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<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group>
<journal-title>PLoS ONE</journal-title></journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc></publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="publisher-id">PONE-D-13-37881</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0094299</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology and life sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Comparative anatomy</subject></subj-group></subj-group><subj-group><subject>Nutrition</subject></subj-group><subj-group><subject>Physiology</subject><subj-group><subject>Physiological parameters</subject><subj-group><subject>Body weight</subject><subj-group><subject>Obesity</subject></subj-group></subj-group></subj-group></subj-group><subj-group><subject>Population biology</subject></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine and health sciences</subject><subj-group><subject>Epidemiology</subject><subj-group><subject>Pediatric epidemiology</subject></subj-group></subj-group><subj-group><subject>Pediatrics</subject><subj-group><subject>Adolescent medicine</subject><subject>Child health</subject></subj-group></subj-group><subj-group><subject>Public and occupational health</subject><subj-group><subject>Behavioral and social aspects of health</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Research and analysis methods</subject><subj-group><subject>Research design</subject><subj-group><subject>Clinical research design</subject><subject>Cross-sectional studies</subject></subj-group></subj-group></subj-group></article-categories>
<title-group>
<article-title>Trends in a Life Threatening Condition: Morbid Obesity in Dutch, Turkish and Moroccan Children in The Netherlands</article-title>
<alt-title alt-title-type="running-head">Morbid Obesity in Children in The Netherlands</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>van Dommelen</surname><given-names>Paula</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib>
<contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Schönbeck</surname><given-names>Yvonne</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib>
<contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>van Buuren</surname><given-names>Stef</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib>
<contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>HiraSing</surname><given-names>Remy A.</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib>
</contrib-group>
<aff id="aff1"><label>1</label><addr-line>Department of Life Style, TNO, Leiden, The Netherlands</addr-line></aff>
<aff id="aff2"><label>2</label><addr-line>Department of Child Health, TNO, Leiden, The Netherlands</addr-line></aff>
<aff id="aff3"><label>3</label><addr-line>Department of Methodology and Statistics, University Utrecht, Utrecht, The Netherlands</addr-line></aff>
<aff id="aff4"><label>4</label><addr-line>EMGO Institute of Health Care Research, VU University Medical Centre Amsterdam, Amsterdam, The Netherlands</addr-line></aff>
<contrib-group>
<contrib contrib-type="editor" xlink:type="simple"><name name-style="western"><surname>Bruce</surname><given-names>Amanda</given-names></name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"/></contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Missouri-Kansas City, United States of America</addr-line></aff>
<author-notes>
<corresp id="cor1">* E-mail: <email xlink:type="simple">Paula.vanDommelen@tno.nl</email></corresp>
<fn fn-type="conflict"><p>The authors have declared that no competing interests exist.</p></fn>
<fn fn-type="con"><p>Conceived and designed the experiments: PvD YS SvB RAH. Performed the experiments: PvD. Analyzed the data: PvD. Contributed reagents/materials/analysis tools: PvD YS SvB. Wrote the paper: PvD YS SvB RAH.</p></fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year></pub-date>
<pub-date pub-type="epub"><day>14</day><month>4</month><year>2014</year></pub-date>
<volume>9</volume>
<issue>4</issue>
<elocation-id>e94299</elocation-id>
<history>
<date date-type="received"><day>31</day><month>8</month><year>2013</year></date>
<date date-type="accepted"><day>14</day><month>3</month><year>2014</year></date>
</history>
<permissions>
<copyright-year>2014</copyright-year>
<copyright-holder>van Dommelen et al</copyright-holder><license xlink:type="simple"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/" xlink:type="simple">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions>
<abstract><sec>
<title>Background</title>
<p>Morbid obesity can be a life threatening condition. The aim of our study is to assess the trend in morbid obesity in The Netherlands among children of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997.</p>
</sec><sec>
<title>Methods and Findings</title>
<p>Cross-sectional height and weight data of children of Dutch, Turkish and Moroccan origin aged 2–18 years were selected from three national Dutch Growth Studies performed in 1980, 1997 and 2009 (n = 54,814). Extended international (IOTF) cut-offs in childhood were used to define morbid obesity (obesity class II and III combined). The morbidity index for overweight was calculated as the prevalence of morbid obesity divided by the prevalence of overweight. Our study showed that the prevalence of morbid obesity in children of Dutch origin was 0.59% in boys and 0.53% in girls in 2009. Significant upward trends occurred since 1980 and 1997. The prevalence was three to four fold higher in Turkish children compared to Dutch children. The Turkish children also had an upward trend since 1997, but this was only statistically significant in boys. The prevalence of morbid obesity in Moroccan children was two to three fold higher than in Dutch children, but it remained almost stable between 1997 and 2009. The Dutch and Turkish children showed an upward trend in morbidity index for overweight since respectively 1980 and 1997, while the Moroccan children showed a downward trend since 1997. In 2009, children of low educated parents had the highest prevalence rates of morbid obesity; 1.06% in Dutch, 2.11% in Turkish and 1.41% in Moroccan children.</p>
</sec><sec>
<title>Conclusions and Significance</title>
<p>An upward trend of morbid obesity in Dutch and Turkish children in The Netherlands occurred. Monitoring and reducing the prevalence of childhood morbid obesity is of high importance for these children, health care and the community.</p>
</sec></abstract>
<funding-group><funding-statement>The authors have no support or funding to report.</funding-statement></funding-group><counts><page-count count="5"/></counts></article-meta>
</front>
<body><sec id="s1">
<title>Introduction</title>
<p>Over the past three decades childhood overweight and obesity have reached epidemic proportions in most industrialized countries <xref ref-type="bibr" rid="pone.0094299-World1">[1]</xref>. Although the Dutch prevalence rates of childhood overweight and obesity are still low compared to other developed countries <xref ref-type="bibr" rid="pone.0094299-Livingstone1">[2]</xref>, <xref ref-type="bibr" rid="pone.0094299-Schnbeck1">[3]</xref>, both rates were higher than in 1980. In 2009, fourteen percent of Dutch children were overweight and two percent were obese <xref ref-type="bibr" rid="pone.0094299-Schnbeck1">[3]</xref>. This is a two to three fold higher prevalence in overweight and four to six fold increase in obesity since 1980 <xref ref-type="bibr" rid="pone.0094299-Roede1">[4]</xref>. Upward trends were also found in the two largest ethnic minorities in The Netherlands originating from Turkey and Morocco.</p>
<p>Obesity is a leading preventable cause of chronic illnesses and death and has emerged as one of the most serious public health concerns in the 21st century <xref ref-type="bibr" rid="pone.0094299-Barness1">[5]</xref>. Excessive body weight is associated with various diseases like cardiovascular diseases, diabetes mellitus type 2, and certain types of cancer <xref ref-type="bibr" rid="pone.0094299-Haslam1">[6]</xref>. The risks increase with higher BMI levels at the upper end of the distribution <xref ref-type="bibr" rid="pone.0094299-ProspectiveStudies1">[7]</xref>. Obesity has been found to reduce life expectancy by two to four years, while morbid obesity even reduces life expectancy by ten years <xref ref-type="bibr" rid="pone.0094299-ProspectiveStudies1">[7]</xref>. Therefore, in adults obesity has been broken down into three classes; class I obesity (30.0–34.9 kg/m<sup>2</sup>), class II obesity (35.0–39.9 kg/m<sup>2</sup>) and class III obesity (≥40.0 kg/m<sup>2</sup>). Only recently, in 2012, extended international (IOTF) cut-offs for childhood obesity classes II and III were presented <xref ref-type="bibr" rid="pone.0094299-Cole1">[8]</xref>. Also in children, morbid obesity can be a life threatening condition <xref ref-type="bibr" rid="pone.0094299-Molnr1">[9]</xref>. Childhood morbid obesity often causes hypertension, dyslipidemia, insulin resistance/diabetes, fatty liver disease, and psychosocial complications <xref ref-type="bibr" rid="pone.0094299-vanEmmerik1">[10]</xref>. In a study in 2005–2007 in The Netherlands among 307 children with severely obesity, 56% had hypertension and 67% had at least one cardiovascular risk factor <xref ref-type="bibr" rid="pone.0094299-Daniels1">[11]</xref>. A study among 230,000 Norwegian adolescents showed that morbid obesity was associated with increased mortality in middle age from a wide variety of systemic diseases <xref ref-type="bibr" rid="pone.0094299-Bjrge1">[12]</xref>.</p>
<p>The aim of our study is to apply the extended international (IOTF) cut-offs on the national Dutch growth studies to assess the trend in morbid obesity (class II and III combined) in The Netherlands among children of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997. The Dutch growth studies offer a unique opportunity to study trends covering the time period before which the worldwide obesity epidemic emerged.</p>
</sec><sec id="s2" sec-type="methods">
<title>Methods</title>
<sec id="s2a">
<title>Ethics Statement</title>
<p>Data collection of growth studies is part of routine youth health care in The Netherlands, and is not regarded as medical research. In the Dutch nationwide surveys, written informed consent was not needed. Verbal consent was obtained from each child (and parent for children younger than 16 years) before measurement. To document the process, cooperation, or lack thereof, was registered on the questionnaire. The Medical Ethical Review Board of Leiden University Medical Centre approved of the study and the way consent was obtained.</p>
</sec><sec id="s2b">
<title>Data</title>
<p>Cross-sectional height and weight data of children of Dutch, Turkish and Moroccan origin aged 2–18 years living in The Netherlands were selected from the Third Growth Study in 1980 (n = 30,020) <xref ref-type="bibr" rid="pone.0094299-Roede1">[4]</xref>, the Fourth Growth Study in 1997 (n = 13,900) <xref ref-type="bibr" rid="pone.0094299-Fredriks1">[13]</xref> and the Fifth Growth Study in 2009 (n = 10,894) <xref ref-type="bibr" rid="pone.0094299-Schnbeck1">[3]</xref>. Data were obtained at Well Baby Clinics, Municipal Health Services (MHS), schools and a festival (in 1997 and 2009). To obtain sufficient samples of Turkish and Moroccan children, oversampling was done in the four major cities Amsterdam, Rotterdam, The Hague, and Utrecht, where most children of Turkish and Moroccan origin in The Netherlands live. Measurements in all Dutch Growth studies were identical and were standardized and performed by trained health care professionals. Height was measured to the nearest 0.1 cm. Children were weighed, wearing underwear only, or a correction was made for clothes, on calibrated mechanical or electronic step scales. Weight was rounded to the nearest 0.1 kg. Children with diagnosed growth disorders and those on medication known to interfere with growth were excluded from these surveys. More details on the design of these surveys have been published before <xref ref-type="bibr" rid="pone.0094299-Schnbeck1">[3]</xref>, <xref ref-type="bibr" rid="pone.0094299-Roede1">[4]</xref>, <xref ref-type="bibr" rid="pone.0094299-Fredriks1">[13]</xref>.</p>
</sec><sec id="s2c">
<title>Statistical analyses</title>
<p>Dutch origin was defined as both mother and father born in The Netherlands, Turkish origin was defined as mother born in Turkey, or mother born in The Netherlands and father born in Turkey. Similarly, Moroccan origin was defined as mother born in Morocco, or mother born in The Netherlands and father born in Morocco. Parental education was defined as the educational level of the highest educated parent and categorized into low, medium and high <xref ref-type="bibr" rid="pone.0094299-Verweij1">[14]</xref>. Prevalence rates for morbid obesity were calculated with the extended international (IOTF) cut-offs (class II and III combined) for children <xref ref-type="bibr" rid="pone.0094299-Cole1">[8]</xref>. These cut-offs were obtained by a centile at the growth curve of six large nationally representative cross-sectional growth studies, including The Third Dutch Growth Study in 1980 <xref ref-type="bibr" rid="pone.0094299-Roede1">[4]</xref>. At age 18 years, this centile passed through the cut-off point of 35 kg/m<sup>2</sup> for adults class II obesity. Since the number of children was not evenly distributed across age years, we first calculated the prevalence rates per year of age, and then averaged these rates. Chi-square and Fisher's exact tests were performed to test for differences in prevalence rates. A log-binomial model was used to test if differences in prevalence rates between ethnic groups in 2009 are due to differences in the educational level of the parents, after adjustment for sex and age of the child. P-values &lt;0.05 (two-sided) were considered statistically significant. As the risk of morbidity in overweight children increases with higher BMI, we calculated the morbidity index for overweight. The morbidity index is used in other studies to categorize the severity of a disease, for example diabetes mellitus <xref ref-type="bibr" rid="pone.0094299-Kaplan1">[15]</xref> and coronary risk factors <xref ref-type="bibr" rid="pone.0094299-Hsieh1">[16]</xref>. In our study, the morbidity index for overweight was calculated as the prevalence of morbid obesity divided by the prevalence of overweight expressed as a percentage. The statistical analyses were performed in SPSS version 20.0 for Windows (SPSS Inc., Chicago, IL, USA).</p>
</sec></sec><sec id="s3">
<title>Results</title>
<sec id="s3a">
<title>Morbid obesity in children of Dutch origin</title>
<p><xref ref-type="fig" rid="pone-0094299-g001">Figure 1</xref> and <xref ref-type="table" rid="pone-0094299-t001">Table 1</xref> show the trend in morbid obesity in The Netherlands among children of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997. <xref ref-type="table" rid="pone-0094299-t001">Table 1</xref> shows that the overall trends and prevalence rates were almost similar between boys and girls of Dutch origin. Between 1980 and 1997 there has been an upward trend in the prevalence of morbid obesity in boys and girls of Dutch origin (respectively, p&lt;0.001 and p&lt;0.01). Upward trends were also found between 1997 and 2009 in boys and girls (both p&lt;0.05). Almost in all age groups, there has been an increase in the prevalence of morbid obesity. In 2009, 0.59% in boys and 0.53% in girls were morbidly obese.</p>
<fig id="pone-0094299-g001" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0094299.g001</object-id><label>Figure 1</label><caption>
<title>The trend in morbid obesity in The Netherlands among children of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997.</title>
</caption><graphic mimetype="image" xlink:href="info:doi/10.1371/journal.pone.0094299.g001" position="float" xlink:type="simple"/></fig><table-wrap id="pone-0094299-t001" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0094299.t001</object-id><label>Table 1</label><caption>
<title>The trend in morbid obesity in The Netherlands among children of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997.</title>
</caption><alternatives><graphic id="pone-0094299-t001-1" position="float" mimetype="image" xlink:href="info:doi/10.1371/journal.pone.0094299.t001" xlink:type="simple"/>
<table><colgroup span="1"><col align="left" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/></colgroup>
<thead>
<tr>
<td align="left" rowspan="1" colspan="1">Group</td>
<td align="left" rowspan="1" colspan="1">Age (y)</td>
<td align="left" rowspan="1" colspan="1">% of morbid obesity (N) in 1980</td>
<td align="left" rowspan="1" colspan="1">% of morbid obesity (N) in 1997</td>
<td align="left" rowspan="1" colspan="1">% of morbid obesity (N) in 2009</td>
</tr>
</thead>
<tbody>
<tr>
<td align="left" rowspan="1" colspan="1">Dutch boys</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1">0.14 (4943)</td>
<td align="left" rowspan="1" colspan="1">0.44 (961)</td>
<td align="left" rowspan="1" colspan="1">0.53 (757)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1">0.12 (4611)</td>
<td align="left" rowspan="1" colspan="1">0.37 (1367)</td>
<td align="left" rowspan="1" colspan="1">0.62 (1158)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1">0.00 (5818)</td>
<td align="left" rowspan="1" colspan="1">0.08 (2667)</td>
<td align="left" rowspan="1" colspan="1">0.60 (1210)**</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1">0.07 (15372)</td>
<td align="left" rowspan="1" colspan="1">0.27 (4995)***</td>
<td align="left" rowspan="1" colspan="1">0.59 (3125)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Dutch girls</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1">0.32 (4747)</td>
<td align="left" rowspan="1" colspan="1">0.37 (980)</td>
<td align="left" rowspan="1" colspan="1">1.00 (817)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1">0.03 (4609)</td>
<td align="left" rowspan="1" colspan="1">0.05 (1361)</td>
<td align="left" rowspan="1" colspan="1">0.63 (1318)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1">0.00 (5292)</td>
<td align="left" rowspan="1" colspan="1">0.34 (2292)***</td>
<td align="left" rowspan="1" colspan="1">0.17 (1360)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1">0.08 (14648)</td>
<td align="left" rowspan="1" colspan="1">0.24 (4633)**</td>
<td align="left" rowspan="1" colspan="1">0.53 (3495)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Turkish boys</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.37 (194)</td>
<td align="left" rowspan="1" colspan="1">4.58 (543)**</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.84 (400)</td>
<td align="left" rowspan="1" colspan="1">2.53 (281)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.59 (525)</td>
<td align="left" rowspan="1" colspan="1">1.36 (255)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.04 (1119)</td>
<td align="left" rowspan="1" colspan="1">2.53 (1079)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Turkish girls</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.06 (156)</td>
<td align="left" rowspan="1" colspan="1">1.54 (501)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.66 (399)</td>
<td align="left" rowspan="1" colspan="1">3.50 (291)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.90 (469)</td>
<td align="left" rowspan="1" colspan="1">0.27 (244)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.27 (1024)</td>
<td align="left" rowspan="1" colspan="1">1.71 (1036)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Moroccan boys</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">2.66 (179)</td>
<td align="left" rowspan="1" colspan="1">1.78 (485)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.67 (390)</td>
<td align="left" rowspan="1" colspan="1">0.43 (371)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.35 (507)</td>
<td align="left" rowspan="1" colspan="1">1.22 (204)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.00 (1076)</td>
<td align="left" rowspan="1" colspan="1">1.07 (1060)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Moroccan girls</td>
<td align="left" rowspan="1" colspan="1">2–5 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">2.84 (187)</td>
<td align="left" rowspan="1" colspan="1">2.24 (444)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6–11 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.99 (384)</td>
<td align="left" rowspan="1" colspan="1">1.25 (403)</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">12–18 y</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">0.29 (482)</td>
<td align="left" rowspan="1" colspan="1">1.65 (252)*</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">Total</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">1.49 (1053)</td>
<td align="left" rowspan="1" colspan="1">1.65 (1099)</td>
</tr>
</tbody>
</table>
</alternatives></table-wrap></sec><sec id="s3b">
<title>Morbid obesity in children of Turkish origin</title>
<p><xref ref-type="table" rid="pone-0094299-t001">Table 1</xref> shows that the prevalence of morbid obesity is higher in Turkish children compared to the Dutch. An upward trend was noticed in Turkish boys between 1997 and 2009 (p&lt;0.05). In 2009, 2.53% of the Turkish boys were morbidly obese. In 2009, the prevalence in Turkish girls was slightly higher (1.71%) than in 1997 (1.27%). There was a rise in the prevalence up to twelve years of age, significantly in 2–5 year old boys (p&lt;0.01) and 6–11 year old girls (p&lt;0.05).</p>
</sec><sec id="s3c">
<title>Morbid obesity in children of Moroccan origin</title>
<p>The overall prevalence of morbid obesity in Moroccan boys and girls remained almost stable over time (see <xref ref-type="table" rid="pone-0094299-t001">Table 1</xref>). However, in the age group 12–18 years, there was an upward trend in girls (p&lt;0.05) and a (non-significant) upward trend in boys, while the other age groups showed a (non-significant) downward trend. In all age groups, girls had higher prevalence rates than boys in 2009. The overall prevalence of morbid obesity in 2009 was 1.07% in boys and 1.65% in girls.</p>
</sec><sec id="s3d">
<title>Morbidity index for overweight</title>
<p><xref ref-type="table" rid="pone-0094299-t002">Table 2</xref> presents the morbidity index for overweight among Dutch children between 1980 and 2009 and among Turkish and Moroccan children between 1997 and 2009. In 2009, the highest morbidity index for overweight was found in Turkish boys (7.76%). Moroccan and Turkish girls had the second and third highest morbidity index for overweight of respectively 5.83% and 5.48%. The lowest morbidity index for overweight (3.61%) was found in Dutch girls. The Dutch and Turkish children showed an upward trend in morbidity index for overweight since respectively 1980 and 1997, while the Moroccan children showed a downward trend since 1997.</p>
<table-wrap id="pone-0094299-t002" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0094299.t002</object-id><label>Table 2</label><caption>
<title>The trend in morbidity index for overweight defined as the prevalence of morbid obesity divided by the prevalence of overweight (%) in The Netherlands among children (2–18 years) of Dutch origin since 1980, and among children of Turkish and Moroccan origin since 1997.</title>
</caption><alternatives><graphic id="pone-0094299-t002-2" position="float" mimetype="image" xlink:href="info:doi/10.1371/journal.pone.0094299.t002" xlink:type="simple"/>
<table><colgroup span="1"><col align="left" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/><col align="center" span="1"/></colgroup>
<thead>
<tr>
<td align="left" rowspan="1" colspan="1"/>
<td colspan="3" align="left" rowspan="1">Boys</td>
<td colspan="3" align="left" rowspan="1">Girls</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Ethnicity</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 1980</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 1997</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 2009</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 1980</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 1997</td>
<td align="left" rowspan="1" colspan="1">MI-O (%) in 2009</td>
</tr>
</thead>
<tbody>
<tr>
<td align="left" rowspan="1" colspan="1">Dutch</td>
<td align="left" rowspan="1" colspan="1">1.52</td>
<td align="left" rowspan="1" colspan="1">3.03</td>
<td align="left" rowspan="1" colspan="1">4.72</td>
<td align="left" rowspan="1" colspan="1">1.13</td>
<td align="left" rowspan="1" colspan="1">2.09</td>
<td align="left" rowspan="1" colspan="1">3.61</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Turkish</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">4.37</td>
<td align="left" rowspan="1" colspan="1">7.76</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">4.31</td>
<td align="left" rowspan="1" colspan="1">5.48</td>
</tr>
<tr>
<td align="left" rowspan="1" colspan="1">Moroccan</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6.33</td>
<td align="left" rowspan="1" colspan="1">4.31</td>
<td align="left" rowspan="1" colspan="1"/>
<td align="left" rowspan="1" colspan="1">6.39</td>
<td align="left" rowspan="1" colspan="1">5.83</td>
</tr>
</tbody>
</table>
</alternatives><table-wrap-foot><fn id="nt101"><label/><p>MI-O: Morbidity Index for Overweight.</p></fn></table-wrap-foot></table-wrap></sec><sec id="s3e">
<title>Morbid obesity and educational level in 2009</title>
<p>In 2009, 18% of Dutch children had low educated parents, while this was 58% in Turkish and 60% in Moroccan children. Dutch children of low educated parents had the highest prevalence of morbid obesity (1.06%), while those of medium and high educated parents had the lowest prevalence rates of morbid obesity (respectively 0.51% and 0.16%). Similar results were found in children of Turkish and Moroccan origin. For Turkish children, the prevalence of morbid obesity was 2.11% in low educated parents, 1.09% in medium, and 1.10% in high educated parents. In Moroccan children, these rates were respectively 1.41%, 0.68%, and 1.16%. After adjustment for educational level, the differences in morbid obesity rates between Turkish and Dutch children (from relative risk (RR) = 4.1, 95%CI(2.7–6.3) to RR = 2.0, 95%CI(0.97–4.3)) and between Moroccan and Dutch children (from RR = 2.7, 95%CI(1.7–4.4) to RR = 1.3, 95%CI(0.5–3.1)) were less pronounced.</p>
</sec></sec><sec id="s4">
<title>Discussion</title>
<p>This study is the first that presents trends of morbid obesity based on the extended international (IOTF) cut-offs in Dutch children, and also in Turkish and Moroccan children living in The Netherlands. We showed that the prevalence of morbid obesity in children of Dutch origin was 0.59% in boys and 0.53% in girls in 2009. Significant upward trends occurred since 1980 and 1997. The prevalence rates were much higher in children of Turkish (2.53% in boys and 1.71% in girls) and Moroccan (1.07% in boys and 1.65% in girls) origin in 2009. Turkish children showed an upward trend before twelve years of age, while the results of the Moroccan children showed the opposite; an upward trend aged twelve years onwards. The morbidity index for overweight was highest among the Turkish and Moroccan children, which reveals that overweight is more severe in children of Turkish and Moroccan origin compared to children of Dutch origin. The severity of overweight increased between 1980 and 2009 in Dutch children, and between 1997 and 2009 in Turkish children, while a decrease between 1997 and 2009 was observed in Moroccan children. Part of the ethnic differences in morbid obesity rates can be explained by the educational level of the parents, as more Turkish and Moroccan children have low educated parents and morbid obesity is more prevalent among children of low educated parents.</p>
<p>The extended (IOTF) cut-offs encourage direct comparison of trends in child morbid obesity worldwide. The cut-offs are less arbitrary and more internationally applicable than other definitions, such as centiles on the United States (US) growth charts <xref ref-type="bibr" rid="pone.0094299-Kuczmarski1">[17]</xref>. Until now, the prevalence of morbid obesity by the extended international (IOTF) cut-offs has only been reported in one study in New Zealand <xref ref-type="bibr" rid="pone.0094299-Farrant1">[18]</xref>. This study was limited to secondary school students and did not report information on trends. They showed that among 9,107 secondary school students in 2007, the prevalence of morbid obesity was 2.5%. Our study showed that the prevalence of morbid obesity in secondary school children of Dutch, Turkish and Moroccan origin was much lower in 2009 than the New Zealand secondary school children in 2007. Other studies applied as cut-off for extreme or severe obesity the 99<sup>th</sup> percentile or a BMI≥120% of the 95<sup>th</sup> percentile <xref ref-type="bibr" rid="pone.0094299-Pan1">[19]</xref>, <xref ref-type="bibr" rid="pone.0094299-Lo1">[20]</xref> for age and sex according to the growth charts of the 2000 Center for Disease Control (CDC) <xref ref-type="bibr" rid="pone.0094299-Kuczmarski1">[17]</xref>, which complicates a fair comparison. At eighteen years, a BMI≥120% of the 95<sup>th</sup> CDC growth chart corresponds to a BMI of 34.8 kg/m<sup>2</sup> in boys and 36.4 kg/m<sup>2</sup> in girls. A study in millions of US pre-school children living in low-income families showed that the prevalence of extreme obesity (≥120% of the P95 CDC) increased from 1.75% in 1998 to 2.22% in 2003 and decreased to 2.07% in 2010 <xref ref-type="bibr" rid="pone.0094299-Pan1">[19]</xref>. Another study among 42,559 US children aged 3–5 years between 2007 and 2010 reported a prevalence of extreme obesity (≥120% of the P95 CDC) of 1.6% <xref ref-type="bibr" rid="pone.0094299-Lo1">[20]</xref>. Among US children aged 2 to 19 years, the prevalence of extreme obesity (≥P99 CDC) was 3.8% <xref ref-type="bibr" rid="pone.0094299-Skelton1">[21]</xref> and in 6.9% of U.S. sixth graders in the HEALTHY cohort <xref ref-type="bibr" rid="pone.0094299-Marcus1">[22]</xref>. A study in New Zealand among 3,275 schoolchildren aged 4–15 year showed that the prevalence of extreme obesity (≥P99 CDC) was 2.7% in 2002 <xref ref-type="bibr" rid="pone.0094299-Goulding1">[23]</xref>.</p>
<p>In agreement with our study, high differences in prevalence rates among ethnic groups within countries were reported <xref ref-type="bibr" rid="pone.0094299-Farrant1">[18]</xref>–<xref ref-type="bibr" rid="pone.0094299-Goulding1">[23]</xref>. In our study part of the ethnic differences in morbid obesity rates can be explained by the educational level of the parents. Families with low educated parents may lack resources, both economical and knowledge, which can reduce their ability to control weight gain by making healthy food choices and taking opportunities for physical activity <xref ref-type="bibr" rid="pone.0094299-Clarke1">[24]</xref>–<xref ref-type="bibr" rid="pone.0094299-Hosper1">[26]</xref>. Ethnic differences in morbid obesity may also be explained by differences in cultural opinions about body shape and acceptable weight gain <xref ref-type="bibr" rid="pone.0094299-Nicolaou1">[27]</xref>–<xref ref-type="bibr" rid="pone.0094299-Doolen1">[29]</xref>. Also, cultural and religious norms influencing dietary and physical activity patterns may play a role <xref ref-type="bibr" rid="pone.0094299-Nicolaou1">[27]</xref>–<xref ref-type="bibr" rid="pone.0094299-Doolen1">[29]</xref>. It is reported that children of Turkish origin in The Netherlands watch more TV <xref ref-type="bibr" rid="pone.0094299-Veldhuis1">[30]</xref>, play less outdoor <xref ref-type="bibr" rid="pone.0094299-Kocken1">[31]</xref>, have a higher snack intake <xref ref-type="bibr" rid="pone.0094299-Kocken1">[31]</xref>, and less often have breakfast <xref ref-type="bibr" rid="pone.0094299-Veldhuis1">[30]</xref> compared to children of Dutch origin. All these results show that interventions or prevention programs should pay attention to the cultural aspects and educational level of the targeted population.</p>
<p>A particular strength of our study is the consistent methodology and inclusion/exclusion criteria, and objective measurements of height and weight in the large national growth studies between 1980 and 2009. The baseline growth study was performed in 1980, before the worldwide obesity epidemic started. Therefore, the growth studies offer a unique opportunity to monitor trends in a period of increasing levels of BMI. The data were collected from all regions in The Netherlands and are, therefore, assumed to be generalizable for the results of The Netherlands. A limitation of our study is that we only present the prevalence rates of morbid obesity in children of Turkish and Moroccan origin in 1997 and 2009, since the 1980 study did not provide a sufficiently large sample of children of Turkish and Moroccan origins. Another limitation is the limited sample size within the three age categories of the Turkish and Moroccan children that complicates a good insight into age-related trends. Further research is needed to evaluate the trends of morbid obesity within age categories of children of non-Dutch origin.</p>
<p>An upward trend in overweight and obesity between 1980 and 2009 was already reported in The Netherlands <xref ref-type="bibr" rid="pone.0094299-Schnbeck1">[3]</xref>. Our findings show upward trends in morbid obesity as well. Monitoring and reducing the prevalence of childhood morbid obesity is of high importance for these children, health care and the community. Childhood obesity leads to chronic illnesses <xref ref-type="bibr" rid="pone.0094299-vanEmmerik1">[10]</xref>, <xref ref-type="bibr" rid="pone.0094299-Daniels1">[11]</xref> and increased risk of mortality in middle age <xref ref-type="bibr" rid="pone.0094299-Bjrge1">[12]</xref>. Therefore, an upward trend in morbid obesity and morbidity index for overweight may have a higher impact on health costs, than an upward trend in overweight. For this reason, it is important to monitor not only overweight, but also morbid obesity and the morbidity index for overweight. The Partnership Overweight Netherlands (PON) provides an integrated health care standard for obesity involving strategies for diagnosis and early detection of high-risk individuals as well as appropriate combined lifestyle interventions for those who are overweight and obese and, when appropriate, additional medical therapies <xref ref-type="bibr" rid="pone.0094299-Seidell1">[32]</xref>.</p>
</sec><sec id="s5">
<title>Conclusions</title>
<p>Upward trends of morbid obesity in Dutch and Turkish children in The Netherlands occurred since respectively 1980 and 1997, while this prevalence remained almost stable in Moroccan children since 1997. The Dutch and Turkish children also showed an upward trend in morbidity index for overweight since respectively 1980 and 1997, while the Moroccan children showed a downward trend since 1997. Monitoring trends of morbid obesity according to international comparable cut-offs for BMI is important, because of the great impact on health care and costs.</p>
</sec></body>
<back>
<ack>
<p>We thank all children, their parents and the community health care workers who participated in the studies.</p>
</ack>
<ref-list>
<title>References</title>
<ref id="pone.0094299-World1"><label>1</label>
<mixed-citation publication-type="other" xlink:type="simple">World Health Organization (2013) Factsheet No311, Obesity and overweight. World Health Organization. Available: <ext-link ext-link-type="uri" xlink:href="http://www.who.int/mediacentre/factsheets/fs311/en/" xlink:type="simple">http://www.who.int/mediacentre/factsheets/fs311/en/</ext-link>. Accessed 2014 Mar 20.</mixed-citation>
</ref>
<ref id="pone.0094299-Livingstone1"><label>2</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Livingstone</surname><given-names>MB</given-names></name> (<year>2001</year>) <article-title>Childhood obesity in Europe: a growing concern</article-title>. <source>Public Health Nutr</source> <volume>4</volume>: <fpage>109</fpage>–<lpage>116</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Schnbeck1"><label>3</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Schönbeck</surname><given-names>Y</given-names></name>, <name name-style="western"><surname>Talma</surname><given-names>H</given-names></name>, <name name-style="western"><surname>van Dommelen</surname><given-names>P</given-names></name>, <name name-style="western"><surname>Bakker</surname><given-names>B</given-names></name>, <name name-style="western"><surname>Buitendijk</surname><given-names>SE</given-names></name>, <etal>et al</etal>. (<year>2011</year>) <article-title>Increase in prevalence of overweight in Dutch children and adolescents: a comparison of nationwide growth studies in 1980, 1997 and 2009</article-title>. <source>PLoS One</source> <volume>6(11)</volume>: <fpage>e27608</fpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Roede1"><label>4</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Roede</surname><given-names>MJ</given-names></name>, <name name-style="western"><surname>van Wieringen</surname><given-names>JC</given-names></name> (<year>1985</year>) <article-title>Growth diagrams 1980: Netherlands third nation-wide survey</article-title>. <source>Tijdschr Soc Gezondheidsz</source> <volume>63</volume> suppl<fpage>1</fpage>–<lpage>34</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Barness1"><label>5</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Barness</surname><given-names>LA</given-names></name>, <name name-style="western"><surname>Opitz</surname><given-names>JM</given-names></name>, <name name-style="western"><surname>Gilbert-Barness</surname><given-names>E</given-names></name> (<year>2007</year>) <article-title>Obesity: genetic, molecular, and environmental aspects</article-title>. <source>Am J Med Genet A</source> <volume>143A</volume>: <fpage>3016</fpage>–<lpage>3034</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Haslam1"><label>6</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Haslam</surname><given-names>DW</given-names></name>, <name name-style="western"><surname>James</surname><given-names>WP</given-names></name> (<year>2005</year>) <article-title>Obesity</article-title>. <source>Lancet</source> <volume>366</volume>: <fpage>1197</fpage>–<lpage>1209</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-ProspectiveStudies1"><label>7</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Prospective Studies</surname><given-names>Collaboration</given-names></name>, <name name-style="western"><surname>Whitlock</surname><given-names>G</given-names></name>, <name name-style="western"><surname>Lewington</surname><given-names>S</given-names></name>, <name name-style="western"><surname>Sherliker</surname><given-names>P</given-names></name>, <name name-style="western"><surname>Clarke</surname><given-names>R</given-names></name>, <etal>et al</etal>. (<year>2009</year>) <article-title>Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies</article-title>. <source>Lancet</source> <volume>373</volume>: <fpage>1083</fpage>–<lpage>1096</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Cole1"><label>8</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Cole</surname><given-names>TJ</given-names></name>, <name name-style="western"><surname>Lobstein</surname><given-names>T</given-names></name> (<year>2012</year>) <article-title>Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity</article-title>. <source>Pediatr Obes</source> <volume>7</volume>: <fpage>284</fpage>–<lpage>294</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Molnr1"><label>9</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Molnár</surname><given-names>D</given-names></name>, <name name-style="western"><surname>Erhardt</surname><given-names>E</given-names></name> (<year>2008</year>) <article-title>Severe childhood obesity: what are the keys for management?</article-title> <source>Int J Pediatr Obes</source> <volume>3</volume> Suppl 2<fpage>9</fpage>–<lpage>14</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-vanEmmerik1"><label>10</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>van Emmerik</surname><given-names>NM</given-names></name>, <name name-style="western"><surname>Renders</surname><given-names>CM</given-names></name>, <name name-style="western"><surname>van de Veer</surname><given-names>M</given-names></name>, <name name-style="western"><surname>van Buuren</surname><given-names>S</given-names></name>, <name name-style="western"><surname>van der Baan-Slootweg</surname><given-names>OH</given-names></name>, <etal>et al</etal>. (<year>2012</year>) <article-title>High cardiovascular risk in severely obese young children and adolescents</article-title>. <source>Arch Dis Child</source> <volume>97</volume>: <fpage>818</fpage>–<lpage>821</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Daniels1"><label>11</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Daniels</surname><given-names>SR</given-names></name> (<year>2009</year>) <article-title>Complications of obesity in children and adolescents</article-title>. <source>Int J Obes (Lond)</source> <volume>33</volume> Suppl 1<fpage>S60</fpage>–<lpage>5</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Bjrge1"><label>12</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Bjørge</surname><given-names>T</given-names></name>, <name name-style="western"><surname>Engeland</surname><given-names>A</given-names></name>, <name name-style="western"><surname>Tverdal</surname><given-names>A</given-names></name>, <name name-style="western"><surname>Smith</surname><given-names>GD</given-names></name> (<year>2008</year>) <article-title>Body mass index in adolescence in relation to cause-specific mortality: a follow-up of 230,000 Norwegian adolescents</article-title>. <source>Am J Epidemiol</source> <volume>168</volume>: <fpage>30</fpage>–<lpage>37</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Fredriks1"><label>13</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Fredriks</surname><given-names>AM</given-names></name>, <name name-style="western"><surname>Van Buuren</surname><given-names>S</given-names></name>, <name name-style="western"><surname>Hirasing</surname><given-names>RA</given-names></name>, <name name-style="western"><surname>Wit</surname><given-names>JM</given-names></name>, <name name-style="western"><surname>Verloove-Vanhorick</surname><given-names>SP</given-names></name> (<year>2005</year>) <article-title>Alarming prevalences of overweight and obesity for children of Turkish, Moroccan and Dutch origin in The Netherlands according to international standards</article-title>. <source>Acta Paediatr</source> <volume>94</volume>: <fpage>496</fpage>–<lpage>498</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Verweij1"><label>14</label>
<mixed-citation publication-type="other" xlink:type="simple">Verweij A (2008) [Categorising educational level]. In: Volksgezondheid Toekomst Verkenning, ed. [The Dutch 2008 Public Health Status and Forecast Report].Bilthoven, The Netherlands: RIVM.</mixed-citation>
</ref>
<ref id="pone.0094299-Kaplan1"><label>15</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Kaplan</surname><given-names>MH</given-names></name>, <name name-style="western"><surname>Feinstein</surname><given-names>AR</given-names></name> (<year>1974</year>) <article-title>The importance of classifying initial co-morbidity in evaluating the outcome of diabetes mellitus</article-title>. <source>J Chron Dis</source> <volume>27</volume>: <fpage>387</fpage>–<lpage>404</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Hsieh1"><label>16</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Hsieh</surname><given-names>SD</given-names></name>, <name name-style="western"><surname>Yoshinaga</surname><given-names>H</given-names></name>, <name name-style="western"><surname>Muto</surname><given-names>T</given-names></name> (<year>2003</year>) <article-title>Waist-to-height ratio, a simple and practical index for assessing central fat distribution and metabolic risk in Japanese men and women</article-title>. <source>Int J Obes Relat Metab Disord</source> <volume>27</volume>: <fpage>610</fpage>–<lpage>6</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Kuczmarski1"><label>17</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Kuczmarski</surname><given-names>RJ</given-names></name>, <name name-style="western"><surname>Ogden</surname><given-names>CL</given-names></name>, <name name-style="western"><surname>Guo</surname><given-names>SS</given-names></name>, <name name-style="western"><surname>Grummer-Strawn</surname><given-names>LM</given-names></name>, <name name-style="western"><surname>Flegal</surname><given-names>KM</given-names></name>, <etal>et al</etal>. (<year>2002</year>) <article-title>2000 CDC Growth Charts for the United States: methods and development</article-title>. <source>Vital Health Stat</source> <volume>11</volume>: <fpage>1</fpage>–<lpage>190</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Farrant1"><label>18</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Farrant</surname><given-names>B</given-names></name>, <name name-style="western"><surname>Utter</surname><given-names>J</given-names></name>, <name name-style="western"><surname>Ameratunga</surname><given-names>S</given-names></name>, <name name-style="western"><surname>Clark</surname><given-names>T</given-names></name>, <name name-style="western"><surname>Fleming</surname><given-names>T</given-names></name>, <etal>et al</etal>. (<year>2013</year>) <article-title>Prevalence of severe obesity among New Zealand adolescents and associations with health risk behaviors and emotional well-being</article-title>. <source>J Pediatr</source> <volume>163</volume>: <fpage>143</fpage>–<lpage>149</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Pan1"><label>19</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Pan</surname><given-names>L</given-names></name>, <name name-style="western"><surname>Blanck</surname><given-names>HM</given-names></name>, <name name-style="western"><surname>Sherry</surname><given-names>B</given-names></name>, <name name-style="western"><surname>Dalenius</surname><given-names>K</given-names></name>, <name name-style="western"><surname>Grummer-Strawn</surname><given-names>LM</given-names></name> (<year>2012</year>) <article-title>Trends in the prevalence of extreme obesity among US preschool-aged children living in low-income families, 1998–2010</article-title>. <source>JAMA</source> <volume>308</volume>: <fpage>2563</fpage>–<lpage>2565</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Lo1"><label>20</label>
<mixed-citation publication-type="other" xlink:type="simple">Lo JC, Maring B, Chandra M, Daniels SR, Sinaiko A, <etal>et al</etal>.. (2013) Prevalence of obesity and extreme obesity in children aged 3–5 years. Pediatr Obes May 15 [Epub ahead of print].</mixed-citation>
</ref>
<ref id="pone.0094299-Skelton1"><label>21</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Skelton</surname><given-names>JA</given-names></name>, <name name-style="western"><surname>Cook</surname><given-names>SR</given-names></name>, <name name-style="western"><surname>Auinger</surname><given-names>P</given-names></name>, <name name-style="western"><surname>Klein</surname><given-names>JD</given-names></name>, <name name-style="western"><surname>Barlow</surname><given-names>SE</given-names></name> (<year>2009</year>) <article-title>Prevalence and trends of severe obesity among US children and adolescents</article-title>. <source>Acad Pediatr</source> <volume>9</volume>: <fpage>322</fpage>–<lpage>329</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Marcus1"><label>22</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Marcus</surname><given-names>MD</given-names></name>, <name name-style="western"><surname>Baranowski</surname><given-names>T</given-names></name>, <name name-style="western"><surname>DeBar</surname><given-names>LL</given-names></name>, <name name-style="western"><surname>Edelstein</surname><given-names>S</given-names></name>, <name name-style="western"><surname>Kaufman</surname><given-names>FR</given-names></name>, <etal>et al</etal>. (<year>2010</year>) <article-title>Severe obesity and selected risk factors in a sixth grade multiracial cohort: the HEALTHY study</article-title>. <source>J Adolesc Health</source> <volume>47</volume>: <fpage>604</fpage>–<lpage>607</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Goulding1"><label>23</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Goulding</surname><given-names>A</given-names></name>, <name name-style="western"><surname>Grant</surname><given-names>AM</given-names></name>, <name name-style="western"><surname>Taylor</surname><given-names>RW</given-names></name>, <name name-style="western"><surname>Williams</surname><given-names>SM</given-names></name>, <name name-style="western"><surname>Parnell</surname><given-names>WR</given-names></name>, <etal>et al</etal>. (<year>2007</year>) <article-title>Ethnic Differences in Extreme Obesity</article-title>. <source>J Pediatr</source> <volume>151</volume>: <fpage>542</fpage>–<lpage>544</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Clarke1"><label>24</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Clarke</surname><given-names>P</given-names></name>, <name name-style="western"><surname>O'Malley</surname><given-names>PM</given-names></name>, <name name-style="western"><surname>Johnston</surname><given-names>LD</given-names></name>, <name name-style="western"><surname>Schulenberg</surname><given-names>JE</given-names></name> (<year>2009</year>) <article-title>Social disparities in BMI trajectories across adulthood by gender, race/ethnicity and lifetime socio-economic position: 1986–2004</article-title>. <source>Int J Epidemiol</source> <volume>38</volume>: <fpage>499</fpage>–<lpage>509</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Dijkshoorn1"><label>25</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Dijkshoorn</surname><given-names>H</given-names></name>, <name name-style="western"><surname>Nierkens</surname><given-names>V</given-names></name>, <name name-style="western"><surname>Nicolaou</surname><given-names>M</given-names></name> (<year>2008</year>) <article-title>Risk groups for overweight and obesity among Turkish and Moroccan migrants in The Netherlands</article-title>. <source>Public Health</source> <volume>122</volume>: <fpage>625</fpage>–<lpage>630</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Hosper1"><label>26</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Hosper</surname><given-names>K</given-names></name>, <name name-style="western"><surname>Nicolaou</surname><given-names>M</given-names></name>, <name name-style="western"><surname>Van Valkengoed</surname><given-names>I</given-names></name>, <name name-style="western"><surname>Nierkens</surname><given-names>V</given-names></name>, <name name-style="western"><surname>Stronks</surname><given-names>K</given-names></name> (<year>2011</year>) <article-title>Social and cultural factors underlying generational differences in overweight: a cross-sectional study among ethnic minorities in the Netherlands</article-title>. <source>BMC Publ Health</source> <volume>11</volume>: <fpage>105</fpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Nicolaou1"><label>27</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Nicolaou</surname><given-names>M</given-names></name>, <name name-style="western"><surname>Doak</surname><given-names>CM</given-names></name>, <name name-style="western"><surname>van Dam</surname><given-names>RM</given-names></name>, <name name-style="western"><surname>Brug</surname><given-names>J</given-names></name>, <name name-style="western"><surname>Stronks</surname><given-names>K</given-names></name>, <etal>et al</etal>. (<year>2009</year>) <article-title>Cultural and Social Influences on Food Consumption in Dutch Residents of Turkish and Moroccan Origin: A Qualitative Study</article-title>. <source>J Nutr Educ Behav</source> <volume>41</volume>: <fpage>232</fpage>–<lpage>241</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-YoungHyman1"><label>28</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Young-Hyman</surname><given-names>D</given-names></name>, <name name-style="western"><surname>Herman</surname><given-names>LJ</given-names></name>, <name name-style="western"><surname>Scott</surname><given-names>DL</given-names></name>, <name name-style="western"><surname>Schlundt</surname><given-names>DG</given-names></name> (<year>2000</year>) <article-title>Care giver perceptions of children's obesity-related health risk: a study of African American families</article-title>. <source>Obes Res</source> <volume>8</volume>: <fpage>241</fpage>–<lpage>248</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Doolen1"><label>29</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Doolen</surname><given-names>J</given-names></name>, <name name-style="western"><surname>Alpert</surname><given-names>PT</given-names></name>, <name name-style="western"><surname>Miller</surname><given-names>SK</given-names></name> (<year>2009</year>) <article-title>Parental disconnect between perceived and actual weight status of children: A metasynthesis of the current research</article-title>. <source>Journal of the American Academy of Nurse Practitioners</source> <volume>21</volume>: <fpage>160</fpage>–<lpage>166</lpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Veldhuis1"><label>30</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Veldhuis</surname><given-names>L</given-names></name>, <name name-style="western"><surname>van Dooremaal</surname><given-names>M</given-names></name>, <name name-style="western"><surname>Kroeze</surname><given-names>W</given-names></name>, <name name-style="western"><surname>Renders</surname><given-names>CM</given-names></name>, <name name-style="western"><surname>Hirasing</surname><given-names>RA</given-names></name>, <etal>et al</etal>. (<year>2013</year>) <article-title>Ethnic Background and Overweight among 5-Year-Old Children: The “Be Active, Eat Right” Study</article-title>. <source>ISRN Pediatr</source> <volume>2013</volume>: <fpage>861246</fpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Kocken1"><label>31</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Kocken</surname><given-names>PL</given-names></name>, <name name-style="western"><surname>Schönbeck</surname><given-names>Y</given-names></name>, <name name-style="western"><surname>Henneman</surname><given-names>L</given-names></name>, <name name-style="western"><surname>Janssens</surname><given-names>ACJW</given-names></name>, <name name-style="western"><surname>Detmar</surname><given-names>SB</given-names></name> (<year>2012</year>) <article-title>Ethnic differences and parental beliefs are important for overweight prevention and management in children: a cross-sectional study in the Netherlands</article-title>. <source>BMC Public Health</source> <volume>12</volume>: <fpage>867</fpage>.</mixed-citation>
</ref>
<ref id="pone.0094299-Seidell1"><label>32</label>
<mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Seidell</surname><given-names>JC</given-names></name>, <name name-style="western"><surname>Halberstadt</surname><given-names>J</given-names></name>, <name name-style="western"><surname>Noordam</surname><given-names>H</given-names></name>, <name name-style="western"><surname>Niemer</surname><given-names>S</given-names></name> (<year>2012</year>) <article-title>An integrated health care standard for the management and prevention of obesity in The Netherlands</article-title>. <source>Fam Pract</source> <volume>29</volume> Suppl 1<fpage>i153</fpage>–<lpage>i156</lpage>.</mixed-citation>
</ref>
</ref-list></back>
</article>