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Body Mass Index: From Quételet to Evidence ... - Giorgio Bedogni

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In: <strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: New Research ISBN 1-59454-282-1<br />

Edi<strong>to</strong>r: Linda A. Ferrera, pp. 1-12 © 2004 Nova Science Publishers, Inc.<br />

<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: <strong>From</strong> <strong>Quételet</strong><br />

<strong>to</strong> <strong>Evidence</strong>-Based Medicine<br />

Chapter 1<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, ∗<br />

Centro Studi Fega<strong>to</strong>, AREA Science Park, Basovizza, Trieste, Italy;<br />

Cattedra di Nutrizione Umana, Università di Modena and Reggio Emilia, Italy<br />

Claudio Tiribelli and Stefano Bellentani<br />

Centro Studi Fega<strong>to</strong>, AREA Science Park, Basovizza, Trieste, Italy<br />

Abstract<br />

The ratio of body weight <strong>to</strong> squared stature, nowadays known as the body mass index<br />

(BMI), was proposed as an index of body shape in the late 19 th century. BMI was<br />

rediscovered in the late 20 th century as an index of body fat and started <strong>to</strong> be employed in<br />

population studies <strong>to</strong> investigate the association between body adiposity and disease. <strong>From</strong><br />

these studies, BMI emerged as an important predic<strong>to</strong>r of morbidity and mortality. However,<br />

BMI is not a pure index of adiposity because its numera<strong>to</strong>r (body weight) is the sum of fat-<br />

and fat-free-tissues. Moreover, its association with disease is influenced by other fac<strong>to</strong>rs such<br />

as age, gender, ethnic background, dietary habits and physical activity. Despite these limits, in<br />

our era of <strong>Evidence</strong>-based Medicine, the assessment of BMI is a central step in the evaluation<br />

and treatment of obesity, diabetes, hypertension and dyslipidemia and other complications of<br />

overweight.<br />

∗ Send correspondence <strong>to</strong>: Dr <strong>Giorgio</strong> <strong>Bedogni</strong>, Centro Studi Fega<strong>to</strong>, Bldg Q, AREA Science Park,<br />

Strada Statale 14 / km 163.5, 34012 Basovizza (Trieste), ITALY. Phone: +39-040-3757840; Fax: +39-<br />

040-3757832; E-mail: giorgiobedogni@libero.it.


2<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, Claudio Tiribelli and Stefano Bellentani<br />

<strong>Quételet</strong>’ s <strong>Index</strong><br />

The ratio of body weight <strong>to</strong> squared stature (W/S 2 ), nowadays known as the body mass<br />

index (BMI), was proposed as a measure of body shape by the Belgian anthropologist<br />

Adolphe <strong>Quételet</strong> in the late 19 th century [1-4]. W/S 2 was then just one of the many indexes<br />

used by anthropologists <strong>to</strong> control body weight for stature, i.e. <strong>to</strong> measure body shape [5], and<br />

was the option preferred by <strong>Quételet</strong> for adults [2, 3]. Of the plethora of weight-stature<br />

indexes developed in the last two hundred years [5], W/S 2 is however the only one still in use<br />

<strong>to</strong>day. Surprisingly, it is also the only one not <strong>to</strong> be remembered with the name of its inven<strong>to</strong>r<br />

[3, 5]. Even if <strong>Quételet</strong> did not use W/S 2 as an adiposity or prognostic index as we do <strong>to</strong>day,<br />

the lack of acknowledgement for its discovery is surprising in view of the immense<br />

contributions given by this man <strong>to</strong> the fields of anthropology and statistics (not <strong>to</strong> mention<br />

sociology and astronomy) [2, 4, 6]. For instance, by showing that the heights of French<br />

conscripts and the chest circumferences of Scottish soldiers tended <strong>to</strong> be normally distributed,<br />

<strong>Quételet</strong> made the fundamental discovery that the normal curve could be used other than an<br />

error law applied <strong>to</strong> the movements of planets. He literally brought the normal curve from the<br />

skies <strong>to</strong> the earth, in the hope of building a new science of man [1]. This finding was central<br />

<strong>to</strong> the development of both anthropometry and statistics. Thus, even if W/S 2 is not used <strong>to</strong>day<br />

as it was by <strong>Quételet</strong>, we should always recall the great contributions of its inven<strong>to</strong>r <strong>to</strong><br />

anthropometry when using “his” index [3].<br />

<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong> as an <strong>Index</strong> of Adiposity<br />

W/S 2 might have been one of the many forgotten weight-stature indexes if it had not been<br />

rediscovered as an index of adiposity more than one hundred years after its introduction. The<br />

demonstration of an association between W/S 2 and body fat gave a new life <strong>to</strong> <strong>Quételet</strong>’ s<br />

index and the new name of BMI [5, 7-10]. As a demonstration of the success encountered by<br />

W/S 2 , the term “body mass index” entered the Medical Subject Heading of the National<br />

Library of Medicine in 1990. Here, BMI is defined as “one of anthropometric measures of<br />

body mass; it has the highest correlations with skinfolds and body density”. This definition<br />

reflects the fact that skinfolds [11] and body densi<strong>to</strong>metry [12] were used <strong>to</strong> measure body fat<br />

in the first validation studies of BMI.<br />

The search for anthropometric indexes of adiposity has been fuelled by the hypothesis<br />

that excess body fat could be a risk fac<strong>to</strong>r for chronic disease [13]. Due <strong>to</strong> its simplicity, BMI<br />

offered the opportunity <strong>to</strong> study the relationship between body fat and disease in population<br />

studies. However, even if BMI is associated with fat-free tissues less than other weightstature<br />

indexes [5, 13], its numera<strong>to</strong>r (weight) is the sum of fat and fat-free tissues so that<br />

BMI cannot be considered a pure index of adiposity (Figure 1). It should also be noted that,<br />

while the association of BMI with morbidity and mortality is now very clear (see next<br />

paragraph), only recently the association between body fat and chronic disease started <strong>to</strong> be<br />

investigated. The measurement of body fat requires in fact methods that are difficult <strong>to</strong> use in


<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: <strong>From</strong> <strong>Quételet</strong> <strong>to</strong> <strong>Evidence</strong>-Based Medicine 3<br />

population studies because of logistical, economical and technical problems, besides the<br />

invasive nature of some of them [14].<br />

Figure 1. The two- and five-compartment models of body composition applied <strong>to</strong> the reference man.<br />

<strong>Body</strong> weight (BW) is the sum of fat mass (FM) and fat-free mass (FFM), which in turn is the sum of<br />

<strong>to</strong>tal body water (TBW), protein mass (PM), mineral mass (MM) and glycogen.<br />

BMI explains from 36 <strong>to</strong> 64% of the variability of percent body fat in adults and from 20<br />

<strong>to</strong> 75% in children [15-18]. The error made by BMI in estimating percent body fat is usually<br />

acceptable at the population level but not at the individual level. To avoid misunderstandings,<br />

it must be pointed out that this is a problem of every indirect body composition technique, i.e.<br />

of every technique making use of predictive algorithms <strong>to</strong> estimate a body compartment [13].<br />

The limitation of BMI as a measure of adiposity in the individual is exemplified by Figure 2<br />

which reports the results obtained in 1413 Italian women aged 60-88 years [18]. The standard<br />

error of the estimate associated with the prediction of percent body fat from BMI in this<br />

population is 4.1%. The percent standard error of the estimate, obtained by dividing the<br />

standard error of the estimate by the mean value of percent body fat, is 11%. Even if this<br />

value is somewhat high, it can still be accepted for population studies. However, since the<br />

inter-individual variability in the percent body fat-BMI relationship is high, BMI cannot be<br />

used as an index of adiposity at the individual level. For instance, by looking at the regression<br />

plot in Figure 2, it may be observed that a woman with a BMI of 28 kg / m 2 may have a<br />

percent body fat comprised between 30 and 50%.


4<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, Claudio Tiribelli and Stefano Bellentani<br />

Figure 2. Relationship between percent body fat and BMI in a sample of 1423 Italian elderly women.<br />

Abbreviations: R 2 = coefficient of determination; SEE = standard error of the estimate; SEE% = percent<br />

standard error of the estimate. Modified from <strong>Bedogni</strong> et al. [18].<br />

The traditional approach <strong>to</strong> establish the accuracy of BMI as an index of body fat is <strong>to</strong><br />

perform a regression analysis as described above. Another approach, which is more suitable<br />

for screening purposes, is based on the calculation of the sensitivity (true positive rate) and<br />

specificity (true negative rate) of BMI in detecting excess body fat [19]. BMI has generally a<br />

low sensitivity and a high specificity in detecting excess adiposity. For instance, in a study of<br />

934 Italian children aged 8-12 years [20], sensitivity and specificity of BMI in detecting a<br />

value of percent body fat greater than the 85 th percentile were 0.39 and 0.99 for the 95 th<br />

percentile and 0.65 and 0.95 for the 85 th percentile of BMI, respectively. When a direct<br />

measure of adiposity is needed, skinfold thicknesses offer a low-cost and easy way <strong>to</strong><br />

evaluate subcutaneous adipose tissue [17]. In the study performed on Italian children [20], the<br />

sensitivity of the log-transformed sum of four skinfolds (biceps, triceps, subscapular and<br />

suprailiac [14]) in detecting excess adiposity were 0.75 and 0.94 for the 85 th percentile. Thus,<br />

the use of the 85 th percentile of the sum of four skinfolds instead of the 85 th percentile of BMI<br />

may increase the sensitivity of screening programs of excess adiposity in children without any<br />

relevant loss in specificity.<br />

The use of BMI as an index of adiposity is more difficult in children than in adults<br />

because of varying growth rates and maturity levels [21]. Standardization of BMI for age is<br />

always necessary in children <strong>to</strong> avoid spurious interpretations [21]. Likewise, similar values<br />

of BMI may reflect a different body composition in elderly as compared <strong>to</strong> young adults [22].<br />

For instance, when matched with young women of similar weight and stature, elderly women<br />

have higher body fat and lower fat-free mass, <strong>to</strong>tal body water and bone mineral content [23].<br />

There is also increasing evidence that the relationship between body fat and BMI may differ<br />

among individuals of different ethnic background [24, 25]. This evidence, <strong>to</strong>gether with that<br />

derived from epidemiological studies of morbidity and mortality (see next paragraph), has<br />

suggested the need of ethnic-specific BMI cut-off points [26].


<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: <strong>From</strong> <strong>Quételet</strong> <strong>to</strong> <strong>Evidence</strong>-Based Medicine 5<br />

<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong> as A Prognostic Indica<strong>to</strong>r<br />

The great success encountered by BMI in our century is largely explained by its<br />

prognostic ability [22, 27-30]. The degree <strong>to</strong> which the association between BMI and disease<br />

is influenced by body fat is not yet known but it must remembered that BMI is not a pure<br />

index of body fat [5, 13]. For instance, both BMI and skinfolds are associated with disease<br />

[31-33] but the relationships are different so that studies using BMI as an index of adiposity<br />

should be interpreted with caution [33]. In addition, many fac<strong>to</strong>rs influence the association<br />

between BMI and disease, the most significant being age, gender, ethnic background, dietary<br />

habits, physical activity and body fat distribution [13].<br />

After an extensive review of the literature, the World Health Organization has classified<br />

the diseases associated with a high BMI in adults in three categories [27]: 1) the first (slightly<br />

increased risk, i.e. relative risk comprised between 1.0 and 2.0) includes cancer (breast,<br />

endometrium and colon), alterations of reproduction and fertility, polycystic ovary syndrome,<br />

low back pain, increased anesthetic risk and fetal defects; 2) the second (moderately<br />

increased risk, i.e. relative risk comprised between 2.0 and 3.0) includes chronic heart<br />

disease, hypertension, osteoarthritis (knees), hyperuricemia and gout; and 3) the third (greatly<br />

increased risk, i.e. relative risk greater than 3.0) includes gallbladder disease, dyslipidemia,<br />

insulin resistance, breathlessness and sleep apnea. In the last years, obesity has also emerged<br />

a strong risk fac<strong>to</strong>r for fatty liver [34]. In line with this conclusion is the finding that BMI is<br />

the single best predic<strong>to</strong>r of an elevated alanine aminotransferase level in the general<br />

population [35].<br />

BMI may be associated with disease also during childhood and adolescence [15, 16, 36].<br />

The World Health Organization has classified the health consequences of obesity in children<br />

in three categories [27]: 1) the first category (high prevalence) includes faster growth,<br />

psychosocial problems, persistence in<strong>to</strong> adulthood (for late onset and severe obesity),<br />

dyslipidemia and high blood pressure (not frank hypertension); 2) the second category<br />

(intermediate prevalence) includes fatty liver, abnormal glucose metabolism and persistence<br />

in<strong>to</strong> adulthood (depending on age of onset and severity); and 3) the third category (low<br />

prevalence) includes orthopedic complications, sleep apnea, polycystic ovary syndrome,<br />

pseudotumor cerebri, gallbladder disease and hypertension.<br />

Most of the available data on the relationship between weight and mortality support the<br />

hypothesis of a curvilinear (J-shaped) association, with an increased risk of death among the<br />

very heavy and the very lean [37-52]. However, most of the studies suggesting that leanness<br />

may be a risk fac<strong>to</strong>r for death have been criticized for not having excluded smokers and<br />

subjects with coexisting disease [27, 53, 54]. On the other hand, some studies controlling for<br />

smoking status and concomitant disease have suggested that the relationship between excess<br />

weight and the risk of death may be linear, without an excess of mortality among the very<br />

lean [45, 46, 49, 51]. However, the lowest mortality rate was always found in subjects with a<br />

value of BMI comprised between 18.5 and 25.0 kg/m 2 and this explains the choice of the cutpoints<br />

for normal weight made by the World Health Organization [27] (see next paragraph).<br />

A recent study, performed in more than 1 million US individuals followed for 14 years,<br />

supports the hypothesis of a J-shaped relationship between BMI and mortality [55]. A


6<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, Claudio Tiribelli and Stefano Bellentani<br />

curvilinear association between BMI and mortality was in fact detected in: 1) current or<br />

former smokers with a his<strong>to</strong>ry of disease; 2) current or former smokers without a his<strong>to</strong>ry of<br />

disease; 3) subjects who had never smoked and with a his<strong>to</strong>ry of disease; and 4) subjects who<br />

had never smoked and without a his<strong>to</strong>ry of disease. In line with the expectations, smoking and<br />

a his<strong>to</strong>ry of disease increased the risk of mortality among the very lean and the very heavy. In<br />

healthy people who had never smoked, the nadir of the curve for BMI and mortality was<br />

found at a value of BMI of 23.5 <strong>to</strong> 24.9 kg / m 2 in men and 22.0 <strong>to</strong> 23.4 kg / m 2 in women.<br />

White males and females with BMI of 40.0 kg / m 2 and over had a relative risk of death of<br />

2.58 and 2.00, respectively, as compared with those with a BMI between 23.5 and 24.9 kg /<br />

m 2 (Figure 3). Black men and women with the highest BMI had however lower risks of death<br />

(1.35 and 1.21). A high BMI was most predictive of death from cardiovascular disease,<br />

especially in men. Collectively, the risk of death from all causes increased throughout the<br />

range of moderate and severe overweight for both men and women in all age groups.<br />

Figure 3. Relationship between the risk of death and BMI in US white mean and women. The graph<br />

was drawn from the data of Calle et al. [55].


<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: <strong>From</strong> <strong>Quételet</strong> <strong>to</strong> <strong>Evidence</strong>-Based Medicine 7<br />

A recent study, performed on about 900000 US individuals followed for 16 years, offers<br />

important new information on the relationship between BMI and the risk of death from cancer<br />

[56]. In men with BMI ≥ 40 kg/m 2 , the relative risk of death from cancer was 1.52 as<br />

compared <strong>to</strong> men with BMI between 18.5 and 24.9 kg/m 2 ; in women with BMI ≥ 40 kg/m 2 ,<br />

the relative risk of death from cancer was 1.62 as compared <strong>to</strong> women with BMI between<br />

18.5 and 24.9 kg/m 2 . In both genders, BMI was significantly associated with higher rates of<br />

death due <strong>to</strong> cancer of the esophagus, colon and rectum, liver, gallbladder, pancreas, and<br />

kidney; the same was observed also for death due <strong>to</strong> non-Hodgkin’s lymphoma and multiple<br />

myeloma. Significant trends of increasing risk with higher BMI values were observed for<br />

death from cancers of the s<strong>to</strong>mach and prostate in men and for death from cancers of the<br />

breast, uterus, cervix, and ovary in women. On the basis of these associations, it was<br />

estimated that the current patterns of overweight in the United States may account for 14 and<br />

20 percent of all deaths from cancer in men and women respectively [56].<br />

<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong> at Work<br />

The classification of overweight proposed by the World Health Organization for adults is<br />

given in Table 1 [27]. This classification, based on the association between BMI and<br />

mortality (see previous paragraph), may not apply <strong>to</strong> non-caucasian populations [27]. This has<br />

been reemphasized more recently by an ad hoc committee of the World Health Organization<br />

asked <strong>to</strong> assess the need of different BMI cut-points for different ethnic backgrounds [26]. It<br />

should be noted that in this classification the term “overweight” applies <strong>to</strong> every value of<br />

BMI equal or greater than 25.0 kg/m 2 so that obesity (BMI equal or greater than 30 kg/m 2 ) is<br />

a “special case” of overweight [27]. In the classification of the US Expert Panel on the<br />

Identification, Evaluation and Treatment of Overweight in Adults [29], the term “overweight”<br />

is used instead <strong>to</strong> label a value of BMI comprised between 25.0 and 29.9 kg/m 2 . A<br />

classification of overweight for children should ideally be based on an association of BMI<br />

with disease such as that recognized for adults [57-59]. Because of the scarcity of data,<br />

however, BMI has been proposed as an index of adiposity in children mainly because of its<br />

association with adult BMI [15, 16, 60, 61]. The International Obesity Task Force (IOTF) has<br />

suggested <strong>to</strong> employ a value of BMI greater than the 95 th percentile for age <strong>to</strong> diagnose<br />

“overweight” and one comprised between the 85 th and 95 th percentile for age <strong>to</strong> diagnose a<br />

“risk of overweight” in children [15, 16, 62]. Cole et al. have developed international<br />

reference values of BMI <strong>to</strong> be used in children and adolescents [62]. They have averaged the<br />

centile curves of about 190000 children aged 2-18 years obtained from six cross-sectional<br />

studies (Brazil, Great Britain, Hong Kong, Netherlands, Singapore and United States) and<br />

developed age- and sex-specific cut-points that, at an age of 18 years, pass through the cutpoints<br />

of 25.0 and 30.0 kg/m 2 , the values used <strong>to</strong> define adult overweight and obesity (Table<br />

2). Even if this definition is less arbitrary than others and offers the possibility of performing<br />

international comparisons, it should not be considered alternative <strong>to</strong> the use of local reference<br />

values (when available) because the two methods give often discordant results [63-65]. There<br />

is also some controversy as <strong>to</strong> whether BMI has the same prognostic value in adult and<br />

elderly subjects. The relative risk of death associated with adiposity seems in fact <strong>to</strong> decrease


8<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, Claudio Tiribelli and Stefano Bellentani<br />

with increasing age [40, 46, 47, 50, 51]. In the study of Calle et al. [55], however, both<br />

relative and absolute measures of risk indicated that heavier men and women have an<br />

increased risk of death at all ages. The optimal BMI for longevity fell between 20.5 and 24.9<br />

kg/m 2 for men and women at all ages.


<strong>Body</strong> <strong>Mass</strong> <strong>Index</strong>: <strong>From</strong> <strong>Quételet</strong> <strong>to</strong> <strong>Evidence</strong>-Based Medicine 9<br />

Table 1. Classification of <strong>Body</strong> <strong>Mass</strong> <strong>Index</strong> (BMI) for Adults [17] (See Text)<br />

Classification BMI (kg / m 2 ) Risk of co-morbidities<br />

Underweight < 18.5 Low (but risk of other problems increased)<br />

Normal range 18.5 – 24.9 Average<br />

Overweight ≥ 25.0 -<br />

Pre-obese 25.0 – 29.9 Increased<br />

Obese class I 30.0 – 34.9 Moderate<br />

Obese class II 35.0 – 39.9 Severe<br />

Obese class III ≥ 40.0 Very severe<br />

Table 2. International cut-off Points of BMI<br />

for the Diagnosis of Overweight and Obesity in Children Defined<br />

<strong>to</strong> Pass through BMI of 25 and 30 kg/m 2 at Age 18 [62] (See Text)<br />

Age (years) BMI 25 kg / m2 BMI 30 kg / m 2<br />

Males Females Males Females<br />

2 18.41 18.02 20.09 19.81<br />

2.5 18.13 17.76 19.80 19.55<br />

3 17.89 17.56 19.57 19.36<br />

3.5 17.69 17.40 19.39 19.23<br />

4 17.55 17.28 19.29 19.15<br />

4.5 17.47 17.19 19.26 19.12<br />

5 17.42 17.15 19.30 19.17<br />

5.5 17.45 17.20 19.47 19.34<br />

6 17.55 17.34 19.78 19.65<br />

6.5 17.71 17.53 20.23 20.08<br />

7 17.92 17.75 20.63 20.51<br />

7.5 18.16 18.03 21.09 21.01<br />

8 18.44 18.35 21.60 21.57<br />

8.5 18.76 18.69 22.17 22.18<br />

9 19.10 19.07 22.77 22.81<br />

9.5 19.46 19.45 23.39 23.46<br />

10 19.84 19.86 24.00 24.11<br />

10.5 20.20 20.29 24.57 24.77<br />

11 20.55 20.74 25.10 25.42<br />

11.5 20.89 21.20 25.58 26.05<br />

12 21.22 21.68 26.02 26.67<br />

12.5 21.56 22.14 26.43 27.24<br />

13 21.91 22.58 26.84 27.76<br />

13.5 22.27 22.98 27.25 28.20<br />

14 22.62 23.34 27.63 28.57<br />

14.5 22.96 23.66 27.98 28.87<br />

15 23.29 23.94 28.30 29.11<br />

15.5 23.60 24.17 28.60 29.29<br />

16 23.90 24.37 28.88 29.43<br />

16.5 24.19 24.54 29.14 29.56<br />

17 24.46 24.70 29.41 29.69<br />

17.5 24.73 24.85 29.70 29.84<br />

18 25 25 30 30


10<br />

<strong>Giorgio</strong> <strong>Bedogni</strong>, Claudio Tiribelli and Stefano Bellentani<br />

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