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PLOS ONE

Neck circumference cutoff point as a predictor of metabolic syndrome in Brazilian rural


workers
--Manuscript Draft--

Manuscript Number: PONE-D-23-39135

Article Type: Research Article

Full Title: Neck circumference cutoff point as a predictor of metabolic syndrome in Brazilian rural
workers

Short Title: Neck circumference cutoff point in Brazilian rural workers

Corresponding Author: Manoela Cassa Libardi, M.D.


Universidade Federal do Espirito Santo
Vitória, Espírito Santo BRAZIL

Keywords: neck circumference, metabolic syndrome, rural workers, cardiometabolic risk, cutoff
point

Abstract: Neck circumference (NC) is a predictive measure for the diagnosis of Metabolic
Syndrome (MS). The aim of the present study was to establish cutoff points for NC as
a predictor of the presence of MS in Brazilian rural workers, based on the MS
components according to the IDF and NCEP-ATP III criteria. This is a cross-sectional
study carried out with rural workers in the municipality of Santa Maria de Jetibá, in the
state of Espírito Santo, Brazil. The ROC curve was calculated and the cutoff points for
predicting the risk of developing MS were stipulated from the NC, identified by the area
under the curve, using different methods of criteria for determining MS. Sensitivity,
specificity, positive and negative predictive values and Youden index were applied.
The significance level adopted was 5%. The cutoff points were different for males,
resulting in 39.725 cm (AUC 0.861) according to the NCEP-ATP III criterion and 39.125
cm (AUC 0.885) according to the IDF criterion. For women, the cutoffs were similar,
resulting in a single cutoff of 34.725 cm (AUC 0.845 for NCEP-ATP III and 0.816 for
IDF). The cutoff points defined for men and women for NC showed good sensitivity and
specificity for predicting MS in the studied population. The NC measurement proved to
be a simple, low-cost and accurate measure for assessing this morbidity in Brazilian
rural workers.

Order of Authors: Manoela Cassa Libardi, M.D.

Cleodice Alves Martins, MSc

Júlia Rabelo Santos Ferreira, MSc

Glenda Blaser Petarli, DSc

Monica Cattafesta, DSc

Olívia Maria de Paula Alves Bezerra, DSc

Eliana Zandonade, DSc

Carlos Eduardo Gomes Siqueira, DSc

Luiz Carlos Abreu, DSc

Jonathan Filippon, DSc

Luciane Bresciani Salaroli, DSc

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Cover Letter

Cover letter for submission on Plos One

Dear Editor,

We are pleased to submit an original research article entitled “Neck circumference cutoff

point as a predictor of metabolic syndrome in Brazilian rural workers” for consideration

for publication in the Plos One. In this manuscript, by defining cut-off points for neck

circumference using the metabolic syndrome criteria, the results found can be used in

clinical practice for the population of rural workers, being a method of early and periodic

anthropometric assessment in the system health, especially within the scope of primary

care.

Considering that the Plos One cover topics relevant to clinical and basic studies relevant

to man, we believe that this manuscript is appropriate for publication, contributing to

nutritionists and researchers in the field of healthcare professionals.

This manuscript was not published and is not under consideration for publication

elsewhere. The article has been professionally reviewed. We have no conflicts of interest

to disclose. If requested, the authors will provide the data on which the manuscript is

based for examination by the editors or their assignees.

Thank you for your consideration.

The authors.
Manuscript Click here to access/download;Manuscript;Manuscript.docx

1 Neck circumference cutoff point as a predictor of metabolic syndrome

2 in Brazilian rural workers

4 Manoela Cassa Libardi1¶, Cleodice Alves Martins1¶, Júlia Rabelo Santos Ferreira1&, Glenda

5 Blaser Petarli2&, Monica Cattafesta1&, Olívia Maria de Paula Alves Bezerra3&, Eliana

6 Zandonade2&, Carlos Eduardo Gomes Siqueira4&, Luiz Carlos de Abreu1&, Jonathan

7 Filippon5&, Luciane Bresciani Salaroli1,6¶

1
9 Graduate Program in Collective Health, Health Sciences Center, Universidade Federal do

10 Espírito Santo, Brazil

2
11 Health Sciences Center, at the Universidade Federal do Espírito Santo, Brazil

3
12 Universidade Federal de Ouro Preto, Brazil

4
13 Massachusetts University, Boston, Massachusetts, United States of America

5
14 Queen Mary University of London, London, United Kingdom

6
15 Graduate Program Nutrition and Health, Health Sciences Center, Universidade Federal do

16 Espírito Santo, Brazil

17

18 * Corresponding author

19 E-mail: manoelalibardi@gmail.com

20


21 These authors contributed equally to this work.
22

1
&
23 These authors also contributed equally to this work.
24

25

26 Abstract
27 Neck circumference (NC) is a predictive measure for the diagnosis of Metabolic Syndrome

28 (MS). The aim of the present study was to establish cutoff points for NC as a predictor of the

29 presence of MS in Brazilian rural workers, based on the MS components according to the IDF

30 and NCEP-ATP III criteria. This is a cross-sectional study carried out with rural workers in the

31 municipality of Santa Maria de Jetibá, in the state of Espírito Santo, Brazil. The ROC curve

32 was calculated and the cutoff points for predicting the risk of developing MS were stipulated

33 from the NC, identified by the area under the curve, using different methods of criteria for

34 determining MS. Sensitivity, specificity, positive and negative predictive values and Youden

35 index were applied. The significance level adopted was 5%. The cutoff points were different

36 for males, resulting in 39.725 cm (AUC 0.861) according to the NCEP-ATP III criterion and

37 39.125 cm (AUC 0.885) according to the IDF criterion. For women, the cutoffs were similar,

38 resulting in a single cutoff of 34.725 cm (AUC 0.845 for NCEP-ATP III and 0.816 for IDF).

39 The cutoff points defined for men and women for NC showed good sensitivity and specificity

40 for predicting MS in the studied population. The NC measurement proved to be a simple, low-

41 cost and accurate measure for assessing this morbidity in Brazilian rural workers.

42 Keywords: neck circumference, metabolic syndrome, rural workers, cardiometabolic risk,

43 cutoff point

44

45 Introduction
46 Metabolic syndrome (MS) corresponds to the set of metabolic changes that, when present in

47 the individual, increase the chance of developing cardiometabolic diseases, such as heart

2
48 disease, stroke and diabetes. These factors are related to insulin resistance and increased blood

49 glucose, blood pressure, dyslipidemia, obesity and central body fat deposition [1-3]. MS is still

50 considered a possible positive predictor of morbidity and mortality from cardiovascular

51 diseases [4].

52 Anthropometric assessment is one of the criteria for the diagnosis of MS and is commonly used

53 to measure body parameters as it is a method used internationally and applied to assess

54 indicators in large populations [5, 6] due to it being low cost, easy to apply and noninvasive [7,

55 8].

56 Neck circumference (NC) is an anthropometric measurement recommended for use in clinical

57 practice as a low-cost and easy-to-train method [9] for the assessment of excess body weight,

58 contributing to the diagnosis of overweight, obesity and associated diseases [10]. Despite its

59 importance, there are few studies that relate the use of NC cutoff points to predict MS and other

60 chronic diseases in rural workers [11-14], and so far there is no consensus on the definition of

61 cutoff points and studies published in Brazil for this population.

62 This study aims to establish cutoff points for NC as a predictor of the risk of developing MS in

63 Brazilian rural workers, based on MS components according to the International Diabetes

64 Federation (IDF) and the National Cholesterol Education Program's Adult Treatment Panel III

65 (NCEP-ATP III).

66

67 Methods

68 Study design and population

69 This is a cross-sectional epidemiological study, part of the project “Health condition and

70 associated factors: a study with rural workers in Espírito Santo - AgroSaúdES,” funded by the

71 Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES).

3
72 This study has been approved by the Research Ethics Committee of the Health Sciences Center

73 of the Federal University of Espírito Santo, reference number 2091172 (CAAE

74 52839116.3.0000.5060), meeting the requirements demanded by the Resolution of the National

75 Health Council nº 466/ 12 and the Declaration of Helsinki and its supplements for research

76 involving human beings. Subjects signed the written Free and Informed Consent Term to

77 participate in the study.

78 The study was carried out in the municipality of Santa Maria de Jetibá, in the state of Espírito

79 Santo, located in southeastern Brazil, and obtained a representative sample of rural workers,

80 according to the following inclusion criteria: age between 19 and 59 years; not being pregnant;

81 having agriculture as the main source of income; and being at least six months in full

82 employment.

83 To identify eligible rural workers in the original study, data available in the individual and

84 family records of the Family Health Strategy teams were used, covering 100% of the 11 health

85 regions of the municipality. The survey identified 4,018 families and a total of 7,287 rural

86 workers. From this universe, a sample was calculated for the original project considering 50%

87 of expected prevalence of abdominal obesity (to maximize the sample), 3.5% of sampling error

88 and a significance level of 95%, making a minimum sample of 708 rural workers for the

89 original study. A total of 806 rural workers were invited to compensate for possible losses. All

90 sample size calculations were performed using the EPIDAT program (version 3.1).

91 Data collection took place from December, 8, 2016 to April, 4, 2017 on the premises of the

92 municipality’s health units by trained researchers. The details involved in data collection and

93 research development are described in the article by Petarli and collaborators [15].

94

95

96

4
97 Data collection

98 Blood was collected from rural workers for biochemical tests. The analysis of HDL and

99 triglycerides and the measurement of systolic blood pressure (SBP) and diastolic blood

100 pressure (DBP) are detailed in the article by Petarli et al. [15]. The measurement of weight,

101 height, WC and BMI assessment are detailed in the article by Prado et al. [16].

102 The NC was obtained with the individual with the head in the Frankfurt position, that is, with

103 the eyes facing forward, placing a flexible inextensible measuring tape Sanny model TR-4010®

104 (Promohealth trade of medical and specialized products, Bauru, São Paulo, Brazil), at the point

105 just below the prominence of the larynx and was expressed in centimeters [17].

106 For all measurements, three nonconsecutive repetitions were performed, the first being

107 discarded and the average of the last two considered as the final measurement. The equipment

108 was calibrated and validated by the National Institute of Metrology, Quality and Technology

109 (INMETRO).

110 To establish the NC cutoff point for both sexes, the MS criteria

111 according to the IDF and NCEP-ATP III were used. For the IDF,

112 individuals are considered to have MS if they have abdominal

113 obesity assessed by a WC ≥ 84 cm for women and ≥ 94 cm for men, with

114 the presence of two more criteria: fasting glucose ≥ 100 mg/dL; SBP

115 ≥ 130 mmHg or DBP ≥ 85 mmHg; TG ≥ 150 mg/dL and HDL-c < 40 mg/dL

116 for men and < 50 mg/dL for women. Regarding the NCEP-ATP III,

117 individuals were considered to have MS with the following criteria:

118 WC > 82 cm for women and > 102 cm for men; HDL-c < 40 mg/dL for men

119 and < 50 mg/dL for women; TG ≥ 150 mmg/dL; SBP ≥ 130 mmHg and DBP

120 ≥ 85 mmHg and fasting blood glucose ≥ 100 mg/dL. For both

5
121 classifications, the use of antihypertensive, hypoglycemic and/or

122 medication for dyslipidemia were considered criteria for MS, as they

123 classify the individual with hypertension, diabetes and/or

124 dyslipidemia, respectively [1].

125

126 Statistical analysis

127 To describe the study variables, absolute and relative frequencies were used. Data were

128 submitted to a receiver operating characteristic (ROC) curve analysis to establish the cutoff

129 points for NC, according to the set of conditions that make up the criteria for MS in both

130 diagnostic criteria mentioned above. Cutoff points were defined based on the Youden Index,

131 specificity and sensitivity.

132 All analyses were performed using the R software (4.0.3) for Windows. The significance level

133 adopted was 5%.

134

135 Results
136 The analysis of the ROC curve for males is shown in Fig 1. For the NCEP-ATP III criterion,

137 the area under the curve (AUC) was 0.861 (CI = 0.798–0.925, p < 0.001) and for the IDF

138 criterion, the area under the curve (AUC) was 0.885 (CI = 0.846–0.924, p < 0.001).

139 Fig 1. NC ROC curve for the diagnosis of MS in men, using the NCEP-ATP III (1A) e

140 IDF (1B) criteria, respectively. AUC: area under the curve; MS: metabolic syndrome; NC:

141 neck circumference; NCEP-ATP III: National Cholesterol Education Program; IDF:

142 International Diabetes Federation.

6
143 The results of the analysis of the ROC curve for females are shown in Fig 2. For the NCEP

144 criterion, the AUC was 0.845 (CI = 0.799–0.892, p < 0.001) and for the IDF criterion, the AUC

145 was 0.816 (CI = 0.767–0.865, p < 0.001).

146 Fig 2. NC ROC curve for the diagnosis of MS in women, using the NCEP-ATP III (2A) e

147 IDF (2B) criteria, respectively. AUC: area under the curve; MS: metabolic syndrome; NC:

148 neck circumference; NCEP-ATP III: National Cholesterol Education Program; IDF:

149 International Diabetes Federation.

150 For males, the cutoff points were different between the NCEP and IDF criteria, namely 39.725

151 (Youden Index 0.674) and 39.125 (Youden Index 0.681), respectively. For women, the cutoff

152 points were the same between the NCEP-ATP III and IDF criteria, 34.725 (Youden Index 0.543

153 and 0.508, respectively), as shown in Table 1.

154 Table 1. Cutoff points and diagnostic performance measures for NC by gender for

155 the diagnosis of MS.

Variables Men (95% CI) Women (95% CI)

NCEP-ATP III IDF NCEP-ATP III IDF

Cutoff points 39.725 39.125 34.725 34.725

AUC 0.861 (0.798– 0.885 (0.846– 0.845 (0.799– 0.816 (0.767–


0.925) 0.924) 0.892) 0.865)

Accuracy 0.794 (0.793– 0.777 (0.776– 0.694 (0.693– 0.702 (0.701–


0.795) 0.778) 0.695) 0.703)

Sensitivity 0.889 (0.786– 0.926 (0.856– 0.887 (0.808– 0.840 (0.757–


0.992) 0.996) 0.966) 0.923)

Specificity 0.785 (0.744– 0.755 (0.710– 0.656 (0.604– 0.668 (0.615–


0.827) 0.799) 0.709) 0.721)

7
PPV 0.283 (0.200– 0.362 (0.282– 0.337 (0.265– 0.387 (0.312–
0.366) 0.443) 0.410) 0.461)

NPV 0.987 (0.974– 0.985 (0.971– 0.967 (0.943– 0.944 (0.913–


1.000) 1.000) 0.991) 0.975)

Youden Index 0.674 0.681 0.543 0.508

156 AUC: area under the curve; PPV: positive predictive value; NPV: negative predictive
157 value; CI: confidence interval.
158

159 The prevalence of MS for males according to the classification according to the defined NC

160 cutoff points was 27.36% according to the NCEP-ATP III criterion and 33.41% according to

161 the IDF criterion. For females, the prevalence of MS according to the classification according

162 to the defined NC cutoff points was 43.09% for both criteria.

163

164 Discussion
165 This is the first study to identify NC cutoff points for the diagnosis of MS in rural workers in

166 Brazil. This measurement is a known method of anthropometric assessment; however, it is still

167 seldomly used in clinical practice, due to the absence of specific standardized cutoff points as

168 a reference for the diagnosis of diseases and comorbidities. In rural populations, studies are

169 even more scarce.

170 The results found in the present study show that differences were found in the cutoff points

171 defined for the male population, contrary to the results observed in the female population,

172 which presented the same value for both criteria. This fact can be explained by the lower

173 variability of the data collected in the female population, compared to the male population, in

174 relation to the criteria used for the diagnosis of MS.

175 Vague (1956) [18] proposed for the first time the association between the accumulation of fat

176 predominantly in the upper part of the body with metabolic disturbances; however, for several

8
177 decades, studies were focused on the evaluation of body fat distribution from WC

178 measurements and hip circumference (HC) and the waist–hip ratio (WHR) [19].

179 Currently, studies point out that the location of body fat is an important factor in determining

180 health risk and the development of cardiometabolic diseases [20], since the deposition of the

181 upper body, such as the neck, seems to be related to a greater release of acids plasma free fatty

182 acids, with a greater relation to increased cardiovascular risk and greater insulin resistance,

183 such as visceral fat [21, 22].

184 Thus, interest in studies of the association between body fat distribution in the upper body has

185 increased, specifically in research regarding the neck region [23], recognizing its relationship

186 with cardiometabolic risk, independent of other measures of adiposity [22, 24].

187 Studies over the last decade have shown that the NC measurement has a strong association with

188 WC, HC, WHR and BMI measurements and the identification of obesity [5, 25-29].

189 It was also evaluated that NC is an important predictor for the diagnosis of overweight and

190 obesity [30], MS [29, 31] and central obesity [29], in addition to being associated with glucose

191 intolerance, hyperinsulinemia, diabetes and hypertriglyceridemia [26] and being an important

192 anthropometric measure to assess cardiovascular risk factors [29, 32], increased blood pressure,

193 LDL-c [8; 25], inflammatory markers [33] and coronary artery disease [34], predicting a higher

194 incidence of fatal and nonfatal cardiovascular events [32].

195 Ebrahimi et al. [29], in 2021, evaluated the ideal NC cutoff point for the diagnosis of MS in the

196 adult Iranian population and observed that the measure was a predictive factor for the

197 development of MS, showing correlation with central obesity, increased fasting glucose,

198 arterial hypertension and dyslipidemia. In this population, the NC defined for the diagnosis of

199 MS was 36 cm for women and 42 cm for men, values above those found in the present study.

200 In contrast, lower cutoff points were determined in a survey carried out with a Korean

201 population, aged 40 to 65 years. NC was positively correlated with BMI and WC in men and

9
202 women, increased blood pressure and dyslipidemia. According to the authors, the cutoff points

203 of 38.5 cm for men and 33.65 cm for women were able to predict the development of MS in

204 this population [25].

205 Hoebel, Malan and Rider (2012) [35] evaluated male and female adult African and Caucasian

206 teachers in South Africa. NC determined the risk for MS in all Caucasian groups. The groups

207 of Caucasian men and African women had cutoff values above those found in the present study,

208 with measurements of 40 and 41 cm for younger and older Caucasian men, respectively, and

209 35 cm for older African women. It is currently known that age contributes to the onset of MS

210 and other metabolic disorders [36].

211 Similar associations were found in a recent study by Zanuncio et al. in 2022 [32], where

212 increased CP was associated with greater risks of developing MS. The authors found values of

213 39.5 cm and 33.3 cm for men and women, respectively.

214 In the study by Silva et al. (2020) [22], it was observed that a 1 cm increase in NC was

215 associated with a 3% increase in the arithmetic mean risk of cardiovascular disease in men and

216 5% in women. The authors also observed a positive association between the increase in NC

217 and the cardiovascular risk in 10 years, suggesting the findings of the study to estimate the

218 cardiovascular risk.

219 However, none of the cited studies that found associations between NC and MS were carried

220 out with rural populations of the countries.

221 Among the few studies that use the diagnosis of MS based on the identification of NC cutoff

222 points for the rural population, we found the following: in Ukraine, NC cutoff points of 36.5

223 cm for women and 38.5 cm for men were definedfor the diagnosis of type 2 diabetes mellitus

224 [11]; in Thailand, NC was associated with systemic arterial hypertension above 37.5 cm for

225 men and 32.5 cm for women [12]; In India, in both urban and rural populations, high and

10
226 normal NC was positively correlated with BMI and increased blood pressure, with greater

227 statistical significance in the urban population when compared to the rural population [37].

228 In the present study, the female population had a higher prevalence of MS (43.09%) than the

229 male population (27.36% according to the NCEP criterion and 33.41% according to the IDF

230 criterion).

231 Obesity and related diseases, such as MS, can be related to food insecurity and malnutrition,

232 critical determinants of health.

233 Malnutrition is the main cause of illness in the world [38]. The worsening of living and working

234 conditions, topped up and increased by social inequality, can affect basic living conditions and

235 needs, such as access to food [39]; the effects on the acquisition of food can be the reduction

236 or total absence of fruits and vegetables purchases, while likely increasing the consumption of

237 ultra-processed and ready-to-eat foods [40].

238 This situation leads the population to a greater risk of developing nontransmissible chronic

239 diseases related to food, such as obesity, high blood pressure, diabetes and MS, due to a diet of

240 low nutritional quality [41, 42]. Decreased consumption of culinary ingredients can increase

241 the risk of abdominal fat accumulation by between 1.57 and 1.66 times [16].

242 In the study by Cattafesta et al. (2020), carried out with the same population as the present

243 study and previously published, the higher caloric intake of ultra-processed foods was

244 associated with the higher caloric content of the diet and the lower consumption of all 23

245 nutrients analyzed [43].

246 In Brazil, food insecurity is greater in rural regions of the country and is present in more than

247 60% of households, including those where there are rural workers and small farm producers

248 [44].

249 Thus, the results found can be used in clinical practice and in epidemiological studies for the

250 studied population, and the NC can be used as a method of evaluating the distribution of body

11
251 fat early and periodically in the health system, especially within the scope of primary health

252 care (PHC), where resources are constrained and often the only gateway for access to

253 healthcare by the rural population.

254 This is a low-cost and effective way of increasing prevention and early action by healthcare

255 professionals based at PHC settings in rural areas; due to its ease of application and replication

256 among health workers, it could be implemented as part of routine anthropometric reviews,

257 either at PHC settings or home visits, which are common practice in the Brazilian National

258 Health System (Sistema Único de Saúde). Such preventative actions are especially relevant in

259 a scenario of cost containment in the medium to long run of healthcare financing in low- and

260 middle-income countries such as Brazil, as they offer numerous positive factors, allowing

261 preventative measures against NCDs and likely reducing resource use related to future

262 healthcare utilization.

263 The limitation of this study is its cross-sectional nature, which must be taken into account when

264 interpreting the results found due to the possibility of reverse causality. Furthermore, due to

265 the availability of few articles in the literature using the same methodology in a similar

266 population, the results could not be compared with greater precision.

267 In conclusion, the cutoff points of 39.125 cm and 34.725 cm for women for the NC showed

268 good sensitivity and specificity for the diagnosis of MS in the studied population. NC proved

269 to be a simple, easy-to-apply, low-cost and accurate measure for assessing MS in Brazilian

270 rural workers.

271

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