Usefulness of a salt check sheet for elementary school and junior high school children

Abstract

There are no known methods to easily evaluate the dietary salt intake of children. We hypothesized that the salt check sheet, for which validity has been confirmed in both hypertensive outpatients and in the general population, can be used to assess dietary salt intake in children. We enrolled 188 healthy schoolchildren (mean age 11.2 ± 1.1 years, 53.2% boys) and asked them to answer both the salt check sheet and a brief self‐administered dietary history questionnaire for Japanese schoolchildren aged 6‐18 years (BDHQ15y). The mean total salt check‐sheet score was 12.7 ± 4.0 points (range: 4‐24 points), and the estimated daily salt intake from the BDHQ15y was 12.1 ± 3.7 g (range: 4.7‐27.2 g). The total check‐sheet score was significantly positively correlated with the estimated daily salt intake from the BDHQ15y (r = 0.408, P < 0.001). Thirty‐one study participants were assigned to the “low” salt group (total score on the salt check sheet was 0‐8 points), 78 participants to the “medium” salt group (9‐13 points), and 79 participants to the “high and very high” salt group (≥14 points), and a comparison estimating daily salt intake from the BDHQ15y among the three groups was performed. Daily salt‐intake levels tended to increase as the group of total check‐sheet scores increased: “low” vs “medium” vs “high and very high” salt group levels were 9.5 ± 3.1 vs 11.6 vs 13.5 ± 3.9, respectively (P < 0.001). This demonstrates that the salt check sheet is a useful tool to easily assess dietary salt intake in children.

1. INTRODUCTION

Salt restriction starting from childhood is an important strategy for the prevention of cardiovascular disease (CVD) in adulthood. Salt intake is positively associated with elevated blood pressure (BP) levels, even in children,1 and can lead to high CVD risks in adulthood.2 In the Japanese populace, there is high salt intake compared to other populations, and excessive salt intake remains a societal problem.3 In addition, it has been reported that excessive dietary salt intake of parents is associated with that of their children.4 As reducing dietary salt intake could reduce CVD events,5 appropriate salt restriction should be recommended beginning in childhood.

Accurate assessments of dietary salt intake are invaluable for both education and prevention against CVD events in adulthood. These assessments are also important to conduct during childhood, since the habit of excessive dietary salt intake may begin during this time.6 In Japan, a brief‐type, self‐administered diet history questionnaire (BDHQ) has been used in several epidemiological studies of childhood,7, 8 and the validity of this questionnaire had been confirmed.9, 10 However, the BDHQ is four pages long and takes approximately 15 minutes to complete, suggesting that it is not easy to complete or evaluate repeatedly, especially for children. Questionnaires for assessing dietary salt intake that can be easily completed by children are unknown.

The salt check sheet is widely used in general practice to assess salt intake of both outpatients with hypertension and the general population.11, 12 It comprises 13 questions regarding daily salt intake and takes only 3‐5 minutes to complete, which makes it practical to use.12 The validity of salt check sheet has been confirmed for outpatients with hypertension11 and the general population12; however, its usefulness for assessing dietary salt intake of children is unknown.

Therefore, we evaluated the usefulness of the salt check sheet for assessing dietary salt intake in children and hypothesized that the salt check sheet is an adequate tool for making this assessment.

2. METHODS

2.1. Study participants

One hundred and eighty‐eight (boys/girls: 100/88) healthy children from the fifth‐grade student population of elementary schools and the first‐grade student population of junior high schools were recruited in Higashiagatsuma town, Gunma Prefecture, in Japan (Figure S1). The BDHQ for Japanese schoolchildren aged 6‐18 years (BDHQ15y)7 is regularly administered each year to children during these school years as part of an educational and health service program in Higashiagatsuma town and is administered when they have annual medical checkups that include anthropometric measurements and blood tests. The current study was conducted in May 2017. The study protocol was explained in details to children and their parents using an explanation document, and an opportunity to opt out of the study was provided. The Ethics Committee of the Jichi Medical University School of Medicine (Shimotsuke, Japan) approved the study.

Body mass index was calculated using the following formula: body mass index = bodyweight/height² (kg/m²). The degree of obesity was calculated using the following formula: degree of obesity = (height − [standard weight by sex, age, and height])/[standard weight by sex, age, and height] × 100 (%). This formula was based on the “Evaluation of Physical Build of Japanese Children” published by the Japanese Society of Pediatric Endocrinology (standard body weight was calculated by sex, age, and height; Table S1).13 A student was classified as obese if his or her degree of obesity was ≥20%.

2.2. Salt check sheet

The salt check sheet is comprised of 13 questions and takes 3‐5 minutes to complete (Table 1). The questions are categorized as follows: seven items evaluate the intake of salty meals such as miso soup, ham or sausage, and noodles such as udon and ramen; four items evaluate the use of salty sauces, the opportunity of consuming udon or ramen, eating out, and home‐meal replacement; and two items evaluate the seasoning content and size of homemade meals. Each question is scored up to three points for a total of 35 points. Salt content is characterized as low (0‐8 points), medium (9‐13 points), high (14‐19 points), or very high (>20 points).11, 12

Table 1.

Salt check sheet. Your salt check sheet: Circle the response that best fits you and write the total score at the end

	3 points	2 points	1 point	0 point
Frequency of eating these foods
Miso (fermented soybean paste) soup, other soups, etc	More than 2 bowls a day	About 1 bowl a day	Two‐three bowls a week	Hardly eat
Pickles, pickled plums, etc	More than twice a day	About once a day	Two‐three times a week	Hardly eat
Fish‐paste products such as chikuwa (tubular fish sausage) and kamaboko (steamed fish paste)		Eat frequently	Two‐three times a week	Hardly eat
Horse mackerel cut open lengthwise and dried, dried fish seasoned with mirin (sweetened alcohol for use in cooking), salted salmon, etc		Eat frequently	Two‐three times a week	Hardly eat
Ham or sausage		Eat frequently	Two‐three times a week	Hardly eat
Noodles such as udon (Japanese wheat noodles) and ramen (Japanese‐style Chinese noodles)	Almost every day	2 or 3 bowls a week	Less than once a week	Don't eat
Senbei (Japanese crackers), okaki (thinly cut and dried rice cakes), potato chips, etc		Frequently	Two‐three times a week	Hardly eat
How frequently do you season with soy sauce or other sauces?	Season frequently (almost each meal)	Once a day	Season sometimes	Don't season
How much udon, ramen, or other soups do you consume?	an entire bowl	About half a bowl	Some	Little
Do you eat out or have convenience‐store‐bought bento (lunch plate) for lunch?	Almost every day	About 3 times a week	About once a week	No
Do you eat out or have ready‐made side dishes for dinner?	Almost every day	About 3 times a week	About once a week	No
How salty are your homemade dishes compared with those you eat out?	Heavily salted	The same		Lightly salted
Do you think you eat a lot?	More than others		The same as others	Less than others
Total score of the items you circled	3 points × –––	2 points × –––	1 point × –––	1 point × –––
Subtotal	––– points	––– points	––– points	––– points
Total points	––– points
	Check below ☑	Total points	Evaluation
	□	0‐8	>You are not taking excess salt. Maintain this diet for salt restriction
	□	9‐13	Your salt intake is average. Start a little stricter salt restriction
	□	14‐19	You have excessive salt intake. You need to lower your salt intake by changing the salt content of your diet and your eating habits
	□	≥20	You have too much salt intake. You need to completely change the salt content of your diet and your eating habits

For fifth‐grade students in elementary school, we distributed the salt check sheet at school and asked that it be filled out at home by both the child and his or her parents. The first‐grade students in junior high school answered the questions on the salt check sheet themselves with the support of a trained dietitian from Higashiagatsuma town (K.K). In Higashiagatsuma town, the dietary salt intake of schoolchildren has been assessed using the salt check sheet every year since 2015.

2.3. Brief‐type, self‐administered diet history questionnaire

All participants completed the BDHQ15y at the same time that they completed the salt check sheet. The BDHQ15y questionnaire asks about dietary habits during the previous month.

The BDHQ15y is a four‐page, structured, self‐administered questionnaire that asks about the consumption frequency of selected foods to estimate the dietary salt intake of 67 food and beverage items during the preceding month. It consists of 4 sections: (a) intake frequency of food and nonalcoholic beverage items, (b) daily intake of rice and miso soup, (c) usual cooking methods, and (d) general dietary behavior. The intake of four seasonings was estimated using qualitative information from usual cooking methods and general dietary behavior. Each consumption frequency item included seven response options, ranging from “more than twice per day” to “almost never”.

We distributed the BDHQ15y to all study participants. In the present study, the parents of the schoolchild assisted with answering the questionnaire, as self‐completion was difficult. After completion, the questionnaires were collected and sent to an external institution (Gender Medical Research, Co., Lid.) for dietary intake assessments. Estimates of dietary intake for the 67 food and beverage items were calculated using an ad hoc computer algorithm (including weighting factors).

2.4. Statistical analysis

All statistical analyses were performed using SPSS software ver. 24.0 (SPSS). Descriptive statistics are presented as means, standard deviations (SD), and proportions, where appropriate. The Mann‐Whitney U test was used to compare clinical parameters within two groups. Clinical parameters evaluated as percentages were compared using chi‐squared statistics. Spearman's correlation coefficient was used for the dietary salt intake from the BDHQ15y and the total salt check‐sheet score. One‐way analysis of variance was used to compare three groups with the Bonferroni correction. To identify which factors in the salt check sheet correlated most strongly with the total salt intake from the BDHQ15y, the association between each question of the salt check sheet and salt intake was examined. We calculated the standardized regression coefficients of each question on the salt check sheet by performing univariate regression analyses for the total salt intake from the BDHQ15y. For the multivariate regression analyses, we used a stepwise forward selection approach in each model to select an array of questions from the salt check sheet that affected the total salt intake from the BDHQ15y. No other factors were adjusted in this study. The F test was used to decide whether to include questions from the salt check sheet into the model or exclude them. A P‐value < 0.05 was required for inclusion into the model, and a P‐value ≥ 0.10 was required for exclusion. Akaike's information criterion (AIC) was used to compare the goodness of fit among models containing questions from the salt cheek sheet. We tested synergistic effects on the total score of the salt check sheet among age, sex, and the presence of obesity using multiple regression analysis with two interaction terms added into the model. All statistical tests were performed using a two‐tailed design with a significance level (P‐value) of <0.05.

3. RESULTS

The characteristics of the study participants are shown in Table 2. The mean age of study participants was 11.2 ± 1.1 years. Approximately 15.1% of children were classified as obese (boys/girls: 16.2%/13.8%, P = 0.686). The mean estimated daily energy intake for boys and girls was 2565.2 ± 862.8 kcal and 2078.2 ± 530.1 kcal, respectively (P < 0.001).

Table 2.

Characteristics of the students in this study (n = 188)

Age, y	11.2 ± 1.1
Sex (boys/girls), n (%)	100 (53.2)/88 (46.8)
Body mass index, kg/m2	18.9 ± 2.9
Degree of obesity, %	4.2 ± 16.8
Systolic blood pressure, mm Hg	115.4 ± 12.4
Diastolic blood pressure, mm Hg	63.0 ± 7.7
Total cholesterol, mg/dL	164.9 ± 26.0
High‐density lipoprotein cholesterol, mg/dL	61.3 ± 12.4
Energy intake, kcal/d	2337.2 ± 764.3

The mean total salt check‐sheet score was 12.7 ± 4.0 points (range: 4‐24 points) (Figure 1A and Table S2). The estimated daily salt intake was 12.1 ± 3.7 g (range: 4.7‐27.2 g; Figure 1B). The total check‐sheet score was significantly positively associated with the estimated daily salt intake from the BDHQ15y (Figure 2A). Thirty‐one study participants (16.5%) were assigned to the “low” salt group (total score of the salt check sheet was 0‐8 points), 78 participants (41.5%) were assigned to the “medium” salt group (9‐13 points), and 79 participants (42.0%) were assigned to the “high and very high” salt group (≥14 points), respectively. We compared the “low,” “medium,” and “high and very high” salt groups in terms of the estimated daily salt intake from the BDHQ15y and found that the daily salt‐intake levels tended to increase as the group of total check‐sheet scores increased. There were significant differences between the three groups as follows: “low” salt group vs “medium” salt group, 9.5 ± 3.1 vs 11.6 ± 2.9 (P = 0.011); “low” salt group vs “high and very high” salt group, 9.5 ± 3.1 vs 13.5 ± 3.9 (P < 0.001); and “medium” salt group vs “high and very high” salt group, 11.6 ± 2.9 vs 13.5 ± 3.9 (P = 0.001) (Figure 2B).

Figure 1.

(A) Distribution of total salt check‐sheet scores. (B) Distribution of dietary salt intake. Descriptive statistics are presented as means and standard deviations (SD)

Figure 2.

(A) Association between dietary salt intake and total salt check‐sheet scores. (B) Relationship between salt‐intake levels using the salt check sheet and dietary salt intake. Descriptive statistics are presented as means and standard deviations (SD)

We analyzed the univariate association between each question of the salt check sheet and the estimated daily salt intake from the BDHQ15y (Table 3). Significant positive associations were found between the scores of questions that contained the following food type and eating habits “Pickles, pickled plum, etc” (β = 0.222, P = 0.002); “Opened dry horse mackerel, mirin‐seasoned dried fish, salted salmon, etc” (β = 0.388, P < 0.001); “Noodles such as udon and ramen” (β = 0.377, P < 0.001); “Frequency of seasoning with soy sauce, sauce, etc” (β = 0.246, P = 0.001); “Do you consume udon, ramen or other soups?” (β = 0.171, P = 0.019); “Taste of your homemade dishes: comparison with those you eat out” (β = 0.203, P = 0.005); and “Amount of food” (β = 0.198, P = 0.007; Table 3).

Table 3.

Association of salt intake and the scores in the salt check‐sheet items (n = 188)

	Univariate analysis
	β	P‐value
Frequency of high‐salt diet intake
Miso soup, other soup, etc	0.126	0.085
Pickles, pickled plums, etc	0.222	0.002
Fish‐paste products such as chikuwa and kamaboko	0.053	0.471
Opened and dried horse mackerel, mirin‐seasoned dried fish, salted salmon, etc	0.388	<0.001
Ham or sausage	0.094	0.202
Noodles such as udon and ramen	0.377	<0.001
Senbei, okaki, potato chips, etc	0.054	0.458
Additional seasoning, frequency of eating out, and home‐meal replacement
Frequency of seasoning with soy sauce, other sauces, etc	0.246	0.001
Consumption of udon, ramen, or other soups	0.171	0.019
Eating out or having convenience‐store‐bought bento (lunch plate) for lunch	0.114	0.120
Eating out or having ready‐made side dishes for dinner	0.050	0.492
Taste of homemade dishes, amount of food
Taste of homemade dishes: comparison with those eaten out	0.203	0.005
Amount of food	0.198	0.007

Abbreviations: β, standardized regression coefficient.

Next, we investigated the best model containing questions from the salt check sheet to assess dietary salt intake from the BDHQ15y for children. The model containing questions that referred to “Opened dry horse mackerel, mirin‐seasoned dried fish, salted salmon, etc”; “Noodles such as udon and ramen”; “Amount of food”; and “Taste of your homemade dishes: comparison with those you eat out” showed a better goodness of fit (lower AIC) than other models (Table 4). From this pool of questions, the one containing “Noodles such as udon and ramen” showed the largest standardized regression coefficient when compared to the other three.

Table 4.

Multiple regression analysis for the association of salt intake and the scores in the salt check‐sheet items (n = 188)

	B	SE	β	VIF	SE of estimates	R 2	Adjusted R 2	R 2 change	F change	AIC
Model 1
Opened and dried horse mackerel, mirin‐seasoned dried fish, salted salmon, etc	2.422	0.422	0.388 ‡	1.000	3.391	0.151	0.146	0.151	32.962 ‡	461.194
Model 2
Opened and dried horse mackerel, mirin‐seasoned dried fish, salted salmon, etc	1.866	0.426	0.299 ‡	1.110	3.254	0.222	0.214	0.072	17.068 ‡	446.603
Noodles such as udon and ramen	1.668	0.404	0.282 ‡	1.110
Model 3
Opened and dried horse mackerel, mirin‐seasoned dried fish, salted salmon, etc	1.821	0.422	0.292 ‡	1.113	3.215	0.245	0.233	0.023	5.560*	443.060
Noodles such as udon and ramen	1.599	0.400	0.270 ‡	1.117
Amount of food	0.798	0.338	0.152*	1.011
Model 4
Opened and dried horse mackerel, mirin‐seasoned dried fish, salted salmon, etc	1.671	0.425	0.268 ‡	1.148	3.188	0.262	0.245	0.016	4.067*	440.873
Noodles such as udon and ramen	1.630	0.397	0.276 ‡	1.118
Amount of food	0.722	0.338	0.137*	1.023
Taste of homemade dishes: comparison with those eaten out	0.832	0.421	0.131*	1.047

Abbreviations: AIC, Akaike's information criterion; B, regression coefficient; R ², coefficient of determination; SE, standard error; VIF, variance inflation factor; β, standardized regression coefficient.

^* P < 0.05,

^† P < 0.01,

^‡ P < 0.001.

In the subgroup analyses, we compared the scores from the salt check‐sheet items between fifth‐grade students from elementary schools and first‐grade students from junior high schools, separating boys from girls. There were no significant differences in the total scores of the salt check sheet even when they were classified by grade or sex (Tables S3 and S4). However, the total check‐sheet score did show a significant association with the estimated daily salt intake from BDHQ15y when classified by grade or sex (Figures S2A‐S5A). In addition, when we compared the “low,” “medium,” and “high and very high” salt groups in terms of the estimated daily salt intake from BDHQ15y by grade or sex, the daily salt‐intake levels tended to increase as the group of total check‐sheet scores increased in all subgroups (Figures S2B‐S5B). In the multivariate analyses, we investigated the association between the total score of the salt check sheet and the baseline characteristics of study participants by age, sex, and the presence of obesity. There were no significant interactions between these factors and the association with the total score of the salt check sheet (Table S5).

In the sensitivity analyses, we investigated whether other categorized groups by the salt check sheet showed an association between higher scores on the salt check sheet and higher levels of dietary salt intake. The results were similar to the subgroup analyses.

4. DISCUSSIONS

This is the first study to demonstrate a significant association between the total score of the salt check sheet and the estimated dietary salt intake from the BDHQ15y. A positive correlation was found between the total check‐sheet score and the estimated daily salt intake from the BDHQ15y. In addition, dietary salt‐intake levels tended to increase as the total check‐sheet score increased. These results indicate that the salt check sheet is a useful tool to assess dietary salt intake in children.

We have shown that the salt check sheet is a simple tool that can be used to estimate dietary salt intake in children. Several methods have been proposed to assess salt intake, and they have both merits and limitations.14 However, there is no established method for the evaluation of salt intake during childhood. In clinical practice, the gold standard method to evaluate salt intake is to measure sodium excretion in 24‐hour pooled urine.15 This method is highly reliable; however, it is too complicated to perform in children. As an alternative method, an assessment of the sodium/creatinine ratio using second a urine sample collected early in the morning, or, alternatively, spot urine, is widely used for the evaluation of dietary salt intake at general medical facilities.14 Although this method is simple, it is not easy to repeatedly perform in children. The BDHQ has been used in several epidemiological studies for dietary assessment during childhood, including salt intake.7, 8 Sakata et al demonstrated that the estimated salt intake evaluated by the BDHQ significantly, although weakly, correlated with 24‐hour urinary salt excretion.16 Taking into consideration our results demonstrating that the total check‐sheet score was significantly correlated with estimated dietary salt intake from the BDHQ15y, this indicates that the salt check sheet could provide approximate information regarding the dietary salt intake of children. Further studies are needed to evaluate the accuracy of the salt check sheet for this estimation in children.

The present study revealed that the estimation of salt intake in children is surprisingly high. The standard dose of salt intake for children in Japan (10‐11 years of age) is <6.5 g/d for boys and <7.0 g/d for girls.17 Our results suggest that education and a plan for reducing dietary salt intake for both children and their parents should be given. Since reducing salt intake beginning in childhood can improve health and reduce the rate of cardiovascular death,6 it is important to reduce it starting from childhood. This may lead to a reduction in the long‐term economic costs associated with cardiovascular risk factors. In 2017, the Japanese Circulation Society declared it necessary to provide children with knowledge that enabled them to prevent the onset of cardiovascular disease and helped them undertake social measures, such as self‐aware behavioral changes, to enact these measures. This was necessary as lifestyle‐related diseases, including the onset of cardiovascular diseases, were manifesting at lower ages due to recent changes in lifestyle and the social environment. Furthermore, the World Health Organization (WHO) strongly recommends a reduction in salt intake to control BP in children (2‐15 years of age).18 The recommended maximum level of salt intake of 5 g/d in adults should be adjusted downward based on the energy requirements of children relative to those of adults.18 The WHO has also recommended that monitoring of salt intake at the country level is needed to adjust salt consumption over time (depending on observed salt‐intake levels in the population) to ensure that individuals are consuming the recommended amount of salt.18 An accurate assessment of dietary salt intake in children is both necessary and urgent for the education and prevention of BP elevation during childhood as well as the onset of CVD events in adulthood. The salt check sheet could be one method used to reduce the amount of dietary salt intake via school education programs in Japan. We expect that the salt check sheet will be widely used in school education for dietary salt reduction.

In the results from our multivariate regression analyses, the questions containing “Noodles such as udon and ramen” and “Opened dry horse mackerel, mirin‐seasoned dried fish, salted salmon, etc” showed larger standardized regression coefficients than other questions. Udon is a thick white noodle made of wheat flour and served in a soy sauce–based soup. Ramen is made from wheat flour, water, salt, eggs, and other ingredients and is served in several types of soup, including soy sauce flavored, salt flavored, and soybean flavored. Opened and dried horse mackerel is prepared by cutting a horse mackerel open, removing its scales and internal organs, and then drying for long‐term storage. Mirin‐seasoned dried fish is marinated in mirin (a type of sweet sake used in cooking) and then dried. Salted salmon is salmon with sprinkled sea salt on all sides, including the skin.

Interestingly, our results reflect the regional characteristics of Higashiagatsuma town. In this area, wheat, as the base of udon, has been grown for many years and the people in this community, including the children, eat udon as a staple food. In addition, they keep fish dried and salted for long‐term storage, as the town is inland. The salt check sheet cannot only estimate the dietary salt intake of children, but it has the potential to reflect the regional characteristics of dietary patterns. This suggests that modification in the question of the salt check sheet that reflects regional characteristics may increase the accuracy of estimated dietary salt intake. We anticipate that various types of modified salt check sheets will be utilized that reflects the regional characteristics.

This study has some limitations. First, the sample size was small. Second, we examined the validity of the salt check sheet for children only once. Therefore, the reproducibility of the salt check sheet is unclear. Third, we could not directly evaluate dietary salt intake from participant's meals; instead, it was estimated from the BDHQ15y questionnaire. Fourth, the estimated salt intake of children obtained from questionnaires might be biased, depending on the child's cognitive ability. Fifth, the individuals who answered the salt check sheet and the BDHQ15y were different. Finally, the participants of this study may not be representative of Japanese children in general. Further studies are needed to assess the usefulness of salt check sheets for children in other areas.

In conclusion, we have demonstrated that there is a significant positive association between the total score of the salt check sheet and estimated dietary salt intake from the BDHQ15y. This result indicates that the salt check sheet is a useful tool to assess dietary salt intake in children. We believe that more detailed guidance for salt restriction can be provided by using a combination of the salt check sheet and other tools, such as the urinary salt excretion assessment and information obtained from dietary questionnaires, such as the BDHQ15y. We also hope that the education needed to reduce childhood dietary salt intake is obtained using the salt check sheet.

CONFLICT OF INTEREST

The authors declare that they have no potential conflicts of interest.

AUTHOR CONTRIBUTIONS

T. Fujiwara and K. Kikuchi involved in conception and design. T. Fujiwara and S. Hoshide involved in analysis and interpretation of data. T. Fujiwara, S. Hoshide, T. Tsuchihashi, and K. Kario drafted the manuscript or critically revised for important intellectual content. K. Kario approved the final version of the submitted manuscript.

Supporting information

 

 

 

 

 

 

  

 

 

 

 

Fujiwara T, Kikuchi K, Hoshide S, Tsuchihashi T, Kario K. Usefulness of a salt check sheet for elementary school and junior high school children. J Clin Hypertens. 2019;21:722–729. 10.1111/jch.13549