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PLOS One logoLink to PLOS One
. 2020 Jul 17;15(7):e0235951. doi: 10.1371/journal.pone.0235951

The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

Haiquan Xu 1, Olivier Ecker 2, Qian Zhang 3, Songming Du 4, Ailing Liu 3, Yanping Li 5, Xiaoqi Hu 3, Tingyu Li 6, Hongwei Guo 7, Ying Li 8, Guifa Xu 9, Weijia Liu 10, Jun Ma 11, Junmao Sun 1, Kevin Chen 2,12,*, Ma Guansheng 13,*
Editor: Seth Adu-Afarwuah14
PMCID: PMC7367455  PMID: 32678852

Abstract

Background

Little evidence from developing countries on dietary transition demonstrates the effects of comprehensive childhood obesity interventions on dietary diversity and food variety among younger children. This study aimed to evaluate the effects of comprehensive childhood obesity interventions on dietary diversity among younger children.

Methods

A total of 4846 children aged 7–13 years were included based on a multicenter randomized controlled trial for childhood obesity interventions in 38 primary schools. Nutrition education intervention (NE), physical activity intervention (PA) and comprehensive intervention including both NE and PA (CNP) were carried out separately for 2 semesters. Dietary Diversity Score (DDS9 and DDS28 for 9 and 28 food groupings, respectively), Food Variety Score (FVS, the number of food items) and the proportions of different foods consumed were calculated according to the food intake records collected with the 24-h dietary recall method.

Results

The intervention effects per day of comprehensive intervention group were 0 (95% Confidence Interval (CI): 0, 0.1; p = 0.382) on DDS9, 0.1 (95% CI: -0.1, 0.2; p = 0.374) on DDS28 and 0.1 (95% CI: -0.1, 0.3; p = 0.186) on FVS of overall diet, which was 0.1 (95% CI: 0, 0.1; p < 0.001) on DDS9, 0 (95% CI: 0, 0.1; p = 0.168) on DDS28 and 0.1 (95% CI: 0, 0.1; p = 0.067) on FVS of dietary scores of breakfast only. Additionally, CNP group had greater increases in cereals, meat and fruits, and more decreases in eggs, fish and dried legumes consumption proportions as compared with the control group. Decreasing side effect on dietary diversity and food variety were found for PA intervention, but not for NE intervention only.

Conclusions

Though the comprehensive obesity intervention didn’t improve the overall dietary diversity per day, the positive intervention effects were observed on breakfast foods and some foods’ consumption.

Introduction

With the economic development in China, the increase in unhealthy body weight has led to a fast increase in obesity prevalence among children. The Chinese Residents’ Nutrition and Chronic Disease Report (2015) showed that the prevalence of overweight and obesity among children aged 6–17 years increased from 6.6% in 2002 to 16.0% in 2012 [1]. To control childhood obesity, school-based intervention programs focusing on nutrition education, physical activity or both have increasingly emerged as important strategies in China, mainly focused on shaping healthy eating habits and balancing energy intake and expenditure [2].

Dietary diversity, representing the consumption of various food items within and between food groups, is a strong predictor of dietary quality, defined as micronutrient adequacy, in developing countries [3]. Previous studies revealed that dietary diversity is associated with the micronutrient adequacy of diets and anthropometry in children [3, 4]. According to the dietary guidelines in many countries, dietary diversity is one of the characteristics of a healthy diet [5, 6]. By testing different food groupings, food groups (ranging from 7 to 21 groups) and accuracy of indicators, dietary diversity score (DDS) and food variety score (FVS) have been widely used as effective indicators [7, 8]. In addition to a positive relationship between DDS and nutrient intake being reported, the inverse association between DDS and chronic diseases [911] have been revealed by several studies.

Research has also revealed the dietary diversity associated with high energy intake [12]. Nutrition education is viewed as a key strategy for promoting healthy eating habits, while a physical activity-friendly school environment is also associated with a lower risk of obesity [13]. Many researchers found that diet quality could increase among children after nutrition education intervention, and some studies indicate that a lifestyle intervention plus nutrition education could improve dietary diversity [14, 15]. One multicenter randomized controlled trial of a comprehensive school-based intervention study focusing on childhood obesity was implemented in China [16]. The evaluation indicated that comprehensive intervention was more effective than only nutrition education or only physical activity on childhood obesity prevention [17, 18]. And we observed a moderately significant effect on the combined prevalence of overweight and obesity, which increased by 1.5 percent in the control group and 0.2 percent in the CNP group after intervention. The effect was significantly stronger among girls than boys (-1.4% vs. -0.9%). However, we did not find a significant effect in the nutrition education group or the physical activity group. Several school-based interventions for childhood obesity have revealed a positive effect on changing eating behaviors and improving vegetable and fruit consumption and the availability of healthy foods, but few have focused on dietary diversity or food variety [1921]. Though research showed that school children with a high level of physical activity presented a better quality of the diet [22], we wanted to know whether childhood obesity intervention will increase dietary diversity. To our knowledge, little previous research has evaluated the effects of childhood obesity interventions on dietary diversity among younger children in developing countries undergoing dietary transition. Therefore, the objective of this study was to explore the effects of nutrition education and physical activity as childhood obesity interventions on dietary diversity among younger children in China.

Materials and methods

Study design and sample size

This trial was designed into two parts. One study was a cluster-randomized controlled trial for nutrition education intervention (NE) and physical activity intervention (PA) separately in Beijing. The other one was a multicenter cluster-randomized controlled trial for a comprehensive intervention including nutrition education and physical activity (CNP) in 5 centers, in Shanghai, Chongqing, Guangzhou, Jinan and Harbin. Multi-step randomized cluster sampling method was used for subjects’ selection. First, 1–3 districts were selected randomly in the lottery in each city, then the schools were selected randomly in the lottery in each selected district. The schools were selected according to some inclusion criteria: 1) non-boarding school; 2) the prevalence of obesity, based on the routine physical examination records, was above 10%; 3) Providing school lunch feeding, and more than 50% students have lunch at school. Eight schools selected randomly were divided into three groups (3 schools for NE, 3 schools for PA and 2 schools as a shared control) in Beijing, and six schools from each other city were randomly sorted into 2 groups (3 for CNP and 3 for control). In total, 38 primary schools were included in this trial. Two classes were selected from each grade (1st to 5th) in every school, but only grades 2 to 4 were designed to collect the dietary records. The program was implemented for 2 semesters from May 2009 to May 2010. NE was also targeted towards parents, teachers, and health workers in treated schools. The detailed design information has been described in previous articles [16, 18].

This trial was approved by the Ethical Review Committee of the National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention. The informed consent was voluntarily signed by the participants’ parents or their guardians. The trial was registered at the Chinese Clinical Trial Register (number ChiCTR-PRC-09000402).

The present analysis on dietary diversity was not the primary outcome for this trial. The calculation of sample size was performed according to the changes of DDS9 in the CNP. The interclass correlation coefficient for DDS9 was 0.18. with a sample size of 4051, we will have 90% power to detective an effect size of as much as 0.6 from 30 schools located in 5 centers, at double side 0.05 level. Our effect size was 0.61, with sample size of 4069, stronger than the minimum detectable level. Only the children in 2nd grade or higher had their dietary records collected, 4933 (both in 5 centers and in Beijing) children with dietary records were extracted from the total participants. Finally, 4846 subjects’ information with both baseline and ending dietary records was used. The trial profile for data analysis is shown in Fig 1.

Fig 1. The trial profile for data analysis.

Fig 1

Intervention implementation

Table 1 shows the intervention measures for different intervention groups. In NE intervention schools, one nutrition education handbook was developed [23] for the students, courses on nutrition and health for the students, parents, teachers and health workers were designed separately. Furthermore, “Dietary Pagoda for Chinese people” posters were displayed in the classrooms for NE intervention groups. In PA intervention schools, the “Happy 10”, which was a classroom-based physical activity program for primary school students was used [18, 24]. Furthermore, students, parents, health workers and teachers received the PA education from the program. To improve the home environment, the parents in the intervention groups were also involved, including but not limited to sending them physical activity education bulletins. In CNP schools, all above interventions including both NE and PA were implemented. In order to ensure the normal operation of the intervention, the supervisors from project office went to each center to carry out project supervision during the program period. The process evaluation indicated that the school carried out as proposal. The physical activity level was measured with energy monitor among 868 students (304 in CNP group and 301 in control group in 5 cities, 111 in PA group and 112 in NE group in Beijing). The energy expenditure increased higher in CNP group (77.0 kcal/day) than in control group (63.5 kcal/day, p = 0.967) in five cities study, higher in PA group (96.4 kcal/day) than in NE group (76.7 kcal/day, p = 0.408) in Beijing study.

Table 1. The interventions for different intervention groups.

Intervention groups Interventions Sites
Nutrition education (NE) 1. The nutrition handbook was distributed to students. Beijing
2. Courses on nutrition and health were given 6 times to students, 2 times to parents and 4 times to teachers and health workers. The content included proportion of three meals, how to choose healthy food, reducing eating out, unhealthy fast food sugar sweetened beverage and snacks.
3. Displaying poster of “Dietary Pagoda for Chinese people”.
4. Two class meetings for nutrition and health.
Physical activity (PA) 1. Course on physical activity given to parents Beijing
2. Twenty-minute “Happy 10” physical activity for students on each school day
3. Two class meetings for physical activity and health.
Comprehensive intervention including nutrition education and physical activity (CNP) All the above interventions including both NE and PA were implemented. The other 5 cities (Jinan, Chongqing, Harbin, Guangzhou and Shanghai)

Anthropometric measurements

The physical examination was carried out in school. Height was measured to an accuracy of 1 mm with a free-standing stadiometer mounted on a rigid tripod (GMCS-I, Xindong Huateng Sports Equipment Co. Ltd., Beijing, China). One overnight fasting body weight was measured to the nearest 0.1 kg on a digital scale (RGT-140, Wujin Hengqi Co. Ltd., Changzhou, China). Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared (kg/m2). Overweight, obesity and thinness were defined per the China national standard for screening for overweight and obesity among school-age children and adolescents with BMI at baseline [25].

Sociodemographic information

Sociodemographic information was collected with a parent questionnaire. Parental education level was defined by maternal education level when available, which was supplemented by paternal education level as a surrogate when maternal education level was not available. The family’s income level was classified as household income per capita monthly in 2009.

Dietary diversity and food variety measurements

Information on dietary intake was collected with a 24-h dietary recall method for three consecutive days (two weekdays and one weekend day); the records were administered by the subjects themselves or with their parents’ help. The children were taught how to fill out the dietary records by the trained research assistants. DDS and FVS per day were used as primary outcome indicators for assessing dietary diversity and food variety. Literature reveals that the quality of breakfast is more important [26, 27] than the others, so the DDS and FVS per meal (breakfast, lunch and supper) were calculated separately as the second outcome indicators.

DDS9 was calculated based on 9 food groups’ consumption. The food groups were categorized according to the FAO protocol in 2013 as Starchy staples; Dark-green leafy vegetables; Other vitamin A-rich fruits and vegetables; Other fruits and vegetables; Organ meat; Meat and fish; Eggs; Legumes, nuts and seeds; and Milk and milk products [28]. One score was assigned if at least 1 food from a given food group was consumed and 0 if not. First, the score for each day was calculated according to the assignment method, and then the average of three-day DDS was taken as the subject’s final score. FVS was calculated by counting all the food items recorded in dietary records with the same method as DDS. The different food items were defined according to China Food Composition Tables 2004.

DDS28, as another food grouping method based on 28 food groups, was referred to confirm the robustness of the evaluation of dietary diversity. The 28 food groups were categorized as follows: Wheat; Fried wheat; Rice; Refined grains; Other cereals; Starch tubers; Beans; Soybean products; Nuts; Deep-color vegetables (carotene content ≥ 500 μg/100 g); Light-color vegetables (carotene content < 500 μg/100 g); Pickled vegetables; Edible fungi and algae; Fruits; Pork; Poultry; Beef/lamb/other red meat; Seafood; Organ meat; Processed meat; Eggs; Milk powder and cheese; Milk and yogurt; Catsup; Beverages; Sugar; Fast food; and Cakes [29].

Proportions of different foods’ consumption

To observe the effects of different interventions on main food consumption, we analyzed the changes in the proportion of subjects consuming some specific foods over 3 days. The foods were categorized according to the China Food Composition Tables 2004 as Cereals (>3 times /3 days); Meat (>3 times /3 days); Vegetables (>3 times /3 days); Fruits (≥1 time /3 days); Dairy (≥1 time /3 days); Eggs (≥1 time /3 days); Fish and shellfish (≥1 time /3 days); Fungi and algae (≥1 time /3 days); Dried legumes (≥1 time /3 days); Nuts and seeds (≥1 time /3 days); Snack (≥1 time /3 days); Fast foods (≥1 time /3 days); Beverages (≥1 time /3 days); Sugars and preserves (≥1 time /3 days).

Statistical analysis

The continuous variables are expressed as mean and standard deviation. The intra-cluster correlation coefficient was 0.18, 0.13 and 0.13 for DDS9, DDS28 and FVS in CNP study respectively. The liner regression model was used for the estimation of the intervention effect on DDS, FVS and the proportion of children consuming different food groups. A linear mixed model adjusting for confounding factors (weight status, sex, age, parental education level and family income level) was used to compare the changes in continuous variables between the intervention groups and control group. The proportions were compared with the generalized linear mixed model (GLMM). The school was used as a random-effect variable. The fixed-effect variables included sex, age, parental education level, family income level and intervention type. The statistical significance level was set at P < 0.05 for overall and P < 0.05/n for subgroup (n represented the number of subgroups). The SAS software package version 9.2 (SAS Institute Inc., Cary, NC) was used for analysis.

The treatment effects were estimated using Eq (1) for DDS and FVS and Eq (2) for proportions of children consuming certain foods.

Yij=γ00+β0Cluster+β01Treat+β1X1ij+βƤXƤij+εij (1)
Logit(Pij)=γ00+β0Cluster+β01Treat+β1X1ij+βƤXƤij+εij (2)

In Eq (1), Yij is the outcome of change from baseline to end for child i at level j; γ00 is the intercept parameter; Cluster is random effect indicator; β01 reveals the intervention effect; Treat is an indicator that equals 1 if the student is in the treatment arm and 0 otherwise; X1ij is the outcome at baseline and XƤij is a vector of control variables at baseline. The same linear Eq (2) was applied to binary outcomes with a logit link as part of generalized linear models.

Results

Baseline characteristics

The sample size of children was 4846 in total (777 in Beijing and 4069 in the other five cities) in this analysis. Tables 2 and 3 present the characteristics of the subjects in comprehensive intervention study and single intervention study respectively, including age, sex, parental educational level and family economic level. Except for the significant economic and educational level differences between the CNP and its control group and the significant sex proportion difference among the NE group, PA group and their control groups, no other significant difference was found between the intervention and control groups in basic characteristics.

Table 2. Characteristics of the subjects at baseline in comprehensive intervention study.

Characteristic Control group CNP group
Total, (N) 1916 2153
Age, (years, mean ± SD) 9.0±1.2 9.0±1.2
Sex, (N (%))
 Boys 927 (48.4) 1037 (48.2)
 Girls 989 (51.6) 1116 (51.8)
BMI, (kg/m2, mean ± SD) 17.1±3.1 17.2±3.3
Weight status, (N (%))
 Thinness 261 (14.3) 312 (16.2)
 Normal weight 1159 (63.4) 1161 (60.1)
 Overweight 209 (11.4) 245 (12.7)
 Obesity 200 (10.9) 213 (11.0)
Parental educational level, (N (%))
 Low 18 (1.0) 21 (1.0) **
 Middle 813 (43.9) 787 (37.6)
 High 1023 (55.2) 1287 (61.4)
Family’s economic level (Yuan/month/per family member), N (%)
 ≤1,500 830 (45.0) 846 (40.8) *
 1,501–2,500 483 (26.2) 591 (28.5)
 >2,500 533 (28.9) 638 (30.7)

BMI, body mass index; CNP, comprehensive intervention including nutrition education and physical activity; NE, nutritional education intervention; PA, physical activity intervention.

The category of parental educational level: low: illiterate; middle: elementary or middle school; high: high school or above.

Mixed-effects model was used for comparison,

** p < 0.01,

* p < 0.05.

Table 3. Characteristics of the subjects at baseline in NE or PA intervention study.

Characteristic Control group NE group PA group
Total, (N) 122 352 303
Age, (years, mean ± SD) 9.1±1.4 9.4±1.3 9.0±1.3**
Sex, (N (%))
 Boys 70 (57.4) 148 (42.0) 141 (46.5) *
 Girls 52 (42.6) 204 (58.0) 162 (53.5)
BMI, (kg/m2, mean ± SD) 16.3±2.5 16.9±2.9 16.8±3.1
Weight status, (N (%))
 Thinness 12 (9.8) 31 (8.8) 23 (7.6)
 Normal weight 93 (76.2) 268 (76.1) 224 (73.9)
 Overweight 10 (8.2) 28 (8.0) 27 (8.9)
 Obesity 7 (5.7) 25 (7.1) 29 (9.6)
Parental educational level, (N (%))
 Low 2 (1.7) 10 (2.9) 8 (2.7)
 Middle 84 (71.8) 236 (69.2) 190 (64.6)
 High 31 (26.5) 95 (27.9) 96 (32.7)
Family’s economic level (Yuan/month/per family member), N (%)
 ≤1,500 62 (54.4) 162 (48.2) 157 (53.0)
 1,501–2,500 28 (24.6) 92 (27.4) 83 (28.0)
 >2,500 24 (21.1) 82 (24.4) 56 (18.9)

BMI, body mass index; CNP, comprehensive intervention including nutrition education and physical activity; NE, nutritional education intervention; PA, physical activity intervention.

The category of parental educational level: low: illiterate; middle: elementary or middle school; high: high school or above.

Mixed-effects model was used for comparison,

** p < 0.01,

* p < 0.05.

Dietary diversity and food variety

The intervention effects on DDS and FVS according to dietary intake are shown in Table 4 for CNP study and in Table 5 for NE or PA study. Compared with the control group, the effects of CNP were 0 (95% Confidence Interval (CI): 0, 0.1; p = 0.382) on DDS9, 0.1 (95% CI: -0.1, 0.2; p = 0.374) on DDS28 and 0.1 (95% CI: -0.1, 0.3; p = 0.186) on FVS. No significant difference of intervention effects was found across subgroups. When we evaluated the dietary scores based on the breakfast foods only, positive intervention effects of CNP group were observed significant on DDS9 (0.1; 95% CI: 0, 0.1; p < 0.001), and nonsignificant on DDS28 (0; 95% CI: 0, 0.1; p = 0.168) and FVS (0.1; 95% CI: 0, 0.1; p = 0.067).

Table 4. The outcomes for intervention on DDS and FVS in CNP intervention study (mean ± SD).

Group Variable Control group CNP group
Baseline Change Baseline Change Effect (95% CI) P-value
For one day
Total DDS9 4.3±1.2 -0.2±1.4 4.4±1.0 -0.2±1.3 0 (0, 0.1) 0.382
DDS28 6.7±2.2 -0.5±2.6 6.7±1.9 -0.5±2.3 0.1(-0.1, 0.2) 0.374
FVS 8.7±3.7 -0.9±4.3 8.5±2.9 -0.7±3.3 0.1 (-0.1, 0.3) 0.186
Boys DDS9 4.2±1.2 -0.2±1.4 4.3±1.0 -0.3±1.3 0 (-0.1, 0.1) 0.807
DDS28 6.4±2.1 -0.6±2.5 6.5±1.9 -0.6±2.3 0.1 (-0.1, 0.2) 0.453
FVS 8.2±3.5 -1.0±4.1 8.2±2.9 -0.9±3.3 0.1 (-0.1, 0.4) 0.324
Girls DDS9 4.4±1.2 -0.2±1.5 4.4±1.0 -0.1±1.2 0 (0, 0.1) 0.334
DDS28 6.9±2.2 -0.5±2.7 6.8±1.9 -0.4±2.2 0 (-0.1, 0.2) 0.643
FVS 9.1±3.8 -0.9±4.5 8.8±2.9 -0.6±3.3 0.1 (-0.1, 0.3) 0.411
Normal weight & thinness DDS9 4.3±1.2 -0.2±1.4 4.4±1.0 -0.2±1.3 0.1 (-0.1, 0.2) 0.488
DDS28 6.7±2.2 -0.6±2.6 6.7±1.9 -0.5±2.3 0.2 (-0.1, 0.4) 0.162
FVS 8.8±3.7 -1.0±4.3 8.6±2.9 -0.7±3.3 0.3 (0, 0.7) 0.086
Overweight & obesity DDS9 4.1±1.1 -0.2±1.4 4.3±1.1 -0.2±1.3 0 (0, 0.1) 0.525
DDS28 6.4±2.1 -0.4±2.7 6.7±1.9 -0.4±2.2 0 (-0.1, 0.1) 0.836
FVS 8.1±3.5 -0.7±4.3 8.4±3.0 -0.6±3.3 0.1(-0.1, 0.2) 0.608
For single meal
Breakfast DDS9 1.8±0.7 -0.1±0.9 1.9±0.7 0±0.8 0.1 (0, 0.1) <0.001
DDS28 2.2±0.8 -0.1±1.1 2.2±0.8 -0.1±0.9 0 (0, 0.1) 0.168
FVS 2.3±0.9 -0.2±1.2 2.3±0.8 -0.1±1.0 0.1 (0, 0.1) 0.067
Lunch DDS9 2.1±0.7 -0.1±0.9 2.1±0.7 0±0.9 -0.1 (-0.1,0) 0.045
DDS28 2.4±1 -0.2±1.2 2.4±0.9 -0.1±1.1 -0.1 (-0.2, 0) 0.022
FVS 2.6±1.1 -0.3±1.4 2.5±1 -0.1±1.2 -0.1 (-0.2, 0) 0.007
Supper DDS9 2.8±0.9 -0.1±1.1 2.8±0.7 -0.1±0.9 0 (0, 0.1) 0.162
DDS28 3.5±1.3 -0.2±1.7 3.5±1.1 -0.3±1.4 0 (0, 0.1) 0.378
FVS 3.9±1.8 -0.3±2.2 3.8±1.4 -0.3±1.6 0.1 (0, 0.2) 0.118

CI, Confidence Interval; CNP, comprehensive intervention including nutrition education and physical activity; DDS, Dietary Diversity Score; DDS9: Dietary Diversity Score for 9 food groups; DDS28: Dietary Diversity Score for 28 food groups; FVS, Food Variety Score.

A linear mixed model was used for comparison, the effect was adjusted for weight status, sex, age, parental education level and family income level.

Table 5. The outcomes of the intervention on DDS and FVS in NE or PA intervention study (mean ± SD).

Group Variable Control group NE group PA group
Baseline Change Baseline Change Effect (95% CI) P-value Baseline Change Effect (95% CI) P-value
For one day
Total DDS9 4.0±1.2 0.1±1.5 4.3±1.1 0.1±1.1 0.1 (-0.1, 0.3) 0.294 4.1±1.0 -0.2±1.2 -0.1 (-0.2, 0) 0.037
DDS28 5.8±2.1 0.6±2.8 6.9±1.9 0.1±1.9 0.1 (-0.3, 0.4) 0.747 6.2±1.7 0±1.9 -0.3 (-0.4, -0.1) 0.005
FVS 6.9±3.1 0.7±4.1 8.6±3.1 0.2±2.8 0.4 (-0.2, 0.9) 0.201 7.6±2.3 -0.2±2.6 -0.3 (-0.6, 0) 0.021
Boys DDS9 3.9±1.2 0.1±1.5 4.3±1.0 -0.1±1.2 0.1 (-0.2, 0.4) 0.381 4.0±1.0 -0.2±1.2 -0.1 (-0.3, 0) 0.147
DDS28 5.7±2.2 0.4±2.8 6.9±1.9 -0.2±2.0 0.1(-0.4, 0.6) 0.64 5.9±1.7 -0.2±1.8 -0.2 (-0.5, 0) 0.103
FVS 6.8±3.1 0.5±3.8 8.6±3.2 -0.3±3.1 0.5 (-0.2, 1.3) 0.162 7.2±2.3 -0.5±2.5 -0.2 (-0.6, 0.1) 0.187
Girls DDS9 4.2±1.1 0.2±1.4 4.3±1.1 0.1±1.1 0.1 (-0.2, 0.4) 0.431 4.3±1.0 -0.1±1.2 -0.1 (-0.2, 0.1) 0.218
DDS28 6.0±2.0 0.8±2.8 6.9±1.9 0.3±1.8 0 (-0.5, 0.6) 0.892 6.4±1.7 0.1±1.9 -0.3 (-0.5, 0) 0.042
FVS 7.1±3.1 1.0±4.4 8.6±3.0 0.5±2.5 0.3 (-0.6, 1.1) 0.527 7.9±2.3 0±2.7 -0.4 (-0.8, 0) 0.081
Normal weight & thinness DDS9 4±1.2 0.2±1.5 4.3±1.0 0.1±1.1 0.4 (-0.2, 1.0) 0.162 4.1±1.0 -0.1±1.2 0.1 (-0.1, 0.4) 0.286
DDS28 5.9±2.2 0.7±2.9 6.9±1.9 0.1±1.9 1.0 (0, 2.0) 0.057 6.1±1.7 -0.1±1.8 0.4 (-0.1, 0.9) 0.093
FVS 7.0±3.3 0.8±4.3 8.6±3.1 0.2±2.8 1.6 (0.1, 3.2) 0.041 7.5±2.4 -0.3±2.5 0.5 (-0.2, 1.2) 0.135
Overweight & obesity DDS9 4.2±0.9 -0.3±1.3 4.4±1.1 -0.2±1.3 0.1 (-0.1, 0.3) 0.519 4.4±1.1 -0.2±1.4 -0.2 (-0.3,0) 0.006
DDS28 5.6±1.2 0±1.9 6.8±2.0 -0.2±2.0 -0.1 (-0.5, 0.3) 0.719 6.3±1.7 0.1±2.3 -0.4 (-0.6, -0.2) 0
FVS 6.5±1.6 -0.2±2.5 8.7±2.9 -0.2±2.9 0.2 (-0.4, 0.8) 0.569 7.8±2.3 -0.2±3.0 -0.5 (-0.8, -0.2) < 0.001
For single meal
Breakfast DDS9 1.7±0.7 0.2±1.0 2.1±0.7 0.1±0.9 0.1 (-0.1, 0.3) 0.44 1.9±0.7 0.1±1.0 0 (-0.1, 0.1) 0.754
DDS28 2.1±0.9 0.3±1.2 2.7±0.8 0.1±1.0 0.2 (0, 0.4) 0.126 2.2±0.7 0.1±1.1 0 (-0.1, 0.1) 0.903
FVS 2.1±0.9 0.3±1.3 2.8±1.0 0.1±1.0 0.2 (-0.1, 0.4) 0.155 2.3±0.8 0.1±1.1 0 (-0.1, 0.1) 0.973
Lunch DDS9 2.1±0.8 0.2±1.1 2.4±0.7 0±0.9 0.3 (0.2, 0.5) 0 2.2±0.8 0.1±1.1 0 (-0.1, 0.1) 0.94
DDS28 2.3±1 0.3±1.5 2.9±0.9 0±1 0.3 (0, 0.5) 0.03 2.5±0.9 0.2±1.3 -0.1 (-0.2, 0) 0.082
FVS 2.4±1.1 0.4±1.6 3.1±1.1 -0.1±1.1 0.5 (0.2, 0.8) 0.001 2.5±0.9 0.2±1.3 -0.1 (-0.2, 0.1) 0.197
Supper DDS9 2.5±0.9 0.1±1.3 2.7±1 0.2±1 0.2 (0, 0.4) 0.029 2.5±0.8 0±1 -0.1 (-0.2, 0) 0.046
DDS28 3±1.2 0.2±1.6 3.3±1.2 0.2±1.3 0.3 (0, 0.5) 0.018 3.1±1 -0.1±1.2 -0.1 (-0.3, 0) 0.023
FVS 3.2±1.5 0.2±2.1 3.7±1.6 0.3±1.7 0.3 (0,0.6) 0.054 3.4±1.2 -0.1±1.5 -0.2 (-0.3, 0) 0.017

CI, Confidence Interval; DDS, Dietary Diversity Score; DDS9: Dietary Diversity Score for 9 food groups; DDS28: Dietary Diversity Score for 28 food groups; FVS, Food Variety Score; NE, nutrition education intervention; PA, physical activity intervention.

A linear mixed model was used for comparison, the effect was adjusted for weight status, sex, age, parental education level and family income level.

The effects on DDS9, DDS28 and FVS were 0.1 (95% CI: -0.1,0.3; p = 0.294), 0.1 (95% CI: -0.3, 0.4; p = 0.747) and 0.4 (95% CI: -0.2,0.9; p = 0.201) in the NE group and -0.1 (95% CI: -0.2, 0; p = 0.037), -0.3 (95% CI: -0.4,-0.1; p = 0.005) and -0.3 (95% CI: -0.6, 0; p = 0.021) in the PA group, respectively. No significant effects on DDS or FVS were found at breakfast in NE group or PA group.

Food group consumption changes

The effects of the three interventions on food group consumption changes are shown in Tables 6 and 7. Compared with the control group, the proportions of children consuming cereals (> 3 times/3 days) and fruits (≥ 1 time/3 days) increased significantly, and Eggs (≥1 time /3 days), fish (≥1 time /3 days) and dried legumes (≥1 time /3 days) decreased significantly in the CNP group, with changes of 5.4 (-5.4 vs. -10.8 for treat vs. control; Odds Ratio (OR): 1.4 (95% CI: 1.1,1.7); p = 0.009) and 6.9 (5.0 vs. -1.9; OR: 1.4 (95% CI: 1.1,1.7); p = 0.003) percent, -4.3 (-0.1 vs. 4.2 for treat vs. control; OR: 0.8 (95% CI: 0.7,1.0); p = 0.031), -5.9 (-8.4 vs. -2.5; OR: 0.7 (95% CI: 0.6,0.9); p = 0.005) and -10.8 (-8.3 vs. 2.5; OR: 0.6 (95% CI: 0.5,0.7); p < 0.001) percent, respectively. The proportion changes among the NE group in the consumption of vegetables (> 3 time /3 days), fruits (≥ 1 time/3 days), Fungi and algae (≥1 time /3 days), dried legumes (≥ 1 time/3 days), snack (≥ 1 time/3 days) and fast foods (≥1 time / 3 days) were 20.2 (13.7 vs. -6.5 for treat vs. control; OR: 2.2 (95% CI: 1.2,4.5); p = 0.014), -26.7 (-20.2 vs. 6.5; OR: 0.3 (95% CI: 0.2,0.6); p = 0.001), 22.3 (25.6 vs. 3.3; OR: 2.5 (95% CI: 1.1,5.0); p = 0.024), -16.9 (2.0 vs. 18.9; OR: 0.5 (95% CI: 0.2,0.8); p = 0.011), -22.5 (-30.7 vs. -8.2; OR: 0.3 (95% CI: 0.1,0.7); p = 0.006) and -22.1 (-13.1 vs. 9.0; OR: 0.4 (95% CI: 0.2,0.7); p = 0.002) percent, respectively. The PA group showed no significant increases but significant decreases (or relative decreases) in the proportions of children consuming fruits (≥ 1 time/3 days), dried legumes (≥ 1 time/3 days) and fast foods (≥ 1 time/3 days), which were -16.8 (-10.3 vs. 6.5 for treat vs. control; OR: 0.5 (95% CI: 0.3,0.9); p = 0.023), -13.6 (5.3 vs. 18.9; OR: 0.6 (95% CI: 0.3,1.0); p = 0.048) and -16.3 (-7.3 vs. 9.0; OR: 0.5 (95% CI: 0.3,0.9); p = 0.027) percent compared with the control group, respectively.

Table 6. The proportion of children consuming different food groups in CNP study.

Food Control group CNP group
Baseline (n (%)) Change (n (%)) Baseline (n (%)) Change (n (%)) Intervention effect (OR, 95% CI) P-value
Cereals (>3 times /3 days) 1530 (79.9) -206 (-10.8) 1690 (78.5) -117 (-5.4) 1.4 (1.1, 1.7) 0.009
Meat (>3 times /3 days) 1130 (59.0) -14 (-0.8) 1345 (62.5) 65 (3.0) 1.2 (1.0, 1.5) 0.091
Vegetables (>3 times /3 days) 1259 (65.7) -8 (-0.4) 1473 (68.4) -35 (-1.6) 0.9 (0.7, 1.1) 0.521
Fruits (≥1 time /3 days) 881 (46.0) -37 (-1.9) 969 (45.0) 108 (5.0) 1.4 (1.1, 1.7) 0.003
Dairy (≥1 time /3 days) 1318 (68.8) -86 (-4.5) 1536 (71.4) -85 (-4.0) 1.0 (0.8, 1.2) 0.832
Eggs (≥1 time /3 days) 1424 (74.3) 81 (4.2) 1688 (78.4) -3 (-0.1) 0.8 (0.7, 1.0) 0.031
Fish and shellfish (≥1 time /3 days) 1039 (54.2) -48 (-2.5) 1231 (57.1) -181 (-8.4) 0.7 (0.6, 0.9) 0.005
Fungi and algae (≥1 time /3 days) 676 (35.3) -10 (-0.5) 758 (35.2) -14 (-0.6) 1.0 (1.2, 1.2) 0.702
Dried legumes (≥1 time /3 days) 1032 (53.9) 48 (2.5) 1270 (59.0) -179 (-8.3) 0.6 (0.5, 0.7) 0.001
Nuts and seeds (≥1 time /3 days) 312 (16.3) -64 (-3.4) 265 (12.3) -59 (-2.7) 0.9 (0.7, 1.2) 0.665
Snack (≥1 time /3 days) 352 (18.4) -39 (-2.1) 432 (20.1) -90 (-4.2) 0.8 (0.7, 1.1) 0.162
Fast foods (≥1 time /3 days) 1349 (70.5) -109 (-5.8) 1510 (70.1) -120 (-5.6) 1.0 (0.9, 1.2) 0.841
Beverages (≥1 time /3 days) 665 (34.7) -202 (-10.5) 672 (31.2) -195 (-9.1) 1.1(0.9, 1.4) 0.561
Sugars and preserves (≥1 time /3 days) 450 (23.5) -66 (-3.5) 445 (20.7) -64 (-3.0) 1.0 (0.8,1.2) 0.839

CI, Confidence Interval; CNP, comprehensive intervention including nutrition education and physical activity; OR, Odds Ratio.

A generalized linear mixed model was used for comparison, the effect was adjusted for sex, age, parental education level and family income level.

Table 7. The proportion of children consuming different food groups in NE or PA study (%).

Food Control group NE group PA group
Baseline (n (%)) Change (n (%)) Baseline (n (%)) Change (n (%)) Intervention effect (OR, 95% CI) P Baseline (n (%)) Change (n (%)) Intervention effect (OR, 95% CI) P-value
Cereals (>3 times /3 days) 88 (72.1) 7 (5.8) 301 (85.5) 20 (5.7) 0.8 (0.3, 1.2) 0.634 258 (85.1) 6 (2.0) 0.8 (0.3, 1.2) 0.650
Meat (>3 times /3 days) 42 (34.4) -5 (-4.1) 136 (38.6) 31 (8.8) 1.5 (0.8,3) 0.199 86 (28.4) 4 (1.3) 1.2 (0.6, 2.5) 0.557
Vegetables (>3 times /3 days) 63 (51.6) -8 (-6.5) 238 (67.6) 48 (13.7) 2.2 (1.2, 4.5) 0.014 224 (73.9) -50 (-16.5) 0.6 (0.3, 1.0) 0.061
Fruits (≥1 time /3 days) 44 (36.1) 8 (6.5) 208 (59.1) -71 (-20.2) 0.3 (0.2, 0.6) 0.001 149 (49.2) -31 (-10.3) 0.5 (0.3, 0.9) 0.023
Dairy (≥1 time /3 days) 96 (78.7) -17 (-13.9) 262 (74.4) -20 (-5.6) 1.4 (0.7, 2.5) 0.459 210 (69.3) -35 (-11.5) 1.0 (0.6,2.2) 0.837
Eggs (≥1 time /3 days) 93 (76.2) 1 (0.8) 328 (93.2) -9 (-2.6) 0.5 (4.5, 1.2) 0.123 245 (80.9) 9 (2.9) 0.9 (2.2, 2.0) 0.865
Fish and shellfish (≥1 time /3 days) 22 (18.0) 3 (2.5) 88 (25.3) -5 (-1.7) 0.8 (0.4, 1.7) 0.527 64 (21.1) -10 (-3.3) 0.7 (0.3, 1.4) 0.260
Fungi and algae (≥1 time /3 days) 22 (18.0) 4 (3.3) 120 (34.1) 90 (25.6) 2.5 (1.1, 5.0) 0.024 81 (26.7) -2 (-0.6) 0.7 (0.3, 1.4) 0.275
Dried legumes (≥1 time /3 days) 47 (38.5) 23 (18.9) 213 (60.5) 7 (2.0) 0.5 (0.2, 0.8) 0.011 157 (51.8) 16 (5.3) 0.6 (0.3, 1.0) 0.048
Nuts and seeds (≥1 time /3 days) 13 (10.7) -4 (-3.3) 60 (17.0) 19 (5.4) 2.2 (1.2, 6.1) 0.103 51 (16.8) -13 (-4.3) 0.9 (0.3, 2.5) 0.875
Snack (≥1 time /3 days) 19 (15.6) -10 (-8.2) 151 (42.9) -108 (-30.7) 0.3 (0.1, 0.7) 0.006 65 (21.5) -41 (-13.6) 0.7 (0.3, 1.8) 0.44
Fast foods (≥1 time /3 days) 71 (58.2) 11 (9.0) 248 (70.5) -46 (-13.1) 0.4 (0.2, 0.7) 0.002 172 (56.8) -22 (-7.3) 0.5 (0.3, 0.9) 0.027
Beverages (≥1 time /3 days) 31 (25.4) -2 (-1.6) 147 (41.8) -25 (-7.1) 0.9 (0.5, 1.8) 0.697 111 (36.6) -22 (-7.2) 0.8 (0.4, 1.7) 0.641
Sugars and preserves (≥1 time /3 days) 16 (13.1) 6 (4.9) 53 (15.1) 1 (0.2) 0.7 (0.3, 1.5) 0.309 40 (13.2) -2 (-0.7) 0.6 (0.2, 1.4) 0.189

CI, Confidence Interval; NE, nutrition education intervention; OR, Odds Ratio; PA, physical activity intervention.

A generalized linear mixed model was used for comparison, the effect was adjusted for sex, age, parental education level and family income level.

Discussion

This study indicated that the CNP for childhood obesity had no significant effect on either the dietary diversity or the food variety per day, but the significant effects at breakfast and on some foods’ consumption (such as cereals and fruits) appeared in 5 cities. For the separate childhood obesity intervention in Beijing, a significant decreasing effect appeared on dietary diversity and food variety in the physical activity group. By analyzing different food consumption, the proportions of children increased more for fruits and decreased less for cereals in the CNP group than the control group after the intervention. The cereals and fruits were the important energy and micronutrient sources, so these findings revealed that these consumption behavior changes may lead to the improvement of diet quality in comprehensive intervention groups. The breakfast is generally taken as the most important meal of the day and is purported to confer a number of benefits for diet quality, health and academic performance. Study reveals that children who habitually consume high quality breakfast are more likely to have better nutrient intake [30]. So, the improvement of dietary diversity and food variety at breakfast could increase the diet quality and benefit the children.

Much evidence indicates that physical activity can considerably influence childhood growth [31, 32], while nutrition education provides children with necessary dietary knowledge. There’s also study finding that encouraging physical activity could decrease the likelihood of choosing healthy food [33]. In PA group, the significant decreasing effects on dietary diversity and food variety appeared and some healthy food consumption proportions decreased, such as of vegetables, fruits, fungi and algae, nuts and seeds, and fish and shellfish. Most people who have not received nutrition training may intuitively choose to decrease their food intake rather than adjusting to healthy dietary patterns for obesity prevention, such as reducing high-energy food and increasing fruits and vegetables. This may lead the children who only undergo PA to reduce the attention to diet. It implied that the side effect of PA on diet should be noticed in the future program.

It has been demonstrated that both nutrition education and lifestyle intervention could improve the dietary diversity among children or adults [15, 34]. An analysis of over 300 studies shows that nutrition education is more likely to be effective when it focuses on behavior/action (rather than knowledge only) and systematically links relevant theory, research and practice [3538]. The estimated probabilities for obesity were 13.5 percentage points higher among children who consumed a healthy diet but were physically inactive and 3.1 percentage points higher among children who consumed an unhealthy diet but were physically active compared with those who consumed a healthy diet and physically active [39]. This result indicates that PA is much more likely to have a decreasing effect on BMI compared with NE alone. Although the effect of NE intervention on weight reduction was not as obvious in the short term, it is important to help children shape their health diet habits for the long run. Previous research has demonstrated that multicomponent programs involving parents aiming at food sources both in and outside of school and focusing on a variety of unhealthy food items seem less likely to fail [40]. The parents and canteen staff also play important roles in children’s eating habits and food choices. The importance of participatory approaches and parental support for school-based health promotion have been demonstrated by many studies. The qualitative research data showed that low parental response could aggravate their children’s unhealthy eating behavior [4144]. Therefore, both of them were covered in our program.

China is experiencing an accelerated process of nutritional transition. During this process, very rapid changes, such as the increase in obesity and obesity-related chronic diseases, have occurred. Studies have identified that these changes are due to a broader dietary offering, changes in eating patterns and a considerable increase in sedentary behaviors/lifestyle [45, 46]. To resolve this problem, some school-based programs for childhood obesity prevention were implemented to develop a strategy of obesity prevention and control. School-based interventions have been clearly shown to be more effective than interventions in other settings [47, 48]. The school-based nutrition education has more extrusive advantages for students than community-based nutrition education, such as offering interacting with educators delivering the intervention and positive school infrastructure and environment. The frequent interactions of policies, curricula and personnel also increases the familiarity with and use of nutrition knowledge among students [4951]. To promote nutrition education, some developed countries have developed strategies for school-based nutrition education. The state-level school nutrition coordinators setting reflects the greater historical emphasis on school nutrition and food service policies than on physical activity in the USA, and more types of implementation support to schools for nutrition and food service than for physical activity could be provided by state agencies [52]. However, in China, nutrition education has not attracted enough attention from schools before [53]. With recent the advancement of the State Council’s Action Plan for Healthy China, nutrition and health education for children has also been included in the action plan [54]. This will help to promote widespread nutrition education in school.

The main limitation of this study is that the measurements were obtained during only one school year, without evaluation of the long-term impact. Tracking the children for another year would have been very difficult in practice, and students in grade 5 graduated from primary schools and attended different middle schools. For such large-scale follow-up in six cities, much more expense would be needed. Another limitation of our study was the intervention in urban areas but not in rural areas. The prevalence of childhood obesity in rural areas has been increasing more quickly, so the nutrition education is equally important in rural areas. In particular, children in rural areas of China have access to many unhealthy snack foods in recent years. Additionally, some students always had lunch in private canteens outside of school, but our intervention could not cover such canteens, which may have influenced the intervention effect on the diet. At last, the subgroup analysis results should be treated cautiously, because the subgroup was not considered in the sample design.

Conclusions

These results indicated that though CNP had no significant effect on overall dietary diversity and food variety per day, the significant effects were shown on some foods’ consumption, and the dietary diversity and food variety increases appeared at breakfast significantly. Children exposed only to the physical activity intervention or nutrition education intervention as an obesity intervention didn’t appear the positive effect on dietary diversity either. We should pursue a comprehensive intervention approach to changing school policies and practices that addresses both nutrition education and physical activity over time.

Supporting information

S1 Data

(XLSX)

S1 Checklist. CONSORT checklist.

(DOCX)

S1 File. Study protocol (main points).

(DOC)

S2 File

(PDF)

Acknowledgments

We would like to acknowledge the support from all the team members and the participating students, teachers, parents and local education and health staff.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This study was funded by China Ministry of Science & Technology [2008BAI58B05], Chinese National Natural Science Foundation Project [71804079] and Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences [CAAS-ASTIP-2019-IFND]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Mahdieh Abbasalizad Farhangi

27 Oct 2019

PONE-D-19-24892

Childhood obesity interventions only focusing on physical activity decreases dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

PLOS ONE

Dear Dr. Xu,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

We would appreciate receiving your revised manuscript by Dec 11 2019 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

Please include the following items when submitting your revised manuscript:

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Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

We look forward to receiving your revised manuscript.

Kind regards,

Mahdieh Abbasalizad Farhangi

Academic Editor

PLOS ONE

Journal Requirements:

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3. We noticed you have some minor occurrence(s) of overlapping text with the following previous publication(s), which needs to be addressed:

https://doi.org/10.1186/s12991-017-0162-2

https://doi.org/10.6133/apjcn.112016.05

https://doi.org/10.1371/journal.pone.0043183

https://doi.org/10.1186/s12937-017-0299-5

https://doi.org/10.1186/s12889-016-3878-z

http://dx.doi.org/10.5888/pcd13.160032

In your revision ensure you cite all your sources (including your own works), and quote or rephrase any duplicated text outside the Methods section. Further consideration is dependent on these concerns being addressed.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

Reviewer #3: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: No

Reviewer #3: Yes

**********

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Childhood obesity interventions only focusing on physical activity decreases dietary

diversity among younger children: Evidence from a school-based randomized

controlled trial in China

The title of study highlighted that focusing on physical activity decrease dietary diversity among children, while the evidences provided in the introduction, method, result and discussion weren’t enough to convince the readers. I am interested to know how Pa interventions decrease DDS but unfortunately couldn’t find strong procedure to prove it.

Method

The intervention elements are unclear for all comprehensive, nutrition education, and PA. Please, clarify the interventions program in details.

PA interventions exist but I can’t find any information about PA measurements in method and results.

Reviewer #2: This paper reported a secondary analysis of the multicentre cluster-randomized controlled trial conducted in China between 2009 and 2010 that aimed to evaluate the effects of a comprehensive school-based intervention on childhood obesity prevention. The main trial was designed into two separate studies, conducted in Beijing and other 5 cities separately. The Beijing study involved 8 schools with 3 schools randomly allocated to receive nutrition education (NE) only, 3 school to receive physical activity (PA) only, and 2 control schools with no intervention. The other study recruited 6 schools in each of the 5 cities (30 schools in total), with 3 schools randomly allocated to receive a comprehensive intervention including both NE and PA (CNP), and 3 control schools with no intervention. The programme was implemented for 2 semesters over one year, and data were collected at baseline and at the end of the study. Among the 38 primary schools included in the trial, two classes were selected from each grade (1-5) per school, but only grades 2-4 were designed to collect the dietary records using 24-h dietary recall for 3 consecutive days. The current study aimed to explore the effects of NE and PA on dietary diversity compared to the control groups, measured using dietary diversity scores (DDS9 and DDS28) and food variety score (FVS). The proportions of different foods consumed were also calculated.

The manuscript was well written, and the study design was clearly documented. My major comments are on the statistical analysis and results reported in this paper, which should follow the CONSORT 2010 guidelines with extension to cluster randomised trials.

As a cluster randomised trial conducted separately in different cities in China, it is important to provide more information on the schools recruited to this study and how they were allocated to each group. Was this decided pragmatically or allocated using random numbers? What factors were considered in the selection of schools and were they stratified in randomisation?

As shown in Table 1, the CNP group (15 schools in 5 cities) received all the NE and PA interventions that was implemented separately in 3 schools in Beijing. With a much larger sample size and comprehensive interventions, the results didn’t show significant effects on the outcomes. In comparison, both NE and PA groups in Beijing schools showed some effects at the end of the trial, especially in the PA group compared to the 2 control schools. Were any process evaluations conducted during the trial that could assess the delivery of different intervention components and the level of protocol compliance?

Although the present analysis on dietary diversity was not the primary outcome of the trial, it would still be useful to prioritize the outcomes considered in this study and define the minimal effect sizes so that both clinical and statistical significances could be established and used in interpretation.

To clarify, were the outcomes defined at the end of study or as the change from baseline? Were the subgroup analyses by gender and weight status pre-defined or determined post-hoc? What was the rationale to evaluate the outcomes for breakfast separately? They should be described in the statistical analysis section.

For randomised controlled trials, it is not recommended to include baseline outcome measured prior to randomisation as part of the outcome variable assessed post randomisation. As suggested in the EMA guideline on adjustment for baseline covariates in clinical trials, the baseline value of a continuous outcome measure should usually be included as a covariate. This applies whether the outcome variable is defined as the ‘raw outcome’ or as the ‘change from baseline’. In current statistical analysis models, however, a time variable was added with 0 = baseline and 1 = the end of study on the outcome measure with an interaction term between time and treatment group. What terms were used to estimate the intervention effects reported in the table? A more accurate regression model is to fit the outcome measured at the end of the study, with the baseline value and other pre-defined confounders added to the model as covariates for adjustment. The intervention effect is then estimated using the model coefficient for treatment group.

As school was the randomisation unit rather than school class, what was the rationale to fit class as the random effect only?

Please follow the CONSORT 2010 statement with extension to cluster randomised trials in reporting figures and tables. The flow diagram should indicate the follow up schedule, and report both numbers of schools and students in each group. Baseline table should not report p-values, and include both school- and individual-level data collected. The result tables are hard to read with too much information in one table. I would suggest reporting the CNP study and NE/PA study in separate tables, with the randomised groups reported in columns and the outcome measures in rows. Intra-cluster correlation coefficient needs to be reported on each outcome, which is strongly recommended in cluster randomised trials. For the trial conducted in Beijing that included three randomised arms (NE, PA, control), the results for each outcome should be reported together as a multi-arm study rather than two separate analyses for NE vs control and PA vs control.

With numerous statistical tests conducted overall and by subgroup, the results must be interpreted with caution as the Type 1 error rate would be inflated without adjustment for multiple comparisons.

Based on the results from 3 intervention schools and 2 control schools in Beijing, the title and conclusions focusing only on the significant effects of PA on dietary diversity seem too strong. For example on page 17, line 270, it was reported that the effects on DDS9, DDS28 and FVS were -0.12 (95% CI: -0.38, 0.14; p = 0.365), -0.61 (95% CI: -1.04, -0.17; p = 0.007) and -0.71 (95% CI: -1.35, -0.08; p = 0.028) in the NE group and -0.34 (95% CI: -0.61, -0.08; p = 0.011), -0.73 (95% CI: -1.18, -0.28; p = 0.001) and -1.1 (95% CI: -1.74, -0.45; p = 0.001) in the PA group, respectively. On page 26, line 400, the authors concluded that this result indicated that CNP and NE had no significant effect on the dietary diversity but the dietary diversity decreased in children exposed only to the physical activity intervention. Was this based on DDS9 which was one of the study outcomes? As mentioned earlier, it would be useful to prioritize the outcomes and define the minimal effect sizes so that both clinical and statistical significances could be established and used in interpretation.

Reviewer #3: Childhood obesity and overweight are public health problems and represent an important issue in china population. In this regard different interventions (dietary and PA interventions) are designed for children in schools. The study aimed to understand the association of the type of intervention and dietary diversity score among young children. This is an important topic that could be used for planning a proper prevention program in this age group.

The article is well written however, it presents some critical points:

1. In the introduction: please add some studies that assess the effect of education or PA on diet quality or diversity.

2. from the introduction section, it is not inferred that why the authors assume that the type of obesity programs could affect on DDS differently.

3. in the method section, please add the method of randomization.

4. from the method, it is not obvious that how these 38 schools were selected.

5. it is better to add flow chart for schools selections and in this indicate how many school were invited to take part in these programs and how many accepted it.

6. IN TABLES: Please the statistical analysis used for comparisons or associations as a table footnote.

7. Table 3, 4: it seems that the data presented in table 3 and 4 could be merged, so the comparisons become more understandable.

8. Table 5, 6: it seems that the data presented in table 5 and 6 could be merged, so the comparisons become more understandable

9. Why the authors analysed the data secretively for breakfast?

10. the second paragraph of discussion is not related to this part. it may be more suitable for introduction section.

11. in the discussion section it is recommended to discuss the finding of the present study. In this part, the author mostly discussed about obesity, not diet quality and diversity.

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

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Decision Letter 1

Seth Adu-Afarwuah

23 Apr 2020

PONE-D-19-24892R1

The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

PLOS ONE

Dear Dr. Xu,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. In your revised version, please format the tables properly, so that they can be read more easily by reviewers.

We would appreciate receiving your revised manuscript by Jun 07 2020 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

We look forward to receiving your revised manuscript.

Kind regards,

Seth Adu-Afarwuah

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

Reviewer #3: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: Thank you for the revised paper and responses to all the comments. With further clarification on the original trial design, my concerns remain on the overall conduct of the two studies and the analysis results reported using the specified models.

As shown in Table 1, the two separate cluster randomised trials conducted in Beijing and other 5 cities used same intervention components on PA and NE (separately or combined). The authors stated that all the schools implemented the programme as proposed. If this was the case, it would be hard to evaluate the intervention effects with observed differences on the demographic characteristics and estimated effect sizes between two studies. There are also large geographic differences between these cities in China, and how similar the selected schools were between groups is unknown. If the CNP study was the fundamental part of the trial, the authors should perhaps focus on this main study only and report the change on both BMI (primary outcome) and dietary diversity in the paper.

For a cluster randomised trial, the unit of randomisation is at the cluster level while the data collection may include both cluster and individual participants’ data. The regression models should consider the within- and between-cluster variations, and fit both fixed and random effects using the mixed models. Fitting baseline outcome value as a covariate in the fixed effect model is applicable to both continuous and categorical outcomes, not just the change from baseline scores. The revised equation (1) was fitted using a standard linear regression model without a random effect. The equation (2) fitted the baseline value as part of the outcome measures in the GLMM model. When an interaction term was added in the logistic model, the beta coefficient for the interaction term should not be interpreted independently from the main terms on treatment and time. The model-adjusted group difference needs to be estimated at the end of the study using the odds ratio (i.e. exponential of the raw model estimate).

Reviewer #3: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2020 Jul 17;15(7):e0235951. doi: 10.1371/journal.pone.0235951.r004

Author response to Decision Letter 1


7 May 2020

Dear Dr. Seth Adu-Afarwuah, Editors and Reviewers:

We very much appreciate your thoughtful comments on our manuscript (PONE-D-19-24892R1, “The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China”). We have carefully considered each comment and responded point-by-point below. We have made corresponding changes in the manuscript with tracked changes highlighting both additions and deletions.

In addition, we have carefully checked the format requirement and revised the manuscript according to the requirement of PLOS ONE.

We believe that your comments and our responses to them have improved our manuscript considerably, and we hope you find our revised manuscript suitable for publication.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 2

Seth Adu-Afarwuah

1 Jun 2020

PONE-D-19-24892R2

The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

PLOS ONE

Dear Dr. Xu,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Jul 16 2020 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Seth Adu-Afarwuah

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: I would like to suggest the following minor changes to the manuscript.

In statistical analysis section, the authors stated that Pij in equation (2) is the change of probability of an event from baseline to end for child i at level j. I disagree with this statement as the logit link is suitable to a binary outcome (Yes or No), which cannot be calculated as change from baseline for each participant. Using same notations as equation (1), the authors should say that the same linear equation was applied to binary outcomes with a logit link as part of generalised linear models. With no time effect in the model, the sentence "The effect of the intervention was evaluated by testing the interaction term between time and treatment" should be removed.

In the results, the authors have used the difference in change of proportions between two groups to quantify the intervention effect on food group consumption, rather than the estimated odds ratio and 95% CI. Although I understand that the difference in proportions is more intuitive to interpret, the adjusted model estimate is more robust which has taken into account baseline covariates and random cluster effect.

Please follow the CONSORT 2010 Explanation and Elaboration in reporting tables and figures, with the extension to cluster randomised trials.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2020 Jul 17;15(7):e0235951. doi: 10.1371/journal.pone.0235951.r006

Author response to Decision Letter 2


6 Jun 2020

Dear Dr. Seth Adu-Afarwuah, Editors and Reviewers:

We very much appreciate your thoughtful comments on our manuscript (PONE-D-19-24892R2, “The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China”). We have carefully considered each comment and responded point-by-point below. We have made corresponding changes in the manuscript with tracked changes highlighting both additions and deletions.

In addition, we have carefully checked the format requirement and revised the manuscript according to the requirement of PLOS ONE.

We believe that your comments and our responses to them have improved our manuscript considerably, and we hope you find our revised manuscript suitable for publication.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 3

Seth Adu-Afarwuah

26 Jun 2020

The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

PONE-D-19-24892R3

Dear Dr. Xu,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Seth Adu-Afarwuah

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: (No Response)

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: (No Response)

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: (No Response)

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

Acceptance letter

Seth Adu-Afarwuah

7 Jul 2020

PONE-D-19-24892R3

The effect of comprehensive intervention for childhood obesity on dietary diversity among younger children: Evidence from a school-based randomized controlled trial in China

Dear Dr. Xu:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Seth Adu-Afarwuah

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Data

    (XLSX)

    S1 Checklist. CONSORT checklist.

    (DOCX)

    S1 File. Study protocol (main points).

    (DOC)

    S2 File

    (PDF)

    Attachment

    Submitted filename: Response to Reviewers.docx

    Attachment

    Submitted filename: Response to Reviewers.docx

    Attachment

    Submitted filename: Response to Reviewers.docx

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.


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