 0.17 1.11 ± 0.16 0.01 (-0.03, 0.04) 0.64 Women Number of Subjects 252 255 Age (years) 50.4 ± 15.1 50.6 ± 15.9 -0.2 (-2.9, 2.4) 0.853 Body weight (kg) 55.5 ± 8.9 55.9 ± 10.5 -0.4 (-2.0, 1.4) 0.718 Height (cm) 154.7 ± 5.4 152.1 ± 5.2 2.6 (1.6, 3.5) <0.001 Body Mass Index (kg/m 2 ) 23.2 ± 3.8 24.1 ± 4.0 -0.9 (-1.5, -0.1) 0.017 Bone Mineral Density (g/cm 2 )  Femoral neck 0.79 ± 0.13 0.87 ± 0.19 -0.08 (-0.11, -0.05) <0.001  Lumbar spine 1.05 ± 0.18 1.01 ± 0.21 0.04 (-0.11, 0.08) 0.16 All values are shown in mean ± standard deviation (SD). In the entire sample, higher weight was associated with higher BMD in men ( r  = 0.13,  P  = 0.017 for femoral neck, and  r  = 0.37,  P  < 0.001 for lumbar spine) and in women ( r  = 0.33,  P  < 0.001 for femoral neck, and  r  = 0.33,  P  < 0.001 for lumbar spine). On the other hand, advancing age was associated with a significant reduced BMD in men ( r  = -0.53,  P  < 0.001 for femoral neck, and  r  = -0.15,  P  = 0.007 for lumbar spine) and women ( r  = -0.63,  P  < 0.001 for femoral neck, and  r  = -0.60,  P  < 0.001 for lumbar spine). However, the strength of relationship between age and BMD in urban subjects was less pronounced than in rural subjects, such that rural women had a higher cross-sectional "rate of bone loss" than urban women, particularly at the femoral neck. For example, in women, each 5-year increase in age was estimated to associate with a 2.1% and 1.2% decrease in femoral neck BMD for rural and urban group, respectively; in men, the respective rate of decrease was 1.3% and 0.8%. As a result, among those aged 50 +  years, BMD in rural subjects tended to be lower than (or converged to) BMD in urban subjects (Figure). Figure 1 Interaction effects of age and residence variable on bone mineral density at the femoral neck in men (A) and women (C), and at the lumbar spine in men (B) and women (D).
Demographic characteristics
After excluding 25 subjects, data from 847 subjects (340 men and 507 women) were analysed. There was no significant difference between urban and rural subjects with respect to age or sex distribution. The mean age was 49 and 50 years old in men and women, respectively. However, urban men had higher weight and greater height than rural men ( P  < 0.001), whereas urban women had a greater height ( P  < 0.001) but equivalent weight ( P  = 0.72) compared with rural women (Table  1 ).PPPCharacteristics of study subjectsPMenWomenAll values are shown in mean ± standard deviation (SD).In the entire sample, higher weight was associated with higher BMD in men ( r  = 0.13,  P  = 0.017 for femoral neck, and  r  = 0.37,  P  < 0.001 for lumbar spine) and in women ( r  = 0.33,  P  < 0.001 for femoral neck, and  r  = 0.33,  P  < 0.001 for lumbar spine). On the other hand, advancing age was associated with a significant reduced BMD in men ( r  = -0.53,  P  < 0.001 for femoral neck, and  r  = -0.15,  P  = 0.007 for lumbar spine) and women ( r  = -0.63,  P  < 0.001 for femoral neck, and  r  = -0.60,  P  < 0.001 for lumbar spine).rPrPrPrPrPrPrPrPHowever, the strength of relationship between age and BMD in urban subjects was less pronounced than in rural subjects, such that rural women had a higher cross-sectional "rate of bone loss" than urban women, particularly at the femoral neck. For example, in women, each 5-year increase in age was estimated to associate with a 2.1% and 1.2% decrease in femoral neck BMD for rural and urban group, respectively; in men, the respective rate of decrease was 1.3% and 0.8%. As a result, among those aged 50 +  years, BMD in rural subjects tended to be lower than (or converged to) BMD in urban subjects (Figure).Urban-rural difference in BMD In both sexes, after adjusting for age and weight, BMD in rural individuals was significantly higher than in urban individuals. For instance, femoral neck BMD in rural men and women was 0.22 and 0.23 g/cm 2  significantly higher ( P  < 0.001) than in urban men and women, respectively; but the difference was lower for the lumbar spine BMD (0.12 g/cm 2  in men,  P  = 0.017 and 0.05 g/cm 2  in women,  P  = 0.293). The statistical significance of the age-by-residence interaction term in the ANCOVA model suggested that the urban-rural difference in BMD decreased with advancing age (Table  2 ). Table 2 Effects of age, weight and residence on bone mineral density: estimates of parameters of the analysis of covariance stratified by sex and BMD site Effect Estimate ± SE P  value Men Femoral neck BMD  Age (+5 yr) -0.020 ± 0.003 <0.001  Weight (+5 kg) 0.015 ± 0.004 <0.001  Residence (Rural) 0.222 ± 0.046 <0.001  Age × Residence (Rural) -0.012 ± 0.004 0.008 Lumbar spine BMD  Age (+5 yr) -0.001 ± 0.003 0.874  Weight (+5 kg) 0.030 ± 0.004 <0.001  Residence (Rural) 0.122 ± 0.051 0.017  Age × Residence (Rural) -0.010 ± 0.004 0.048 Women Femoral neck BMD  Age (+5 yr) -0.026 ± 0.002 <0.001  Weight (+5 kg) 0.026 ± 0.003 <0.001  Residence (Rural) 0.233 ± 0.034 <0.001  Age × Residence (Rural) -0.015 ± 0.003 <0.001 Lumbar spine BMD  Age (+5 yr) -0.033 ± 0.003 <0.001  Weight (+5 kg) 0.031 ± 0.003 <0.001  Residence (Rural) 0.047 ± 0.045 0.293  Age × Residence (Rural) -0.009 ± 0.004 0.036 SE, Standard Error. Notes: Since height was not a significant factor in the analysis of covariance model, it was removed from the final model with no significant change of the results. Further analyses stratified by sex, age group, and BMI category indicated that the urban-rural difference in femoral neck BMD was more pronounced in the younger age group (< 50 years old) and higher BMI (≥ 25 kg/m 2 ). This trend was consistent for men and women. However, for lumbar spine BMD, no significant urban-rural difference was observed in most subgroups, with the exception of women aged ≥ 50 years and BMI < 25 kg/m 2  in whom BMD was lower in the rural group compared to the urban group (Table  3 ). Table 3 Bone mineral density in urban and rural men and women by age group and body mass index (a) Lumbar spine BMD Sex Age (years) BMI (kg/m 2 ) Bone mineral density (g/cm 2 ) Urban Rural Mean difference and 95% CI Men < 50 < 25 0.94 ± 0.16 1.05 ± 0.16 -0.11 a  (-0.16, -0.06) ≥ 25 0.89 ± 0.12 1.04 ± 0.17 -0.15 b  (-0.26, -0.03) ≥ 50 <25 0.80 ± 0.15 0.86 ± 0.15 -0.06 b  (-0.12, -0.01) ≥ 25 0.83 ± 0.11 0.92 ± 0.15 -0.09 b  (-0.17, -0.01) Women < 50 < 25 0.85 ± 0.11 0.97 ± 0.13 -0.12 a  (-0.16, -0.09) ≥ 25 0.92 ± 0.11 1.04 ± 0.13 -0.12 b  (-0.20, -0.05) ≥ 50 <25 0.70 ± 0.11 0.71 ± 0.15 -0.01 (-0.05, 0.03) ≥ 25 0.76 ± 0.11 0.82 ± 0.15 -0.06 b  (-0.11, -0.01) (b) Femoral neck BMD Sex Age (years) BMI (kg/m 2 ) Bone mineral density (g/cm 2 ) Urban Rural Mean difference and 95% CI Men < 50 < 25 1.12 ± 0.14 1.13 ± 0.15 -0.01 (-0.06, 0.04) ≥ 25 1.11 ± 0.09 1.14 ± 0.16 -0.03 (-0.13, 0.08) ≥ 50 < 25 1.05 ± 0.18 1.06 ± 0.16 -0.01 (-0.07, 0.05) ≥ 25 1.21 ± 0.19 1.19 ± 0.20 0.02 (-0.11, 0.14) Women < 50 < 25 1.14 ± 0.13 1.13 ± 0.14 0.01 (-0.04, 0.04) ≥ 25 1.21 ± 0.15 1.15 ± 0.13 0.06 (-0.02, 0.15) ≥ 50 < 25 0.92 ± 0.14 0.83 ± 0.19 0.09 b  (0.03, 0.14) ≥ 25 1.02 ± 0.17 0.97 ± 0.21 0.05 (-0.01, 0.13) Statistical significance at  a P  < 0.001 and  b P  < 0.05. Statistical significance is indicated by bold-faced letters.
Urban-rural difference in BMD
In both sexes, after adjusting for age and weight, BMD in rural individuals was significantly higher than in urban individuals. For instance, femoral neck BMD in rural men and women was 0.22 and 0.23 g/cm 2  significantly higher ( P  < 0.001) than in urban men and women, respectively; but the difference was lower for the lumbar spine BMD (0.12 g/cm 2  in men,  P  = 0.017 and 0.05 g/cm 2  in women,  P  = 0.293). The statistical significance of the age-by-residence interaction term in the ANCOVA model suggested that the urban-rural difference in BMD decreased with advancing age (Table  2 ).PPPEffects of age, weight and residence on bone mineral density: estimates of parameters of the analysis of covariance stratified by sex and BMD sitePMenFemoral neck BMDLumbar spine BMDWomenFemoral neck BMDLumbar spine BMDSE, Standard Error.Notes: Since height was not a significant factor in the analysis of covariance model, it was removed from the final model with no significant change of the results.Further analyses stratified by sex, age group, and BMI category indicated that the urban-rural difference in femoral neck BMD was more pronounced in the younger age group (< 50 years old) and higher BMI (≥ 25 kg/m 2 ). This trend was consistent for men and women. However, for lumbar spine BMD, no significant urban-rural difference was observed in most subgroups, with the exception of women aged ≥ 50 years and BMI < 25 kg/m 2  in whom BMD was lower in the rural group compared to the urban group (Table  3 ).Bone mineral density in urban and rural men and women by age group and body mass index(a) Lumbar spine BMD-0.11 a  (-0.16, -0.06)-0.15 b  (-0.26, -0.03)-0.06 b  (-0.12, -0.01)-0.09 b  (-0.17, -0.01)-0.12 a  (-0.16, -0.09)-0.12 b  (-0.20, -0.05)-0.06 b  (-0.11, -0.01)(b) Femoral neck BMD0.09 b  (0.03, 0.14)Statistical significance at  a P  < 0.001 and  b P  < 0.05. Statistical significance is indicated by bold-faced letters.PPDiscussion Osteoporosis has emerged as one of the most common diseases in the aged population, and represents one of the most significant public health problems in Asia [ 2 , 16 , 17 ]. A consistent trend in osteoporosis is that the incidence of fracture is higher in developed countries than in developing countries; and in any country, the incidence is higher in urban than in rural communities [ 5 - 11 ]. While many factors are hypothesized to be responsible for this trend, BMD is thought to be a primary determinant, because it is the most consistent and robust predictor of fracture risk [ 1 , 11 ]. In the present population-based study, we have shown that BMD in a rural Thai population was significantly higher than in urban population, particularly at femoral neck. The magnitude of difference was more than 1 standard deviation which is clinically relevant. It is difficult to compare the present study's results to previous studies' due to differences in methodology and study design. For instance, Sundberg et al [ 12 ] reported that lumbar spine BMD (measured by DXA) in rural adolescents was significantly higher than that in urban adolescents, but there was no significant difference in femoral neck BMD. Furthermore, a study from Southern Sweden suggested that bone mass at the forearm (measured by single-photon absorptiomety) in rural population was significantly higher than in urban population and the difference was more pronounced when comparing a true urban population who had lived their entire life in a city with a true rural population who had never lived in a city [ 13 ]. A study from Eastern Poland found that the mean lumbar spine BMD values in every age range were higher in rural population than in urban population, but the difference was not statistically significant [ 14 ]. Taken together, these results including ours, suggest that rural subjects tend to have higher BMD than in urban subjects. The present study's data and design can not elucidate any underlying factors that are responsible for the difference but some propositions could be put forward. The urban-rural difference in femoral neck BMD could be due to the difference in the peak of bone mass levels. In this study, both rural men and women aged between 20 and 30 years had significantly higher BMD than urban counterparts. For example, young rural men and women had significantly higher than urban subjects (1.17  vs.  1.03 g/cm 2 , [95% CI: 0.07–0.22] in men and 1.02  vs.  0.86 g/cm 2 , [95% CI: 0.10–0.22] in women). This finding was partially consistent with a previous study [ 12 ] and could be explain the fact that the urban-rural difference was mainly found in younger age groups. This study also found that the urban-rural difference in femoral neck BMD decreased with advancing age. The difference may be attributed to the difference in physical activity between the two populations. Rural populations were generally more physically active than urban populations [ 18 , 19 ]. The rural population in this study was mainly farmers who spend most of their time in rice field long hours of physical activity. However, the difference was sex- and site- dependent. The difference in femoral neck BMD was much more pronounced than that in lumbar spine and this was more transparent before the age of 50 in men and before the menopause in women. After this age the difference was no longer significant. The data suggested that the rate of bone loss in rural population may be more rapid than in urban population. However, this finding was not consistent with a previous study which demonstrated that the rate of bone loss was higher in urban population compared with rural population [ 13 ]. The reason(s) for the higher rate of bone loss in rural population in this study is unknown, but low dietary calcium intake could be a contributory factor [ 20 - 22 ]. The present findings must be interpreted in the context of a number of potential strengths and weaknesses. The data were obtained from a large and well-defined rural  vs.  urban area, which allowed the rural and urban difference to be reliably delineated. The study subjects were Thai, among whom, cultural backgrounds and environmental living conditions are different from Western populations. Thus care should be taken when extrapolating these results to other populations.
Discussion
Osteoporosis has emerged as one of the most common diseases in the aged population, and represents one of the most significant public health problems in Asia [ 2 , 16 , 17 ]. A consistent trend in osteoporosis is that the incidence of fracture is higher in developed countries than in developing countries; and in any country, the incidence is higher in urban than in rural communities [ 5 - 11 ]. While many factors are hypothesized to be responsible for this trend, BMD is thought to be a primary determinant, because it is the most consistent and robust predictor of fracture risk [ 1 , 11 ].In the present population-based study, we have shown that BMD in a rural Thai population was significantly higher than in urban population, particularly at femoral neck. The magnitude of difference was more than 1 standard deviation which is clinically relevant. It is difficult to compare the present study's results to previous studies' due to differences in methodology and study design. For instance, Sundberg et al [ 12 ] reported that lumbar spine BMD (measured by DXA) in rural adolescents was significantly higher than that in urban adolescents, but there was no significant difference in femoral neck BMD. Furthermore, a study from Southern Sweden suggested that bone mass at the forearm (measured by single-photon absorptiomety) in rural population was significantly higher than in urban population and the difference was more pronounced when comparing a true urban population who had lived their entire life in a city with a true rural population who had never lived in a city [ 13 ]. A study from Eastern Poland found that the mean lumbar spine BMD values in every age range were higher in rural population than in urban population, but the difference was not statistically significant [ 14 ]. Taken together, these results including ours, suggest that rural subjects tend to have higher BMD than in urban subjects.The present study's data and design can not elucidate any underlying factors that are responsible for the difference but some propositions could be put forward. The urban-rural difference in femoral neck BMD could be due to the difference in the peak of bone mass levels. In this study, both rural men and women aged between 20 and 30 years had significantly higher BMD than urban counterparts. For example, young rural men and women had significantly higher than urban subjects (1.17  vs.  1.03 g/cm 2 , [95% CI: 0.07–0.22] in men and 1.02  vs.  0.86 g/cm 2 , [95% CI: 0.10–0.22] in women). This finding was partially consistent with a previous study [ 12 ] and could be explain the fact that the urban-rural difference was mainly found in younger age groups.vs.vs.This study also found that the urban-rural difference in femoral neck BMD decreased with advancing age. The difference may be attributed to the difference in physical activity between the two populations. Rural populations were generally more physically active than urban populations [ 18 , 19 ]. The rural population in this study was mainly farmers who spend most of their time in rice field long hours of physical activity.However, the difference was sex- and site- dependent. The difference in femoral neck BMD was much more pronounced than that in lumbar spine and this was more transparent before the age of 50 in men and before the menopause in women. After this age the difference was no longer significant. The data suggested that the rate of bone loss in rural population may be more rapid than in urban population. However, this finding was not consistent with a previous study which demonstrated that the rate of bone loss was higher in urban population compared with rural population [ 13 ]. The reason(s) for the higher rate of bone loss in rural population in this study is unknown, but low dietary calcium intake could be a contributory factor [ 20 - 22 ].The present findings must be interpreted in the context of a number of potential strengths and weaknesses. The data were obtained from a large and well-defined rural  vs.  urban area, which allowed the rural and urban difference to be reliably delineated. The study subjects were Thai, among whom, cultural backgrounds and environmental living conditions are different from Western populations. Thus care should be taken when extrapolating these results to other populations.vs.Conclusions These data have demonstrated that femoral neck BMD in rural men and women was higher than their counterparts in urban areas. This difference could potentially explain part of the urban-rural difference in fracture incidence.
Conclusions
These data have demonstrated that femoral neck BMD in rural men and women was higher than their counterparts in urban areas. This difference could potentially explain part of the urban-rural difference in fracture incidence.List of abbreviations All abbreviations are defined in the text.
List of abbreviations
All abbreviations are defined in the text.Competing interests The author(s) declare that they have no competing interests.
Competing interests
The author(s) declare that they have no competing interests.Authors' contributions Chatlert Pongchaiyakul had an active role in the conduct of this study, obtained and analysed data, and drafted the manuscript. Tuan V Nguyen was involved in the conceptual discussion of this study, and had an active role in data analysis, drafting of the manuscript. Vongsvat Kosulwat, Nipa Rojroongwasinkul, and Somsri Charoenkiatkul had an active role in the study design, and was involved in the conceptual discussion. Rajata Rajatanavin conducted and established this study. All authors contributed to the last version of the manuscript.
Authors' contributions
Chatlert Pongchaiyakul had an active role in the conduct of this study, obtained and analysed data, and drafted the manuscript. Tuan V Nguyen was involved in the conceptual discussion of this study, and had an active role in data analysis, drafting of the manuscript. Vongsvat Kosulwat, Nipa Rojroongwasinkul, and Somsri Charoenkiatkul had an active role in the study design, and was involved in the conceptual discussion. Rajata Rajatanavin conducted and established this study. All authors contributed to the last version of the manuscript.Pre-publication history The pre-publication history for this paper can be accessed here:
Pre-publication history
The pre-publication history for this paper can be accessed here:


Background Intestinal parasitic infections are amongst the most common infections worldwide. Epidemiological research carried out in different countries has shown that the social and economical situation of the individuals is an important cause in the prevalence of intestinal parasites. Previous studies in Turkey revealed a high prevalence of intestinal parasitic infection. The objectives of the current study were to determine the prevalence of intestinal parasitic infections in Aydin among 7–14 years old school children and to identify associated socio-demographic and environmental factors, behavioral habits and also related complaints.
Background
Intestinal parasitic infections are amongst the most common infections worldwide. Epidemiological research carried out in different countries has shown that the social and economical situation of the individuals is an important cause in the prevalence of intestinal parasites. Previous studies in Turkey revealed a high prevalence of intestinal parasitic infection. The objectives of the current study were to determine the prevalence of intestinal parasitic infections in Aydin among 7–14 years old school children and to identify associated socio-demographic and environmental factors, behavioral habits and also related complaints.Methods Multistage sampling was used in the selection of the study sample. A questionnaire, cellulose adhesive and a stool specimen examination were done.
Methods
Multistage sampling was used in the selection of the study sample. A questionnaire, cellulose adhesive and a stool specimen examination were done.Results A total of 456 stool specimens were collected. 145 students (31.8%) were infected with one or more intestinal parasites. 29 (6.4%) of the students were infected more than one parasite, 26 (5.7%) with two parasites and 3 (0.7%) with three parasites. The three most common were  E. vermicularis ,  G. intestinalis  and  E. coli . Intestinal parasite prevalence was higher in rural area, in children with less than primary school educated mother, in children who use hands for washing anal area after defecation, and in children who use toilet paper sometimes or never. The relation between child health and mother education is well known. Children were traditionally taught to wash anal area by hand. Toiler paper usage was not common and might be due to low income or just a behavioral habit also. Most of the complaints of the study population were not significantly related with the intestinal parasitic infection.
Results
A total of 456 stool specimens were collected. 145 students (31.8%) were infected with one or more intestinal parasites. 29 (6.4%) of the students were infected more than one parasite, 26 (5.7%) with two parasites and 3 (0.7%) with three parasites. The three most common were  E. vermicularis ,  G. intestinalis  and  E. coli . Intestinal parasite prevalence was higher in rural area, in children with less than primary school educated mother, in children who use hands for washing anal area after defecation, and in children who use toilet paper sometimes or never. The relation between child health and mother education is well known. Children were traditionally taught to wash anal area by hand. Toiler paper usage was not common and might be due to low income or just a behavioral habit also. Most of the complaints of the study population were not significantly related with the intestinal parasitic infection.E. vermicularisG. intestinalisE. coliConclusions Intestinal parasitic infection is an important public health problem in Aydin, Turkey. Rural residence, mother education less than primary school, sometimes or never usage of toilet paper, and washing anal area by hands after defecation were the significant associations. Interventions including health education on personal hygiene to the students and to the parents, especially to mothers are required. The ratio of uneducated women should be declined with specific programs. A multisectoral approach is needed.
Conclusions
Intestinal parasitic infection is an important public health problem in Aydin, Turkey. Rural residence, mother education less than primary school, sometimes or never usage of toilet paper, and washing anal area by hands after defecation were the significant associations. Interventions including health education on personal hygiene to the students and to the parents, especially to mothers are required. The ratio of uneducated women should be declined with specific programs. A multisectoral approach is needed.

Background Intestinal parasitic infections are amongst the most common infections worldwide. It is estimated that some 3.5 billion people are affected, and that 450 million are ill as a result of these infections, the majority being children. These infections are regarded as serious public health problem, as they cause iron deficiency anemia, growth retardation in children and other physical and mental health problems [ 1 ]. Epidemiological research carried out in different countries has shown that the social and economical situation of the individuals is an important cause in the prevalence of intestinal parasites. In addition, poor sanitary and environmental conditions are known to be relevant in the propagations of these infectious agents [ 2 - 4 ]. Previous studies at various institutions in Turkey revealed a high prevalence of intestinal parasitic infections among the following populations: 6–16 year olds (10.8%), 12–16 year olds (48.0%), 7–15 year olds (55.1%), and 6–12 year olds (88.0%) [ 5 - 8 ]. However, almost all of the studies were performed in isolated groups, such as collecting all samples from children attending the same school. Furthermore the majority of the studies were performed in the eastern part of Turkey. They have limitations in regards to giving an idea about all age groups in the region. Although there are studies on interactions between infection and socio-demographic, environmental factors, and behavioral habits from eastern regions, to our knowledge, there is lack of adequate information for the western part of Turkey [ 7 , 9 ]. The objectives of this current study were to determine the prevalence of intestinal parasitic infections in Aydin among 7–14 year old school children and its relation to socio-demographic factors, environmental factors, behavioral habits and complaints related to intestinal infections.
Background
Intestinal parasitic infections are amongst the most common infections worldwide. It is estimated that some 3.5 billion people are affected, and that 450 million are ill as a result of these infections, the majority being children. These infections are regarded as serious public health problem, as they cause iron deficiency anemia, growth retardation in children and other physical and mental health problems [ 1 ].Epidemiological research carried out in different countries has shown that the social and economical situation of the individuals is an important cause in the prevalence of intestinal parasites. In addition, poor sanitary and environmental conditions are known to be relevant in the propagations of these infectious agents [ 2 - 4 ].Previous studies at various institutions in Turkey revealed a high prevalence of intestinal parasitic infections among the following populations: 6–16 year olds (10.8%), 12–16 year olds (48.0%), 7–15 year olds (55.1%), and 6–12 year olds (88.0%) [ 5 - 8 ]. However, almost all of the studies were performed in isolated groups, such as collecting all samples from children attending the same school. Furthermore the majority of the studies were performed in the eastern part of Turkey. They have limitations in regards to giving an idea about all age groups in the region. Although there are studies on interactions between infection and socio-demographic, environmental factors, and behavioral habits from eastern regions, to our knowledge, there is lack of adequate information for the western part of Turkey [ 7 , 9 ].The objectives of this current study were to determine the prevalence of intestinal parasitic infections in Aydin among 7–14 year old school children and its relation to socio-demographic factors, environmental factors, behavioral habits and complaints related to intestinal infections.Methods Study population The data for the present study was acquired from the primary schools in urban and rural areas of Aydin, a city in the western part of Turkey. The study design was cross-sectional. The sample size was calculated on a prevalence of 30%, d = 0.05 at a confidence level of 95%. A design effect of 2 was used to allow for multistage sampling [ 10 ]. The calculated study population size was 639. Multistage sampling was used in the selection of the study sample. Aydin was separated into four regions according to the socio-economic and health data taken from Directorate of Health. From these regions two schools were selected randomly, one from the urban communities and one from rural. The children were selected from the classes randomly based on the age, gender and weight for the population. First to eighth graders were included in the study, and the total numbers of the students enrolled in the classes were 74, 60, 70, 72, 72, 107, 104, and 81 students, respectively. Permission was obtained from Directorate of Education. The questionnaire and family information form The questionnaire contained four sections: 1. Socio-demographic data: age, gender, residence, education and occupation of parents, number of adults and children in the family and birth order of the child; 2. Environmental factors: housing conditions (ownership of the house, number of rooms and bathrooms) and water supply; 3. Behavior habits: type of toilet commonly used, hand washing (no washing/washing with only water/washing with soap), washing anal area by hands after defecation (yes/no), usage of toilet paper (always/sometimes/never); 4. Complaints: abdominal pain, nausea/vomiting, lack of appetite, abdominal distention, intestinal dismotility, salivation during sleeping, headache, irritability in sleeping, perianal itching, teeth grinding, and history of parasitic infections. An informational document about the study, including how to supply a stool specimen and a cellulose tape slide, was given to each participant for their family. Intestinal parasitic examination Mothers were asked to perform one cellulose tape test on their child who was participating in the study. Laboratory slides were provided with cellulose tape attached to them. The mother collected material for examination in the early morning prior to bathing or defecation. On the same morning a field worker collected these slides to be microscopically examined. The stool specimens (0.5–1.5 gr) were collected in labeled plastic vials without preservatives and transported to the laboratory within four hours after collection. They were examined for the presence of parasites by direct wet mount, Lugol's iodine solution and modified formaline-ethyl acetate sedimentation techniques. The presence of parasites was confirmed when observed by any of the methods above. Statistical analysis A computer program was used for data analysis. The descriptive data was given as a mean ± standard deviation (SD). The chi-squared test and Student t-test were used for the analytic assessment. The differences were considered to be statistically significant when the p-value obtained was less than 0.05.
Methods
Study population The data for the present study was acquired from the primary schools in urban and rural areas of Aydin, a city in the western part of Turkey. The study design was cross-sectional. The sample size was calculated on a prevalence of 30%, d = 0.05 at a confidence level of 95%. A design effect of 2 was used to allow for multistage sampling [ 10 ]. The calculated study population size was 639. Multistage sampling was used in the selection of the study sample. Aydin was separated into four regions according to the socio-economic and health data taken from Directorate of Health. From these regions two schools were selected randomly, one from the urban communities and one from rural. The children were selected from the classes randomly based on the age, gender and weight for the population. First to eighth graders were included in the study, and the total numbers of the students enrolled in the classes were 74, 60, 70, 72, 72, 107, 104, and 81 students, respectively. Permission was obtained from Directorate of Education.
Study population
The data for the present study was acquired from the primary schools in urban and rural areas of Aydin, a city in the western part of Turkey. The study design was cross-sectional.The sample size was calculated on a prevalence of 30%, d = 0.05 at a confidence level of 95%. A design effect of 2 was used to allow for multistage sampling [ 10 ]. The calculated study population size was 639. Multistage sampling was used in the selection of the study sample. Aydin was separated into four regions according to the socio-economic and health data taken from Directorate of Health. From these regions two schools were selected randomly, one from the urban communities and one from rural. The children were selected from the classes randomly based on the age, gender and weight for the population. First to eighth graders were included in the study, and the total numbers of the students enrolled in the classes were 74, 60, 70, 72, 72, 107, 104, and 81 students, respectively. Permission was obtained from Directorate of Education.The questionnaire and family information form The questionnaire contained four sections: 1. Socio-demographic data: age, gender, residence, education and occupation of parents, number of adults and children in the family and birth order of the child; 2. Environmental factors: housing conditions (ownership of the house, number of rooms and bathrooms) and water supply; 3. Behavior habits: type of toilet commonly used, hand washing (no washing/washing with only water/washing with soap), washing anal area by hands after defecation (yes/no), usage of toilet paper (always/sometimes/never); 4. Complaints: abdominal pain, nausea/vomiting, lack of appetite, abdominal distention, intestinal dismotility, salivation during sleeping, headache, irritability in sleeping, perianal itching, teeth grinding, and history of parasitic infections. An informational document about the study, including how to supply a stool specimen and a cellulose tape slide, was given to each participant for their family.
The questionnaire and family information form
The questionnaire contained four sections: 1. Socio-demographic data: age, gender, residence, education and occupation of parents, number of adults and children in the family and birth order of the child; 2. Environmental factors: housing conditions (ownership of the house, number of rooms and bathrooms) and water supply; 3. Behavior habits: type of toilet commonly used, hand washing (no washing/washing with only water/washing with soap), washing anal area by hands after defecation (yes/no), usage of toilet paper (always/sometimes/never); 4. Complaints: abdominal pain, nausea/vomiting, lack of appetite, abdominal distention, intestinal dismotility, salivation during sleeping, headache, irritability in sleeping, perianal itching, teeth grinding, and history of parasitic infections.An informational document about the study, including how to supply a stool specimen and a cellulose tape slide, was given to each participant for their family.Intestinal parasitic examination Mothers were asked to perform one cellulose tape test on their child who was participating in the study. Laboratory slides were provided with cellulose tape attached to them. The mother collected material for examination in the early morning prior to bathing or defecation. On the same morning a field worker collected these slides to be microscopically examined. The stool specimens (0.5–1.5 gr) were collected in labeled plastic vials without preservatives and transported to the laboratory within four hours after collection. They were examined for the presence of parasites by direct wet mount, Lugol's iodine solution and modified formaline-ethyl acetate sedimentation techniques. The presence of parasites was confirmed when observed by any of the methods above.
Intestinal parasitic examination
Mothers were asked to perform one cellulose tape test on their child who was participating in the study. Laboratory slides were provided with cellulose tape attached to them. The mother collected material for examination in the early morning prior to bathing or defecation. On the same morning a field worker collected these slides to be microscopically examined.The stool specimens (0.5–1.5 gr) were collected in labeled plastic vials without preservatives and transported to the laboratory within four hours after collection. They were examined for the presence of parasites by direct wet mount, Lugol's iodine solution and modified formaline-ethyl acetate sedimentation techniques.The presence of parasites was confirmed when observed by any of the methods above.Statistical analysis A computer program was used for data analysis. The descriptive data was given as a mean ± standard deviation (SD). The chi-squared test and Student t-test were used for the analytic assessment. The differences were considered to be statistically significant when the p-value obtained was less than 0.05.
Statistical analysis
A computer program was used for data analysis. The descriptive data was given as a mean ± standard deviation (SD). The chi-squared test and Student t-test were used for the analytic assessment. The differences were considered to be statistically significant when the p-value obtained was less than 0.05.Results A total of 456 (71.4%) samples for both stool specimens and cellulose tape slides were collected. The response rate to the questionnaire was lower with 367 (57.4 %). The mean age was 10.34 ± 2.27, 10.17 ± 2.30 for girls and 10.51 ± 2.23 for boys. Important socio-demographic characteristics, housing conditions and hygienic habits of children are given in Table  1 . Table 1 Important socio-demographic characteristics, housing conditions and hygienic habits of children Characteristics No % Socio-demographic characteristics Residence Urban 258 56.6 Rural 198 43.4 Gender Female 232 50.9 Male 224 49.1 Education of mother No education/primary school incomplete 68 19.0 Primary/secondary school 269 75.4 High school and more 20 5.6 Education of father No education/primary school incomplete 21 5.8 Primary/secondary school 292 81.4 High school and more 46 12.8 Housing conditions Owner 239 66.0 3 rooms and less 154 43.5 4 rooms and more 200 56.5 1 toilet 180 49.9 2 and more toilet 181 50.1 5 and less people living in 267 74.4 6 and more people living in 92 25.6 Municipal water network 232 68.6 Hygienic habits Type of toilet commonly used Modern style 86 26.5 Traditional style 135 41.5 Both 104 32.0 Toilet paper Always 206 57.1 Sometimes 105 29.1 Never 50 13.9 Washing anal area by hands after defecation Yes 138 39.4 No 212 60.6 Washing hands with soap after toilet Always 308 85.3 Sometimes 51 14.1 Never 2 0.6 Taking a bath Once a day 18 5.2 Three times a week 161 46.1 Once a week or less 170 48.7 In all, 145 students (31.8%) were infected with one or more intestinal parasites. 29 (6.4%) of the students were infected with more than one parasite, 26 (5.7%) with two parasites and 3 (0.7%) with three parasites. The most common was  Enterobius vermicularis (E. vermicularis ) with 63 (13.8%) pure and 20 (4.4%) with multiple infections, in total 83 (18.2%) infected children. The second was  Giardia intestinalis  ( G. intestinalis ) with 28 (6.1%) pure and 21 (4.6%) with multiple infections, in total 49 (10.7%) infected children. The third one was  Entamoeba coli  ( E. coli ) with 21(4.6%) pure and 15 (3.3%) multiple infections, in total 36 (7.9%) infected children.  G. intestinalis  was the most commonly found parasite in multiple infections. The distribution of parasites is given in Table  2 . Table 2 The parasites distribution of the study population Parasites No. % Single E. vermicularis 63 13.8 G. intestinalis 28 6.1 E. coli 21 4.6 H. nana 4 0.9 Total 116 25.4 Multiple E. vermicularis+G. intestinalis 11 2.4 E. vermicularis+E. coli 8 1.8 G. intestinalis+E. coli 4 0.9 G. intestinalis+H. nana 2 0.4 G. intestinalis+Taenia spp. 1 0.2 G. intestinalis+E. coli+H.nana 2 0.4 E. vermicularis+G. intestinalis+E. coli 1 0.2 Total 29 6.4 Overall total 145 31.8 No statistically significant difference was observed between presence of intestinal parasites and gender, (p = 0.805), and also age (p = 0.916). The prevalence of intestinal parasites were significantly higher (p = 0.042) in the rural area (36.9%) than in the urban area (27.9%). A summary of significant relations observed in overall intestinal parasitic infections for the study population are given in Table  3 . Table 3 Significant relations for the intestinal parasitic infection in the study population Risk Factor Overall infection χ 2 p n % Residence Urban 72 27.9 4.415 0.042 Rural 73 36.9 Mother education Less than primary school 29 42.6 4.436 0.035 Primary school and more 85 29.4 Toilet paper Always 50 24.3 13.596 0.000 Sometimes/never 66 42.6 Washing anal area by hands after defecation Yes 55 39.9 5.503 0.019 No 59 27.8 Parasite-specific significant relations were the following: The prevalence of E. coli infections was significantly higher (p = 0.010) in the rural area (11.1%) than in the urban area (5.0%). Mother education less than a primary school education (p = 0.012), washing anal area by hands after defecation (p = 0.013) were the significant relations for  G. intestinalis , where sometimes or non-usage of toilet paper was significant for  G. intestinalis  (p = 0.008) and for  E. vermicularis  (p = 0.024) both. Family size was larger in the group infected with  G. intestinalis  (p = 0.029). The prevalence of intestinal parasitic infection was 31.0% in the group using a municipal water network and 34% in the group lacking a municipal system (p = 0.592). The prevalences of  G. intestinalis  in these two groups were 9.9% and 16.0% (p = 0.106) respectively. No further significant relationships were found between intestinal parasitic infection and environmental or behavioral factors. The most frequent complaint related with any parasite infection was intestinal dismotility (40.0%). Nausea/vomiting (37.7%) was second and abdominal distention (37.1%) was third. All of the complaints were seen in higher prevalence for  E. vermicularis  infections than  G. intestinalis  and  E. coli .
Results
A total of 456 (71.4%) samples for both stool specimens and cellulose tape slides were collected. The response rate to the questionnaire was lower with 367 (57.4 %). The mean age was 10.34 ± 2.27, 10.17 ± 2.30 for girls and 10.51 ± 2.23 for boys. Important socio-demographic characteristics, housing conditions and hygienic habits of children are given in Table  1 .Important socio-demographic characteristics, housing conditions and hygienic habits of childrenIn all, 145 students (31.8%) were infected with one or more intestinal parasites. 29 (6.4%) of the students were infected with more than one parasite, 26 (5.7%) with two parasites and 3 (0.7%) with three parasites. The most common was  Enterobius vermicularis (E. vermicularis ) with 63 (13.8%) pure and 20 (4.4%) with multiple infections, in total 83 (18.2%) infected children. The second was  Giardia intestinalis  ( G. intestinalis ) with 28 (6.1%) pure and 21 (4.6%) with multiple infections, in total 49 (10.7%) infected children. The third one was  Entamoeba coli  ( E. coli ) with 21(4.6%) pure and 15 (3.3%) multiple infections, in total 36 (7.9%) infected children.  G. intestinalis  was the most commonly found parasite in multiple infections. The distribution of parasites is given in Table  2 .Enterobius vermicularis (E. vermicularisGiardia intestinalisG. intestinalisEntamoeba coliE. coliG. intestinalisThe parasites distribution of the study populationNo statistically significant difference was observed between presence of intestinal parasites and gender, (p = 0.805), and also age (p = 0.916). The prevalence of intestinal parasites were significantly higher (p = 0.042) in the rural area (36.9%) than in the urban area (27.9%). A summary of significant relations observed in overall intestinal parasitic infections for the study population are given in Table  3 .Significant relations for the intestinal parasitic infection in the study populationParasite-specific significant relations were the following: The prevalence of E. coli infections was significantly higher (p = 0.010) in the rural area (11.1%) than in the urban area (5.0%). Mother education less than a primary school education (p = 0.012), washing anal area by hands after defecation (p = 0.013) were the significant relations for  G. intestinalis , where sometimes or non-usage of toilet paper was significant for  G. intestinalis  (p = 0.008) and for  E. vermicularis  (p = 0.024) both. Family size was larger in the group infected with  G. intestinalis  (p = 0.029). The prevalence of intestinal parasitic infection was 31.0% in the group using a municipal water network and 34% in the group lacking a municipal system (p = 0.592). The prevalences of  G. intestinalis  in these two groups were 9.9% and 16.0% (p = 0.106) respectively. No further significant relationships were found between intestinal parasitic infection and environmental or behavioral factors.G. intestinalisG. intestinalisE. vermicularisG. intestinalisG. intestinalisThe most frequent complaint related with any parasite infection was intestinal dismotility (40.0%). Nausea/vomiting (37.7%) was second and abdominal distention (37.1%) was third. All of the complaints were seen in higher prevalence for  E. vermicularis  infections than  G. intestinalis  and  E. coli .E. vermicularisG. intestinalisE. coliDiscussion It was found that approximately one-third (31.8%) of the students, ages 7 to 14, in Aydin were infected by intestinal parasites. In a sample within the same age group in Izmir, a city also in the western part of Turkey, the prevalence for intestinal parasites was 22.4%, with  E. vermicularis  (16.0%) and  G. intestinalis  (11.9%) being the two most common infections, as was observed in Aydin [ 11 ]. In another study performed in Izmir, the prevalence of infection was 45.3% for  E. vermicularis , 21% for  G. intestinalis , 10% for  H. nana , 4.3% for  E. coli , 0.03% for  Ascaris lumbricoides  ( A. lumbricoides ), and 0.03% for  Trichuris trichiura  ( T. trichiura ). No  Taenia  was found [ 12 ]. In this current study; the most frequently observed parasites were  E. vermicularis ,  G. intestinalis , and  E. coli , 18.2%, 10.7% and 7.9%, respectively. Higher prevalence was found in the studies from the eastern part of Turkey, where the socio-economic and environmental conditions were lower. Additionally, it was observed that the types of parasites found in this study where different than those found in the eastern part of Turkey. A survey conducted among 1001 children in four elementary schools in Sanliurfa found parasites in 88% of the stool samples examined (50%  A. lumbricoides , 53%  T. trichiura , 22%  G. intestinalis , and 11%  E. coli ); unfortunately, no data on  E. vermicularis  was given, because samples with cellulose tape slides were not taken [ 7 ]. In an another study from the eastern region, in an elementary school age group, 48.12%  A. lumbricoides , 4.43%  T. trichiura  and 15.35%  G. intestinalis  were found [ 13 ]. In the last study, samples with cellulose tape slides were not taken. Geohelmint infections ( Ascaris ,  Strongyloides  and  Trichuris ) were of lower prevalence in the western part of Turkey, but of higher prevalence in the eastern part. This difference may be due to improper toilet facilities which require individuals to defecate in areas around their homes as well as the use of fecal material for fertilizer in gardens in the eastern parts of Turkey [ 13 - 15 ]. In a study from the eastern region, 42.2% of children were found to be working in gardens watered with contaminated sewage and eating the vegetables of those gardens. There were 44.7%  A. lumbricoides , 11.7%  T. trichiura  infections in these children while there was 12.2 % A. lumbricoides  and 6.6%  T. trichiura  infections in the control groups [ 14 ]. Enterobiasis occurs worldwide, usually involving school-aged children [ 16 ]. In general  E. vermicularis  infection is transmitted by hand to mouth and/or person to person directly. High prevalence of  E. vermicularis  in the current study might be due to improper hygiene including not washing hands with soap after defecation, before eating and preparing foods. In the study area, there are two traditional methods of cleaning anal areas after defecation: (1) washing the anal area by hand with tap water (2) a piece of cloth is used to clean the anal area after defecation. The cloth is used multiple times until the person decides that it has become too dirty after which it is washed and reused. These improper cleaning practices after defecation could be the probable causes behind autoinfection. The higher prevalence of  E. vermicularis  could also be explained by the highly infectious nature of the parasites. G. intestinalis  and  E. coli  were the most common intestinal protozoa among the study population. Both can be transmitted orally by drinking infected water and both are environmental contaminants of the water supply. The water supply is really an important risk factor for the Giardiasis, and several large outbreaks of giardiasis have resulted from the contamination of municipal water supplies with human waste [ 17 ]. The ingestion of contaminated water is a common problem in Turkey countrywide due to the lower quality of water and faulty sewage lines. The problem is greater in the rural areas that do not have a municipal water network or sewage system [ 18 ]. Contamination of drinking water with  Giardia spp . has been increasingly recognized over the past 10 years as a cause of water-borne diseases in humans [ 19 ].  Giardia  cysts have been isolated from water supplies in different parts of the world [ 20 , 21 ]. Epidemic giardiasis may be related to drinking water [ 22 ].  G. intestinalis  and  E. coli  are most common in the western part of Turkey [ 11 ]. In a study assessing giardiasis cases in Turkey published within the last 15 years, the prevalence of  G. intestinalis  was found 11.6% in the western part of Turkey [ 23 ]. From the study, 68.6% of the study group uses municipal water, while the others either use a chlorinated collection tank with a crude water network or purchase bottled water. Although no statistically significant difference was observed, the prevalence of  G. intestinalis  was lower in the group using municipal water (9.9%) than the other group (16.0%) in the current study. It is thought that an in-depth assessment should be done on the ways that drinking water becomes contaminated. In this current study, there were no cases of  Taenia spp . Since the consumption of pork and pork products are forbidden for Muslims this may account for the absence of  T. solium  cases in the population. It is also a common practice to eat uncooked meat in the eastern part of Turkey, but not in the western part.  T. saginata  infections are observed in the eastern studies, with prevalence of 13.8% and 12.9% [ 19 , 24 ]. However, in the western region infections by this parasite were not observed in this or in another previous study [ 12 ]. Differences due to gender were not observed in this current study. These results were similar to a study conducted in the central part of Turkey [ 24 ]. In this current study; the prevalence of intestinal parasitic infection was higher in the rural areas. A similar result was found in the central region of Turkey where the prevalence of intestinal parasites was higher in the rural area [ 25 ]. In this current study, most of the complaints by the study population were not significantly related with the intestinal parasitic infection. For example, perianal itching was noted in 15.8 % of the study population. There was no significant difference in the prevalence of this symptom in pinworm infected and non-infected children. Furthermore, no association was found between the prevalence of pinworm infection and a history of teeth grinding, colic, enuresis, and irritability. The complaints may not have been assessed effectively through the use of only a questionnaire without an interview, or they might not be useful for every individual's diagnosis. The prevalence of intestinal parasites was higher in groups where the mother in the household had less than a primary school education, where the hand is habitually used for the cleaning of the anal area and where toilet paper is seldom or never used. The relation between a child's health and the mother's education is well known. Health indicators of children whose mother's education level is lower are always worse [ 26 ]. In the last two groups, the habits of the children are a factor, along with a cultural dimension. They were taught to clean the anal area by washing with the hand. Toiler paper usage was not common, possibly due to low income. Usage of a piece of cloth instead of toilet paper was also common. The major limitation of the current study was a low response rate. The assessment would have been more valuable if a higher response rate could have been obtained. But, it was thought that the results were still important because there is little knowledge on the data of the region. Additionally, the current study was the first population-based study for the region. Although an important number of risk factors were discussed, a few risk factors (e.g.: shoe wearing) were not evaluated in the current study. This might have been another limitation of the study. The important risk factors for the region were evaluated in the study.
Discussion
It was found that approximately one-third (31.8%) of the students, ages 7 to 14, in Aydin were infected by intestinal parasites. In a sample within the same age group in Izmir, a city also in the western part of Turkey, the prevalence for intestinal parasites was 22.4%, with  E. vermicularis  (16.0%) and  G. intestinalis  (11.9%) being the two most common infections, as was observed in Aydin [ 11 ]. In another study performed in Izmir, the prevalence of infection was 45.3% for  E. vermicularis , 21% for  G. intestinalis , 10% for  H. nana , 4.3% for  E. coli , 0.03% for  Ascaris lumbricoides  ( A. lumbricoides ), and 0.03% for  Trichuris trichiura  ( T. trichiura ). No  Taenia  was found [ 12 ]. In this current study; the most frequently observed parasites were  E. vermicularis ,  G. intestinalis , and  E. coli , 18.2%, 10.7% and 7.9%, respectively. Higher prevalence was found in the studies from the eastern part of Turkey, where the socio-economic and environmental conditions were lower. Additionally, it was observed that the types of parasites found in this study where different than those found in the eastern part of Turkey. A survey conducted among 1001 children in four elementary schools in Sanliurfa found parasites in 88% of the stool samples examined (50%  A. lumbricoides , 53%  T. trichiura , 22%  G. intestinalis , and 11%  E. coli ); unfortunately, no data on  E. vermicularis  was given, because samples with cellulose tape slides were not taken [ 7 ]. In an another study from the eastern region, in an elementary school age group, 48.12%  A. lumbricoides , 4.43%  T. trichiura  and 15.35%  G. intestinalis  were found [ 13 ]. In the last study, samples with cellulose tape slides were not taken.E. vermicularisG. intestinalisE. vermicularisG. intestinalisH. nanaE. coliAscaris lumbricoidesA. lumbricoidesTrichuris trichiuraT. trichiuraTaeniaE. vermicularisG. intestinalisE. coliA. lumbricoidesT. trichiuraG. intestinalisE. coliE. vermicularisA. lumbricoidesT. trichiuraG. intestinalisGeohelmint infections ( Ascaris ,  Strongyloides  and  Trichuris ) were of lower prevalence in the western part of Turkey, but of higher prevalence in the eastern part. This difference may be due to improper toilet facilities which require individuals to defecate in areas around their homes as well as the use of fecal material for fertilizer in gardens in the eastern parts of Turkey [ 13 - 15 ]. In a study from the eastern region, 42.2% of children were found to be working in gardens watered with contaminated sewage and eating the vegetables of those gardens. There were 44.7%  A. lumbricoides , 11.7%  T. trichiura  infections in these children while there was 12.2 % A. lumbricoides  and 6.6%  T. trichiura  infections in the control groups [ 14 ].AscarisStrongyloidesTrichurisA. lumbricoidesT. trichiuraA. lumbricoidesT. trichiuraEnterobiasis occurs worldwide, usually involving school-aged children [ 16 ]. In general  E. vermicularis  infection is transmitted by hand to mouth and/or person to person directly. High prevalence of  E. vermicularis  in the current study might be due to improper hygiene including not washing hands with soap after defecation, before eating and preparing foods. In the study area, there are two traditional methods of cleaning anal areas after defecation: (1) washing the anal area by hand with tap water (2) a piece of cloth is used to clean the anal area after defecation. The cloth is used multiple times until the person decides that it has become too dirty after which it is washed and reused. These improper cleaning practices after defecation could be the probable causes behind autoinfection. The higher prevalence of  E. vermicularis  could also be explained by the highly infectious nature of the parasites.E. vermicularisE. vermicularisE. vermicularisG. intestinalis  and  E. coli  were the most common intestinal protozoa among the study population. Both can be transmitted orally by drinking infected water and both are environmental contaminants of the water supply. The water supply is really an important risk factor for the Giardiasis, and several large outbreaks of giardiasis have resulted from the contamination of municipal water supplies with human waste [ 17 ]. The ingestion of contaminated water is a common problem in Turkey countrywide due to the lower quality of water and faulty sewage lines. The problem is greater in the rural areas that do not have a municipal water network or sewage system [ 18 ]. Contamination of drinking water with  Giardia spp . has been increasingly recognized over the past 10 years as a cause of water-borne diseases in humans [ 19 ].  Giardia  cysts have been isolated from water supplies in different parts of the world [ 20 , 21 ]. Epidemic giardiasis may be related to drinking water [ 22 ].  G. intestinalis  and  E. coli  are most common in the western part of Turkey [ 11 ]. In a study assessing giardiasis cases in Turkey published within the last 15 years, the prevalence of  G. intestinalis  was found 11.6% in the western part of Turkey [ 23 ]. From the study, 68.6% of the study group uses municipal water, while the others either use a chlorinated collection tank with a crude water network or purchase bottled water. Although no statistically significant difference was observed, the prevalence of  G. intestinalis  was lower in the group using municipal water (9.9%) than the other group (16.0%) in the current study. It is thought that an in-depth assessment should be done on the ways that drinking water becomes contaminated.G. intestinalisE. coliGiardia sppGiardiaG. intestinalisE. coliG. intestinalisG. intestinalisIn this current study, there were no cases of  Taenia spp . Since the consumption of pork and pork products are forbidden for Muslims this may account for the absence of  T. solium  cases in the population. It is also a common practice to eat uncooked meat in the eastern part of Turkey, but not in the western part.  T. saginata  infections are observed in the eastern studies, with prevalence of 13.8% and 12.9% [ 19 , 24 ]. However, in the western region infections by this parasite were not observed in this or in another previous study [ 12 ].Taenia sppT. soliumT. saginataDifferences due to gender were not observed in this current study. These results were similar to a study conducted in the central part of Turkey [ 24 ]. In this current study; the prevalence of intestinal parasitic infection was higher in the rural areas. A similar result was found in the central region of Turkey where the prevalence of intestinal parasites was higher in the rural area [ 25 ].In this current study, most of the complaints by the study population were not significantly related with the intestinal parasitic infection. For example, perianal itching was noted in 15.8 % of the study population. There was no significant difference in the prevalence of this symptom in pinworm infected and non-infected children. Furthermore, no association was found between the prevalence of pinworm infection and a history of teeth grinding, colic, enuresis, and irritability. The complaints may not have been assessed effectively through the use of only a questionnaire without an interview, or they might not be useful for every individual's diagnosis.The prevalence of intestinal parasites was higher in groups where the mother in the household had less than a primary school education, where the hand is habitually used for the cleaning of the anal area and where toilet paper is seldom or never used. The relation between a child's health and the mother's education is well known. Health indicators of children whose mother's education level is lower are always worse [ 26 ]. In the last two groups, the habits of the children are a factor, along with a cultural dimension. They were taught to clean the anal area by washing with the hand. Toiler paper usage was not common, possibly due to low income. Usage of a piece of cloth instead of toilet paper was also common.The major limitation of the current study was a low response rate. The assessment would have been more valuable if a higher response rate could have been obtained. But, it was thought that the results were still important because there is little knowledge on the data of the region. Additionally, the current study was the first population-based study for the region. Although an important number of risk factors were discussed, a few risk factors (e.g.: shoe wearing) were not evaluated in the current study. This might have been another limitation of the study. The important risk factors for the region were evaluated in the study.Conclusion As a conclusion, intestinal parasitic infection is an important public health problem in Aydin, Turkey. Rural residence, households where the mother has less than a primary school education, periodic or non-usage of toilet paper, and the washing of the anal area by hand after defecation were the significant associations. Interventions including health education on personal hygiene to the students and to the parents, especially to mothers are required. The ratio of uneducated women should decline with specific programs. A multisectoral approach is needed.
Conclusion
As a conclusion, intestinal parasitic infection is an important public health problem in Aydin, Turkey. Rural residence, households where the mother has less than a primary school education, periodic or non-usage of toilet paper, and the washing of the anal area by hand after defecation were the significant associations. Interventions including health education on personal hygiene to the students and to the parents, especially to mothers are required. The ratio of uneducated women should decline with specific programs. A multisectoral approach is needed.Competing interests The author(s) declare that they have no competing interests.
Competing interests
The author(s) declare that they have no competing interests.Authors' contributions PO planned the research, performed the sampling and statistical analyzes and wrote draft and final version of the manuscript. SE contributed in planning the research, performed parasitic examinations and contributed discussing the results and writing manuscript. BG performed parasitic examinations and contributed discussing the results. OO organized the work in the schools and participated in its design. EB participated in initial study design, coordinated the study and revised the manuscript. All authors read and approved the final manuscript.
Authors' contributions
PO planned the research, performed the sampling and statistical analyzes and wrote draft and final version of the manuscript. SE contributed in planning the research, performed parasitic examinations and contributed discussing the results and writing manuscript. BG performed parasitic examinations and contributed discussing the results. OO organized the work in the schools and participated in its design. EB participated in initial study design, coordinated the study and revised the manuscript. All authors read and approved the final manuscript.Pre-publication history The pre-publication history for this paper can be accessed here:
Pre-publication history
The pre-publication history for this paper can be accessed here: