Abstract
This study investigated the association between the daily salt intake of 3‐year‐old children and that of their mothers. A total of 641 children were studied. The daily salt intake of the children and their mothers was estimated by morning and spot urine methods, respectively. In the multivariable analysis, a 1 g higher maternal daily salt intake was associated with a 0.14 g (95% confidence interval [CI], 0.07‐0.22, P < .001) higher salt intake of her children. In the secondary analysis, the odds ratios for excess salt intake of children were 1.61 (95% CI, 1.01‐2.55, P = .045) and 1.81 (95% CI, 1.12‐2.91, P = .015) for 9.7‐11.5 g and 11.5 g or more of maternal daily salt intake, respectively. Our findings could help to convince mothers of the importance of appropriate salt intake, not only for themselves but also for their children.
Keywords: community based studies, diet/nutrition/hypertension, sodium
1. INTRODUCTION
Hypertension can begin early in childhood,1, 2 and it is known that excessive salt intake in early childhood leads to hypertension and cardiovascular diseases later in life.3 This effect is modifiable, and trials of salt‐reduced diets in children have led to lower blood pressures and even prevention of subsequent hypertension.3, 4 In Japan, one of the countries with the highest salt intake, the mean salt intake in 3‐year‐old children is quite high at 4.4 g/d.5 According to the Japanese Ministry of Health, Labour and Welfare, the recommended daily salt intake for 3‐year‐old children is less than 4.5 g for girls and less than 4.0 g for boys.6 Thus, for the sake of preventing future hypertension, it seems important to increase awareness among parents and caretakers of appropriate childhood salt intake.
Although it has been reported that mothers’ dietary habits significantly affect the nutrition of their children,7, 8, 9 very few studies have assessed the association between the salt consumption of children and that of their mothers. Revealing such association could be effective in convincing mothers of the importance of appropriate salt intake, not only for themselves but also for their children. Furthermore, children should establish healthy nutritional habits as early as possible.10, 11 Although some studies have evaluated the association between the salt intake of school‐aged children and their mothers,12, 13 there has been only one study assessing such association for younger children (3‐5 years old), and it used food diaries.9 Accordingly, the aim of the present study was to use objective measures to investigate the influence of maternal salt intake on the salt intake of 3‐year‐old children.
2. METHODS
2.1. Study design and setting
We conducted a cross‐sectional study in the setting of municipal health checkups for 3‐year‐old children in Shirakawa city, Fukushima, Japan. Shirakawa city is a local municipality in the southern part of Fukushima Prefecture; the population is 61 228 (November 2017). In Japan, per the Maternal and Child Health Act, health checkups are mandatory for 3‐year‐old children.14
2.2. Participants
We included children and their mothers who participated in the checkups for 3‐year‐olds between April 2016 and September 2017. The rate of participation in health checkups for 3‐year‐old children during the study period was approximately 99%.
We excluded subjects if urine samples could not be obtained from either the mother or the 3‐year‐old. Mothers during the menstrual period at the time of checkups were also excluded. A few potential subjects who declined to participate were not included.
2.3. Data collection
Health checkups for 3‐year‐old children in Japan are aimed at maintaining and promoting the health of children and their mothers. The following data are routinely collected for the child: age; sex; head and chest circumferences; height; body weight; dietary, sleeping, and exercise habits; physical, mental, and social development; physical, neurological, ophthalmological, and dental examinations; and a urine dipstick test. In addition to these, we collected data on several other items considered potentially associated with daily salt intake in 3‐year‐old children. These items were chosen based on findings of previous studies5, 10, 12, 13, 15, 16, 17 and discussion among researchers (general internist [TT], nephrologists [SS and SF]), a registered dietitian (MI, see acknowledgement), and public health nurses of the municipality. The additional data collected for the children included family structure, living with grandparents, child's primary caretaker, primary food preparer for the family, daycare or kindergarten attendance, and daily salt intake estimated by the morning urine method. The additional data collected for the mothers included age, height, weight, smoking and alcohol consumption habits, working status, lifestyle diseases (hypertension, diabetes, and hyperlipidemia), and daily salt intake estimated by the spot urine method.
The urine samples from the children and mothers were collected on the same day. Sodium and creatinine concentrations were analyzed by electrode and enzyme methods, respectively. For estimation of 24‐hour salt excretion of the mothers, we applied the formula recommended by the Japanese Society of Hypertension.18 It is a simple method for obtaining a valid approximation of 24‐hour urinary sodium excretion using spot urine as follows19: 24‐hour salt excretion (g/d) = 0.0585 × 21.98 × {(NaS/CrS) × Pr.UCr24}0.392, where NaS is the sodium concentration in the spot urine (mEq/L), CrS is the creatinine concentration in the spot urine (mg/L), Pr.UCr24 is the estimated 24‐hour urinary creatinine excretion (mg/d), and Pr.UCr24 = −2.04 × age + 14.89 × body weight (kg) + 16.14 × height (cm) − 2244.45. The daily salt intake of the mothers was calculated by dividing the estimated 24‐hour salt excretion by 0.86.20 The recommended daily salt intake for adult women is less than 7 g according to the Japanese Ministry of Health, Labour and Welfare.6
2.4. Main outcome measure
Our primary outcome was the daily salt intake of 3‐year‐old children. Although the ideal method for estimating daily salt excretion is 24‐hour urine collection, it is very difficult to collect 24‐hour urine from a 3‐year‐old child; according to a previous study, only about half of such attempts are successful.21 We therefore used a formula developed by Morinaga and colleagues5 that estimates daily salt excretion based on a first morning urine sample. The formula, which assumes a 24‐hour urinary creatinine excretion in 3‐year‐old children of 300 mg,21 is as follows: 24‐hour salt excretion (g/d) = 0.0585 × 300 × (NaM/CrM), where NaM is the sodium concentration in the first morning urine (mEq/L) and CrM is the creatinine concentration in the first morning urine (mg/L). As is the case with that of the mothers, the daily salt intake of the 3‐year‐old children was calculated by dividing the estimated 24‐hour salt excretion by 0.86.20
The secondary outcome was excess salt intake by the 3‐year‐old children, which was defined as a daily salt intake of 4.5 g or more for girls and 4.0 g or more for boys, as recommended by the Japanese Ministry of Health, Labour and Welfare.6 These cut‐off values for excess salt intake were calculated based on values recommended by the World Health Organization and on the reported median values of sodium intake of preschool children from the Japanese National Health and Nutrition Survey.17
2.5. Statistical analysis
We used descriptive statistics to summarize participants’ characteristics as counts and percentages for categorical variables and as mean and standard deviation (SD) for continuous variables. The association between the daily salt intake of the children and that of the mothers was assessed using a robust regression model fitted with MM‐estimators,22 as there were outliers among the values for the daily salt intake of the children. The model also included these variables that we considered possibly associated with daily salt intake in 3‐year‐old children: age, sex, Kaup index, family structure (having older or younger siblings), living with grandparents, child's primary caretaker (mother or others), primary food preparer for the family (mother or others), and daycare or kindergarten attendance. The model was also adjusted for the following maternal variables: age, body mass index, smoking and alcohol consumption habits, working status, and lifestyle diseases (hypertension, diabetes, and hyperlipidemia). Because the estimation of the daily salt intake of the children was based on the assumption that their 24‐hour urinary creatinine excretion was 300 mg, the physiques of the children were not taken into account. Therefore, we conducted the sensitivity analysis using the model that did not include the Kaup index as an explanatory variable. For the analysis of the secondary outcome, excess salt intake by the children, we used a multiple logistic model and included the same variables as in the primary analysis. To simplify the interpretation of the results, we also conducted the secondary analysis using maternal daily salt intake categorized into quartiles.
To account for missing data, we carried out 20 imputations using the Markov Chain Monte Carlo method. A two‐sided P value less than .05 was considered statistically significant. We conducted statistical analyses using a commercial software package (STATA, version 14.2 SE; StataCorp LP, College Station, TX).
2.6. Ethical considerations
This study was performed in accordance with the Declaration of Helsinki and the Ethical Guidelines for Medical and Health Research Involving Human Subjects by the Japanese Ministry of Health, Labour and Welfare. The study protocol was approved by the Ethics Committee of Shirakawa Kosei General Hospital (HAKURIN 16‐004). Public health nurses of the municipality explained the project and obtained written consent from all participating mothers. Participants were informed that they were free to decline participation without penalty.
3. RESULTS
Of the 720 potential subjects identified through health checkups, 77 were unable to collect the required urine samples, 2 declined to participate, and 641 were enrolled as participants. Participant characteristics are shown in Table 1. The mean age of the children was 41.7 months (SD 0.7) and 52.0% were boys. About 90% of the mothers were both primary caretakers of their children and primary food preparers for their families. The mean age of the mothers was 33.7 years. About 60% of the mothers had jobs and very few had lifestyle diseases. The mean estimated daily salt intake was 4.5 g (SD 2.8) for the children and 10.1 g (SD 2.3) for the mothers. Almost half of the children and 90% of the mothers exceeded the recommended amount of salt intake.
Table 1.
Basic characteristics of participants
| Children | |
| Age (mo) | 41.7 ± 0.7 |
| Male (%) | 333 (52.0) |
| Height (cm) | 95.5 ± 3.5 |
| Weight (kg) | 14.6 ± 1.7 |
| Kaup index (kg/m2) | 16.0 ± 1.3 |
| No siblings (%) | 148 (23.1) |
| Having older siblings (%) | 342 (53.4) |
| Having younger siblings (%) | 216 (33.7) |
| Living with grandparent (%) | 208 (32.4) |
| Primary caretaker (%) | |
| Mother | 593 (92.5) |
| Grandmother | 42 (6.6) |
| Others | 6 (0.9) |
| Primary food preparer for the family (%) | |
| Mother | 575 (89.7) |
| Grandmother | 60 (9.4) |
| Others | 6 (0.9) |
| Daycare or kindergarten attendance (%) | 525 (81.9) |
| Eating sweets almost every day (%) | 289 (45.2) |
| Eating between meals more than twice a day (%) | 382 (59.6) |
| Daily salt intake estimated by morning urine (g) | 4.5 (2.8) |
| Excess salt intake (%) | 292 (45.6) |
| Mothers | |
| Age (y) | 33.7 (4.9) |
| Height (cm) | 158.4 (5.3) |
| Weight (kg) | 55.1 (10.2) |
| Body mass index (kg/m2) | 22.0 (3.9) |
| Smoking (%) | 69 (10.8) |
| Alcohol (%) | 150 (23.4) |
| Job (%) | 382 (59.6) |
| Hypertension (%) | 16 (2.5) |
| Diabetes (%) | 2 (0.3) |
| Hyperlipidemia (%) | 3 (0.5) |
| Daily salt intake estimated by spot urine (g) | 10.1 (2.3) |
| Excess salt intake (%) | 597 (93.1) |
3.1. Association between daily salt intake of the children and that of their mothers
Figure 1 shows the distribution of the estimated daily salt intake of the children and their mothers. In the multivariable adjusted robust regression model with MM‐estimators, the daily salt intake of the mothers showed significant correlation with that of their children. A 1 g higher maternal daily salt intake was associated with a 0.14 g (95% CI, 0.07‐0.22, P < .001) higher salt intake in their children (Table 2). Also, a 1 kg/m2 higher Kaup index for children was significantly associated with a 0.17 g (95% CI, 0.01‐0.33, P = .039), and maternal hypertension was associated with a 2.09 g (95% CI, 0.90‐3.28, P = .001) higher daily salt intake in their children. The sensitivity analysis showed similar findings, with a 1 g higher maternal daily salt intake and maternal hypertension associated with a 0.14 g (95% CI, 0.06‐0.21, P < .001) and a 1.90 g (95% CI, 0.65‐3.13, P = .003) higher salt intake in their children, respectively.
Figure 1.
Distribution of estimated daily salt intake of the children and their mothers. The gray line represents the regression line
Table 2.
Results of the multivariable adjusted robust regression model with MM‐estimators
| β | P | 95% confidence interval | ||
|---|---|---|---|---|
| Children | ||||
| Age (mo) | −0.01 | .919 | −0.29 | 0.27 |
| Male | −0.30 | .087 | −0.65 | 0.04 |
| Kaup index | 0.17 | .039 | 0.01 | 0.33 |
| Having older siblings | 0.07 | .728 | −0.32 | 0.45 |
| Having younger siblings | −0.02 | .918 | −0.47 | 0.42 |
| Living with grandparent | −0.24 | .245 | −0.66 | 0.17 |
| Primary caretaker: other than mother | −0.53 | .096 | −1.16 | 0.09 |
| Primary food preparer: other than mother | 0.30 | .386 | −0.38 | 0.97 |
| Daycare or kindergarten attendance | 0.35 | .196 | −0.18 | 0.87 |
| Mothers | ||||
| Age (y) | −0.01 | .462 | −0.05 | 0.02 |
| Body mass index | −0.03 | .282 | −0.08 | 0.02 |
| Smoking | 0.39 | .164 | −0.16 | 0.95 |
| Alcohol | −0.14 | .523 | −0.59 | 0.30 |
| Job | −0.24 | .22 | −0.63 | 0.15 |
| Hypertension | 2.09 | .001 | 0.90 | 3.28 |
| Diabetes | −0.22 | .799 | −1.96 | 1.51 |
| Hyperlipidemia | 0.70 | .264 | −0.53 | 1.94 |
| Daily salt intake estimated by spot urine (g) | 0.14 | <.001 | 0.07 | 0.22 |
3.2. Association between excess salt intake by the children and daily salt intake of their mothers
In multivariable logistic analysis of excess salt intake by the children, maternal daily salt intake and hypertension were the only factors that showed significant correlation. We found that on average, the odds ratio (OR) of a child consuming excess salt was 1.13 (95% CI, 1.05‐1.22, P = .001) for each additional daily gram of salt intake by their mother. The OR of maternal hypertension for excess salt intake by children was 3.15 (95% CI, 1.01‐9.83, P = .049).
We also conducted the secondary analysis using maternal daily salt intake categorized into quartiles as follows: less than 8.4 g, 8.4 g to less than 9.7 g, 9.7 g to less than 11.5 g, and 11.5 g or more. The ORs for excess salt intake by children were 0.94 (95% CI, 0.59‐1.49, P = .777) for 8.4 g to less than 9.7 g, 1.61 (95% CI, 1.01‐2.55, P = .045) for 9.7 g to less than 11.5 g, and 1.81 (95% CI, 1.12‐2.91, P = .015) for 11.5 g or more (Figure 2). In this analysis, the OR of maternal hypertension for excess salt intake by the children was 3.37 (95% CI, 1.09‐10.47, P = .035).
Figure 2.
Odds ratios of excess salt intake by children for categories of maternal salt intake. *P < .05
4. DISCUSSION
Our analysis showed significant associations between the daily salt intake of 3‐year‐old children and that of their mothers, and the risk of excess salt intake is higher for 3‐year‐old children of mothers who consume more salt. This could be explained by the fact that mothers and their children tend to show similar patterns of food acceptance and preference.15 Mothers who consume high amounts of salt are likely to expose their children to excess salt as well, and this could result in children acquiring a preference for it, beginning at ages as young as 2‐6 months.23
Because food preferences in infancy are reflected in dietary behaviors later in life,16, 24 it is important to establish healthy eating habits and appropriate patterns of salt intake early in childhood.10 According to a previous meta‐analysis,25 salt reduction in infants led to a significant decrease in systolic blood pressure. In a blinded randomized controlled trial among 476 newborn infants, a sodium reduction of approximately 30% was significantly associated with a 2.1 mm Hg decrease in systolic blood pressure.3 Furthermore, in a study of 167 of the participants of that same trial who were followed for 15 years, the adjusted systolic blood pressure was 3.6 mm Hg lower and the diastolic pressure was 2.2 mm Hg lower in the low sodium diet group, with statistical significance.4 Thus, salt intake in childhood is modifiable, and appropriate salt reduction could prevent or decrease the risk of future hypertension.
There has been one other study of the association between the daily salt intake of infants and that of their mothers. In this study, the daily salt intake was estimated using food diaries; however, the daily salt intake estimated by a food diary does not correlate well with actual salt intake.18 There have also been investigations of the associations between the daily salt intake of school‐aged children and that of their mothers. A study in Australia reported findings consistent with our own: a 1 g increase in the daily salt intake of mothers was associated with 0.2 g increase in that of school‐aged children of mean age 9.1 years (SD 2.0).12 Likewise, a 1 g increase in the daily salt intake of mothers was associated with a 0.19 g increase in that of Japanese school‐aged children of mean age 9.6 years (SD 2.4).13
In our analyses, maternal hypertension showed significant association with higher daily salt intake of the children, even when adjusted for maternal daily salt intake. Although only 2.5% of the mothers had hypertension, its effect on the salt intake of their children seemed relevant. The mechanism of the association between maternal hypertension and the salt intake of children remains unknown. There could be some effect of unmeasurable confounding factors like socioeconomic factors.
We also evaluated the associations between the daily salt intake of the children and several other factors, including family structure. We hypothesized that living with grandparents could result in higher salt intake of the children, as elderly people in Japan tend to consume more salt than young people do,26 and their taste preference for salt might influence salt consumption in their grandchildren. Moreover, it has been suggested that having older siblings might be related to increased salt intake in children, though this was based only on univariate analysis.5 It is possible that older siblings who enjoy salty snacks are likely to expose younger siblings to them early, but our analysis found no significant associations between the daily salt intake of the children and family structure.
The strength of our study was its use of objective measurement (urine analysis) to investigate associations between maternal and child daily salt intake for children younger than those previously included in such studies. Recently, the effectiveness of a family‐based approach for salt reduction and cardiovascular health has been reported.27, 28, 29 Its success is attributed to several mechanisms, including mutual interdependence of the family system, shared environment, parenting style, caregiver perceptions, and genomics.29 The results of our study could be effective for increasing mothers’ awareness of appropriate salt consumption in children and for reinforcing the importance of the family‐based approach for salt reduction. Policies and strategies targeting mothers and their children are expected to establish eating habit recommendations, including appropriate salt intake for early childhood, and to help prevent future hypertension and cardiovascular disease.
5. LIMITATIONS
Our analysis had several limitations. First, the daily salt intake of the children was estimated based on the assumption that 24‐hour urinary creatinine excretion in 3‐year‐old children is 300 mg. Therefore, the daily salt intake could be under/overestimated in children with larger/smaller muscle volume. Given that the ideal method for estimating daily salt, 24‐hour urine collection, is not feasible for 3‐year‐olds, we resorted to the first morning urine method. Second, for the sake of convenience, we estimated the daily salt intake of the mothers using the spot urine method, which is less reliable than estimations based on 24‐hour urine collection.18 Furthermore, we did not exclude pregnant mothers, for whom the spot urine method has not been validated. Recognizing that the values of daily salt intake for both the children and their mothers might be imprecise, we conducted secondary analyses using categorical variables for salt intake, and it showed similar results to those of our primary analysis. Third, we assessed the daily salt intake of the children and that of their mothers on only 1 day. To prove the consistency of our findings, it would be preferable to conduct the assessment over several days. However, there were issues associated with cost and burden on the participants. Fourth, we did not collect any specific information on the food consumed by the children or their mothers. To give more practical advice, the effect of the types of food consumed on salt intake should be further investigated. Finally, this study was conducted in the southern part of Fukushima Prefecture, a relatively rural area of Japan. Family relationships in rural areas could be relatively stronger than those in urban areas. Therefore, further investigations are necessary to assess the external validity of our findings.
6. CONCLUSION
Our analyses demonstrate significant associations between the daily salt intake of 3‐year‐old children and that of their mothers. Higher daily salt intake by mothers could lead to excess salt intake by their children. Interventions targeting mothers and children are expected to reduce future hypertension and cardiovascular disease.
CONFLICT OF INTEREST
None.
AUTHOR CONTRIBUTIONS
TT had full access to all of the data in the study; he takes responsibility for the integrity of the data and accuracy of the data analysis and wrote the first draft. S Fukuma and SS designed the study, interpreted the data, and drafted the paper. MH, JM, and TA collected and interpreted the data. S Fukuma and S Fukuhara supervised the research and revised the work critically for important intellectual content.
ACKNOWLEDGMENTS
We thank the public health nurses of Shirakawa city for managing the project, Miyuki Imamoto for practical advice from the perspective of a registered dietitian, Kaori Omata of Shirakawa Kosei General Hospital for data management, and all the children and mothers who participated in the study.
Takada T, Fukuma S, Shimizu S, et al. Association between daily salt intake of 3‐year‐old children and that of their mothers: A cross‐sectional study. J Clin Hypertens. 2018;20:730–735. 10.1111/jch.13256
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