1. Introduction
Normal-weight obesity (NWO) is characterized by elevated total body fat (TBF) levels, typically exceeding 30% in women and 25% in men, despite having a normal body mass index (BMI) [
1,
2]. Increased TBF, waist circumference (WC), and BMI (≥30 kg/m
2) are indicators of general obesity. Both conditions are associated with an abnormal metabolic profile related to excessive total, visceral, and subcutaneous body fat, suggesting potential health risks and the necessity for effective prevention strategies [
3]. Individuals with NWO exhibit reduced insulin sensitivity, increased visceral adiposity, a more atherogenic lipid profile, and elevated blood pressure [
3]. The combination of these factors increases risks of hyperinsulinemia, insulin resistance, type II diabetes, hypertriglyceridemia, and cardiovascular disease [
1,
3,
4,
5,
6,
7,
8,
9,
10]. Identifying subjects with NWO is crucial, as they may experience hidden health risks despite normal weight. Inclusive health assessments, including body composition analysis and lifestyle inquires, are essential for individuals not only with overweight and general obesity but also with normal weight (BMI < 25 kg/m
2). A fast and convenient ultrasound method for evaluating TBF and subcutaneous body fat can effectively be utilized for this purpose. It shows high reliability and validity, allowing precise measurement of subcutaneous fat thickness (SFT) and offering valuable insights into body composition and fat distribution in individuals with NWO [
11,
12,
13,
14].
Identifying factors that influence NWO risk enables the creation of targeted interventions and effective public health strategies, addressing this increasing health concern more efficiently. Urban “obesogenic” environments contribute to chronic energy imbalance, promoting increased adiposity through factors like easy access to unhealthy foods and limited opportunities for physical activity, exacerbating obesity-related health issues [
15]. Men and women may react differently to ‘obesogenic’ environmental cues, which can significantly affect their dietary habits, physical activity level, and NWO prevalence [
15]. Despite women generally being more concerned about weight maintenance and diet, they face a higher risk of developing NWO and general obesity compared to men [
2,
16]. NWO prevalence in women is two to six times higher than in men [
2]. This disparity prompts research to investigate dietary habits and physical activity in women with NWO. Numerous studies reported NWO prevalence and its association with obesity risk factors; however, the results were inconsistent [
17,
18,
19,
20,
21].
The present study aimed to (a) assess NWO and general obesity prevalence among women of different ages residing in urban areas, (b) evaluate SFT in women with NWO, (c) establish SFT cutoff points for distinguishing NWO, and (d) explore eating habits linked to NWO.
This study proposes that women with NWO have a body composition and SFT profile similar to those with overweight and general obesity, possibly influenced by their eating habits.
4. Discussion
This study examined body composition and lifestyle differences among women with NWNO, NWO, overweight, and general obesity, aiming to identify indicators and predictors of NWO. Women with NWO exhibit similarities in body composition, fat distribution, and frequency of consuming unhealthy food with women who were with overweight and general obesity, but not with NWNO.
The present study utilized quick and convenient ultrasound method to evaluate total and subcutaneous body fat. The 2.5 MHz amplitude (A)-mode ultrasound scanner (BodyMetrix™; BodyMetrix Pro System BX2000; Livermore, CA, USA) has undergone validation in several cohorts, confirming its effectiveness for body composition and SFT assessment [
13,
14,
23,
25,
26,
27]. This method demonstrates excellent test–retest and interrater reliability [
11,
13,
14]. A-mode relies on detecting the fat-muscle interface and accurately measures SFT with a precision of 1 mm at all measurement sites. Ultrasound scanning offers advantages over caliperometry by assessing subcutaneous fat thickness without the limitations of grasping, enabling measurement in individuals with high body fat content [
26]. In the present study, the JP7 formula was utilized for evaluating body composition. In women and men with normal weight (BMI < 25 kg/m
2), the mean difference between air displacement plethysmography (ADP), bioimpedance analysis (BIA) and the JP7 (BodyMetrix™) is insignificant [
25]. The agreement between the 3C model and JP7 formula is lower in individuals with overweight and obesity [
11]. BodyMetrix™ tends to underestimate BFP, indicating accuracy limitations for this group. [
11]. The present study is the first one to employ ultrasound (A-mode) for evaluating the prevalence of NWO. The present study described a curvilinear relationship between BMI and BFP, aligning with prior research findings [
18]. BFP can be predicted accurately when BMI values exceed approximately 25 kg/m
2. BMI explained 23% of BFP variance in the group of women with BMI ≥ 25 kg/m
2 and 19% in women with BMI under 25 kg/m
2. Women with BMI < 25 kg/m
2 had greater variation in BFP than women with BMI ≥ 25 kg/m
2. Greater discrepancies of BFP at lower BMI values may be associated with cases of NWO. Although BMI is a common measure of adiposity, relying solely on it tends to underestimate the prevalence of obesity, as it does not account for body composition variations. Individuals with normal weight but increased adiposity have a higher risk of metabolic syndrome and its components than their counterparts with normal weight without obesity [
3,
4,
5,
6,
7,
8,
9,
10]. Comprehensive examination, including body composition analysis and evaluation of body fat distribution, is recommended in all nutritional status groups. When using a 30% BFP threshold, the overall NWO prevalence was nearly 20%. One in four women with BMI < 25 kg/m
2 had BFP exceeding 30%. Previous studies reported notable prevalence of NWO in children, adolescents, and individuals under 30 years [
2,
8]. At a young age, NWO is already associated with a high risk of metabolic disorders [
8].
BMI shows a curvilinear relationship with age, while total body fat increases linearly [
28,
29]. BMI underestimated adiposity in women over 45 years due to significant changes in body composition. Body composition shifts with age, showing increased total body fat accumulation and decreased fat-free mass in middle-aged (over 45 years) women. After adjusting for nutritional status, the analysis showed no significant age-related differences in subcutaneous fat accumulation, suggesting body fat redistribution and visceral fat accumulation. Aging leads to a loss of fat-free mass, primarily muscle mass, resulting in decreased strength and mobility, which leads to an increase in body fat accumulation and potential health risks. Muscle mass peaks in the fourth decade and subsequently declines [
29]. During this age period, weight gain is primarily linked to the accumulation of body fat, specifically visceral fat [
29]. A longitudinal study found significant increases in body weight and total body fat after age 45, while subcutaneous fat levels showed variability, either increasing or decreasing [
30]. Increases in fat mass with aging are accompanied with a redistribution of fat from extremity to trunk and visceral fat accumulation [
30]. In the present study, SFT in extremes and trunk were mostly associated with nutritional status rather than with age. In women over 45, elevated TBF may be linked to the rising prevalence of NWO and general obesity. A study of 564,254 adult women in Russia revealed that general obesity prevalence nearly doubled by age of 50–64 years, indicating significant age-related increases in obesity rates [
31]. Adverse age-related changes in body composition, such as increased body fat, particularly visceral fat, and decreased fat-free mass, are associated with higher risk metabolic abnormalities [
7]. Women with BFP exceeding 37% have been identified as being at a heightened risk for metabolic syndrome [
7]. As individuals age, physical activity levels decline, increasing the risk of general obesity and NWO [
29]. Post-menopause, women experience unique nutritional needs that differ from those of the general population [
29,
32]. Adopting healthy eating habits and engaging in regular resistance training can mitigate age-related changes in body composition, promoting better health outcomes in women over 45 years. In the present study, women over 45 years who did at least 180 min of physical exercise per week and did not snack frequently had significantly lower TBF, subcutaneous body fat and risk of NWO.
A slight increase in body weight in women with NWO was primarily linked to body fat accumulation, but not to fat free mass. They showed no significant differences in FFMI and FFM compared to individuals with NWNO. Subcutaneous fat levels rise with TBF accumulation and typically exhibit an even distribution throughout the body. Commonly used obesity criteria like BMI, waist circumference, and waist-to-hip ratio may not capture cases of NWO. Measuring SFT in addition to body composition analysis can be useful in identifying NWO cases. Women with NWO exhibit similarities in SFT profile with women who are overweight and those with general obesity, rather than with NWNO. The mean value of SFT, calculated as the average of measurements at seven sites, was selected as the best predictor of NWO. Youdin’s statistic was used to determine threshold to effectively distinguish between NWO and NWNO cases in the studied population. The mean SFT was set at 12 mm, aligning with the 66th percentile. The precise level was calculated as 85%. Assessing regional subcutaneous fat, along with total or visceral fat, may be essential for identifying NWO and associated health conditions, especially in women. Higher trunk fat accumulation, both subcutaneous and visceral, is associated with a higher risk of type 2 diabetes in women [
33]. Midthigh SFT beneath the fascia was positively associated with diabetes mellitus [
34]. Individual SFT measurements can be applied; however, accuracy and precision are lower than with mean SFT.
Women with NWO shared similarities in lifestyle with women with general obesity. The frequency of consumption of sweet bakery items, mass-produced food, snacks and sweet beverages, were comparable between women with NWO and general obesity. Previous studies revealed an association of unhealthy dietary patterns with NWO risk [
18]. Individuals with NWO consumed more foods high in fat and sugar, with lower consumption of fish, cereals, root vegetables, nuts, seeds, and fruits. The present study identified variations in lifestyle behaviors based on age, emphasizing the significance of considering age-related differences in lifestyle-body composition association. Unfavorable behaviors, such as meal skipping, frequent snacking, and consuming mass-produced food and sweet bakery items, were noted in women in the age period of emerging adulthood (18–29 years). During emerging adulthood, women transition from high school to university and full-time jobs, leading to significant lifestyle changes [
35]. This period presents challenges related to diet, nutrition, and physical activity changes, as women have new responsibilities. Women in emerging adulthood are experiencing a decline in fruit and vegetable intake, while their consumption of confectionery, sugar-sweetened beverages, and snacks is increasing, reflecting changing dietary patterns [
35]. All these factors can lead to rapid change in weight and body composition. Unhealthy behaviors in this period may result in body fat accumulation, raising the likelihood of developing obesity and related health conditions later in life. In contrast to NWNO, NWO doubles the risk of developing type 2 diabetes, underscoring the importance of addressing body composition and metabolic health beyond just weight status [
3,
4,
5,
6,
7,
8,
9,
10].
The present study has several limitations. First, the sample size of women with NWO and general obesity is low. The NWO and general obesity groups consisted of 30 and 34 individuals, respectively. Future studies should include larger sample sizes to validate the findings. The study did not analyze the association between lifestyle and NWO separately in age groups, as there was a low prevalence of NWO in younger groups of women. Instead, the analysis was conducted on combined age groups (18–23, 24–29, 30–45 together). It should be noted that no notable differences in lifestyle between these age groups were found. The second limitation pertains to the method used for evaluating BFP, which can lead to bias in NWO prevalence. In women with normal weight (BMI < 30 kg/m
2), ultrasound in BFP estimation was more accurate than air displacement plethysmography (ADP) and bioelectrical impedance analysis (BIA) in relation to the DEXA techniques [
17]. The bias in BFP estimation did not exceed 2%. However, reproducibility should be confirmed through comparison with DEXA or other established methods.