Frequency of TV viewing and prevalence of overweight and obesity among adult women in Bangladesh: a cross-sectional study
2017

Bishwajit Ghose
Institute of Nutrition and Food Science
University of Dhaka
DhakaBangladesh

DrBishwajit Ghose
Institute of Nutrition and Food Science
University of Dhaka
DhakaBangladesh

Frequency of TV viewing and prevalence of overweight and obesity among adult women in Bangladesh: a cross-sectional study

BMJ Open
714399201710.1136/bmjopen-2016-014399Received 21 September 2016 Revised 11 January 2017 Accepted 12 January 2017To cite: Ghose B. Frequency of TV viewing and prevalence of overweight and obesity among adult women in Bangladesh: a cross-sectional study. ▸ Prepublication history for this paper is available online. To view these files please visit the journal online Correspondence to
Background: Research in developed countries has demonstrated an association of varying degrees between watching TV and the risk of being overweight and obese. However, there is no evidence of such an association in the context of the South Asian population. Objective: To investigate whether watching TV increases the risk of being overweight and obese among women in Bangladesh. Setting: Rural and urban areas in Bangladesh. Participants: Participants were 16 624 non-pregnant women aged between 15 and 49 years.Methods:The study was based on cross-sectional data from the Bangladesh Demographic and Health Survey (BDHS) conducted in 2014. The main outcome variables were overweight and obesity measured by body mass index. Data were analysed by using descriptive statistics, cross-tabulation and multivariable logistic regression models.Results: The prevalence of overweight and obesity in the sample population were, respectively, 4.5% (4.18% to 4.82%) and 20% (95% CI 19.39% to 20.61%). In the multivariable analysis, no statistically significant association was found between watching TV and being overweight. However, the odds of being obese among rural women were 63% higher (adjusted OR (AOR) 1.625, 95% CI 1.179 to 2.241) among those who watched less than once a week, and 68% (AOR 1.683, 95% CI 1.029 to 2.751) higher among women who watched TV at least once a week compared to those who did not watch TV at all. Urban women who watched TV at least once a week were 67% more likely to be obese (AOR 1.665, 95% CI 1.079 to 2.568) compared to those who did not watch at all.Conclusions: Prevalence of overweight and obesity has risen considerably among women aged between 15 and 49 years since the previous estimates based on BDHS data. Frequent TV watching was associated with a higher risk of being obese among adult women in rural areas.Ghose B.

INTRODUCTION

Overweight and obesity represent major risk factors for non-communicable chronic diseases (NCDs), and are considered major public health hazards in low and middle income countries and in developed countries. 1 2 In 2010, worldwide about 3.4 million deaths, 3.9% of years of life lost, and 3.8% of disability-adjusted life-years (DALYs) were attributable to overweight/obesity alone. 3 In Bangladesh, where the epidemiological trend is usually characterised by high rates of infectious diseases 4 along with childhood and adult undernutrition, overweight and obesity are fast becoming a significant public health concern. 5 The prevalence of overweight and obesity increased about twofold during the period 2004-2011: overweight 7.5% in 2004 versus 13.5% in 2011, and obesity 1.4% in 2004 versus 2.9% in 2011. 6 This rising prevalence is usually attributed to the recent economic progress which has been accompanied by certain demographic and nutritional transitions, urbanisation, and dietary and lifestyle changes. 5 7 Review of the epidemiological studies surrounding the determinants of overweight/obesity suggests attention is growing in regard to the impact of lifestyle related obesogenic behaviours. [8][9][10] Factors that appear most commonly include changing dietary choices, sedentary behaviour, watching TV, playing computer games, and level of physical activity (PA). 5 8-10 Strengths and limitations of this study ▪ This is the first study to investigate the association between TV viewing and overweight/obesity among adult women in a South Asian country. ▪ The sample size was large and representative of the general population. ▪ TV viewing frequency per week was used instead of duration per day which could have produced a more precise picture of the association. ▪ Data were cross-sectional, which precludes any causal inference.

A growing consensus suggests a strong correlation between sedentary lifestyle and inadequate PA and the risk of developing NCDs. 7 9-11 Studies from low and middle income countries have shown that a large proportion of children and adolescents do not meet recommended levels of PA, as lifestyles involving higher PA have been displaced by more sedentary alternatives (satellite TV, computer games, telecommunication technology), thus contributing to reduced PA and energy expenditure. 12 It has been claimed that watching TV not only leads to reduced levels of PA, but involves a set of behaviours whereby sitting/lying is the dominant mode of posture with low energy expenditure, and that getting used to such postural behaviour can be replicated at school and in the workplace. 13 Higher sitting time has been shown to be associated with increased risk of developing overweight and obesity, cancer, and diabetes 14 15 and has been identified as a global public health issue. 16 In addition to reduced levels of PA and low energy expenditure, TV watching also increases the consumption of obesogenic foods. 17 Cross-sectional studies on American and Latino children reported that watching TV during family meals is associated with reduced consumption of fruit and vegetables and higher consumption of soda, chips and sausages. 17 18 However, the levels and type of food intake can depend on the genre of programme being watched and the level of engagement. 19 Arguably, the frequency and duration of TV watching can vary substantially from person to person, depending on the availability of alternative sources of recreation, availability of resources of PA, and social factors that can impact the freedom of movement (eg, age, gender, dietary habit, sociocultural factors, neighbourhood safety, level of socialisation). Therefore, the association between TV viewing and being overweight/obese is not generalisable and needs to be studied and interpreted by taking the local context into consideration. Current evidence on this topic is mostly derived from low and middle income countries with very limited research in South Asian countries. Major barriers to conducting studies in this area are lack of recognition of the problem and want of country-wide data. The present study aims to address the research gap by utilising data from the Bangladesh Demographic and Health Survey (BDHS) 2014 survey which provides quality data on various health indicators for women and children in the country. BDHS does not include any separate section on hours of TV watching, hence the number of days/week, instead of hours and minutes, was used as a proxy measure of duration of TV watching.

METHODS

Study setting

Bangladesh is the third largest country in the South Asian region and also has the third largest economy in terms of gross domestic product (GDP). It is the most densely populated country in the world with a population density of 1070 persons/km 2 (2014 estimate). The life expectancy at birth among women is 72 years versus 69 years among men. Though the economy has been experiencing unprecedented progress in the last few decades, the country's performance is still very low in terms of the Human Development Index (HDI value for 2014 is 0.570), ranking 142nd out of 188 countries (fifth in South Asia). The World Bank classifies Bangladesh as a lower middle income country with a gross national income (GNI) per capita of US $1314 in the fiscal year 2014-2015. 20 Survey and data collection The 2014 BDHS was the sixth survey of its kind to take place in the country. The main objectives of the survey were to provide quality data on a range of health, demographic, and socioeconomic indicators and assist in evidence-based policymaking. The survey was conducted under the authority of the National Institute of Population Research and Training (NIPORT) of the Ministry of Health and Family Welfare and was implemented by Mitra and Associates with technical assistance from ICF International of Rockville, Maryland, USA, and financial support from the US Agency for International Development (USAID). Data collection lasted from 28 June to 9 November 2014.

Bangladesh has seven administrative regions which are divided into 64 districts. The sample population covered the residents in non-institutional dwellings in both urban and rural areas from all 64 districts. The primary sampling units (PSU) for the survey were enumeration areas (EAs) used in the Population and Housing Census in the country in 2011 that was provided by the Bangladesh Bureau of Statistics (BBS). Each EA is a collection of an average of about 120 households. At first, 600 EAs were selected for the survey with 207 EAs in urban areas and 393 in rural areas. In the second stage, on average 30 households were selected from each EA, which summed to about 18 000 households. The 2014 BDHS used three types of questionnaires: Household, Woman's Questionnaire, and Community Questionnaire. The main purpose of the Household Questionnaire was to identify women eligible for the individual interview. A total of 18 245 ever-married women aged between 15 and 49 years were identified in these households from which 17 863 were finally interviewed, producing a response rate of 98%. Data for the present study were extracted from the Woman's Questionnaire which included themes such as basic sociodemographic, anthropometric, reproductive, fertility, immunisation, and HIV knowledge. 4 21 Details of the survey are available in the final report published by NIPORT. 21

Study variables

The outcome variables for this study were overweight and obesity measured by body mass index (BMI), which was defined as weight in kg divided by height in m 2 . BDHS carries out anthropometric measurements such as height and weight for ever-married women aged 15-49 years as an indicator of women's nutritional status. As per WHO recommendations, women were categorised as neither overweight nor obese when BMI was <25 kg/ m 2 , overweight if BMI was 25-29.9 kg/m 2 and obese if BMI was >30 kg/m 2 . Exclusion criteria were being currently pregnant and non-availability of information on height and/or weight.

The explanatory variable of main interest was 'frequency of TV watching'. As the exact durations (hours or minutes/day) were not available, the frequencies per week were used as a proxy measure which included: (1) not watching TV at all, (2) watching less than once a week, and (3) watching at least once a week.

Based on insights from reviewing the literature, the following covariates were deemed relevant to the topic and for inclusion in the study-age: 15-24/25-34/ >35 years; division: Barisal/Chittagong/Dhaka/Khulna/ Rajshahi/Rangpur/Sylhet; educational attainment*: nil/ primary/secondary/higher; husband's educational attainment: nil/primary/secondary/higher; currently employed: yes/no; wealth index**: poorest/poorer/ middle/richer/richest; parity: 1/2/3/3+. *Educational attainment was categorised as per the highest level/class attended, regardless of the completion status of that level/class. Nil refers to no experience of formal education, primary as completing grade 5, secondary as completing grade 10, and higher as those who had pre-university/university level education.

**BDHS surveys provided information on wealth status instead of any direct information on income. Household Wealth Index is a used as a proxy measure for household living status which takes into consideration household possessions (eg, TV, radio, bicycle) and housing quality (eg, type of floor, wall, and roof ). Calculation of the wealth index consists of assigning a factor score for a set of possessions which is generated through principal component analysis (PCA). The scores are then summed and standardised for each household which places them in a continuous scale based on relative wealth scores. Finally, the scores are categorised into quintiles where each household fall into a category, with the lowest scores representing the poorest and the highest scores representing the richest households. 17 Data analysis Data were analysed using STATA V.12 and SPSS V.20. Datasets were checked for missing values and outliers. Weighted baseline sociodemographic information was presented by descriptive statistics. χ 2 tests were performed to examine the group differences (between overweight and obesity) for all the explanatory variables. The variables that showed significance at p≤0.25 were selected for final regression analysis. All variables were checked for multicollinearity and no significant multicollinearity was observed between any variables. The association between BMI and frequency of TV watching was measured by means of multinomial logistic regression. Results of the regression analysis were presented as crude and adjusted ORs with corresponding 95% CIs. All tests were two-tailed and were considered significant at the level of 5%.

Ethics statement

All participants gave informed consent before taking part in the voluntary interview. The survey was approved by the ICF International Institutional Review Board which is responsible for reviewing the procedures and questionnaires for standard BDHS surveys.

RESULTS

Basic characteristics of the sample population are presented in table 1. The table shows that the majority of the women were of rural origin with the highest participation from the Dhaka division (17.4%) and the lowest from Sylhet (11.3%). More than a quarter of the women were in the 15-24 years age group and more than one-third were above 34 years of age, and about two-thirds (65.3%) were of rural origin. The rate of having no formal education was higher among women compared to their husbands (75.7% vs 71.3%). The majority of the women (37%) and their husbands (29.4%) had secondary school level qualification. However, the rate of completion of higher education was lower among women (9.4%) compared to their husbands (14.9%). Less than one-third of the women reported being in employment at the time of interview, and the rate of unemployment was slightly higher among urban women compared to rural women (68.8% vs 66.8%). Regarding household wealth status, the majority of the women belonged to the wealthiest group (21.7%). However, the rate of being in the wealthiest group was noticeably higher among urban women compared to their rural counterparts (44.4% vs 9.6%). More than one-fifth of the women were primiparous and a little less than one-third of the women had experienced more than three childbirths. About two-fifths of the women reported not watching TV at all (39.4%) and more than half reported watching at least once a week. The rate of watching TV at least once a week was almost twice as high among urban women compared to rural women (75.1% vs 39.6%). The prevalence of overweight and obesity in the sample population were, respectively, 4.5% and 20%. Urban women had a higher prevalence of both overweight (27.7% vs 15.9%) and obesity (8.1% vs 2.6%) compared to rural women. Table 2 shows the results of χ 2 tests of association among the three groups according to their BMI status in relation to the explanatory variables. The results show that the prevalence of both overweight and obesity increased with higher age and was most common in Dhaka division. Women who had secondary level education, were currently unemployed, belonged to the wealthier households, and had two children were more likely to be overweight and obese. Participants who reported watching TV at least once a week were also more likely to be overweight and obese compared to those who did not watch at all or watched less than once a week.

Cross-tabulation

The association between frequency of TV watching and BMI status among the sample population was analysed by means of multivariable logistic regression, with normal weight considered as the reference group. The crude and adjusted odds of being overweight and obese are shown in tables 3 and 4, respectively. Compared with women who did not watch TV at all, those who watched at least once a week were 84% (adjusted OR (AOR) 1.840, 95% CI 1.215 to 2.788) and 58% (AOR 1.578, 95% CI 1.189 to 2.094) more likely to be overweight in urban and rural areas, respectively. Urban women who watched TV less than once and at least once per week were 2.1 (AOR 2.075, 95% CI 1.341 to 3.211)) and 4.7 (AOR 4.705, 95% CI 3.184 to 6.954) times more likely to be obese compared to those who did not watch TV at all. The corresponding figures for rural women were, respectively, 2.64 (AOR 2.643, 95% CI 1.639 to 4.264) and 3.6 (AOR 3.611, 95% CI 2.761 to 4.722).

In the adjusted model, however, no statistically significant association was found between TV viewing and being overweight. Urban women who watched TV at least once a week were 67% more likely to be obese (AOR 1.665, 95% CI 1.079 to 2.568) compared to those who did not watch at all. In the rural areas, women who watched TV less than once and at least once per week had, respectively, 63% (AOR 1.625, 95% CI 1.179 to 2.241) and 68% (AOR 1.683, 95% CI 1.029 to 2.751) higher odds of being obese compared to those who did not watch TV at all.

Model goodness-of-fit: Several goodness-of-fit statistics are used to check for internal validity of regression models. However, for this study McFadden R 2 value was used as it is one of the most commonly reported. The McFadden R 2 was 0.197 in the adjusted model, indicating a satisfactory model fitness.

DISCUSSION

Main findings

Based on nationally representative cross-sectional data, this study attempted to show the current prevalence of overweight and obesity among non-pregnant adult women in Bangladesh, and the association between frequency of TV viewing and being overweight and obese. Our findings indicate a net increase in the prevalence of overweight and obesity among women aged between 15 and 49 years. In the 2004 BDHS, which was the first to include anthropometric measurements for adult women, the prevalence of women with BMI ≥25.0 was 8.9% (7.5% overweight and 1.4% obese), which increased to 16.4% (13.5% overweight and 2.9% obese) in 2011 and 24% (19.4% overweight and 4.4% obese) in 2014. As seen in the previous surveys, urban women had a notably higher prevalence of both overweight (27.7% vs 15.9%) and obesity (8.1% vs 2.6%) compared to their rural counterparts.

As expected, the frequency of TV watching was also higher among women in urban areas than in rural areas. This is understandable as urban residents enjoy a   higher coverage of electric grids and access to more diverse TV channels. Another possible reason can be the higher rate of employment among rural women which may allow them less time for recreation. TV watching was significantly associated with obesity among rural women. Women who reported watching TV less than once a week had higher odds of being obese compared to those who did not watch TV at all. Those who watched at least once a week had the highest likelihood of being overweight and obese. Regardless of the frequency of watching TV, urban women had higher odds of being obese than their rural counterparts. This might be due to the type of work they were engaged in and the types of food consumed. Types of employment in rural areas are supposed to be more labour consuming and involve greater movement due to less developed transportation and technological infrastructure. Moreover, the dietary environment in rural areas is also supposed to be less obesogenic than in urban areas due to the lower concentration of fast-food, restaurant and supermarket chains.

Comparison with previous studies

The prevalence of overweight and obesity is rising not only in Bangladesh but also in other South Asian countries, with varying trends across age, sex and region. In India, the percentage of overweight and obese women aged 15-49 years rose from 11% in the National Family Health Survey (NFHS)-2 to 15% in NFHS-3, with the highest rates in Punjab (29.9%) followed by Kerala (28.1%) and Delhi (26.4%). 22 According to WHO estimates, the percentage of overweight and obesity among Pakistani women was, respectively, 25.5% and 3.6% with a higher prevalence of overweight and obesity among women than among men. 23 For Nepal, the increase in the combined prevalence of overweight and obesity was about six times (1.6% in 1996 vs 10.1% in 2006) between 1996 and 2006. 24 Evidence regarding the association between TV viewing and overweight and obesity in South Asia is scarce; however, studies from other countries show that TV viewing is strongly associated with overweight and obesity among preschool children, adolescents and adults of both sexes, [25][26][27][28][29] which is consistent with our findings in adult women in Bangladesh. Similar findings were observed in the USA, 25 Japan 28 and Australia. 29 Among Iranian adolescents, TV viewing was associated with increasing rates of overweight and obesity independent of PA and consumption of obesogenic foods. 27 One review study proposed that TV viewing may act through mechanisms other than reducing the expenditure of energy and increasing the consumption of obesogenic foods, 30 as the amount of obesogenic food consumption is not always related to the length of time the adolescents spent watching TV. 31

RESEARCH IMPLICATIONS AND GENERAL DISCUSSION

Recent research evidence suggests a rapid rise in the burden of overweight/obesity and associated NCDs, which is a growing concern for the underdeveloped healthcare system in Bangladesh. As the country is progressing in terms of socioeconomic development and improved living standards, more and more people are adopting modern technological conveniences and embracing a more western lifestyle. The literacy rate is still low and the general population is largely unaware of the consequences of unhealthy behaviour and lifestyle related risk factors of overweight/obesity and NCDs. Given the rising prevalence of overweight and obesity in the country, there is an urgent need for health policymakers to develop socio-culturally appropriate guidelines and create the opportunities for averting the onset of overweight/obesity among children, and implement interventions among those already overweight and obese. This is certainly a challenging task, the effective implementation of which is reliant on evidence from large scale population-based studies. Though the present study is very limited in its scope, it sets out the path for more in-depth studies to probe into the underlying determinants of inadequate PA and TV watching and the mechanisms through which they are contributing to the increasing prevalence of overweight/obesity among adult women in particular and the population in general.

Strengths and limitations

This study has several important strengths and limitations. To our knowledge, this is the first nationally representative study to investigate the frequency of TV viewing in relation to overweight/obesity among Bangladeshi women, so the findings are generalisable for adult women below the age of 50 years in Bangladesh. The findings are expected to serve as useful tools for developing proper intervention methods. However, as the survey collected data on outcome and explanatory variables at the same point in time, no causal inferences can be made. Secondly, TV viewing frequency per week was used instead of duration per day which could have produced more precise data on the exact number of hours of TV watching. More importantly, women reported the frequency themselves which may be subject to reporting bias and recall error. Future surveys are recommended to focus on the impact of the total number of hours instead of days and also include information on dietary and other behaviours associated with watching TV.

Table 1
1Baseline characteristics of the study population, BDHS 2014Variables
Frequency (%)

Age (years)
15-24
4433 (26.7)
25-34
5969 (35.9)
35/35+
6222 (37.4)
Division
Barisal
1982 (11.9)
Chittagong
2639 (15.9)
Dhaka
2893 (17.4)
Khulna
2460 (14.8)
Rajshahi
2380 (14.3)
Rangpur
2389 (14.4)
Sylhet
1881 (11.3)
Residency
Urban
5764 (34.7)
Rural
10 860 (65.3)
Educational attainment
Nil
4039 (24.3)
Primary
4875 (29.3)
Secondary
6153 (37.0)
Higher
1557 (9.4)
Husbands' educational attainment
Nil
4764 (28.7)
Primary
4503 (27.1)
Secondary
4884 (29.4)
Higher
2473 (14.9)
Currently employment
No
11 221 (67.5)
Yes
5403 (32.5)
Wealth index
Poorest
2999 (18.0)
Poorer
3102 (18.7)
Middle
3382 (20.3)
Richer
3534 (21.3)
Richest
3607 (21.7)
Parity
1
3625 (21.8)
2
4495 (27.0)
3
3238 (19.5)
3+
5266 (31.7)
Frequency of watching TV
Not at all
6544 (39.4)
Less than once a week
1453 (8.7)
At least once a week
8627 (51.9)
BMI
BMI ≥30
748 (4.2)
25≥ BMI <30
3325 (20.0)
BMI <25
12 551 (75.8)

BDHS, Bangladesh Demographic and Health Survey; BMI, body
mass index.

Table 2
2Prevalence of overweight and obesity in the sample population across the explanatory variables, BDHS 2014

BMI status (%)
Variables
BMI ≥30
25≥ BMI <30
BMI <25
χ 2
p Value

Age (years)
428.111
<0.0001
15-24
10.6
15.5
30.6
25-34
37.2
41.2
34.4
35/35+
52.3
43.3
35.0
Division
176.299
<0.0001
Barisal
8.7
10.5
12.5
Chittagong
18.7
18.2
15.1
Dhaka
20.1
19.8
16.6
Khulna
18.4
17.4
13.9
Rajshahi
15.5
14.7
14.2
Rangpur
10.2
11.3
15.4
Sylhet
8.4
8.0
12.4
Residency
Urban
62.3
48.1
29.5
664 562
<0.0001
Rural
37.7
51.9
70.5
Educational attainment
434.825
0.001
Nil
14.2
17.1
26.8
Primary
23.9
25.4
30.7
Secondary
44.9
42.2
35.2
Higher
17.0
15.2
7.4
Husbands' educational attainment
758.122
<0.0001
Nil
14.8
18.6
32.1
Primary
20.1
22.7
28.7
Secondary
34.8
33.8
27.9
Higher
30.3
24.8
11.3
Currently employment
53.861
<0.0001
No
77.8
69.9
66.2
Yes
22.2
30.1
33.8
Wealth index
36.790
0.013
Poorest
3.3
7.5
21.7
Poorer
4.8
11.1
21.5
Middle
12.0
17.4
21.6
Richer
23.7
24.7
20.2
Richest
56.1
39.2
15.0
Parity
154.802
0.004
1
18.7
19.3
22.7
2
31.8
33.1
25.1
3
25.1
20.9
18.8
3+
24.3
26.7
33.4
Frequency of watching TV
18.898
0.001
Not at all
14.2
23.9
45.0
Less than once a week
5.6
7.6
9.2
At least once a week
80.2
68.5
45.8

BDHS, Bangladesh Demographic and Health Survey; BMI, body mass index.

Table 3
3Association (crude) between frequency of watching TV and overweight and obesity among Bangladeshi women,
BDHS 2014

Frequency of
watching TV

Overweight (COR, 95% CI)
Obesity (COR, 95% CI)
Urban
Rural
Urban
Rural

Not at all
1
1
1
1
Less than once a week 1.412 (0.887 to 2.248) 1.542 (0.933 to 2.549) 2.075 (1.341 to 3.211) 2.643 (1.639 to 4.264)
At least once a week
1.840 (1.215 to 2.788) 1.578 (1.189 to 2.094) 4.705 (3.184 to 6.954) 3.611 (2.761 to 4.722)

BDHS, Bangladesh Demographic and Health Survey; COR, crude OR.

Ghose B. BMJ Open 2017;7:e014399. doi:10.1136/bmjopen-2016-014399

Table 4
4Association (adjusted) between frequency of watching TV and overweight and obesity among Bangladeshi women, BDHS 2014 Less than once a week 1.173 (0.728 to 1.891) 1.258 (0.899 to 1.761) 1.210 (0.763 to 1.919) 1.625 (1.179 to 2.241) At least once a week 1.261 (0.801 to 1.985) 1.352 (0.810 to 2.257) 1.665 (1.079 to 2.568) 1.683 (1.029 to 2.751) Adjusted for age, division, educational attainment, husbands' educational attainment, employment status, wealth index, and parity. BDHS, Bangladesh Demographic and Health Survey; AOR, adjusted OR.Overweight (AOR, 95% CI)
Obesity (AOR, 95% CI)
Frequency of
watching TV
Urban
Rural
Urban
Rural

Not at all
1
1
1
1

Acknowledgements The author would like extend sincere thanks to the BDHS for providing the data, and to the participants who agreed to take part in the survey.Contributors BG was responsible for data collection, conceptualisation of the study, data analysis, and preparation of the manuscript.Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.Competing interests None declared.Ethics approval Bangladesh Demographic and Health Survey.Provenance and peer review Not commissioned; externally peer reviewed.Data sharing statement Dataset used for this study was obtained from the BDHS website. The BDHS holds the sole authority to distribute the data through the public domain which is available at: http://dhsprogram.com/data/ available-datasets.cfm.Informed consent Obtained.Open Access This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work noncommercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http:// creativecommons.org/licenses/by-nc/4.0/
The epidemiology of obesity. D M Nguyen, H B El-Serag, 10.1016/j.gtc.2009.12.014Gastroenterol Clin North Am. 39Nguyen DM, El-Serag HB. The epidemiology of obesity. Gastroenterol Clin North Am 2010;39:1-7.

The emerging epidemic of obesity in developing countries. A M Prentice, 10.1093/ije/dyi272Int J Epidemiol. 35Prentice AM. The emerging epidemic of obesity in developing countries. Int J Epidemiol 2006;35:93-9.

Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study. M Ng, T Fleming, M Robinson, 10.1016/S0140-6736(14)60460-8Lancet. 384Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014;384:766-81.

Extent of knowledge about HIV and its determinants among men in Bangladesh. S Yaya, G Bishwajit, G Danhoundo, 10.3389/fpubh.2016.00246Front Public Health. 4246Yaya S, Bishwajit G, Danhoundo G, et al. Extent of knowledge about HIV and its determinants among men in Bangladesh. Front Public Health 2016;4:246.

Nutrition transition in South Asia: the emergence of non-communicable chronic diseases. Version 2. G Bishwajit, 10.12688/f1000research.5732.2F1000Res. 48Bishwajit G. Nutrition transition in South Asia: the emergence of non-communicable chronic diseases. Version 2. F1000Res 2015;4:8.

Dual burden of underweight and overweight among women in Bangladesh: patterns, prevalence, and sociodemographic correlates. Ssm Kamal, H H Che, G M Alam, J Health Pop Nutr. 33Kamal SSM, Che HH, Alam GM. Dual burden of underweight and overweight among women in Bangladesh: patterns, prevalence, and sociodemographic correlates. J Health Pop Nutr, 2015;33:92-105.

Obesogenic behaviours and depressive symptoms in children: a narrative literature review. M Dennison, S B Sisson, A Morris, 10.1111/obr.12419Obes Rev. 17Dennison M, Sisson SB, Morris A. Obesogenic behaviours and depressive symptoms in children: a narrative literature review. Obes Rev 2016;17:735-57.

Obesity prevention and obesogenic behavior interventions in child care: a systematic review. S B Sisson, M Krampe, K Anundson, 10.1016/j.ypmed.2016.02.016Prev Med. 87Sisson SB, Krampe M, Anundson K, et al. Obesity prevention and obesogenic behavior interventions in child care: a systematic review. Prev Med 2016;87:57-69.

Obesity and associated lifestyle in a large sample of multi-morbid German primary care attendees. C Sikorski, M Luppa, S Weyerer, 10.1371/journal.pone.0102587PLoS One. 9102587Sikorski C, Luppa M, Weyerer S, et al. Obesity and associated lifestyle in a large sample of multi-morbid German primary care attendees. PLoS One 2014;9:e102587.

Physical activity and obesity in children. A P Hills, L B Andersen, N M Byrne, 10.1136/bjsports-2011-090199Br J Sports Med. 45Hills AP, Andersen LB, Byrne NM. Physical activity and obesity in children. Br J Sports Med 2011;45:866-70.

Exercise in weight management of obesity. P Poirier, J P Després, 10.1016/S0733-8651(05)70229-0Cardiol Clin. 19Poirier P, Després JP. Exercise in weight management of obesity. Cardiol Clin 2001;19:459-70.

Improving the blood pressure control with the proactive attitude of hypertensive patients seeking follow-up services: evidence from China. S Tang, G Bishwajit, L Ji, 10.1097/MD.0000000000003233Medicine (Baltimore). 953233Tang S, Bishwajit G, Ji L, et al. Improving the blood pressure control with the proactive attitude of hypertensive patients seeking follow-up services: evidence from China. Medicine (Baltimore) 2016;95:e3233.

Sedentary Behaviour and Obesity Expert Working Group. Sedentary behaviour and obesity: review of the current scientific evidence. London, UK: Department of Health. Sedentary Behaviour and Obesity Expert Working Group. Sedentary behaviour and obesity: review of the current scientific evidence. London, UK: Department of Health, 2010.

Objectively measured sedentary time, physical activity, and metabolic risk: the Australian Diabetes, Obesity and Lifestyle Study (AusDiab). G N Healy, K Wijndaele, D W Dunstan, Diabetes Care. 31Healy GN, Wijndaele K, Dunstan DW, et al. Objectively measured sedentary time, physical activity, and metabolic risk: the Australian Diabetes, Obesity and Lifestyle Study (AusDiab). Diabetes Care 2008;31:369-71.

Sedentary behaviours and epithelial ovarian cancer risk. M Zhang, X Xie, A H Lee, 10.1023/B:CACO.0000016633.47025.2aCancer Causes Control. 15Zhang M, Xie X, Lee AH, et al. Sedentary behaviours and epithelial ovarian cancer risk. Cancer Causes Control 2004;15:83-9.

Too much sitting: the population health science of sedentary behavior. N Owen, G N Healy, C E Matthews, 10.1097/JES.0b013e3181e373a2Exerc Sport Sci Rev. 38Owen N, Healy GN, Matthews CE, et al. Too much sitting: the population health science of sedentary behavior. Exerc Sport Sci Rev 2010;38:105-13.

Reducing children's television viewing to prevent obesity: a randomized controlled trial. T N Robinson, 10.1001/jama.282.16.1561JAMA. 282Robinson TN. Reducing children's television viewing to prevent obesity: a randomized controlled trial. JAMA 1999;282:1561-7.

Positive effects of family dinner are undone by television viewing. E Fitzpatrick, L S Edmunds, B A Dennison, 10.1016/j.jada.2007.01.014J Am Diet Assoc. 107Fitzpatrick E, Edmunds LS, Dennison BA. Positive effects of family dinner are undone by television viewing. J Am Diet Assoc 2007;107:666-71.

Watching TV and food intake: the role of content. C D Chapman, V C Nilsson, H Å Thune, 10.1371/journal.pone.0100602PLoS One. 9100602Chapman CD, Nilsson VC, Thune HÅ et al. Watching TV and food intake: the role of content. PLoS One 2014;9:e100602.

Mitra and Associates, and ICF International. M A Rockville, Mitra Usa: Niport, Associates , National Institute of Population Research and Training (NIPORTBangladesh demographic and health surveyNational Institute of Population Research and Training (NIPORT), Mitra and Associates, and ICF International. 2016. Bangladesh demographic and health survey 2014. Rockville, MA, USA: NIPORT, Mitra and Associates, and ICF International.

Trends and determinants of HIV/AIDS knowledge among women in Bangladesh. S Yaya, G Bishwajit, G Danhoundo, 10.1186/s12889-016-3512-0BMC Public Health. 16812Yaya S, Bishwajit G, Danhoundo G, et al. Trends and determinants of HIV/AIDS knowledge among women in Bangladesh. BMC Public Health 2016;16:812.

An epidemiological study of overweight and obesity among women in an urban area of north India. S Girdhar, S Sharma, A Chaudhary, 10.4103/0970-0218.173492Indian J Community Med. 41Girdhar S, Sharma S, Chaudhary A, et al. An epidemiological study of overweight and obesity among women in an urban area of north India. Indian J Community Med 2016;41:154-7.

Underestimation of weight and its associated factors among overweight and obese adults in Pakistan: a cross sectional study. S Bhanji, A K Khuwaja, F Siddiqui, 10.1186/1471-2458-11-363BMC Public Health. 11363Bhanji S, Khuwaja AK, Siddiqui F, et al. Underestimation of weight and its associated factors among overweight and obese adults in Pakistan: a cross sectional study. BMC Public Health 2011;11:363.

Nationally representative surveys show recent increases in the prevalence of overweight and obesity among women of reproductive age in Bangladesh, Nepal, and India. Y Balarajan, E Villamor, 10.3945/jn.109.112029J Nutr. 139Balarajan Y, Villamor E. Nationally representative surveys show recent increases in the prevalence of overweight and obesity among women of reproductive age in Bangladesh, Nepal, and India. J Nutr 2009;139:2139-44.

Physical activity, TV viewing. J C Eisenmann, R T Bartee, M Q Wang, Obes Res. 10Youth Risk Behavior SurveyEisenmann JC, Bartee RT, Wang MQ. Physical activity, TV viewing, and weight in U.S. youth: 1999 Youth Risk Behavior Survey. Obes Res 2002;10:379-85.

Television viewing and television in bedroom associated with overweight risk among low-income preschool children. B A Dennison, T A Erb, P L Jenkins, 10.1542/peds.109.6.1028Pediatrics. 109Dennison BA, Erb TA, Jenkins PL. Television viewing and television in bedroom associated with overweight risk among low-income preschool children. Pediatrics 2002;109:1028-35.

TV viewing, independent of physical activity and obesogenic foods, increases overweight and obesity in adolescents. S Ghavamzadeh, H R Khalkhali, M Alizadeh, J Health Popul Nutr. 31Ghavamzadeh S, Khalkhali HR, Alizadeh M. TV viewing, independent of physical activity and obesogenic foods, increases overweight and obesity in adolescents. J Health Popul Nutr 2013;31:334-42.

Television viewing time is associated with overweight/obesity among older adults, independent of meeting physical activity and health guidelines. S Inoue, T Sugiyama, T Takamiya, 10.2188/jea.JE20110054J Epidemiol. 22Inoue S, Sugiyama T, Takamiya T, et al. Television viewing time is associated with overweight/obesity among older adults, independent of meeting physical activity and health guidelines. J Epidemiol 2012;22:50-6.

Park availability and physical activity, TV time, and overweight and obesity among women: findings from Australia and the United States. J Veitcha, G Abbotta, A T Kaczynski, 10.1016/j.healthplace.2015.12.004Health Place. 38Veitcha J, Abbotta G, Kaczynski AT, et al. Park availability and physical activity, TV time, and overweight and obesity among women: findings from Australia and the United States. Health Place 2016;38:96-102.

Role of television in childhood obesity prevention. M Caroli, L Argentieri, M Cardone, 10.1038/sj.ijo.0802802Int J Obes Relat Metab Disord. 283SupplCaroli M, Argentieri L, Cardone M, et al. Role of television in childhood obesity prevention. Int J Obes Relat Metab Disord 2004;28(Suppl 3):S104-8.

TV viewing and physical activity are independently associated with metabolic risk in children: the European Youth Heart Study. U Ekelund, S Brage, K Froberg, 10.1371/journal.pmed.0030488PLoS Med. 3488Ekelund U, Brage S, Froberg K, et al. TV viewing and physical activity are independently associated with metabolic risk in children: the European Youth Heart Study. PLoS Med 2006; 3:e488.


Breastfeeding and Active Bonding Protects against Children's Internalizing Behavior Problems
2014

Jianghong Liu
Department of Family and Community Health
School of Nursing
University of Pennsylvania
19104PhiladelphiaPAUSA

Patrick Leung email@example.com
Department of Psychology
Chinese University of Hong Kong
Hong KongChina

Amy Yang email@example.com
Department of Biostatistics and Epidemiology
University of Pennsylvania
19104PhiladelphiaPAUSA

Breastfeeding and Active Bonding Protects against Children's Internalizing Behavior Problems

Nutrients
6201410.3390/nu6010076Received: 4 October 2013; in revised form: 4 December 2013 / Accepted: 10 December 2013 /nutrients * Author to whom correspondence should be addressed; E-Mail: firstname.lastname@example.com;breastfeedingbondingattachmentinternalizing behaviors
Breastfeeding is associated with numerous health benefits to offspring and mothers and may improve maternal-infant bonding. Ample evidence suggests breastfeeding can improve child neurodevelopment, but more research is needed to establish whether breastfeeding is linked to the development of child psychopathology. This paper aims to explore the effects of both breastfeeding and mother-child interactions on child behavioral outcomes at a later age. Children from the China Jintan Child Cohort Study (N = 1267), at age six years old were assessed, along with their parents. Children who were breastfed exclusively for a period of time in the presence of active bonding were compared to those who were breastfed in the absence of active bonding as well as to children who were not exclusively breastfed, with or without active bonding. Results from ANOVA and GLM, using SPSS20, indicate that children who were breastfed and whose mothers actively engaged with them displayed the lowest risk of internalizing problems (mean = 10.01, SD = 7.21), while those who were neither exclusively breastfed nor exposed to active bonding had the least protection against later internalizing problems (mean = 12.79, SD = 8.14). The effect of breastfeeding on internalizing pathology likely represents a biosocial and holistic effect of physiological, and nutritive, and maternal-infant bonding benefits.OPEN ACCESSNutrients 2014, 6 77

Introduction

Breastfeeding is associated with a wide range of positive health outcomes in children and mothers. For example, a systematic review and meta-analysis of approximately 400 studies found that breastfeeding was related to a reduced risk of acute ear infections, respiratory tract infections, asthma, obesity, type 1 and 2 diabetes mellitus, and childhood leukemia [1]. The production of prolactin and oxytocin during breastfeeding is associated with lower levels of maternal stress and enhanced bonding [2]. Furthermore, early cessation of breastfeeding or not breastfeeding at all has been linked to an increased risk of maternal postpartum depression [1].

One particular outcome of interest is that of cognitive development in breastfed children. Breast milk is rich in vital nutrients, such as essential fatty acids, vitamins, minerals, and amino acids, that are associated with improved cognitive functioning [3], language development [4], and overall neurological development [2,5]. In addition, breastfeeding has been associated with improved mother-infant bonding [6,7]. For instance, early feeding interactions between mother and infant may result in more positive feeding experiences and produce greater maternal sensitivity and responsiveness to infant needs [8].

Although previous studies have indicated a wealth of nutritional, physiological, and cognitive benefits to children from breastfeeding, little has been done on emotional development and regulation. It is known that childhood internalizing disorders, including depression and anxiety, can affect up to about 20% of children and adolescents [9]. They also increase the risk of future psychopathology in adulthood [10]. The identification of readily modifiable factors, such as breastfeeding, that may protect against childhood internalizing behaviors is therefore important. Studies have not yet found a relationship between breastfeeding and behavioral outcomes during early childhood [11,12]. However, there are limited studies conducted in older age groups. Oddy et al. found that breastfeeding may be associated with adverse mental health outcomes in early adolescents while Kwok et al. found inconsistent associations [13,14]. However, few studies have tested the long term effect of both breastfeeding as well as the mother-infant interaction during feeding on child behavioral outcomes.

The purpose of this study is to examine whether breastfeeding was related to fewer internalizing disorders later in childhood in a large, community-based sample of Chinese children and parents, and to understand whether breastfeeding and active bonding (i.e., verbal interactions during feeding) were associated with the reduced risk of internalizing behaviors. Finally, this study will assess whether there was any breastfeeding duration (or dosage) effect on internalizing behaviors.

Experimental Section

Participants and Sample Design

The current study was part of a larger population-based community cohort study of 1656 Chinese children (55.5% boys, 44.5% girls) initially recruited from four preschools in the town of Jintan, located in the southeastern coastal region of Mainland China. Briefly, all children and parents taking part in the original cohort study were invited to participate for assessment of children's behaviors while the children were in the final few months of their senior year in preschool (Spring 2005 to Spring 2007). At that point, some children dropped out of the study because of changing schools or because bio-markers were not obtained originally; therefore, only 1419 children in the original sample were followed up in the later waves. Detailed sampling and research procedures of this larger cohort study have been described elsewhere [15,16].

We excluded the cases where the children are over six years old (there are quite a few because it was late in the school year) for the purpose of this analysis because we are using Child Behavior Checklist (CBCL) 1.5 to 5 to measure behavioral outcome. We performed a comparison on measures such as mother's age when the children were born, neighborhood problems, gender, parent's education and occupation prestige, as well as whether parents are separated or divorced, and found there is no difference except the older children tend to be boys and have parents who are less educated. We acknowledge that Chinese tradition prefers to hold boys back in the earlier years of education because of the cultural belief that boys develop and mature later than girls, and that more educated parents would want to place their children in school as early as possible.

The analysis sample consists of 1267 complete data. The mean age of the analysis sample was 66.6 months (SD = 5, range = 50.0-71.9). This is close to the common kindergarten age in the US.

Measures

Internalizing Behavior Problems

We used the Internalizing Behavior scale from the Child Behavior Checklist (CBCL)/1.5-5 as the measure for the dependent variable. The factor structures of CBCL/1.5-5 have been validated in our previous study [17]. The internalizing behavior scale consists of 36 items out of 99 items in total, including Emotionally reactive, Anxious/Depressed, Withdrawn and Somatic Complaints. Items are rated on a 3-point scale (0 = not true, 1 = sometimes true, or 2 = often true) [18]. In this study, we utilized both the full Internalizing Behavior scale and the four syndromes as dependent variables. Alpha is 0.87 for the scale in our sample. We used raw scores on all behavioral assessments for the analysis, as recommended by Achenbach [19].

Breastfeeding

Mothers completed a retrospective questionnaire that asked whether they breastfed (78.3%), used formula (5.6%) or both (16%). In this study, we define exclusive breastfeeding as exclusive for a period of time with a minimum of one month. Non-exclusive breastfeeding is defined to include formula only or mixed methods. Mothers were also asked to report breastfeeding duration in months (mean = 8.79, range 0-24). Duration was categorized into three levels: less or equal to 7 months (25%), between 7 and 10 months (51%) and greater or equal to 10 months (24%).

Maternal Interaction

Mothers were asked a follow-up question for (breast) feeding: "Did you talk to the child while (breast) feeding in the first two years" These responses were: 1 = Never, 2 = Sometimes, 3 = Always. In our study, not all mothers were always talking to the child while breastfeeding. We combined the two measured into one and named it "Feeding types and bonding", reflecting the beneficial effects of both nutritional and active communication. In our sample, we identified four groups. 34.8% of the mothers who always use breast milk and always talk to the child while feeding were classified into Breastfed and Active bonding (group 1); 43.5% who never talk to the child even when they used breast milk were assigned into Breastfed and no Active Bonding (group 2); 9% of the mothers were in the group of Non-breastfed and Active Bonding (group 3), and the final 12.7% in the Non-breastfed and no Active Bonding (group 4).

Social Adversity

Parents were asked to fill in a sociodemographic questionnaire at the same time they completed the CBCL when children were six years old. A number of researchers have demonstrated the utility of combining of several individual measurements of psychosocial risk factors in studying child behavior problems [20,21]. The adversity index was created along lines similar to those described by Rutter and Moffitt [20,21]. A total adversity score was derived based on 11 variables. This score was created by adding 1 point (for 9 of the 11 indicators) or 2 points (for 2 indicators) for 11 adversity indicators: mother's low education (below middle school, 8.8%), father's low education (below middle school, 5.4%), mother's low occupational status (3-point scale: 0 = professional or skilled work, 22.2%; 1 = un-skilled worker, 38.9%; and 2 = no occupation, 31.8%), father's low occupational status (3-point scale: 0 = professional or skilled work, 26.8%; 1 = unskilled worker, 60.3%; and 2 = no job, 3.8%), mother's poor health status (2.1%), father's poor health status (3.8%), obstetric complication (bleeding, hypertension, diabetes, Caesarian section, difficult birth, low birth weight, difficulty breathing, 35.6%), divorce (3.3%), absence of biological mother (4.2%), house size below 70 m 2 (8.4%), and poor neighborhood (overcrowded neighborhood, noise pollution, damp, 35.6%). Details on these indicators are given in Liu et al. [22]. The adversity score ranged from 0 to 13 (M = 3.51, SD = 2.04).

Statistical Methods

To test whether there is any social adversity or internalizing behavior score differences between exclusive and non-exclusive breastfeeding groups, independent t tests were employed. Differences in proportions for gender were tested using χ 2 tests. The same tests were conducted again to test differences between active bonding and non-active bonding group. Cohen's d was calculated to show the size of the effect between two comparison groups.

To test for the combined effects of feeding and bonding types on internalizing behaviors, a series of analysis of variance (ANOVA) were performed. "Feeding and bonding types" was a new variable (four groups defined in the method section) created from the two independent binary variables. It was the grouping variable in ANOVA, and the dependent variables were emotionally reactive, Anxious/Depressed, Somatic Complaints, Withdrawn and total internalizing problems respectively. Omega squared w 2 was computed as an index of effect size with several groups.

To test for the effect of social adversity as a potential confound, general linear models were fitted with adversity entered as covariate. The effect moderator of sex was assessed by entering the measure as a factor alongside feeding and bonding type. Gender × breastfeeding and bonding types interaction term was included in the model as well. The interaction effect of breastfeeding types and bonding types was tested in the models besides including these two variables independently in the models. To test for a dose-response relationship between breastfeeding duration and internalizing behavior, the grouping variable of duration took on three levels (≤7 months, 7-10 months and ≥10 months) for univariate ANOVAs. All results were considered significant if P < 0.05 using a two-tailed test. Statistical analyses were conducted by using SPSS version 20.0 (IBM SPSS Statistics).

Results

Single Effect of Breastfeeding or Active Bonding

Of the 1267 participants with completed data, 77% exclusively breastfed their babies and 43.4% always talk to their babies while feeding. Mean (SD) scores, effect sizes (Cohen's d) and results of specific t test comparisons for the two pairs of comparison groups are given in Table 1. The children who were exclusively breastfed had significantly lower mean scores for somatic complaints and total internalizing problems. Active bonded children had significant lower scores across emotionally reactive, anxious/depressed, withdrawn syndromes and total internalizing problems.

Combined Effect of Breastfeeding and Active Bonding

ANOVA results showed significant group differences on mean behavior scores for total internalizing (F(3,1264) = 5.21; P = 0.001), anxious/depression (F(3,1263) = 2.779; P = 0.04), somatic complains (F(3,1264) = 3.20; P = 0.023) and withdrawn (F(3,1264) = 6.75; P < 0.001). Emotionally reactive showed borderline significance (F(3,1261) = 2.38; P = 0.068). Mean (SD) scores, effect sizes (omega squared w 2 ) and P values from ANOVA for the four comparison groups are given in Table 2. Results revealed identical trend across all dependent variables, with group 1 displaying the lowest scores, followed by group 3. Group 4 had the highest scores.

Potential Confounds

Demographic and social variables are known to influence breastfeeding and children's behavior. Our study showed that boys were more likely be fed by formula or a mixed method rather than pure breast milk (χ 2 = 2.17; P = 0.031). Social adversity scores were significantly lower for those whom actively bonded with their baby while feeding (t = 5.18; P < 0.001), indicating they had a better socioeconomic background and health status (Table 1). Consequently, it is possible that social adversity and gender could account for the main effects of breastfeeding and bonding. We also tested the correlations between potential confounders and dependent variables. In our sample, Spearman correlation indicates social adversity was positively correlated to each syndrome and total internalizing problems (P < 0.001 for all), although no significant correlation was detected between gender and dependent variables. As gender and social adversity were correlated to either the breastfeeding and bonding types or the internalizing problems, we entered these two constructs in to a series of general linear models. The main effects remained significant for Anxious/Depressed, Somatic Complaints, Withdrawn and total internalizing (Table 3) after controlling for adversity (F(1,1252) ≥ 10.98; P ≤ 0.001 for all) and gender (F(1,1252) ≤ 1.56; P ≥ 0.212 for all).

Effect Moderator

There was no interaction between breastfeeding and bonding grouping and gender (F(1,1252) ≤ 2.1; P ≥ 0.097 for all), indicating that this measure did not moderate the effects of breastfeeding and bonding.

Dose Response Relationship

Univariate ANOVAs (with three groups: 0-7 months, 7-10 months and 10 months duration levers) were conducted on each syndrome and total internalizing scores. Results showed significant main effect for breastfeeding duration on anxious/depression (F(2,1170) = 3.28; P = 0.038), somatic complains (F(2,1171) = 3.25; P = 0.039) and total internalizing (F(2,1171) = 2.99; P = 0.051). No significant dose-response effect was detected for emotionally reactive (F(2,1170) = 1.21; P = 0.298) and withdrawn (F(2,1171) = 0.910; P = 0.403). The mean scores for each syndrome and total internalizing problems were plotted against breastfeeding duration levels in Figure 1a,b.

Discussion

Three key findings emerged from this study. First, compared to children whose mothers breastfed them, children who were not breastfed showed an increased number of internalizing behavioral problems, particularly anxious/depressed and somatic symptoms. Second, the group of children whose mothers both breastfed and actively interacted with their infants had the least likelihood of displaying internalizing problems. Children who were not breastfed but whose mothers still engaged in active interactions displayed the next-lowest risk, while being neither breastfed nor exposed to active bonding had the smallest effect on internalizing behaviors. Finally, a duration effect (dosage effect) appeared such that breastfeeding for 10 months or longer had the strongest impact on reducing anxious/depressed and somatic symptoms in children.

Breastfeeding confers a strong biological benefit to infants and their development [23]. From a nutritive standpoint, breast milk contains docosahexaenoic acid (DHA) omega-3 fats, the consumption of which, along with eicosapentaenoic acid (EPA) fats, may reduce the risk for affective disorders, including major depression and bipolar disorders, particularly among women [24,25]. However, the overall literature on DHA and depression remains mixed [26,27]. What is known, however, is that DHA plays a vital role in neural development, neurotransmitter transmission, and genetic expression, making it highly relevant to child neurodevelopment as well as developmental disorders, such as attention-deficit/hyperactivity disorder and motor deficits [28].    It may be that the biological benefit offered to breastfed infants plays a role in healthy cognitive maturation which in turn lowers their risk for psychopathology [29]. Feldman and Eidelman report that breastfeeding is associated with improved motor and social skills [5], but other authors have not found an impact on emotional regulation and behavioral disruption, indicating the need for further research on breastfeeding and child psychodevelopment [30]. Interestingly, a recent study examined effects of breastfeeding on mental health outcomes among children at age 14 years and found that breastfeeding at age six months was associated with a lower rate of child psychopathology, including social and attention difficulties and aggression [31]. However, more longitudinal data is needed to better understand the potential long-term benefits of breastfeeding to child mental health. Whether the nutritional, physiological and cognitive benefits from breastfeeding directly enhance mental health via a biological route in our brain may still require further exploration. However, speculatively, the reported nutritional, physiological and cognitive benefits can confer a lot of advantages to a child to negotiate with the challenges of growing up. For example, a healthier, energetic physical body and a faster cognitive growth can help a child to cope with the arduous demands of modern-day schooling, particularly in mainland China, the tradition of which has long emphasized education as the avenue for upward socio-economic migration. A child who excels at school will also be well liked and accepted by parents, relatives, teachers and peers. School success and social popularity are both known key precursors to mental health [32]. Thus, it is likely that there may be both a direct biological route and an indirect psychosocial route from breastfeeding leading to positive mental health or fewer internalizing problems. These dual routes should both be further examined in future study.

Breastfeeding also provides a biological benefit to the mother by reducing blood pressure and pain [33]. Furthermore, the release of hormones oxytocin and prolactin not only confer analgesic and relaxation benefits, but they also appear to play a key role in mother-infant bonding [11,33], which has been shown to reduce emotional and behavior problems in children [6,7].

The attachment aspect of breastfeeding underscores the need to consider its potential mental health benefits. Psychologically, breastfeeding may enhance the mother-infant bonding process via active talking, eye contact, and skin-to-skin touch. This may help mothers form stronger attachments to offspring and improve maternal sensitivity [33], reduce postpartum depression [34], and ward off other negative mood states like maternal stress [35]. This may indirectly benefit a child's mental health, as the literature detailing the impact of maternal depression on increasing the risk of future child and adolescent psychopathology is compelling [36,37].

Infants may similarly derive a mental health benefit from being breastfed, including development of more secure attachments and reduced negative temperament [38]. Several authors have documented analgesic properties of breast milk, along with reductions in salivary cortisol, due to milk odor and skin-to-skin contact [39,40]; these are hypothesized to help alleviate child distress and strengthen bonding.

Taken together, these findings underlie a biopsychological aspect of breastfeeding wherein the physiological benefits of breastfeeding (e.g., pain reduction, stress reduction, healthy cognitive development) coupled with improved pair bonding and mother-infant attachments may provide protective effects against the formation of child internalizing behaviors The biopsychosocial interaction may also provide indirect benefits that operate through mediating or moderating variables [41]. For example, secure parent-child attachment may improve child sleep quality [42], and reduced sleep problems in children has been linked to better emotional and behavioral functioning [43]. In addition, breastfeeding is ultimately a holistic process and there are several aspects that facilitate the process, including how the mother responds to the infant, the physical and social environment around the mother and baby, and the level nutrients in the breast milk. These factors, such as the genetic and environmental influences of nutrient intake (e.g., breast milk) should be considered [44]. Consideration of such in larger samples will require further study before definitive conclusions can be drawn about intervening variables on breastfeeding and internalizing conditions.

In this study, breastfeeding for a longer duration (at least 10 months) had the greatest effect on reducing internalizing symptoms. This is consistent with other authors who report that longer duration of breastfeeding was associated with greater protection against child mental health problems at age five years [45]. Another recent longitudinal cohort study from Oddy and colleagues followed breastfed infants to 14 years of age and found that breastfeeding for six months or less independently predicted greater externalizing and internalizing problems in childhood and adolescence, compared to infants who were breastfed for 6 months duration or longer [14].

Some important limitations on the present study's findings exist. First, the use of retrospective data may involve recall bias. However, in the current literature, it is not rare for studies examining breastfeeding practices to use maternal recall data after much longer periods. For example, a study by Promislow looked at maternal recall of breastfeeding duration of elderly US women from 34 to 50 years ago [46]. Nevertheless, future prospective designs should be considered. As previously mentioned, we also did not include holistic measures in our assessment of breastfeeding as we do not have data available due to the retrospective nature of this study. Instead, we included confounding factors, such as demographic and social background, in our analysis of breastfeeding. Another limitation of the present study is that it does not take into consideration the exact duration of exclusive breastfeeding, which is particularly important given the fact that breastfeeding practices have decreased in recent years, especially among urban and well-educated mothers [47]. Future studies should test if there is a duration-dependent relationship between breastfeeding and internalizing behavior in children. Additionally, as active bonding was one of the key predictors, future studies should employ validated, empirical-based measures on this construct. However, despite the use of such "crude" measures, they are able to produce consistent results, indicating evidently the benefits of breastfeeding on the children's mental health. Furthermore, future studies should stratify by region, given that breastfeeding practices differ by location.

Conclusions

These results indicate that children who were breastfed and exposed to active bonding during feeding displayed the lowest risks of internalizing behavior problems at age six years. Increased duration of breastfeeding (≥10 months) could also help lower internalizing problems in children (i.e., a dosage effect). These findings were independent of several socio-demographic/family characteristics, as well as gender. It is possible that both nutrients (e.g., fatty acids) and maternal bonding interactively work to promote optimal neurodevelopment in early childhood, subsequently protecting children from internalizing disorders, such as depression, anxiety, and somatic complaints [48]. The promotion of active bonding practices during feeding (whether breastfeeding or formula feeding) may help reduce later internalizing behaviors in children by enhancing attachment between the mother and infant.

Figure 1 .
1Dose-response Relationship between duration of breastfeeding and internalizing behavior. (a) Breastfeeding duration and internalizing syndromes; (b) Breastfeeding duration and total internalizing problems.

Table 1 .
1Descriptives of the Breastfeeding and internalizing behavior Outcome (N = 1267).Note: significant results were highlighted in bold; \ not available.Breastfeeding type

Table 2 .
2Combined Effect of Breastfeeding and Active Bonding on Behavior Problems from ANOVA.Group 1
Group 2
Group 3
Group 4

Variables

Exclusive
Breastfeeding with
Active Bonding 34.8%

Exclusive
Breastfeeding without
Active Bonding 43.5%

Non-exclusive
Breastfeeding with
Active Bonding 9%

Non-exclusive
Breastfeeding without
Active Bonding 12.7%

Effect Size (omega
squared w 2 )
P

Emotionally Reactive
2.48 (2.30)
2.73 (2.45)
2.62 (2.22)
3.07 (2.50)
0.003
0.068
Anxious/Depressed
3.11 (2.17)
3.30 (2.34)
3.15 (2.15)
3.71 (2.41)
0.004
0.04
Somatic Complaints
2.56 (2.39)
2.70 (2.53)
2.72 (2.14)
3.27 (2.50)
0.005
0.023
Withdrawn
1.87 (2.20)
2.40 (2.41)
2.13 (2.22)
2.73 (2.53)
0.013
<0.001
Total Internalizing
10.01 (7.21)
11.12 (7.90)
10.61 (6.66)
12.79 (8.14)
0.01
0.001

Note: significant results were highlighted in bold.

Table 3 .
3General linear model statistics of breastfeeding type and bonding against internalizing problems, controlling for gender and social adversity.Dependent Variables Type III Sum of Squares
df
Mean square
F
Significance
Emotionally Reactive
34.4
3, 1255
11
2.045
0.106
Anxious/Depressed
38.12
3, 1257
12.71
2.471
0.06
Somatic Complaints
54.6
3, 1258
18.2
3.108
0.026
Withdrawn
90.07
3, 1258
32.36
6.016
<0.001
Total Internalizing
774.39
3, 1258
258.13
4.573
0.003

Note: significant results (P<0.05) were highlighted in bold.

© 2013 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
AcknowledgementThis study was supported by funding from the National Institute of Environmental Health Sciences/NIH/NIEHS 1-K02-ES-019878 and 1-R01-ES-018858. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Conflicts of InterestThe authors declare no conflicts of interest.
Breastfeeding and maternal and infant health outcomes in developed countries. S Ip, M Chung, G Raman, P Chew, N Magula, D Devine, T Trikalinos, J Lau, Evid. Rep. Technol. Assess. 153Ip, S.; Chung, M.; Raman, G.; Chew, P.; Magula, N.; Devine, D.; Trikalinos, T.; Lau, J. Breastfeeding and maternal and infant health outcomes in developed countries. Evid. Rep. Technol. Assess. 2007, 153, 1-186.

Human milk and breast feeding for optimal mental development. R Uauy, I De Andraca, J. Nutr. 125Uauy, R.; de Andraca, I. Human milk and breast feeding for optimal mental development. J. Nutr. 1995, 125, 2278S-2280S.

The effect of breastfeeding on child development at 5 years: A cohort study. P J Quinn, M O'callaghan, G M Williams, J M Najman, M J Andersen, W Bor, J. Paediatr. Child Health. 37Quinn, P.J.; O'Callaghan, M.; Williams, G.M.; Najman, J.M.; Andersen, M.J.; Bor, W. The effect of breastfeeding on child development at 5 years: A cohort study. J. Paediatr. Child Health 2001, 37, 465-469.

Duration of breastfeeding and language ability in middle childhood. A J Whitehouse, M Robinson, J Li, W H Oddy, Paediatr. Perinat. Epidemiol. 25Whitehouse, A.J.; Robinson, M.; Li, J.; Oddy, W.H. Duration of breastfeeding and language ability in middle childhood. Paediatr. Perinat. Epidemiol. 2011, 25, 44-52.

Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants. R Feldman, A I Eidelman, Dev. Psychobiol. 43Feldman, R.; Eidelman, A.I. Direct and indirect effects of breast milk on the neurobehavioral and cognitive development of premature infants. Dev. Psychobiol. 2003, 43, 109-119.

Breastfeeding and infant-mother interaction. R Zetterstrom, Acta Paediatr. Suppl. 88Zetterstrom, R. Breastfeeding and infant-mother interaction. Acta Paediatr. Suppl. 1999, 88, 1-6.

Breast feeding and later psychosocial adjustment. D M Fergusson, L J Woodward, Paediatr. Perinat. Epidemiol. 13Fergusson, D.M.; Woodward, L.J. Breast feeding and later psychosocial adjustment. Paediatr. Perinat. Epidemiol. 1999, 13, 144-157.

Physical growth of low birthweight infants in the first year of life: Impact of maternal behaviors. S J Dewitt, J W Sparks, P B Swank, K Smith, S E Denson, S H Landry, Early Hum. Dev. 47DeWitt, S.J.; Sparks, J.W.; Swank, P.B.; Smith, K.; Denson, S.E.; Landry, S.H. Physical growth of low birthweight infants in the first year of life: Impact of maternal behaviors. Early Hum. Dev. 1997, 47, 19-34.

Prevalence and development of psychiatric disorders in childhood and adolescence. E J Costello, S Mustillo, A Erkanli, G Keeler, A Angold, Arch. Gen. Psychiatry. 60Costello, E.J.; Mustillo, S.; Erkanli, A.; Keeler, G.; Angold, A. Prevalence and development of psychiatric disorders in childhood and adolescence. Arch. Gen. Psychiatry 2003, 60, 837-844.

Internalizing disorders in childhood. M Kovacs, B Devlin, J. Child Psychol. Psychiatry. 39Kovacs, M.; Devlin, B. Internalizing disorders in childhood. J. Child Psychol. Psychiatry 1998, 39, 47-63.

. M S Kramer, E Fombonne, S Igumnov, I Vanilovich, L Matush, E Mironova, N Bogdanovich, R E Tremblay, B Chalmers, X Zhang, 121Kramer, M.S.; Fombonne, E.; Igumnov, S.; Vanilovich, I.; Matush, L.; Mironova, E.; Bogdanovich, N.; Tremblay, R.E.; Chalmers, B.; Zhang, X.; et al. Effects of prolonged and exclusive breastfeeding on child behavior and maternal adjustment: Evidence from a large, randomized trial. Pediatrics 2008, 121, e435-e440.

Longitudinal associations between breastfeeding and observed mother-child interaction qualities in early childhood. Child Care Health Dev. L M Papp, 10.1111/cch.12106Papp, L.M. Longitudinal associations between breastfeeding and observed mother-child interaction qualities in early childhood. Child Care Health Dev. 2013, doi:10.1111/cch.12106.

Breast feeding and early adolescent behaviour, self-esteem and depression: Hong Kong's "Children of 1997" birth cohort. M K Kwok, G M Leung, C M Schooling, Arch. Dis. Child. 98Kwok, M.K.; Leung, G.M.; Schooling, C.M. Breast feeding and early adolescent behaviour, self-esteem and depression: Hong Kong's "Children of 1997" birth cohort. Arch. Dis. Child. 2013, 98, 887-894.

The long-term effects of breastfeeding on child and adolescent mental health: A pregnancy cohort study followed for 14 years. W H Oddy, G E Kendall, J Li, P Jacoby, M Robinson, N H De Klerk, S R Silburn, S R Zubrick, L I Landau, F J Stanley, J. Pediatr. 156Oddy, W.H.; Kendall, G.E.; Li, J.; Jacoby, P.; Robinson, M.; de Klerk, N.H.; Silburn, S.R.; Zubrick, S.R.; Landau, L.I.; Stanley, F.J. The long-term effects of breastfeeding on child and adolescent mental health: A pregnancy cohort study followed for 14 years. J. Pediatr. 2010, 156, 568-574.

Cohort profile: The China Jintan child cohort study. J Liu, L A Mccauley, Y Zhao, H Zhang, J Pinto-Martin, Int. J. Epidemiol. 39Liu, J.; McCauley, L.A.; Zhao, Y.; Zhang, H.; Pinto-Martin, J. Cohort profile: The China Jintan child cohort study. Int. J. Epidemiol. 2010, 39, 668-674.

Community-based participatory research (CBPR) approach to study children's health in China: Experiences and reflections. J Liu, L Mccauley, P Leung, B Wang, H Needleman, J Pinto-Martin, Int. J. Nurs. Stud. 48Liu, J.; McCauley, L.; Leung, P.; Wang, B.; Needleman, H.; Pinto-Martin, J. Community-based participatory research (CBPR) approach to study children's health in China: Experiences and reflections. Int. J. Nurs. Stud. 2011, 48, 904-913.

The application of the preschool child behavior checklist and the caregiver-teacher report form to mainland Chinese children: Syndrome structure, gender differences, country effects, and inter-informant agreement. J Liu, H Cheng, P W Leung, J. Abnorm. Child Psychol. 39Liu, J.; Cheng, H.; Leung, P.W. The application of the preschool child behavior checklist and the caregiver-teacher report form to mainland Chinese children: Syndrome structure, gender differences, country effects, and inter-informant agreement. J. Abnorm. Child Psychol. 2011, 39, 251-264.

Manual for the ASEBA Preschool Forms & Profiles. T Achenbach, L Rescorla, Burlington, VT, USAUniversity of Vermont Research Center for ChildrenAchenbach, T.; Rescorla, L. Manual for the ASEBA Preschool Forms & Profiles; University of Vermont Research Center for Children, Youth & Families: Burlington, VT, USA, 2000.

Manual for the Child Behavior Checklist/4-18 and 1991 Profile. T M Achenbach, Burlington, VT, USAUniversity of Vermont, Department of PsychiatryAchenbach, T.M. Manual for the Child Behavior Checklist/4-18 and 1991 Profile; University of Vermont, Department of Psychiatry: Burlington, VT, USA, 1991.

Area and School Influences in the Genesis of Conduct Disorders: Aggression and Anti-Social Behaviour in Child-Hood and Adolescence. M Rutter, Family, Rutter, M. Family, Area and School Influences in the Genesis of Conduct Disorders: Aggression and Anti-Social Behaviour in Child-Hood and Adolescence;

. L A Hersov, M Berger, D Shaffer, Pergamon; Oxford, UKHersov, L.A., Berger, M., Shaffer, D., Eds.; Pergamon: Oxford, UK, 1978; pp. 95-113.

Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to age 15. T E Moffit, Child Dev. 61Moffit, T.E. Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to age 15. Child Dev. 1990, 61, 893-910.

Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children. J Liu, J Portnoy, A Raine, Dev. Psychopathol. 24Liu, J.; Portnoy, J.; Raine, A. Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children. Dev. Psychopathol. 2012, 24, 771-782.

Academy of breastfeeding medicine founder's lecture 2008: Breastfeeding-An extrauterine link between mother and child. S Rautava, W A Walker, Breastfeed Med. 4Rautava, S.; Walker, W.A. Academy of breastfeeding medicine founder's lecture 2008: Breastfeeding-An extrauterine link between mother and child. Breastfeed Med. 2009, 4, 3-10.

Selective deficits in erythrocyte docosahexaenoic acid composition in adult patients with bipolar disorder and major depressive disorder. R K Mcnamara, R Jandacek, T Rider, P Tso, Y Dwivedi, G N Pandey, J. Affect. Disord. 126McNamara, R.K.; Jandacek, R.; Rider, T.; Tso, P.; Dwivedi, Y.; Pandey, G.N. Selective deficits in erythrocyte docosahexaenoic acid composition in adult patients with bipolar disorder and major depressive disorder. J. Affect. Disord. 2010, 126, 303-311.

Higher dietary intake of long-chain omega-3 polyunsaturated fatty acids are inversely associated with depressive symptoms in women. L A Colangelo, K He, M A Whooley, M L Daviglus, K Liu, Nutrition. 25Colangelo, L.A.; He, K.; Whooley, M.A.; Daviglus, ML.; Liu, K. Higher dietary intake of long-chain omega-3 polyunsaturated fatty acids are inversely associated with depressive symptoms in women. Nutrition 2009, 25, 1011-1019.

Effect of DHA supplementation during pregnancy on maternal depression and neurodevelopment of young children: A randomized controlled trial. M Makrides, R A Gibson, A J Mcphee, L Yelland, J Quinlivan, P Ryan, JAMA. 304Makrides, M.; Gibson, R.A.; McPhee, A.J.; Yelland, L.; Quinlivan, J.; Ryan, P. Effect of DHA supplementation during pregnancy on maternal depression and neurodevelopment of young children: A randomized controlled trial. JAMA 2010, 304, 1675-1683.

Fish and n-3 polyunsaturated fatty acid intake and depressive symptoms: Ryukyus child health study. K Murakami, Y Miyake, S Sasaki, K Tanaka, M Arakawa, Pediatrics. 126Murakami, K.; Miyake, Y.; Sasaki, S.; Tanaka, K.; Arakawa, M. Fish and n-3 polyunsaturated fatty acid intake and depressive symptoms: Ryukyus child health study. Pediatrics 2010, 126, e623-e630.

Cognitive and mood effects of 8 weeks' supplementation with 400 mg or 1000 mg of the omega-3 essential fatty acid docosahexaenoic aicid (DHA) in healthy children aged 10-12 years. D O Kennedy, P A Jackson, J M Elliot, A B Scholey, B C Robertson, J Greer, B Tiplady, T Buchanan, C F Haskell, Nutr. Neurosci. 12Kennedy, D.O.; Jackson, P.A.; Elliot, J.M.; Scholey, A.B.; Robertson, B.C.; Greer, J.; Tiplady, B.; Buchanan, T.; Haskell, C.F. Cognitive and mood effects of 8 weeks' supplementation with 400 mg or 1000 mg of the omega-3 essential fatty acid docosahexaenoic aicid (DHA) in healthy children aged 10-12 years. Nutr. Neurosci. 2009, 12, 48-56.

Breastfeeding and child cognitive development: A new evidence from a large randomized trial. M S Kramer, F Aboud, E Mironova, I Vanilovich, R W Platt, L Matush, S Igumnov, E Fombonne, N Bogdanovich, T Ducruet, Arch. Gen. Psychiatry. 65Kramer, M.S.; Aboud, F.; Mironova, E.; Vanilovich, I.; Platt, R.W.; Matush, L.; Igumnov, S.; Fombonne, E.; Bogdanovich, N.; Ducruet, T.; et al. Breastfeeding and child cognitive development: A new evidence from a large randomized trial. Arch. Gen. Psychiatry 2008, 65, 578-584.

Association of breastfeeding and adolescents' psychopathology: A large prospective study. M R Hayatbakhsh, M J O'callaghan, W Bor, G M Williams, J M Najman, Breastfeed Med. 7Hayatbakhsh, M.R.; O'Callaghan, M.J.; Bor, W.; Williams, G.M.; Najman, J.M. Association of breastfeeding and adolescents' psychopathology: A large prospective study. Breastfeed Med. 2012, 7, 480-486.

Developing Minds: Challenge and Continuity Across the Life Span. M Rutter, M Rutter, Basic BooksNew York, NY, USARutter, M.; Rutter, M. Developing Minds: Challenge and Continuity Across the Life Span; Basic Books: New York, NY, USA, 1993.

Mental health, attachment and breastfeeding: Implications for adopted children and their mothers. K D Gribble, Int. Breastfeed J. Gribble, K.D. Mental health, attachment and breastfeeding: Implications for adopted children and their mothers. Int. Breastfeed J. 2006, 1, 5.

Breastfeeding, sensitivity, and attachment. J R Britton, H L Britton, V Gronwaldt, Pediatrics. 118Britton, J.R.; Britton, H.L.; Gronwaldt, V. Breastfeeding, sensitivity, and attachment. Pediatrics 2006, 118, e1436-e1443.

Depressed mothers and infants are more relaxed during breastfeeding versus bottlefeeding interactions: Brief report. T Field, M Diego, M Hernandez-Reif, B Figueirdo, S Ezell, V Siblalingappa, Infant Behav. Dev. 33Field, T.; Diego, M.; Hernandez-Reif, M.; Figueirdo, B.; Ezell, S.; Siblalingappa, V. Depressed mothers and infants are more relaxed during breastfeeding versus bottlefeeding interactions: Brief report. Infant Behav. Dev. 2010, 33, 241-244.

Differences between exclusive breastfeeders, formula-feeders, and controls: A study of stress, mood, and endocrine variables. M W Groër, Biol. Res. Nurs. 7Groër, M.W. Differences between exclusive breastfeeders, formula-feeders, and controls: A study of stress, mood, and endocrine variables. Biol. Res. Nurs. 2005, 7, 106-117.

Can maternal depression increase infant risk of illness and growth impairment in developing countries? Child Care Health Dev. A Rahman, R Harrington, J Bunn, 28Rahman, A.; Harrington, R.; Bunn, J. Can maternal depression increase infant risk of illness and growth impairment in developing countries? Child Care Health Dev. 2002, 28, 51-56.

Antepartum and postpartum exposure to maternal depression: Different effects on different adolescent outcomes. D F Hay, S Pawlby, C S Waters, D Sharp, J. Child Psychol. Psychiatry. 49Hay, D.F.; Pawlby, S.; Waters, C.S.; Sharp, D. Antepartum and postpartum exposure to maternal depression: Different effects on different adolescent outcomes. J. Child Psychol. Psychiatry 2008, 49, 1079-1088.

Difficult temperament, breastfeeding, and their mutual prospective effects: The Norwegian Mother and Child Cohort Study. S Niegel, E Ystrom, K A Hagtvet, M E Vollrath, JDBP. 29Niegel, S.; Ystrom, E.; Hagtvet, K.A.; Vollrath, M.E. Difficult temperament, breastfeeding, and their mutual prospective effects: The Norwegian Mother and Child Cohort Study. JDBP 2008, 29, 458-462.

The calming effect of a maternal breast milk odor on the human newborn infant. S Nishitani, T Miyamura, M Tagawa, M Sumi, R Takase, H Doi, H Moriuchi, K Shinohara, Neurosci. Res. 63Nishitani, S.; Miyamura, T.; Tagawa, M.; Sumi, M.; Takase, R.; Doi, H.; Moriuchi, H.; Shinohara, K. The calming effect of a maternal breast milk odor on the human newborn infant. Neurosci. Res. 2009, 63, 66-71.

Skin-to-skin contact is analgesic in healthy newborns. L Gray, L Watt, E M Blass, Pediatrics. 14Gray, L.; Watt, L.; Blass, E.M. Skin-to-skin contact is analgesic in healthy newborns. Pediatrics 2000, 105, e14.

Early health risk factors for violence: Conceptualization, review of the evidence, and implications. J Liu, Aggress. Violent Behav. 16Liu, J. Early health risk factors for violence: Conceptualization, review of the evidence, and implications. Aggress. Violent Behav. 2011, 16, 63-73.

Attachment representations, sleep quality and adaptive functioning in preschool age children. B E Vaughn, M El-Sheikh, N Shin, L Elmore-Staton, L Krzysik, L Monteiro, Attach. Hum. Dev. 13Vaughn, B.E.; El-Sheikh, M.; Shin, N.; Elmore-Staton, L.; Krzysik, L.; Monteiro, L. Attachment representations, sleep quality and adaptive functioning in preschool age children. Attach. Hum. Dev. 2011, 13, 525-540.

Sleep problems, fatigue, and cognitive performance in Chinese kindergarten children. J Liu, G Zhou, J Wang, Y Ai, J Pinto-Martin, X Liu, J. Pediatr. 161e2Liu, J.; Zhou, G.; Wang, J.; Ai, Y.; Pinto-Martin, J.; Liu, X. Sleep problems, fatigue, and cognitive performance in Chinese kindergarten children. J. Pediatr. 2012, 161, 520-525.e2.

Genetic and environmental influences on nutrient intake. J Liu, C Tuvblad, A Raine, L Baker, Genes Nutr. 8Liu, J.; Tuvblad, C.; Raine, A.; Baker, L. Genetic and environmental influences on nutrient intake. Genes Nutr. 2013, 8, 241-252.

Pre-and postnatal influences on preschool mental health: A large-scale cohort study. M Robinson, W Oddy, J Li, G E Kendall, N H De Klerk, S R Silburn, S R Zubrick, J P Newnham, F J Stanley, E Mattes, J. Child Psychol. Psychiatry. 49Robinson, M.; Oddy, W.; Li, J.; Kendall, G.E.; de Klerk, N.H.; Silburn, S.R.; Zubrick, S.R.; Newnham, J.P.; Stanley, F.J.; Mattes, E. Pre-and postnatal influences on preschool mental health: A large-scale cohort study. J. Child Psychol. Psychiatry 2008, 49, 1118-1128.

Maternal recall of breastfeeding duration by elderly women. J Promislow, B Gladen, D Sandler, Am. J. Epidemiol. 161Promislow, J.; Gladen, B.; Sandler, D. Maternal recall of breastfeeding duration by elderly women. Am. J. Epidemiol. 2005, 161, 289-296.

Social and demographic determinants for breastfeeding in a rural, suburban and city area of South East China. J Liu, Z Shi, D Spatz, R Loh, G Sun, J Grisso, Contemp. Nurse. 45Liu, J.; Shi, Z.; Spatz, D.; Loh, R.; Sun, G.; Grisso, J. Social and demographic determinants for breastfeeding in a rural, suburban and city area of South East China. Contemp. Nurse 2013, 45, 234-243.

Childhood internalizing behavior: Analysis and implications. J Liu, X Chen, G Lewis, J. Psychiatr. Ment. Health Nurs. 18Liu, J.; Chen, X.; Lewis, G. Childhood internalizing behavior: Analysis and implications. J. Psychiatr. Ment. Health Nurs. 2011, 18, 884-894.