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Three-Dimensional Soft-Tissue Facial Morphometry in Caucasian Obese Adults

Abstract

Objective:

To evaluate the facial morphology of Caucasian obese adults in relation to normal weight peers, and to study the association between three-dimensional soft-tissue facial measurements and cardiometabolic risk factors.

Material and Methods:

Nineteen Caucasian obese subjects aged 25 to 73 years underwent anthropometric measurements, blood samples and a stereophotogrammetric facial scan. Soft-tissue facial linear distances, angles, and volumes were obtained and compared to those collected on normal weight subjects by computing z-scores. Spearman correlation was used to assess the associations between facial measurements and metabolic parameters. Logistic regression analysis adjusted for sex and age was used to assess the risk of metabolic syndrome associated to the facial measurements.

Results:

Overall, when compared to normal weight persons, obese adults had a wider face in the horizontal dimension, with a middle face (maxilla) that was larger both in absolute value and relatively to the lower face (mandible), and a larger right side gonial angle (Wilcoxon test, p < 0.01). Only the mean (left and right) gonial angle was positively associated to serum triglycerides level, while the other facial measurements were associated with none of the cardiometabolic parameters. Moreover, none of the facial measurements was associated with the risk of metabolic syndrome.

Conclusion:

Despite larger facial dimensions and altered mandible/maxilla volume ratio, three-dimensional soft-tissue facial morphometry in Caucasian obese adults is not related to cardiometabolic risk factors. The actual association between morphological facial characteristics and clinical information on the health conditions of patients is still to be investigated.

Keywords:
Anthropometry; Metabolic Syndrome; Obesity

Introduction

Obesity is constantly increasing worldwide, becoming one of the major health issues. A recent investigation reports that 2.1 billion of people in 2013 were overweight or obese [11 Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384(9945):766-81. https://doi.org/10.1016/S0140-6736(14)60460-8
https://doi.org/10.1016/S0140-6736(14)60...
]. Over consumption of food, low physical activity and environmental and genetic factors are considered the main reasons of the epidemic development of obesity. This health issue is particularly relevant because general and abdominal obesity are the main risk factors for metabolic syndrome (MS), a cluster of risk factors including abdominal obesity, impaired fasting glucose, raised blood pressure, elevated triglyceride levels and low HDL levels, type 2 diabetes, cardiovascular disease and other causes of death [22 Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K, et al. General and abdominal adiposity and risk of death in Europe. N Engl J Med 2008; 359(20):2105-20. https://doi.org/10.1056/NEJMoa0801891
https://doi.org/10.1056/NEJMoa0801891...
,33 Zhang C, Rexrode KM, van Dam RM, Li TY, Hu FB. Abdominal obesity and the risk of all-cause, cardiovascular, and cancer mortality: Sixteen years of follow-up in US women. Circulation 2008; 117(13):1658-67. https://doi.org/10.1161/CIRCULATIONAHA.107.739714
https://doi.org/10.1161/CIRCULATIONAHA.1...
].

Numerous studies on human face suggest that morphological facial characteristics can provide clinical information on the present and future health conditions of patients [44 Levine JA, Ray A, Jensen MD. Relation between chubby cheeks and visceral fat. N Engl J Med 1998; 339(26):1946-7. https://doi.org/10.1056/NEJM199812243392619
https://doi.org/10.1056/NEJM199812243392...

5 Coetzee V, Perrett DI, Stephen ID. Facial adiposity: a cue to health? Perception 2009; 38(11):1700-11. https://doi.org/10.1068/p6423
https://doi.org/10.1068/p6423...

6 Reither EN, Hauser RM, Swallen KC. Predicting adult health and mortality from adolescent facial characteristics in yearbook photographs. Demography 2009; 46(1):27-41.

7 Tinlin RM, Watkins CD, Welling LL, DeBruine LM, Al-Dujaili EA, Jones BC. Perceived facial adiposity conveys information about women's health. Br J Psychol 2013; 104(2):235-48. https://doi.org/10.1111/j.2044-8295.2012.02117.x.1
https://doi.org/10.1111/j.2044-8295.2012...

8 Lee BJ, Kim JY. Predicting visceral obesity based on facial characteristics. BMC Complement Altern Med 2014; 14:248. https://doi.org/10.1186/1472-6882-14-248
https://doi.org/10.1186/1472-6882-14-248...
-99 Nadazdyova1 A, Samohyl M. Gender and BMI differences in adult craniofacial parameters in Caucasian population: A pilot study. Pesqui Bras Odontopediatria Clin Integr 2017; 17(1):e3836. https://doi.org/10.4034/PBOCI.2017.171.60
https://doi.org/10.4034/PBOCI.2017.171.6...
]. One of them reports that cheeks status, neck circumference and craniofacial morphology are associated with type 2 diabetes and hypertension [66 Reither EN, Hauser RM, Swallen KC. Predicting adult health and mortality from adolescent facial characteristics in yearbook photographs. Demography 2009; 46(1):27-41.]. Another study, using computed tomography, reveals that buccal fat is related to visceral abdominal fat, suggesting that plump cheeks could be a potential risk factor for the metabolic allies of obesity [44 Levine JA, Ray A, Jensen MD. Relation between chubby cheeks and visceral fat. N Engl J Med 1998; 339(26):1946-7. https://doi.org/10.1056/NEJM199812243392619
https://doi.org/10.1056/NEJM199812243392...
]. Similarly, further studies, using non-invasive methods, report that facial adiposity is related to Body Mass Index (BMI) and to cardiometabolic risk factors [55 Coetzee V, Perrett DI, Stephen ID. Facial adiposity: a cue to health? Perception 2009; 38(11):1700-11. https://doi.org/10.1068/p6423
https://doi.org/10.1068/p6423...
]. Nevertheless, the association between soft-tissue facial characteristics and MS is not thoroughly investigated. Moreover, limited investigations assessed the differences in facial dimensions between obese and normal weight subjects, despite the availability of novel non-invasive and convenient methods.

Indeed, quantitative soft-tissue facial data in the three dimensions can currently be obtained by digital, computerized anthropometry [1010 de Menezes M, Rosati R, Ferrario VF, Sforza C. Accuracy and reproducibility of a 3-dimensional stereophotogrammetric imaging system. J Oral Maxillofac Surg 2010; 68(9):2129-35. https://doi.org/10.1016/j.joms.2009.09.036
https://doi.org/10.1016/j.joms.2009.09.0...

11 Sforza C, Grandi G, De Menezes M, Tartaglia GM, Ferrario VF. Age- and sex-related changes in the normal human external nose. Forensic Sci Int 2011; 204(1-3):205.e1-9. https://doi.org/10.1016/j.forsciint.2010.07.027
https://doi.org/10.1016/j.forsciint.2010...

12 Sforza C, de Menezes M, Ferrario V. Soft- and hard-tissue facial anthropometry in three dimensions: what's new. J Anthropol Sci 2013; 91:159-84. https://doi.org/10.4436/jass.91007
https://doi.org/10.4436/jass.91007...

13 Knoops PG, Beaumont CA, Borghi A, Rodriguez-Florez N, Breakey RW, Rodgers W, et al. Comparison of three-dimensional scanner systems for craniomaxillofacial imaging. J Plast Reconstr Aesthet Surg 2017; 70(4):441-9. https://doi.org/10.1016/j.bjps.2016.12.015
https://doi.org/10.1016/j.bjps.2016.12.0...

14 Sforza C, Dolci C, Dellavia C, Gibelli DM, Tartaglia GM, Elamin F. Abnormal variations in the facial soft tissues of individuals with Down syndrome: Sudan versus Italy. Cleft Palate Craniofac J 2015; 52(5):588-96. https://doi.org/10.1597/14-082
https://doi.org/10.1597/14-082...

15 Sforza C, Dolci C, Tartaglia GM, Ferrario VF. Soft-tissue 3D facial imaging in children and adolescents: towards the definition of new reference standards. Pesqui Bras Odontopediatria Clin Integr 2018, 18(1):e3854. https://doi.org/10.4034/PBOCI.2018.181.ed3
https://doi.org/10.4034/PBOCI.2018.181.e...

16 Al-Khatib AR, Rajion ZA, Masudi SM, Hassan R, Anderson PJ, Townsend GC. Stereophotogrammetric analysis of nasolabial morphology among Asian Malays: influence of age and sex. Cleft Palate Craniofac J 2012; 49(4):463-71. https://doi.org/10.1597/11-151
https://doi.org/10.1597/11-151...

17 Djordjevic J, Lawlor DA, Zhurov AI, Toma AM, Playle R, Richmond S. A population-based crosssectional study of the association between facial morphology and cardiometabolic risk factors in adolescence. BMJ Open 2013; 3(5):e002910. https://doi.org/10.1136/bmjopen-2013-002910
https://doi.org/10.1136/bmjopen-2013-002...

18 Gibelli D, Pucciarelli V, Cappella A, Dolci C, Sforza C. Are portable stereophotogrammetric devices reliable in facial imaging? A validation study of VECTRA H1 device. J Oral Maxillofac Surg 2018; 76(8):1772-84. https://doi.org/10.1016/j.joms.2018.01.021
https://doi.org/10.1016/j.joms.2018.01.0...

19 Tanikawa C, Zere E, Takada K. Sexual dimorphism in the facial morphology of adult humans: A threedimensional analysis. Homo 2016; 67(1):23-49. https://doi.org/10.1016/j.jchb.2015.10.001
https://doi.org/10.1016/j.jchb.2015.10.0...

20 Pucciarelli V, Bertoli S, Codari M, De Amicis R, De Giorgis V, Battezzati A, et al. The face of Glut1-DS patients: A 3D craniofacial morphometric analysis. Clin Anat 2017; 30(5):644-52. https://doi.org/10.1002/ca.22890
https://doi.org/10.1002/ca.22890...
-2121 Dolci C, Pucciarelli V, Gibelli DM, Codari M, Marelli S, Trifirò G, Pini A, Sforza C. The face in marfan syndrome: A 3D quantitative approach for a better definition of dysmorphic features. Clin Anat 2018; 31(3):380-386. https://doi.org/10.1002/ca.23034
https://doi.org/10.1002/ca.23034...
]. Current technology allows fast and non-invasive optical scans of facial surface, providing a global assessment of patients. Selected three-dimensional anthropometric measurements can be obtained without actual physical contact with the instruments, thus abolishing any kind of compression of cutaneous and subcutaneous tissues.

A previous photographic study on Korean adults reported that frontal plane measurements (mandibular width and the distance between the inferior most points on the ear lobes) are important indicators for discriminating between normal and visceral obese subjects [88 Lee BJ, Kim JY. Predicting visceral obesity based on facial characteristics. BMC Complement Altern Med 2014; 14:248. https://doi.org/10.1186/1472-6882-14-248
https://doi.org/10.1186/1472-6882-14-248...
]. However, this study is limited by interethnic variability in facial dimensions [2222 Fang F, Clapham PJ, Chung KC. A systematic review of interethnic variability in facial dimensions. Plast Reconstr Surg 2011; 127(2):874-81. https://doi.org/10.1097/PRS.0b013e318200afdb
https://doi.org/10.1097/PRS.0b013e318200...
], and the relevant findings cannot be extrapolated to Caucasian adults.

In children and adolescents previous studies reported bimaxillary prognathism and relatively greater horizontal and anteroposterior facial measurements in obese subjects compared to normal-weighted peers [2323 Ohrn K, Al-Kahlili B, Huggare J, Forsberg CM, Marcus C, Dahllöf G. Craniofacial morphology in obese adolescents. Acta Odontol Scand 2002; 60(4):193-7.

24 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.

25 Sadeghianrizi A, Forsberg CM, Marcus C, Dahllöf G. Craniofacial development in obese adolescents. Eur J Orthod 2005; 27(6):550-5. https://doi.org/10.1093/ejo/cji048
https://doi.org/10.1093/ejo/cji048...
-2626 Banabilh SM, Suzina AH, Dinsuhaimi S, Samsudin AR, Singh GD. Craniofacial obesity in patients with obstructive sleep apnea. Sleep Breath 2009; 13(1):19-24. https://doi.org/10.1007/s11325-008-0211-9
https://doi.org/10.1007/s11325-008-0211-...
]. Nevertheless, no evidence that facial morphology is importantly related to cardiometabolic outcomes was found in a large cohort of adolescents [1717 Djordjevic J, Lawlor DA, Zhurov AI, Toma AM, Playle R, Richmond S. A population-based crosssectional study of the association between facial morphology and cardiometabolic risk factors in adolescence. BMJ Open 2013; 3(5):e002910. https://doi.org/10.1136/bmjopen-2013-002910
https://doi.org/10.1136/bmjopen-2013-002...
]. Studies on obese adults mostly focused on patients with obstructive sleep apnea (OSA) [2626 Banabilh SM, Suzina AH, Dinsuhaimi S, Samsudin AR, Singh GD. Craniofacial obesity in patients with obstructive sleep apnea. Sleep Breath 2009; 13(1):19-24. https://doi.org/10.1007/s11325-008-0211-9
https://doi.org/10.1007/s11325-008-0211-...
], while investigations on the relationships among obesity, facial morphometry and MS have not been conducted so far.

In the current investigation, the three-dimensional characteristics of the facial soft tissues have been assessed in a group of adult Caucasian obese patients. The subjects were measured by a non-invasive, stereophotogrammetric instrument, and facial volumes, angles and distances were computed, and compared to those obtained in healthy subjects of the same age, sex and ethnic group. Finally, we studied the association between such facial morphological measurements and MS and its components.

Material and Methods

Subjects

Nineteen Caucasian (Southern Europe) obese subjects (nine men, ten women) aged 25 to 73 years (48 ± 15 years) were recruited at the International Center for the Assessment of Nutritional Status (ICANS, Università degli Studi di Milano). Subjects with previous history of craniofacial surgery, trauma or congenital anomalies were excluded. None reported respiratory problems, or had symptoms/ signs compatible with obstructive sleep apnoea. All subjects underwent anthropometric measurements by a trained dietitian and their faces were scanned using a stereophotogrammetric instrument. Blood samples were obtained in fasting state in order to measure biochemical markers.

Morphological facial data of 355 normal weight subjects obtained in a previous study [2727 Sforza C, Grandi G, Catti F, Tommasi DG, Ugolini A, Ferrario VF. Age- and sex-related changes in the soft tissues of the orbital region. Forensic Sci Int 2009; 185(1-3):115.e1-8. https://doi.org/10.1016/j.forsciint.2008.12.010
https://doi.org/10.1016/j.forsciint.2008...
] were used as standard reference. Reference subjects were divided for sex and age as follows: 18-30 years (80 men and 58 women); 31-40 years (66 men and 28 women); 41-50 years (27 men and 26 women); 51-64 years (19 men and 18 women); 65-80 years (18 men and 15 women).

Based on our previous experience in assessing three-dimensional soft-tissue facial morphometry in normal weight and obese children [2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.], we found that the sample enrolled in the present study ensured for many measurements a statistical power larger than 80% (in some cases, 100%).

Anthropometric Measurements

Anthropometric measurements were performed following international guidelines [2828 Lohmann TG, Roche AF, Martorell R. Anthropometric Standardization Reference Manual. Human Kinetics Books, Champaign, IL, USA, 1988.]. Body weight was measured to the nearest 100 g using a Seca 700 scale and height was measured to the nearest 0.1 cm using a Seca 217 vertical stadiometer (Seca Corporation, Hanover, MD, USA). BMI was calculated as weight (kg)/ height (m2) and classified according to the World Health Organization. Waist circumference was measured midway between the lower rib margin and the superior anterior iliac spine. Skinfolds (triceps, biceps, subscapular and suprailiac) were measured using a Tanner-Whitehouse caliper (Holtain Ltd, Crymych, UK). The skinfolds were then summed to obtain the sum of four skinfolds (SF4). In our Center, the intra-observer coefficient of variation for repeated measurements of these skinfolds is ≤ 2.9%. The sum of the four skinfolds was used to estimate body density using Durnin and Womersley's formula [2929 Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr 1974; 32(1):77-97.]. Later, body density was used to estimate fat mass using Siri's Formula [3030 Siri WE. Body composition from fluid spaces and density: Analysis of methods. 1961. Nutrition 1993; 9(5):480-91.].

Facial Measurements

The data collection procedure for facial measurements took place in two separate steps, and it was followed by off-line calculations [1111 Sforza C, Grandi G, De Menezes M, Tartaglia GM, Ferrario VF. Age- and sex-related changes in the normal human external nose. Forensic Sci Int 2011; 204(1-3):205.e1-9. https://doi.org/10.1016/j.forsciint.2010.07.027
https://doi.org/10.1016/j.forsciint.2010...
,1212 Sforza C, de Menezes M, Ferrario V. Soft- and hard-tissue facial anthropometry in three dimensions: what's new. J Anthropol Sci 2013; 91:159-84. https://doi.org/10.4436/jass.91007
https://doi.org/10.4436/jass.91007...
]. At first, for each patient, a single experienced operator located a set of 50 soft-tissue landmarks by inspection and/or palpation, and marked them on the cutaneous surface using an eye-liner. During landmarking, the patients sat relaxed in a position suitable for a correct identification of facial features.

In the second step, soft-tissue facial morphology was acquired by a three-dimensional stereophotogrammetry imaging system (Vectra-3D; Canfield Scientific Inc., Fairfield, NJ, USA). This imaging system is a modular 3D image capturing system constructed to capture and process stereo images; it consists of two pods, each including three cameras (two black and white, one colour) and a projector. The projector projects a random light pattern onto the face, and the cameras record synchronized pairs of two-dimensional images of the subjects with 2 ms. Using dedicated software, the information is employed to work out a three-dimensional reconstruction that subsequently can be processed, analyzed, manipulated and measured. The colour camera provides a live texture that is added to the three-dimensional data.

The reproducibility of stereophotogrammetric technology was well documented [1616 Al-Khatib AR, Rajion ZA, Masudi SM, Hassan R, Anderson PJ, Townsend GC. Stereophotogrammetric analysis of nasolabial morphology among Asian Malays: influence of age and sex. Cleft Palate Craniofac J 2012; 49(4):463-71. https://doi.org/10.1597/11-151
https://doi.org/10.1597/11-151...
,1818 Gibelli D, Pucciarelli V, Cappella A, Dolci C, Sforza C. Are portable stereophotogrammetric devices reliable in facial imaging? A validation study of VECTRA H1 device. J Oral Maxillofac Surg 2018; 76(8):1772-84. https://doi.org/10.1016/j.joms.2018.01.021
https://doi.org/10.1016/j.joms.2018.01.0...
,1919 Tanikawa C, Zere E, Takada K. Sexual dimorphism in the facial morphology of adult humans: A threedimensional analysis. Homo 2016; 67(1):23-49. https://doi.org/10.1016/j.jchb.2015.10.001
https://doi.org/10.1016/j.jchb.2015.10.0...
,3131 Weinberg SM, Raffensperger ZD, Kesterke MJ, Heike CL, Cunningham ML, Hecht JT, et al. The 3D facial norms database: part 1. A web-based craniofacial anthropometric and image repository for the clinical and research community. Cleft Palate Craniofac J 2016; 53(6):e185-e197. https://doi.org/10.1597/15-199
https://doi.org/10.1597/15-199...

32 Kook MS, Jung S, Park HJ, Oh HK, Ryu SY, Cho JH, et al. A comparison study of different facial soft tissue analysis methods. J Craniomaxillofac Surg 2014; 42(5):648-56. https://doi.org/10.1016/j.jcms.2013.09.010
https://doi.org/10.1016/j.jcms.2013.09.0...
-3333 Andrade LM, Rodrigues da Silva AMB, Magri LV, Rodrigues da Silva MAM. Repeatability study of angular and linear measurements on facial morphology analysis by means of stereophotogrammetry. J Craniofac Surg 2017; 28(4):1107-11. https://doi.org/10.1097/SCS.0000000000003554
https://doi.org/10.1097/SCS.000000000000...
]. In our laboratory, no systematic errors between operators, calibrations and acquisitions were found; random errors in landmark identification were always lower than 1.2 mm [1010 de Menezes M, Rosati R, Ferrario VF, Sforza C. Accuracy and reproducibility of a 3-dimensional stereophotogrammetric imaging system. J Oral Maxillofac Surg 2010; 68(9):2129-35. https://doi.org/10.1016/j.joms.2009.09.036
https://doi.org/10.1016/j.joms.2009.09.0...
], and the repeatability of most linear measurements and angles ranged from 82.2 to 98.7% [1818 Gibelli D, Pucciarelli V, Cappella A, Dolci C, Sforza C. Are portable stereophotogrammetric devices reliable in facial imaging? A validation study of VECTRA H1 device. J Oral Maxillofac Surg 2018; 76(8):1772-84. https://doi.org/10.1016/j.joms.2018.01.021
https://doi.org/10.1016/j.joms.2018.01.0...
].

The three-dimensional images obtained from the subjects were analyzed, and a subset of facial landmarks, 10 on the midline and 10 paired, were identified and digitized for the current study (Figure 1). The x, y, and z coordinates of the landmarks were used to calculate a set of facial linear distances, angles, and volumes [1212 Sforza C, de Menezes M, Ferrario V. Soft- and hard-tissue facial anthropometry in three dimensions: what's new. J Anthropol Sci 2013; 91:159-84. https://doi.org/10.4436/jass.91007
https://doi.org/10.4436/jass.91007...
,1414 Sforza C, Dolci C, Dellavia C, Gibelli DM, Tartaglia GM, Elamin F. Abnormal variations in the facial soft tissues of individuals with Down syndrome: Sudan versus Italy. Cleft Palate Craniofac J 2015; 52(5):588-96. https://doi.org/10.1597/14-082
https://doi.org/10.1597/14-082...
,2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.]:

  • Distances (unit: mm): upper (n-sn) and lower anterior facial heights (sn-pg); middle (zy-zy), and lower facial widths (go-go); landmark-to-line: middle [sn-(tr-tl)], and lower facial depths [pg-(tr-tl)];

  • Angles (unit: degrees): naso-labial angle (prn-sn-ls); interlabial angle ([sn-ls]^[li-sl]); mentolabial angle (li-sl-pg); right and left gonial angles (t-go-pg);

  • Volumes (unit: mm3): volumes of all facial structures from the external cutaneous surface up to a quasi-frontal plane passing through trichion, tragi and gonia; in particular, facial middle (maxilla), and lower third volumes (mandible) were considered; upper and lower lip volumes;

  • a) Facial middle third volume (maxilla): comprised between a quasi-horizontal plane passing through the tragi and the exocanthia, and a plane connecting the cheilion landmarks and the tragi, approximately corresponding to the maxillary and cheek regions;

  • b) Facial lower third volume (mandible): comprised between the cheilion-tragi plane and a plane drawn between pogonion and the gonia, approximately corresponding to the mandibular region;

  • c) Lip volumes: upper lip volume (approximated from the volumes of two tetrahedra: the first tetrahedron has the plane chr, chl, ls as its base and vertex in sn, the second has the plane chr, chl, ls as its base and vertex in sto); lower lip volume (as above, first tetrahedron with the plane chr, chl, li as its base and vertex in sl, the second with the plane chr, chl, li as its base and vertex in sto);

  • Ratio (unit: %): mandibular to maxillary volume.

Figure 1
Soft tissue facial landmarks used in the current study: tr, trichion; g, glabella; n, nasion; prn, pronasale; sn, subnasale; ls, labiale superius; sto, stomion; li, labiale inferius; sl, sublabiale; pg, pogonion; ex, exocanthion; zy, zygion; t, tragion; ch, cheilion; go, gonion.

Metabolic Measurements

Fasting HDL cholesterol, triglycerides and glucose were measured using an enzymatic method (Cobas Integra 400 Plus, Roche Diagnostics, Rotkreuz, Switzerland). Blood pressure was measured by a physician using a random-zero mercury sphygmomanometer following JNC 7 guidelines [3434 Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, et al. Joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. National heart, lung, and blood institute; National high blood pressure education program coordinating committee. Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension 2003; 42(6):1206-52. https://doi.org/10.1161/01.HYP.0000107251.49515.c2
https://doi.org/10.1161/01.HYP.000010725...
].

Metabolic syndrome was diagnosed using the harmonized international definition [3535 Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009; 120(16):1640-5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644
https://doi.org/10.1161/CIRCULATIONAHA.1...
]. Large waist was defined as waist circumference larger than 102 cm in men and 88 cm in women, low HDL-cholesterol as HDL-cholesterol <40 mg/dl in men and <50 mg/dl in women, high triglycerides as triglycerides ≥150 mg/dl, high blood pressure as systolic blood pressure ≥130 mm Hg or diastolic blood pressure ≥85 mm Hg, and high glucose as glucose ≥100 mg/dl. MS was defined when patients had 3 or more of the above components.

Data Analysis

Anthropometric facial data of the patients were compared to those collected in reference subjects by computing z-scores. In the 355 reference, control individuals, descriptive statistics were calculated for each variable separately for each age group and sex. The individual measurements obtained in the 19 patients were transformed to z-scores. The z-score measures the distance between a patient datum and the reference mean expressed in standard deviation units: z-score = (patient value - mean value of the reference group)/ standard deviation of the reference group [1111 Sforza C, Grandi G, De Menezes M, Tartaglia GM, Ferrario VF. Age- and sex-related changes in the normal human external nose. Forensic Sci Int 2011; 204(1-3):205.e1-9. https://doi.org/10.1016/j.forsciint.2010.07.027
https://doi.org/10.1016/j.forsciint.2010...
,1414 Sforza C, Dolci C, Dellavia C, Gibelli DM, Tartaglia GM, Elamin F. Abnormal variations in the facial soft tissues of individuals with Down syndrome: Sudan versus Italy. Cleft Palate Craniofac J 2015; 52(5):588-96. https://doi.org/10.1597/14-082
https://doi.org/10.1597/14-082...
,2020 Pucciarelli V, Bertoli S, Codari M, De Amicis R, De Giorgis V, Battezzati A, et al. The face of Glut1-DS patients: A 3D craniofacial morphometric analysis. Clin Anat 2017; 30(5):644-52. https://doi.org/10.1002/ca.22890
https://doi.org/10.1002/ca.22890...
,2121 Dolci C, Pucciarelli V, Gibelli DM, Codari M, Marelli S, Trifirò G, Pini A, Sforza C. The face in marfan syndrome: A 3D quantitative approach for a better definition of dysmorphic features. Clin Anat 2018; 31(3):380-386. https://doi.org/10.1002/ca.23034
https://doi.org/10.1002/ca.23034...
,2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.]. For each patient, calculations were performed using values of the reference group of the same sex and corresponding age [1111 Sforza C, Grandi G, De Menezes M, Tartaglia GM, Ferrario VF. Age- and sex-related changes in the normal human external nose. Forensic Sci Int 2011; 204(1-3):205.e1-9. https://doi.org/10.1016/j.forsciint.2010.07.027
https://doi.org/10.1016/j.forsciint.2010...
,2020 Pucciarelli V, Bertoli S, Codari M, De Amicis R, De Giorgis V, Battezzati A, et al. The face of Glut1-DS patients: A 3D craniofacial morphometric analysis. Clin Anat 2017; 30(5):644-52. https://doi.org/10.1002/ca.22890
https://doi.org/10.1002/ca.22890...
,2121 Dolci C, Pucciarelli V, Gibelli DM, Codari M, Marelli S, Trifirò G, Pini A, Sforza C. The face in marfan syndrome: A 3D quantitative approach for a better definition of dysmorphic features. Clin Anat 2018; 31(3):380-386. https://doi.org/10.1002/ca.23034
https://doi.org/10.1002/ca.23034...
].

Z-scores were used because the reduced number of patients impeded separate sex- and age- related analyses. Overall, this procedure permits to partially control for the mixed composition of the patient group. The procedure has already been used in previous investigations on the craniofacial characteristics of individuals with genetic or acquired alterations [1414 Sforza C, Dolci C, Dellavia C, Gibelli DM, Tartaglia GM, Elamin F. Abnormal variations in the facial soft tissues of individuals with Down syndrome: Sudan versus Italy. Cleft Palate Craniofac J 2015; 52(5):588-96. https://doi.org/10.1597/14-082
https://doi.org/10.1597/14-082...
,2020 Pucciarelli V, Bertoli S, Codari M, De Amicis R, De Giorgis V, Battezzati A, et al. The face of Glut1-DS patients: A 3D craniofacial morphometric analysis. Clin Anat 2017; 30(5):644-52. https://doi.org/10.1002/ca.22890
https://doi.org/10.1002/ca.22890...
,2121 Dolci C, Pucciarelli V, Gibelli DM, Codari M, Marelli S, Trifirò G, Pini A, Sforza C. The face in marfan syndrome: A 3D quantitative approach for a better definition of dysmorphic features. Clin Anat 2018; 31(3):380-386. https://doi.org/10.1002/ca.23034
https://doi.org/10.1002/ca.23034...
,2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.].

Descriptive statistics (50º percentile and interquartile range) were computed for the values of the soft-tissue facial z-scores, as well as for the anthropometric and metabolic variables. Males and female data were compared by Mann-Whitney test. Significance of the z-scores was assessed by Wilcoxon test (if the patient value is equal to the mean value of the reference group, the z-score is zero; the null hypothesis of the test is that the z-scores are null). Spearman correlation was used to assess the associations between three-dimensional soft-tissue facial distances, angles and volumes of obese subjects and metabolic parameters. Finally, logistic regression analysis was used to assess the risk of metabolic syndrome associated to the higher/lower values of the z-scores of the three-dimensional soft-tissue facial distances, angles and volumes of obese subjects. Several of the analyzed variables were interrelated, and the level of significance was set at 1% (p<0.01), with two-sided tests used for all calculations.

Ethical Aspects

The study was carried out according to the Declaration of Helsinki and all subjects gave written informed consent. The institutional review board approved the study procedures (Ethics Committee of Università degli Studi di Milano, Protocol no. 230 92/2014).

Results

The anthropometric measurements, the metabolic characteristics and the three-dimensional soft-tissue facial distances, angles and volumes (expressed as z-scores) of obese subjects recruited in the current study are reported in Table 1.

Table 1
Anthropometric measurements, metabolic characteristics and three-dimensional soft tissue facial distances, angles and volumes of obese patients.

Metabolic syndrome was identified in nine patients. Significant and expected sex differences were found only for standing height and for percentage fat mass. The discrepancy of soft-tissue facial characteristics from control subjects of the same sex and age (as assessed by z-scores) had no sex-related differences. Therefore, pooled z-scores were used in all subsequent analyses. Overall (Figure 2), the faces of obese patients were significantly larger in the horizontal dimension than those of control subjects (lower facial width, go-go), with a larger middle facial third (maxillary volume), and had a larger right side gonial angle (t-go-pg, Wilcoxon test, p<0.01). The mandible-to-maxilla volume ratio was significantly reduced in obese patients.

Figure 2
Facial soft tissues in obese patients (male and female data pooled). All values are z-scores obtained using sex- and age-related reference data. *The z-score is significantly different from zero (p<0.01, Wilcoxon test).

The associations between soft-tissue facial characteristics and cardiometabolic risk factors are reported in Table 2. The mean (left and right) gonial angle was positively associated to serum triglycerides level. However, the other three-dimensional soft-tissue facial measurements were associated with none of the cardiometabolic parameters considered in the present study. Moreover, the logistic regression adjusted for sex and age showed no associations between the three-dimensional soft-tissue facial distances, angles and volumes with the risk of metabolic syndrome (Table 3). All confidence intervals comprised 1, thus showing no significant increment or decrement of risk.

Table 2
Association between facial anthropometric characteristics and cardiometabolic risk factors.
Table 3
Association between three-dimensional soft-tissue facial distances, angles and volumes and risk of metabolic syndrome.

Discussion

In the current study, we firstly compared the facial characteristics of Southern Europe Caucasian normal weight and obese adults, and, subsequently, we studied the association between such facial morphological measurements and the metabolic syndrome and its risk factors. We found that the faces of obese patients were significantly larger in the horizontal dimension than those of control subjects, with a larger middle facial third, and a larger gonial angle. A reduced mandible-to-maxilla volume ratio was also observed in obese patients. In addition, we found that only the mean gonial angle was positively associated to serum triglycerides level. Nevertheless, none of the facial morphological measurements were associated to the risk of MS. To the best of our knowledge, this is the first study that analyzed the three-dimensional soft-tissue facial characteristics of adult obese Southern Europe Caucasian patients without OSA or other respiratory problems, thus focusing on the problems associated only with an increased body weight. Previous investigations made on adults assessed other ethnic groups [88 Lee BJ, Kim JY. Predicting visceral obesity based on facial characteristics. BMC Complement Altern Med 2014; 14:248. https://doi.org/10.1186/1472-6882-14-248
https://doi.org/10.1186/1472-6882-14-248...
,2626 Banabilh SM, Suzina AH, Dinsuhaimi S, Samsudin AR, Singh GD. Craniofacial obesity in patients with obstructive sleep apnea. Sleep Breath 2009; 13(1):19-24. https://doi.org/10.1007/s11325-008-0211-9
https://doi.org/10.1007/s11325-008-0211-...
], used two-dimensional methods [88 Lee BJ, Kim JY. Predicting visceral obesity based on facial characteristics. BMC Complement Altern Med 2014; 14:248. https://doi.org/10.1186/1472-6882-14-248
https://doi.org/10.1186/1472-6882-14-248...
], or measured patients with OSA [2626 Banabilh SM, Suzina AH, Dinsuhaimi S, Samsudin AR, Singh GD. Craniofacial obesity in patients with obstructive sleep apnea. Sleep Breath 2009; 13(1):19-24. https://doi.org/10.1007/s11325-008-0211-9
https://doi.org/10.1007/s11325-008-0211-...
].

In a previous investigation [2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.], a group of obese adolescents aged 13 to 17 years was evaluated (mean BMI 31.67 kg·m-2, SD 1.58, range from 30.03 to 36.69 kg·m-2). Obese adolescents appeared to possess faces that were significantly wider transversally (skull base width, mandibular width), deeper sagittally (mid and lower face depth, mandibular corpus length), and shorter vertically (upper facial height) than those of the reference group. A cephalometric investigation in 39 obese adolescents aged 14 to 16 years, showed that there was a general increment in facial dimensions, with an increase in mandibular length and a reduction in upper anterior facial height [2626 Banabilh SM, Suzina AH, Dinsuhaimi S, Samsudin AR, Singh GD. Craniofacial obesity in patients with obstructive sleep apnea. Sleep Breath 2009; 13(1):19-24. https://doi.org/10.1007/s11325-008-0211-9
https://doi.org/10.1007/s11325-008-0211-...
]. Previous authors found significantly larger mandibular and maxillary dimensions in 50 obese adolescents than in age- and sex-matched controls [2525 Sadeghianrizi A, Forsberg CM, Marcus C, Dahllöf G. Craniofacial development in obese adolescents. Eur J Orthod 2005; 27(6):550-5. https://doi.org/10.1093/ejo/cji048
https://doi.org/10.1093/ejo/cji048...
]. The increments were both in the anterior-posterior (maxilla and mandible) and in the vertical plane (lower anterior and posterior facial heights). Additionally, obesity was associated with bimaxillary prognathism. Similar findings were reported for female adolescents where a higher body fat proportion was associated with a relatively larger mid and lower face [3636 Windhager S, Patocka K, Schaefer K. Body fat and facial shape are correlated in female adolescents. Am J Hum Biol. 2013;25(6):847-50. https://doi.org/10.1002/ajhb.22444
https://doi.org/10.1002/ajhb.22444...
].

Our study shows that obese adults present a different facial morphology compared to normal weight persons. The increment in facial width observed here is in good accord with previous reports performed in individuals of comparable age but of other ethnic groups [88 Lee BJ, Kim JY. Predicting visceral obesity based on facial characteristics. BMC Complement Altern Med 2014; 14:248. https://doi.org/10.1186/1472-6882-14-248
https://doi.org/10.1186/1472-6882-14-248...
,99 Nadazdyova1 A, Samohyl M. Gender and BMI differences in adult craniofacial parameters in Caucasian population: A pilot study. Pesqui Bras Odontopediatria Clin Integr 2017; 17(1):e3836. https://doi.org/10.4034/PBOCI.2017.171.60
https://doi.org/10.4034/PBOCI.2017.171.6...
,3737 Lee BJ, Do JH, Kim JY. A classification method of normal and overweight females based on facial features for automated medical applications. J Biomed Biotechnol 2012; 2012:834578. https://doi.org/10.1155/2012/834578
https://doi.org/10.1155/2012/834578...
]. Overall, the larger maxillary volume may derive from both an increment in adipose (soft tissue), as well as from a larger skeleton, as found in obese adolescents [2323 Ohrn K, Al-Kahlili B, Huggare J, Forsberg CM, Marcus C, Dahllöf G. Craniofacial morphology in obese adolescents. Acta Odontol Scand 2002; 60(4):193-7.

24 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.
-2525 Sadeghianrizi A, Forsberg CM, Marcus C, Dahllöf G. Craniofacial development in obese adolescents. Eur J Orthod 2005; 27(6):550-5. https://doi.org/10.1093/ejo/cji048
https://doi.org/10.1093/ejo/cji048...
]. However, despite the differences in facial morphology observed between normal weight and obese patients, such facial measurements were not associated to MS and its components with the single exception of serum triglycerides, substantially confirming findings obtained on children [1717 Djordjevic J, Lawlor DA, Zhurov AI, Toma AM, Playle R, Richmond S. A population-based crosssectional study of the association between facial morphology and cardiometabolic risk factors in adolescence. BMJ Open 2013; 3(5):e002910. https://doi.org/10.1136/bmjopen-2013-002910
https://doi.org/10.1136/bmjopen-2013-002...
].

The principal limitation of the present investigation is in the reduced number of patients, spanning a large age range. The analysis was made using z-scores, a method that can partially control for the mixed composition of the group [2020 Pucciarelli V, Bertoli S, Codari M, De Amicis R, De Giorgis V, Battezzati A, et al. The face of Glut1-DS patients: A 3D craniofacial morphometric analysis. Clin Anat 2017; 30(5):644-52. https://doi.org/10.1002/ca.22890
https://doi.org/10.1002/ca.22890...
,2121 Dolci C, Pucciarelli V, Gibelli DM, Codari M, Marelli S, Trifirò G, Pini A, Sforza C. The face in marfan syndrome: A 3D quantitative approach for a better definition of dysmorphic features. Clin Anat 2018; 31(3):380-386. https://doi.org/10.1002/ca.23034
https://doi.org/10.1002/ca.23034...
,2424 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.]. Nonetheless, the biological significance of age and sex differences cannot be fully taken into account. A further limitation is the lack of a history about weight gain. Indeed, a lifelong history of obesity may change several characteristics of the craniofacial hard and soft tissues, as shown by previous investigations [2323 Ohrn K, Al-Kahlili B, Huggare J, Forsberg CM, Marcus C, Dahllöf G. Craniofacial morphology in obese adolescents. Acta Odontol Scand 2002; 60(4):193-7.

24 Ferrario VF, Dellavia C, Tartaglia GM, Turci M, Sforza C. Soft tissue facial morphology in obese adolescents: A three-dimensional noninvasive assessment. Angle Orthod 2004; 74(1):37-42.
-2525 Sadeghianrizi A, Forsberg CM, Marcus C, Dahllöf G. Craniofacial development in obese adolescents. Eur J Orthod 2005; 27(6):550-5. https://doi.org/10.1093/ejo/cji048
https://doi.org/10.1093/ejo/cji048...
]. Furthermore, the metabolic and anthropometric characteristics taken into account were not longitudinally assessed, and we only measured them on a single occasion: we cannot control for their time-related variations.

Conclusion

This study reveals that Caucasian normal weight and obese adults present a different facial morphology. Particularly, most of the differences were observed in the middle and lower parts of the face: when compared to normal weight individuals, obese adults had a wider face in the horizontal dimension, with a middle face that was larger both in absolute value and relatively to the lower face. However, facial morphology does not seem to be importantly related to cardiometabolic outcomes, and the actual association between morphological facial characteristics and clinical information on the health conditions of patients is still to be investigated.

  • Financial Support: None.

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Edited by

Academic Editors: Alessandro Leite Cavalcanti and Wilton Wilney Nascimento Padilha

Publication Dates

  • Publication in this collection
    02 Sept 2019
  • Date of issue
    2019

History

  • Received
    14 Nov 2018
  • Accepted
    28 Nov 2018
  • Published
    05 Dec 2018
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