Introduction {#s1}
============

The 2011 UN High Level Summit gave global prominence to the growing problem of non-communicable diseases (NCDs), particularly heart disease and diabetes for which obesity is a key risk factor [@pone.0090403-Alleyne1].  It is arguably the most complex to address and presents a potentially intractable epidemic in itself [@pone.0090403-Swinburn1].  Cross-country comparisons have played a central role in understanding the association between socio-economic status (SES) and obesity in relation to country levels of economic development [@pone.0090403-Sobal1], [@pone.0090403-Monteiro1], [@pone.0090403-JonesSmith1], [@pone.0090403-Dinsa1].  Most of this research suggests that obesity is a problem of the elites in poorer countries, with a process of gradual reversal occurring as countries develop, and it becomes a problem of the poor in advanced economies. 

Recent studies have disputed whether the reversal is taking place [@pone.0090403-Neuman1], [@pone.0090403-Subramanian1], [@pone.0090403-Subramanian2].  However, they favoured wealth as the better indicator and neglected the possibility that different SES indicators might act differently.  Education has been shown to have a different association with mortality compared with occupation in high-income countries and a different association with heart disease compared with indicators of material circumstances in ex-Communist countries [@pone.0090403-DaveySmith1], [@pone.0090403-Bobk1]. 

In developing economies, rising income or wealth may be used to purchase greater quantities of food which increases obesity risk [@pone.0090403-James1] and this effect may be exacerbated by a mismatch between a biology programmed in early life for scarcity and the exposure in later life to a sudden influx of cheap calories as markets open to the global food system [@pone.0090403-Prentice1].  On the other hand, education may mitigate this effect through cognitive skills that influence information processing and health-related decision-making [@pone.0090403-Cutler1], [@pone.0090403-Mirowsky1].  In other words, individuals may be able to modify their response to an increasingly obesogenic environment by drawing on personal resources such as educational capital and cognitive skills to navigate new disease risks.  This may be useful where interventions targeting the food industry are politically unfeasible. 

In a previous study [@pone.0090403-AitsiSelmi1], we tested the hypothesis that education and wealth may have separate but inter-related effects on obesity in a country with a high level of female obesity (Egypt).  Having confirmed the existence of an interaction whereby education modified the positive wealth-obesity association, we then sought to examine whether this finding could be replicated in other middle-income countries.  In addition, we aimed to test the hypothesis that the protective role of education was dependent on the level of economic development of a country in line with the reversal, such that this protective role would be found in middle-income but not low-income countries.  In the latter, associations between any marker of SES and obesity might be positive.  This is because the food environment is more likely to be dominated by food scarcity rather than obesogenic drivers including increased calorie availability and commercial marketing.  As a result, there would be a minimal role for education to be protective against obesity in low-income countries, where any socioeconomic advantage might be used for calorie accumulation. 

Therefore, this study examines the association between education and wealth in relation to obesity in women in a representative sample of low- and middle-income countries.  It tests the hypothesis that education may protect against the association of wealth with obesity in middle-income countries and that this would not be observed in low-income countries.  It aims to open up new avenues of investigation for the separate and inter-related effects of wealth and education on obesity in emerging economies. 

Methods {#s2}
=======

Dataset {#s2a}
-------

The Demographic and Health Surveys (available: DHS - <http://www.measuredhs.com/Data/>.  Accessed 2013 Jan 1) are a key source of data for studies on obesity [@pone.0090403-Monteiro1], [@pone.0090403-JonesSmith1], [@pone.0090403-Dinsa1], [@pone.0090403-Neuman1], [@pone.0090403-Subramanian1], [@pone.0090403-Martorell1], [@pone.0090403-Puoane1], [@pone.0090403-Ziraba1].  They are a worldwide project funded by the United States Agency for International Development aiming to provide data on demographics and health outcomes, mainly for women and young children.  They are nationally representative household-based, cross-sectional surveys using a multistage stratified probabilistic sampling design.  The primary population surveyed is the universe of all ever-married women aged 15--49 years [@pone.0090403-USAID1].  The standardisation of the methodology and survey instruments combined with extensive interviewer training make them ideal for cross-country comparisons. 

Study sample {#s2b}
------------

All countries for which a DHS survey had been conducted between 2005 and 2010 (the latest wave at the time of this study) were eligible.  They were listed according to sample size using the DHS STAT compiler tool available on the DHS website (available: <http://www.statcompiler.com>.  Accessed 2013 Jan 1).  We selected the six countries with the largest datasets for comparison with the Egyptian DHS dataset used in a previous study [@pone.0090403-AitsiSelmi1].  They included Benin, India, Nigeria, Peru, Jordan and Colombia and represented a range of country income levels based on the World Bank country income classification at the time of the survey (available: <http://data.worldbank.org/about/country-classifications>\> and notes <http://tinyurl.com/cnhf9aw>.  Accessed 2012 Nov 10).  Jordan was selected to satisfy an additional sampling criterion of selecting another country from the Middle East and North Africa (MENA) region to provide a closer comparison with Egypt culturally. [ Table 1](#pone-0090403-t001){ref-type="table"} shows the survey characteristics by country including response rates which were all above 90%.  The DHS survey waves that were selected recorded anthropometry for all ever-married women (unlike earlier waves which took measurements from women with young children only).  We excluded pregnant women (see [Table 1](#pone-0090403-t001){ref-type="table"}), but we did not exclude extreme values as there were too few to influence the estimates and variance. 

10.1371/journal.pone.0090403.t001

###### Sample details by economic classification at the time of the DHS survey for each country included in the analysis. 

![]( pone.0090403.t001){#pone-0090403-t001-1}

                                                                        Benin    India    Nigeria     Egypt                    Jordan                  Peru                  Colombia
  -------------------------------------------------------------------- ------- --------- --------- ----------- -------------------------------------- ------- ---------------------------------------
  GNIpc at time of survey (\$)[1](#nt101){ref-type="table-fn"}           590      720      1170     1250/1880                   3110                   3590                    5510
  Income classification[2](#nt102){ref-type="table-fn"}                  LI       LI        LI         MI                        MI                     MI                      MI
  DHS Year                                                              2006     2005      2008      2005/08                    2007                   2008                    2010
  Number of women interviewed                                           17794   124385     33558      36045                    10876                   16159   53320[3](#nt103){ref-type="table-fn"}
  Response rate of women eligible for interview                          94       95        97        \>99                       98                     98      94[3](#nt103){ref-type="table-fn"}
  Women with complete anthropometry                                     16717   118734     32358      35690     5196[4](#nt104){ref-type="table-fn"}   15228                   49637
  Missing covariates (% of anthropometry sample)                          0     \<0.01%      0          0                        0                       0                     7.6%
  Final analytic sample^5(figures\ below\ relate\ to\ this\ sample)^    14883   113063     28901      32272                     4527                   14483                   47709
                                                                                                                                                              

GNIpc in \$ using Atlas method at time of survey, World Bank classification.  <http://tinyurl.com/3bpg77q>. 

World Bank income classification.  \<<http://data.worldbank.org/about/country-classifications>\> and notes <http://tinyurl.com/cnhf9aw>\>.  LI = low-income; MI = middle-income. 

Includes women 13--49 years (the rest of the figures for Colombia are for women 15--49 years). 

Anthropometry collected in half of the household sample. 

Excludes pregnant women; includes missing covariates. 

Outcome and covariates {#s2c}
----------------------

The model used in this study is based on the literature of multicountry studies examining SES-obesity association and includes a relatively small number of variables [@pone.0090403-Monteiro1], [@pone.0090403-JonesSmith1], [@pone.0090403-Neuman1], [@pone.0090403-Martorell1], [@pone.0090403-Ziraba1].  Body mass index (BMI in kg/m^2^) was calculated as (weight/height^2^) and the cut off for obesity was defined as a BMI≥30 kg/m^2^. Participants were weighed on a digital scale and their weight recorded in kilograms to the nearest 100 grams.  Height was measured using an anthropometer with standard gradations and recorded to the nearest millimetre. 

Education level was based on self-reported educational attainment recorded by the interviewers.  It was coded into two categories (1 = no/primary education, 2 =  secondary/higher education) for the main part of the analysis to ensure sufficient numbers in the subgroups.  A second analysis was conducted with a three-level education variable (1 = no/primary education, 2 =  secondary, 3 = higher) in the middle-income countries to add further differentiation to the education variable and examine dose-response.  Age group in ten year bands and parity (number of children) were included as biological confounders [@pone.0090403-Brooks1], and urban/rural residence as a simple adjustment for environmental exposures. 

Parity was used as a categorical variable with four groups (0; 1--3; 4--6; 7+).  Parity is thought to be an important factor related to obesity in high income countries [@pone.0090403-Wolfe1] and low-and-middle income countries (LMICs) [@pone.0090403-Brooks1].  Women with a greater number of children are more susceptible to excess weight due to a number of factors including physiological and psychological factors.  LMICs have much higher fertility rates than HICs as well as greater variation in the number of children between women of different social groups and, therefore, parity is likely to have even greater importance as a biological confounder [@pone.0090403-Brooks1]. 

The wealth index is generated for each country separately and places individuals in relative position to each other on a locally appropriate continuous scale of economic status [@pone.0090403-Rutstein1].  It was originally developed to measure the ability to pay for health services but is also used as a general indicator of material circumstances [@pone.0090403-Howe1].  Data on the ownership of durable assets such as electrical equipment (e.g. TV, computer), basic amenities (e.g. sanitation, water supply) and housing characteristics (e.g. floor material) are used to generate a wealth index score through principal components analysis based on the Filmer & Pritchett method [@pone.0090403-Rutstein1].  This is a data reduction technique where the correlations between the full set of asset variables are used to generate a number of uncorrelated principal components.  Only the first principal component - the one that explains most of the variance of the indicator variables - is selected to derive a score for each household.  It was divided into quintiles (1 = poorest; 5 = richest) for each country. 

Statistical analysis {#s2d}
--------------------

Each country was analysed separately.  Stata 12 SE® complex survey procedures were used with the survey weights provided with each dataset to account for the design effect and obtain nationally representative prevalence estimates.  To test the hypothesis that education level modified the association between wealth and obesity, an interaction between education and wealth was fitted in the logistic regression models.  Education was used as a categorical variable.  We tested whether the effect of wealth across the quintiles could be adequately described using a single linear term by comparing models with wealth fitted as a categorical or linear term.  This showed that the associations between wealth and obesity were adequately described using wealth as a linear term.  In addition, to check this linearity assumption visually, we plotted the associations, using the log odds ratios, between wealth, education and obesity using wealth as a categorical variable. 

In order to assess for multi-collinearity between the independent variables in the model, variance inflation factors were calculated [@pone.0090403-Harrell1].  The averages of the interaction estimates for the low- and middle-income countries were compared using formal statistical testing. 

Four models are presented.  The first two models provide estimates for the association between each of education and wealth with obesity separately.  The estimates are presented both unadjusted and adjusted for age group, urban/rural residence and parity).  The third model includes both education and wealth.  The fourth model includes education, wealth and an interaction between education and wealth.  The effect of wealth (the effect of an increase in one wealth quintile on the odds of obesity) in the no/primary education group is estimated from this model.  Then, using the interaction estimate for education-by-wealth, we calculated the effect of wealth within the higher education groups.  Likelihood ratio tests comparing the goodness of fit between the third and fourth models allowed the interaction effect between education and wealth to be tested. 

Ethical review {#s2e}
--------------

Demographic and Health Surveys (DHS) data collection procedures were approved by the Measure DHS (Demographic and Health Surveys) (Calverton, MC) Institutional Review Board and by the national body that approves research studies on human studies in each country.  Written consent was obtained by the interviewers from each participant.  The use of the DHS data for this particular study was approved by Measure DHS, and considered exempt from full review by University College London because the study is based on an anonymous, public-use data set with no identifiable information on the survey participants. 

Results {#s3}
=======

[Table 1](#pone-0090403-t001){ref-type="table"} shows details of the seven countries.  Benin, India, Nigeria were low-income (LI) countries, while Egypt, Colombia, Jordan, Peru were middle-income (MI). 

Socio-demographic characteristics {#s3a}
---------------------------------

[Table 2](#pone-0090403-t002){ref-type="table"} shows that the middle-income countries had higher levels of education and more urban populations.  The obesity prevalence was strikingly high in Egypt and Jordan (43.6% and 30.5% respectively) and was more than double that of Peru and Colombia (14.1% and 14.3% respectively) which are richer countries. 

10.1371/journal.pone.0090403.t002

###### Participant sociodemographic characteristic in each country, DHS data. 

![]( pone.0090403.t002){#pone-0090403-t002-2}

                                   Benin     India      Nigeria     Egypt      Jordan      Peru      Colombia                                                                
  ------------------------------- ------- ------------ --------- ------------ -------- ------------ ---------- ------------ ------ ------------ ------- ------------ ------- ------------
  BMI (kg/m^2^)                                                                                                                                                              
  Non-obese                        14090   94.3 (0.3)   109075    97.2 (0.1)   27349    94.0 (0.3)    19146     57.0 (0.6)   2992   69.5 (1.2)   12307   85.7 (0.5)   40573   85.9 (0.2)
  Obese BMI                         793    5.7 (0.3)     3988     2.8 (0.1)     1552    6.0 (0.3)     13126     43.0 (0.6)   1535   30.5 (1.2)   2176    14.3 (0.5)   7136    14.1 (0.2)
  Education                                                                                                                                                                  
  None/primary                     12463   82.9 (0.8)    52274    55.2 (0.6)   16810    54.2 (1.3)    16250     49.1 (0.7)   793    12.7 (0.9)   4462    28.1 (1.3)   13489   24.4 (0.4)
  Secondary/higher                 2420    17.1 (0.8)    60789    44.8 (0.6)   12091    45.8 (1.3)    16022     50.9 (0.7)   3734   87.3 (0.9)   10021   71.9 (1.3)   34220   75.6 (0.4)
  Urban/rural residence                                                                                                                                                      
  Urban                            6407    42.6 (2.1)    51030    32.4 (1.0)    9256    36.4 (1.8)    13349     41.6 (1.5)   3102   84.2 (1.8)   9919    72.9 (2.1)   34210   77.5 (0.8)
  Rural                            8476    57.4 (2.1)    62033    67.6 (1.0)   19645    63.6 (1.8)    18923     58.4 (1.5)   1425   15.8 (1.8)   4564    27.1 (2.1)   13499   22.5 (0.8)
  Age group (years)                                                                                                                                                          
  15--24                           5077    34.6 (0.5)    41156    36.7 (0.2)   10995    37.9 (0.4)     5361     16.3 (0.3)   506    11.8 (0.7)   4903    33.5 (0.5)   14827   30.7 (0.3)
  25--34                           5175    34.7 (0.5)    34726    30.6 (0.2)    8930    31.1 (0.3)    11414     35.4 (0.3)   1726   37.0 (1.1)   4091    28.5 (0.6)   12259   25.6 (0.3)
  35--49                           4631    30.7 (0.4)    37181    32.7 (0.2)    8976    31.0 (0.4)    15497     48.2 (0.4)   2295   51.2 (1.2)   5489    38.0 (0.6)   16864   36.3 (0.3)
  Children born                                                                                                                                                              
  0                                3335    22.9 (0.5)    35590    28.1 (0.2)    8550    30.6 (0.6)     2388     7.1 (0.2)    307    6.4 (0.6)    4466    33.0 (0.7)   16134   35.1 (0.3)
  1--3                             5215    35.3 (0.5)    52839    47.1 (0.3)    8774    30.3 (0.4)    17759     57.2 (0.5)   1693   40.5 (1.1)   6945    47.9 (0.7)   24409   52.6 (0.3)
  4--6                             4055    27.1 (0.4)    20577    20.3 (0.2)    6821    23.4 (0.3)     9386     28.4 (0.3)   1636   37.6 (1.0)   2351    14.9 (0.5)   6010    10.7 (0.2)
  7+                               2278    14.7 (0.4)    4057     4.6 (0.1)     4756    15.6 (0.4)     2739     7.2 (0.2)    891    15.5 (0.9)    721    4.2 (0.3)    1156    1.6 (0.1)
  **Wealth by education level**                                                                                                                                              
  None/primary                                                                                                                                                               
  Poorer 40%                       5334    51.9 (1.6)    23277    70.8 (0.8)   10240    73.0 (1.5)    10338     75.7 (1.0)   563    80.2 (3.0)   2590    74.9 (2.4)   10001   79.0 (0.9)
  Richer 40%                       4510    48.1 (1.6)    15980    29.2 (0.8)    3108    27.0 (1.5)     2753     24.3 (1.0)    82    19.8 (3.0)    711    25.1 (2.4)   1448    21.0 (0.9)
  Secondary/higher                                                                                                                                                           
  Poorer 40%                        153    6.1 (0.7)     5344     16.5 (0.6)    1661    12.7 (1.0)     3032     21.1 (0.9)   1791   48.6 (2.7)   1388    13.9 (1.3)   14421   46.7 (1.0)
  Richer 40%                       2044    93.9 (0.7)    46694    83.5 (0.6)    8190    87.3 (1.0)     9850     78.9 (0.9)   1111   51.4 (2.7)   5970    86.1 (1.3)   12102   53.3 (1.0)

SE  =  standard error of the estimated proportion x 100. 

Obesity prevalence {#s3b}
------------------

[Table 3](#pone-0090403-t003){ref-type="table"} shows that the prevalence of obesity was higher in the wealthier and older women, and tended to be higher in women with a greater number of children.  It increased with education in the poorer countries but decreased with education in the richer countries.  The absolute difference in prevalence between the richest and the poorest wealth groups diminished with increasing education level in the middle-income countries. 

10.1371/journal.pone.0090403.t003

###### Prevalence of obesity by sociodemographic characteristic in each country, DHS data. 

![]( pone.0090403.t003){#pone-0090403-t003-3}

                                   Benin     India      Nigeria     Egypt     Jordan      Peru      Colombia                                                              
  ------------------------------- ------- ------------ --------- ----------- -------- ------------ ---------- ------------ ------ ------------ ------ ------------ ------ ------------
  Education                                                                                                                                                               
  None/primary                      567    4.9 (0.3)     1194     1.7 (0.1)    679     4.4 (0.2)      6682     44.4 (0.7)   355    47.3 (3.3)   799    17.2 (1.1)   2910   21.9 (0.5)
  Secondary/higher                  226    9.8 (0.8)     2794     4.2 (0.2)    873     7.9 (0.4)      6444     41.7 (0.7)   1180   28.0 (1.2)   1377   13.2 (0.5)   4226   11.6 (0.2)
  Wealth quintile                                                                                                                                                         
  Poorest 20%                       30     1.1 (0.2)      31      0.2 (0.0)    104     1.8 (0.2)      1938     30.6 (0.8)   415    30.4 (1.9)    49    4.3 (0.7)    1712   14.0 (0.5)
  Poorer 20%                        41     1.4 (0.2)      73      0.5 (0.1)    134     2.3 (0.2)      2285     37.6 (0.9)   344    27.7 (2.1)   323    9.4 (0.7)    2095   16.1 (0.5)
  Middle 20%                        89     3.2 (0.4)      219     0.9 (0.1)    235     4.1 (0.3)      2654     44.5 (0.9)   362    31.4 (2.7)   626    15.5 (0.9)   1497   14.6 (0.4)
  Richer 20%                        183    5.9 (0.4)      823     2.9 (0.1)    393     6.8 (0.4)      2988     49.2 (1.0)   271    34.7 (2.4)   570    18.0 (1.0)   1101   13.9 (0.5)
  Richest 20%                       450    13.7 (0.7)    2842     8.4 (0.3)    686     12.8 (0.6)     3261     51.4 (1.1)   143    28.4 (4.1)   608    15.6 (0.9)   731    11.9 (0.5)
  Urban/rural residence                                                                                                                                                   
  Urban                             570    9.7 (0.6)     3083     6.1 (0.2)    831     9.5 (0.5)      6416     49.5 (0.8)   1044   29.4 (1.4)   1691   16.2 (0.6)   5048   13.9 (0.2)
  Rural                             223    2.7 (0.2)      905     1.2 (0.1)    721     3.9 (0.2)      6710     38.4 (0.8)   491    36.3 (1.9)   485    9.2 (0.7)    2088   14.9 (0.5)
  Age group                                                                                                                                                               
  15--24                            85     1.8 (0.2)      281     0.5 (0.0)    190     1.7 (0.1)      895      17.8 (0.7)    60    11.8 (2.2)   205    3.9 (0.4)    883    5.3 (0.2)
  25--34                            265    5.5 (0.4)     1071     2.5 (0.1)    516     6.5 (0.4)      3775     34.8 (0.7)   411    21.2 (1.5)   606    13.8 (0.9)   1985   14.7 (0.4)
  35--49                            443    10.3 (0.6)    2636     5.7 (0.2)    846     10.6 (0.5)     8456     57.6 (0.7)   1064   41.5 (1.8)   1365   23.9 (1.1)   4268   23.9 (0.4)
  Children born                                                                                                                                                           
  0                                 83     2.8 (0.4)      444     1.0 (0.1)    239     2.8 (0.2)      653      29.1 (1.2)    72    17.8 (3.4)   201    4.2 (0.5)    856    5.5 (0.2)
  1--3                              304    6.3 (0.4)     2676     4.0 (0.2)    473     6.4 (0.4)      6610     39.4 (0.7)   385    21.6 (1.6)   1255   17.6 (0.8)   4387   17.0 (0.3)
  4--6                              287    7.7 (0.6)      749     2.7 (0.2)    513     8.7 (0.5)      4594     52.0 (0.8)   619    33.0 (1.9)   571    23.7 (1.5)   1597   26.7 (0.8)
  7+                                119    5.2 (0.5)      119     2.1 (0.3)    327     7.3 (0.5)      1269     50.1 (1.2)   459    52.8 (2.8)   149    22.7 (2.7)   296    26.9 (1.8)
  **Wealth by education level**                                                                                                                                           
  None/primary                                                                                                                                                            
  Poorer 40%                        69     1.3 (0.2)      90      0.4 (0.0)    213     2.1 (0.2)      3491     36.8 (0.8)   226    42.3 (3.9)   270    8.7 (0.7)    2027   20.6 (0.6)
  Richer 40%                        415    9.6 (0.5)      944     5.5 (0.3)    316     10.5 (0.6)     1651     60.4 (1.2)    48    56.6 (9.3)   243    34.9 (3.3)   365    24.0 (1.3)
  Secondary/higher                                                                                                                                                        
  Poorer 40%                         2     1.2 (0.9)      14      0.3 (0.1)     25     1.6 (0.4)      732      25.4 (1.0)   533    25.8 (1.3)   102    6.9 (0.9)    1780   10.8 (1.1)
  Richer 40%                        218    11.1 (0.8)    2721     5.8 (0.2)    763     9.7 (0.5)      4598     47.3 (0.9)   366    30.1 (2.4)   935    14.5 (0.7)   1467   12.1 (1.1)

SE  =  standard error of the estimated proportion x 100. 

Separate, independent and interaction effects of education and wealth by level of economic development {#s3c}
------------------------------------------------------------------------------------------------------

The variance inflation factors for the independent variables used in the model were less than three in all countries indicating that multi-collinearity was not a concern for the analysis.  The wealth by education interaction estimates from the logistic regression models were heterogeneous across all seven countries and, in particular, the difference in the average of the interaction estimates in the low-income countries compared with the middle-income countries had a *P*-value of \<0.001, thus, providing strong evidence of a difference between these two groups which are described separately in [Tables 4](#pone-0090403-t004){ref-type="table"} and [5](#pone-0090403-t005){ref-type="table"} respectively. 

10.1371/journal.pone.0090403.t004

###### Separate, independent and interaction effects of education and wealth on obesity in the low-income countries, DHS data. 

![]( pone.0090403.t004){#pone-0090403-t004-4}

                                                                                                                           Benin                                    India                                  Nigeria       
  ----------------------------------------------------------------------------------------------------------------- ------------------- -------------------- ------------------- ------------------- ------------------- -------------------
  **Model using education**                                                                                                                                                                                              
  Education (level)                                                                                                                                                                                                      
  None/primary                                                                                                               1                   1                    1                   1                   1                   1
  Secondary/higher                                                                                                   2.16 (1.84--2.53)   2.01 (1.67--2.44)    2.06 (1.92--2.21)   2.23 (2.07-2.41)    1.84 (1.68--2.04)   2.39 (2.11-2.70)
  Model using wealth                                                                                                                                                                                                     
  Wealth quintile (linear)                                                                                           2.09 (1.94--2.23)   1.99 (1.84--2.16)    2.77 (2.65--2.89)   2.41 (2.30--2.53)   1.76 (1.68--1.83)   1.80 (1.70-1.90)
  **Model both education and wealth**                                                                                                                                                                                    
  Education (level)                                                                                                                                                                                                      
  None/primary                                                                                                                                   1                                        1                                       1
  Secondary/higher                                                                                                                       1.26 (1.04--2.12)                        1.18 (1.09--1.28)                       1.32 (1.16--1.52)
                                                                                                                                                                                                                         
  Wealth quintile (linear)                                                                                                               1.95 (1.79--2.12)                        2.33 (2.23--2.46)                       1.71 (1.62-1.81)
  **Model including education and wealth and a wealth-by-education interaction** [2](#nt109){ref-type="table-fn"}                                                                                                        
  **Wealth effect within education level** [3](#nt110){ref-type="table-fn"}                                                                                                                                              
  None/primary                                                                                                                           1.98 (1.81--2.15)                        2.25 (2.11--2.39)                       1.72 (1.61--1.84)
  Secondary/higher                                                                                                                       1.67 (1.30--2.16)                        2.48 (2.29--2.70)                       1.70 (1.55--1.86)
  Interaction estimate[4](#nt111){ref-type="table-fn"}                                                                                   0.85 (0.65-- 1.10)                       1.10 (1.00--1.21)                       0.99 (0.89--1.10)
  *P*-value for the interaction estimate[5](#nt112){ref-type="table-fn"}                                                                        0.2                                     0.06                                     0.8

Estimates adjusted for age group, urban/rural residence, and parity. 

Estimates for education not shown in this section of the table. 

OR for obesity associated with an increase in one wealth quintile within each education level calculated using the interaction estimate obtained from the model including an interaction between education and wealth. 

Wealth effect in the secondary/higher education divided by the wealth effect in the no/primary education group e.g. for Benin, 0.85 = 1.67/1.98). 

Test of whether the wealth effects differ by education level. 

10.1371/journal.pone.0090403.t005

###### Separate, independent and interaction effects of education and wealth on obesity in the middle-income countries, DHS data. 

![]( pone.0090403.t005){#pone-0090403-t005-5}

                                                                                                                        Egypt                                  Jordan                                   Peru                                  Colombia       
  -------------------------------------------------------------------------------------------------------------- ------------------- ------------------- ------------------- ------------------- ------------------- ------------------- ------------------- -------------------
  **Model using education**                                                                                                                                                                                                                                  
  Education level                                                                                                                                                                                                                                            
  None/primary                                                                                                            1                   1                   1                   1                   1                   1                   1                   1
  Secondary/higher                                                                                                0.96 (0.92--1.00)   1.15 (1.09--1.22)   0.57 (0.49--0.67)   0.98 (0.85--1.12)   0.73 (0.66--0.80)   0.97 (0.86--1.09)   0.51 (0.49--0.54)   0.79 (0.74--0.84)
  Model using wealth                                                                                                                                                                                                                                         
  Wealth quintile (linear)                                                                                        1.28 (1.26--1.30)   1.26 (1.23--1.29)   1.02 (0.98--1.07)   0.95 (0.90--0.99)   1.23 (1.18--1.27)   1.21 (1.15--1.28)   0.96 (0.94--0.98)   0.94 (0.91--0.96)
  **Model using both education and wealth**                                                                                                                                                                                                                  
  Education (level)                                                                                                                                                                                                                                          
  None/primary                                                                                                                                1                                       1                                       1                                       1
  Secondary/higher                                                                                                                    0.86 (0.81--0.92)                       0.86 (0.72--1.02)                       0.84 (0.74--0.95)                       0.81 (0.76--0.86)
                                                                                                                                                                                                                                                             
  Wealth quintile (linear)                                                                                                            1.30 (1.27--1.33)                       0.96 (0.91--1.00)                       1.24 (1.17--1.31)                       0.96 (0.93--0.98)
  **Model including education, wealth and a wealth-by-education interaction** [2](#nt114){ref-type="table-fn"}                                                                                                                                               
  **Wealth effect within education level** [3](#nt115){ref-type="table-fn"}                                                                                                                                                                                  
  None/primary                                                                                                                        1.39 (1.35--1.43)                       1.27 (1.11--1.44)                       1.65 (1.52--1.80)                       1.09 (1.04--1.13)
  Secondary/higher                                                                                                                    1.19 (1.16--1.23)                       0.91 (0.86--0.96)                       1.08 (1.02--1.15)                       0.92 (0.89--.94)
  Interaction estimate[4](#nt116){ref-type="table-fn"}                                                                                0.85 (0.82--0.89)                       0.72 (0.62--0.83)                       0.66 (0.60--0.72)                       0.84 (0.81--0.88)
  *P*-value for the interaction estimate[5](#nt117){ref-type="table-fn"}                                                                   \<0.001                                 \<0.001                                 \<0.001                                 \<0.001

Estimates adjusted for age group, urban/rural residence, and parity. 

Estimates for education not shown in this section of the table. 

OR for obesity associated with an increase in one wealth quintile within each education level calculated using the interaction estimate obtained from the model including an interaction between education and wealth. 

Wealth effect in the secondary/higher education divided by the wealth effect in the no/primary education group e.g. for Egypt, 0.86 = 1.19/1.39). 

Test of whether the wealth effects differ by education level. 

### i.) Low-income countries (Benin, India, and Nigeria) {#s3c1}

The top part of [Table 4](#pone-0090403-t004){ref-type="table"} shows a positive association between each of education and wealth before and after adjustment.  In India (the largest sample), the unadjusted odds of obesity are 2.06 times higher (95%CI: 1.92, 2.21) for the secondary/higher education group *vs.* the group with no/primary education; and 2.23 times higher (95%CI: 2.07, 2.41) after adjustment.  In terms of wealth, the odds of being obese increased by 2.77 times for each increase of one wealth quintile (95%CI: 2.65, 2.89) and remained positive after adjustment (OR; 95%CI: 2.41; 2.30, 2.53).  A similar pattern was observed in Nigeria and Benin. 

The middle part of [Table 4](#pone-0090403-t004){ref-type="table"} shows the independent effects of education and wealth from a model that includes both of these variables.  The effect of education was much smaller in magnitude compared with the first part of the table, but the effect of wealth was little affected.  This suggests that wealth may largely account for the apparent positive association between education and obesity observed in the low-income countries. 

The bottom part of [Table 4](#pone-0090403-t004){ref-type="table"} illustrates the absence of evidence of an interaction (P\>0.05), although the *P-*value for India (*P* = 0.06) was relatively closer to statistical significance than Benin or Nigeria (*P* = 0.2 and 0.8 respectively). 

### ii.)  Middle-income countries (Egypt, Colombia, Jordan, and Peru) {#s3c2}

In contrast to the low-income countries, the associations shown in [Table 5](#pone-0090403-t005){ref-type="table"} between education and obesity in the middle-income countries tended to be negative (OR\<1) both before and after adjustment.  In Colombia (the largest sample), the adjusted OR for the secondary/higher education group compared with the group with no/primary education was 0.79 (95%CI: 0.74--0.84).  There was an inverse wealth-obesity association (adjusted OR; 95%CI: 0.94; 0.91, 0.96). 

The middle part of [Table 5](#pone-0090403-t005){ref-type="table"} shows the independent effects of education and wealth in a model that includes both with the control variables.  In contrast to the low-income countries, the association between education and obesity was inverse (\<1).  In Colombia, the association between wealth and obesity was negative (adjusted OR; 95%CI: 0.96; 0.93, 0.98). 

The results for the regression model including the interaction between education and wealth are shown in the lower part of [Table 5](#pone-0090403-t005){ref-type="table"} as well as [Figure 1](#pone-0090403-g001){ref-type="fig"}.  The comparison of models with wealth fitted as a categorical or linear term showed that the associations between wealth and obesity were adequately described as a linear term. [ Figure 1](#pone-0090403-g001){ref-type="fig"} illustrates these interactions using the log of the adjusted odds ratios and plots the associations between wealth, education and obesity using wealth as a categorical variable.  The plots supported the use of wealth as a linear term.  There was very strong evidence of an interaction for all countries (*P*\<0.001).  In the lowest education group, there was a positive wealth effect in all four countries.  However, in Colombia and Jordan, the wealth effect was negative in the secondary/higher education group (OR; 95%CI: 0.92; 0.89, 0.94 and 0.91; 0.86, 0.96 respectively), while in Egypt and Peru the wealth effect in this group was non-significant.  Of note, in both Jordan and Colombia - the countries with the strongest interaction effect - there is a negative association between wealth and obesity in the model with wealth alone and when wealth and education are mutually adjusted for (see [Tables 5](#pone-0090403-t005){ref-type="table"} and [6](#pone-0090403-t006){ref-type="table"}) rather than a positive association.  For the countries where we were able to split education into three levels, as shown in [Table 6](#pone-0090403-t006){ref-type="table"}, the results show that the positive wealth effect diminished progressively with higher levels of education. 

![ Interaction between education and wealth on the odds of obesity in women in middle-income countries.\
Each point represents the log OR of that combination of education level and wealth quintile compared with the reference category (education level = none/primary and wealth quintile = poorest).  Error bars represent the standard error of the log OR.  All plotted estimates are adjusted for age group urban/rural residence and parity.](pone.0090403.g001){#pone-0090403-g001}

10.1371/journal.pone.0090403.t006

###### Effect of wealth on obesity within three education levels in the middle-income countries, DHS data. 

![]( pone.0090403.t006){#pone-0090403-t006-6}

                                                                                     Egypt              Jordan               Peru              Colombia
  --------------------------------------------------------------------------- ------------------- ------------------- ------------------- -------------------
  **Wealth effect within education level** [3](#nt120){ref-type="table-fn"}                                                               
  None/primary                                                                 1.39 (1.35--1.43)   1.27 (1.11--1.45)   1.65 (1.51--1.80)   1.09 (1.04--1.14)
  Secondary                                                                    1.25 (1.21--1.29)   0.97 (0.90--1.04)   1.15 (1.07--1.25)   0.94 (0.91--0.98)
  Higher                                                                       1.02 (0.93--1.13)   0.84 (0.76--0.93)   1.10 (0.98--1.23)   0.86 (0.82--0.91)
  *P*-value for interaction[4](#nt121){ref-type="table-fn"}                        *\<0.001*           *\<0.001*           *\<0.001*          *\<0.0001*

Model  =  education (three levels)\*wealth quintile (continuous) + age group + urban/rural residence + parity. 

ORs represent the effect of an increase in one wealth quintile on the odds of obesity within each education level. 

Estimates for education not shown. 

Test of whether the wealth effects differ by education level. 

Discussion {#s4}
==========

The objective of this study was to investigate the SES-obesity association in LMICs using two indicators of SES and to test the hypothesis that education may modify the association between wealth and obesity in middle- but not low-income countries.  The findings show that while wealth tended to increase the odds of obesity in all countries, education appeared to have a protective role against the wealth effect in the middle-income countries (Egypt, Jordan, Peru and Colombia) only.  Another finding was that the highest obesity rates were not in the richest countries. 

Comparison with prior studies {#s4a}
-----------------------------

Literature reviews of the SES-obesity association have reported different associations by SES indicator including education and wealth [@pone.0090403-Dinsa1], [@pone.0090403-McLaren1] and a number of single country studies from LMICs have reported separate effects of education and indicators of income or wealth including Peru, the Philippines, China and Brazil [@pone.0090403-Poterico1], [@pone.0090403-Dahly1], [@pone.0090403-Hou1], [@pone.0090403-Monteiro2].  No empirical studies have focused on investigating the relationship between different indicators or how these associations diverge by level of economic development for different indicators, although in a previous study, we have demonstrated an interaction between education and occupation in older Chinese women [@pone.0090403-AitsiSelmi2]. 

The findings in this study corroborate the existence of a changing SES-obesity association dependent on a country\'s level of economic development [@pone.0090403-Sobal1], [@pone.0090403-Monteiro1], [@pone.0090403-JonesSmith1], [@pone.0090403-Dinsa1].  However, two studies claim that DHS data do not provide any evidence of an SES-overweight/obesity reversal [@pone.0090403-Neuman1], [@pone.0090403-Subramanian1].  This may be due to the use of a different outcome (overweight rather than obesity) or the use of fewer middle-income countries compared with a similar study supporting the reversal [@pone.0090403-JonesSmith2].  Notably, the authors place little emphasis on the education variable in their interpretation of the findings and focus on the wealth indicator which could mask the complexity of the social transition experienced in LMICs.  Our findings concur with others emphasising that the social gradient of obesity is positive (high SES-high obesity) in India specifically [@pone.0090403-Subramanian2], but also support the more general notion that obesity is a growing problem among those with lower education in LMICs.  We propose a reinterpretation of the apparently contradictory studies [@pone.0090403-Neuman1], [@pone.0090403-Subramanian1] and suggest that the education-obesity association may reverse before the wealth-obesity association. 

Plausible and competing mechanisms {#s4b}
----------------------------------

There is a generally positive correlation between level of economic development and obesity levels with key correlates being urbanisation, calorie abundance, and women\'s participation in the labour market [@pone.0090403-Swinburn1].  However, urbanisation appears to be less important than previously thought and a rapid rise in obesity levels among rural populations has been reported in middle-income countries recently [@pone.0090403-Wang1], [@pone.0090403-Austin1].  This is reflected in the differences in obesity prevalence by urban and rural residence in this study: the obesity prevalence is higher in both urban and rural areas in middle-income countries compared with low-income countries and the relative difference between the two areas is smaller.  Data from China show that the prevalence of obesity has increased at a faster rate in the poorer rural areas than in the richer urban ones [@pone.0090403-Wang2] and that lower income groups have disproportionately increased their consumption of animal fat and edible oil and reduced their consumption of healthier traditional foods [@pone.0090403-Du1]. 

One explanation is the increasingly widespread availability of processed, high-calorie food and drinks with such extensive supply chains that they are used for the delivery of antiretrovirals in countries where public health infrastructure is inadequate [@pone.0090403-Stuckler1].  Aggressive marketing and strategic pricing in emerging economies are an important source of revenue for transnational corporations whose profits margins are decreasing in the West [@pone.0090403-McKinsey1], [@pone.0090403-Eizenberg1], and new consumers may require greater cognitive resources to navigate these sophisticated economic signals.  Therefore, as populations are increasingly exposed to processed, energy-dense foods, we can expect a general rise in obesity across all socioeconomic groups in middle-income countries, but especially among lower educated urban women. 

The combination of persistent food insecurity in certain geographical areas (rural) and increased calorie availability overall may exacerbate the effects of the nutrition transition.  In environments with longstanding food insecurity, metabolic programming and cultural memes transmitted between generations may favour the accumulation of calories [@pone.0090403-Prentice1], thus explaining the positive association between wealth and obesity.  A rapid integration within the global economy resulting in a sudden influx of high-calorie products may alleviate the drive for calories before public health systems or health knowledge related to non-communicable diseases have taken root.  This may result in a large information asymmetry between buyers and sellers [@pone.0090403-Just1].  Within this environment, having a higher level of education may provide an advantage through cognitive skills that can make up for the information asymmetry.  Knowledge acquisition and information processing skills may assist in correcting cognitive biases created through marketing, thus resulting in clearer risk perception.  In other words, education may extend [capability]{.ul}, defined as a freedom that expands the range of options a person has in deciding what kind of life to lead, as well as developing judgment in relation to the appropriate exercise of choice [@pone.0090403-Saido1]. 

There are a number of other possible pathways for the role of education which have been extensively discussed elsewhere [@pone.0090403-Chandola1], [@pone.0090403-Cutler2].  These include social norms and values since educated women may favour Western norms of thinness as a beauty criterion and use it as a means of social distinction [@pone.0090403-Bartley1].  These norms may be spread or reinforced within the educated elites through social network effects including through educated occupational classes which we could not control for in our analysis [@pone.0090403-Christakis1].  Educated women may come from different family backgrounds and their own mothers may have benefited from better education or food security thus reducing the risk of a metabolic mismatch between early and later life [@pone.0090403-Gluckman1].  Finally, there is a link between marital status and obesity in high-income countries and educated women may be more likely to be unmarried.  However, marital status did not explain the SES-obesity association in women in other LMICs [@pone.0090403-Xiao1]. 

Strengths and limitations {#s4c}
-------------------------

The DHS datasets benefit from a highly standardised survey methodology and the results were remarkably consistent within country income groups.  The cross-sectional nature of the data limits temporal and causal inferences, although this investigation did not seek to provide a causal analysis but to examine differences in patterns of association by level of economic development.  Further research could investigate causal explanations for the country differences and/or possible pathways of explanation for the inverse education-obesity pathways in middle-income countries i.e. why are there opposite associations between education and wealth/income and obesity?  Education may measure different things in different countries and women\'s occupation, marital status, body shape preference and husband\'s SES may have a greater or lesser importance depending on the country context. 

It is also possible that reverse causality and health selection may be operating and that obesity determines educational and wealth opportunities.  The pathways in this sample of countries are likely to be complex and vary from country to country.  In Colombia, it is possible that being thin confers a social advantage while being obese is stigmatised, while the opposite might be the case in a low-income country like Benin.  These cultural preferences are likely to vary by region (urban/rural) and by social group so that a more detailed country analysis and longitudinal data would be required to disentangle the direction of causality.  However, this study aimed to engage with the current literature on the reversal of the SES-obesity gradient in women and makes a step forward in elucidating the complex social epidemiology of obesity in transition settings. 

Finally, women under 17 years will not have had the opportunity to enter university and achieve the highest level of education, thus leading to the possibility of misclassification of education level.  However, the number of women in this group was relatively small and is unlikely to change the patterns observed in these relatively large country samples. 

Conclusion {#s4d}
----------

This study sought to separate the effects of women\'s education and wealth in relation to obesity.  The findings support other studies documenting different SES-obesity associations and that the SES-obesity gradient reverses by level of economic development.  The findings also support the hypothesis that in middle-income countries education may protect against the obesogenic effects of wealth.  We propose that the education gradient may reverse before the wealth gradient.  These findings are particularly pertinent to countries where a rapid integration within the global food market may be occurring.  In these settings, the combination of a longstanding metabolic and psychological drive for calorie accumulation combined with a sudden influx of heavily marketed high-calorie products, while public health systems are ill-equipped to deal with an emerging non-communicable disease burden, might exacerbate the asymmetry of information between sellers and buyers.  This may call for strengthening of global and national governance systems overseeing markets and public health infrastructure alongside promoting access to formal education for women [@pone.0090403-Labonte1].  From this perspective, investment in women\'s education may be viewed as a public health intervention to address obesity and related diseases benefiting from synergies with multiple other development agendas. 

[^1]: **Competing Interests:**The authors have declared that no competing interests exist. 

[^2]: Conceived and designed the experiments: AA-S MJS MGM.  Performed the experiments: AA-S. Analyzed the data: AA-S. Contributed reagents/materials/analysis tools: RB.  Wrote the paper: AA-S MJS.