Body surface area determined by whole-body CT scanning: Need for new formulae? Clinical Physiology...

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ORIGINAL ARTICLE Body surface area determined by whole-body CT scanning: need for new formulae? Chiara Villa 1 , Charlotte Primeau 1 , Ulrik Hesse 2 , Hans Petter Hougen 1 , Niels Lynnerup 1 and Birger Hesse 3 1 Department of Forensic Medicine, University of Copenhagen, 2 Health data and Information and Communication Technology, Statens Serum Institut, and 3 Clinic of Clinical Physiology, Nuclear Medicine and PET, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark Summary Correspondence Chiara Villa, Laboratory of Biological Anthropology, Department of Forensic Medicine, University of Copenhagen, Frederik V’s Vej 11, DK-2100 Copenhagen, Denmark E-mail: [email protected] Accepted for publication Received 11 August 2014; accepted 26 June 2015 Key words body mass index; body surface area; cadavers; CT scans; males; overweight subject Calculation of the estimated body surface area (BSA) by body height and weight has been a challenge in the past centuries due to lack of a well-documented gold standard. More recently, available techniques such as 3D laser surface scanning and CT scanning may be expected to quantify the BSA in an easier and more accurate way. This study provides the first comparison between BSA obtained from post-mortem whole-body CT scans and BSA calculated by nine predictive formulae. The sample consisted of 54 male cadavers ranging from 20 to 87 years old. 3D reconstructions were generated from CT scans using Mimics software, and BSA values were automatically extracted from the program. They were compared with nine predictive equations from the literature. Remarkably, close correlations (r > 0 90) were found between BSA values from CT scans and those from the predictive formulae. A mean BSA of the 54 cadavers of 1 841 87 m 2 was calculated by all formulae except one, SD values varying between 0 171 and 0 223 m 2 . T-tests revealed significant differences between mean BSA values calculated with CT and three of the formulae. Regression analyses showed inter- cepts >(0;0) and slopes <1 0 using all predictive equations, with the CT scan determination as gold standard. It is concluded that DuBois and DuBois’ equation can be safely used in normal-weight male subjects with high accuracy, but it seems likely that BSA is underestimated in underweight subjects and overesti- mated in overweight individuals. Creation of new formulae specific for over- weight subjects and children may be needed. Introduction Body surface area (BSA) is an important measurement in many physiological and pharmacological applications, and in several relations, it has been considered a better indicator of metabolic mass than individual’s weight, height or body mass index (BMI). The determination of BSA has been a challenge in the past centuries, and many BSA formulae have been developed over the years. The DuBois brothers (1916) were the first who empirically measured and derived a BSA equa- tion; their formula is still widely used even though it was based on only nine subjects. In the following years, other researchers proposed new equations based on larger numbers of subjects and using more robust statistical techniques (Boyd, 1935; Gehan & George, 1970; Haycock et al., 1978; Mosteller, 1987; Shuter & Aslani, 2000). However, excellent correlations and very similar results were demonstrated (Verbraecken et al., 2006) and no improvement using new formulae compared to the original one has been created. On the other hand, criticism has been raised about the use of the DuBois and DuBois equation in children and obese patients; indeed, specific formulae have been derived for both categories (Haycock et al., 1978; Livingston & Lee, 2001). After about one century, new formulae are still being developed, in particular using techniques such as 3D laser sur- face scan and CT scanning that may be expected to quantify the BSA in an easier and more accurate way. Surface scanning has been extensively tested by Jones et al. (1994), Tikuisis et al. (2001), Yu et al. (2003; 2010) and discussed in detail by Daniell et al. (2012). Conversely, only one pilot study on eight Clin Physiol Funct Imaging (2015) doi: 10.1111/cpf.12284 1 © 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Transcript of Body surface area determined by whole-body CT scanning: Need for new formulae? Clinical Physiology...

ORIGINAL ARTICLE

Body surface area determined by whole-body CT scanning:need for new formulae?Chiara Villa1, Charlotte Primeau1, Ulrik Hesse2, Hans Petter Hougen1, Niels Lynnerup1 and Birger Hesse3

1Department of Forensic Medicine, University of Copenhagen, 2Health data and Information and Communication Technology, Statens Serum Institut,

and 3Clinic of Clinical Physiology, Nuclear Medicine and PET, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark

Summary

CorrespondenceChiara Villa, Laboratory of Biological

Anthropology, Department of Forensic Medicine,

University of Copenhagen, Frederik V’s Vej 11,

DK-2100 Copenhagen, Denmark

E-mail: [email protected]

Accepted for publicationReceived 11 August 2014;

accepted 26 June 2015

Key words

body mass index; body surface area; cadavers; CT

scans; males; overweight subject

Calculation of the estimated body surface area (BSA) by body height and weighthas been a challenge in the past centuries due to lack of a well-documented goldstandard. More recently, available techniques such as 3D laser surface scanningand CT scanning may be expected to quantify the BSA in an easier and moreaccurate way. This study provides the first comparison between BSA obtainedfrom post-mortem whole-body CT scans and BSA calculated by nine predictiveformulae. The sample consisted of 54 male cadavers ranging from 20 to 87 yearsold. 3D reconstructions were generated from CT scans using Mimics software,and BSA values were automatically extracted from the program. They werecompared with nine predictive equations from the literature. Remarkably, closecorrelations (r > 0�90) were found between BSA values from CT scans and thosefrom the predictive formulae. A mean BSA of the 54 cadavers of 1�84–1�87 m2

was calculated by all formulae except one, SD values varying between 0�171 and0�223 m2. T-tests revealed significant differences between mean BSA valuescalculated with CT and three of the formulae. Regression analyses showed inter-cepts >(0;0) and slopes <1�0 using all predictive equations, with the CT scandetermination as gold standard. It is concluded that DuBois and DuBois’ equationcan be safely used in normal-weight male subjects with high accuracy, but itseems likely that BSA is underestimated in underweight subjects and overesti-mated in overweight individuals. Creation of new formulae specific for over-weight subjects and children may be needed.

Introduction

Body surface area (BSA) is an important measurement in

many physiological and pharmacological applications, and in

several relations, it has been considered a better indicator of

metabolic mass than individual’s weight, height or body mass

index (BMI). The determination of BSA has been a challenge

in the past centuries, and many BSA formulae have been

developed over the years. The DuBois brothers (1916) were

the first who empirically measured and derived a BSA equa-

tion; their formula is still widely used even though it was

based on only nine subjects. In the following years, other

researchers proposed new equations based on larger numbers

of subjects and using more robust statistical techniques (Boyd,

1935; Gehan & George, 1970; Haycock et al., 1978; Mosteller,

1987; Shuter & Aslani, 2000). However, excellent correlations

and very similar results were demonstrated (Verbraecken et al.,

2006) and no improvement using new formulae compared to

the original one has been created.

On the other hand, criticism has been raised about the use

of the DuBois and DuBois equation in children and obese

patients; indeed, specific formulae have been derived for both

categories (Haycock et al., 1978; Livingston & Lee, 2001).

After about one century, new formulae are still being

developed, in particular using techniques such as 3D laser sur-

face scan and CT scanning that may be expected to quantify

the BSA in an easier and more accurate way. Surface scanning

has been extensively tested by Jones et al. (1994), Tikuisis

et al. (2001), Yu et al. (2003; 2010) and discussed in detail by

Daniell et al. (2012). Conversely, only one pilot study on eight

Clin Physiol Funct Imaging (2015) doi: 10.1111/cpf.12284

1© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

whole-body CT scans has been carried out in oncology

patients (Martinez-M€oller et al., 2007), and a formula derived

using parameters was obtained from a single abdominal CT

image (Geraghty & Boone, 2003). The reason for the very

limited number of studies is that healthy individuals should

not be exposed to the rather high radiation exposure from a

whole-body CT scan. On the other hand, CT scans of cadavers

is regularly performed before autopsy in many forensic

departments, with the advantage that an immense amount of

data in digital format is collected. Thus, BSA can be calculated

using postprocessing software.

The purpose of this study was to calculate the BSA using

whole-body CT scans of adult, male cadavers and to compare

the obtained results with those calculated using nine formulae

reported in the literature, to evaluate the necessity of creating

new formulae.

Materials and methods

The sample consisted of 54 whole-body CT scans of male

cadavers of Caucasian origin ranging from 20 to 87 years old

with a varying body mass index (BMI: three underweight

men (BMI <18�5 kg m�2); 32 normal-weight men (BMI

18�5–24�9 kg m�2); 19 overweight men (BMI ≥25 kg m�2).

There was only one obese person (BMI 30�9 kg m�2), and

we decided to group together with the overweight subjects.

All the information for each subject about age, nationality,

weight, height and BMI, as well as BMI group, is reported in

appendix 1. The bodies were scanned within three days from

the time of death and showed no or very limited signs of

decomposition. The scans were performed using a Siemens

Sensation 4 CT scanner with the following scan settings:

120 kV, 112�50 mAs, 3 mm slice thickness, 2 mm increment

and a B31f reconstruction algorithm. The whole-body scans

were performed in two or three (n = 11) parts. All bodies

were scanned in the supine position with the arms over the

head. The head and upper part of the body was scanned first

with the head first in, and then, the body was turned around

on the gantry couch, still in the supine position, and the

lower part of the body was scanned with feet first in. In cases

of three scannings, head, upper body and lower body were

scanned separately, with head first in for the first two scans,

then with feet first in for the lower body. Overlapping areas

were kept to allow registration of the CT scan image. Particu-

lar care was taken to ascertain that good overlapping of the

scans made it possible to accurately align the two (or three)

parts of the body in the computer model. Only, individuals

with intact skin and without post-mortem bloating were

included in the study.

3D visualization of the whole body was created using Mim-

ics software (Materialise Interactive Medical Image Control

System, NV Technologielaan Belgium Materialise), an image

processing software for 3D design and modelling. BSA values

were automatically extracted from the 3D reconstructions of

the bodies generated from the CT scans. All the internal

cavities filled with air were ‘closed’, and surfaces such as

regions between the legs, the arms and the chin, where differ-

ent skin areas are in contact, were separated (Fig. 1). Particu-

lar attention was also paid to the hands, because some

subjects were in a relaxed position while others held their

hands in a clenched fist or somewhere in-between resulting in

incorrect surface area determinations (Fig. 1). The surface of

the hands of 10 individuals (two underweight, four normal-

weight, four overweight subjects) was accurately segmented.

Independently of the BMI, the surface area of the segmented

hands was approximately 5% (ranges 4�0–6�0%) of the

remaining body surface area. Therefore, to calculate the BSA,

we used the surface area obtained from the 3D visualization

of the body without the hands and then added 5% of the val-

ues to obtain total BSA.

The BSA values of the 54 cadavers were also calculated from

their height and weight using nine equations (Table 1)

reported in the literature.

Statistics

The statistical analyses were performed using SPSS version

20 (IBM Corp., Chicago, IL, USA) and SAS version 9.3 (SAS

Institute Inc., Cary, NC, USA). We calculated mean BSA and

SD in m2 of the 54 cadavers from CT scans and estimated

their BSA values using the predictive formulae. Pearson’s

correlation coefficients and average differences (mean and

SD) were calculated between our CT scans and the formulae.

Student’s t-test was performed to evaluate the difference

between the BSA means; linear regression was used to esti-

mate regression lines. In addition, we used scatter plots of

the BSA from CT scans against BSA from the formulae and

Bland–Altman plots (1986) to visualize the agreement

between the methods.

Results

The mean value of BSA determined from CT scans was very

similar to that calculated using previously published predictive

formulae (Table 2): a mean BSA of the 54 male cadavers

between 1�84 and 1�87 m2 was determined by our CT

scanning and those calculated by all the formulae except one

(Yu et al., 2003). SD values varied between 0�171 and 0�223,and the lowest SD being calculated by our determinations.

Using Gehan and George’s formula, slightly higher BSA values

were calculated compared with the determination from our

CT scans, with the lowest average difference of 0�1%. Contrar-ily, the formula of Yu et al. (2003) consistently gave lower

BSA values (1�78 m2) with an average difference of 4�9%.Comparison with our BSA measurements the formula of Yu

et al. (2003) and also the formulae of Shuter & Aslani (2000)

and Tikuisis et al. (2001) gave statistically significant differ-

ences (Table 2). Appendix 1 reports the BSA values for each

subject obtained from CT scans and calculated using the nine

literature formulas.

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al.2

Remarkably close correlations (r > 0�90) were found

between BSA values calculated from the CT scans and those

from the formulae in the literature (Table 2). However,

systematic variations are observed when our own BSA deter-

minations are compared with those calculated using the

formulae of Yu et al. (2003), Shuter & Aslani (2000), and to

some degree also using Tikuisis et al. (2001), cf. Fig. 2: the

majority of the BSA values lie to the left of the line of equal-

ity, that is line of perfect agreement (r = 1). Livingston and

Lee’s formula shows a slightly lower correlation (0�947) with

Table 1 BSA predictive equations used in the study.

References Year

Technique for

BSA determination Subjects

Different

BMI

Children/

Infants Equations

DuBois & DuBois (1916) 1916 Coating 9 Yes Yes BSA = 0�007184 9 H0�725 9 W0�425

Boyd (1935) 1935 Coating, surfaceintegration, triangulation

197 No Yes BSA = 0�017827 9 H0�5 9 W0�484

Gehan & George (1970) 1970 Coating, surfaceintegration, triangulation

401 No Yes BSA = 0�0235 9 H0�42246 9 W0�51456

Haycock et al. (1978) 1978 Linear geometry 81 Yes Yes BSA = 0�024265 9 H0�3964 9 W0�5378

Shuter & Aslani (2000) 2000 Coating andlinear geometry

42 No No BSA = 0�00949 9 H0�655 9 W0�441

Livingston & Lee (2001) 2001 Linear geometry 18 M29 F

Yes No BSA = 0�1173 9 W0�6466

Tikuisis et al. (2001) 2001 Surface scanning 395 M246 F

Yes No BSA = 0�0128 9 H0�6 9 W0�44(male)

Yu et al. (2003) 2003 Surface scanning 1814 M2137 F

No No BSA = 0�015925 9 (H 9 W)0�50

Yu et al. (2010) 2010 Surface scanning 135 M135 F

Yes No BSA = 0�00713989 9 H0�7437 9 W0�4040

BSA is expressed in square metre, height (H) in centimetre and weight (W) in kilogram.

(a) (b)

(c) (d)

Figure 1 3D visualizations of the hands andthe area of the chin/shoulder: (a) and (b)show the unsegmented touching skin surfaces;(c) and (d) show the same surfaces aftermanual editing. The arrows indicate the areaswhere manual separation of the surfaces wasperformed.

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al. 3

our CT scans and has a large SD (0�2 m2): individuals with

BSA lower than 1�7 m2 were always overestimated and those

with BSA of ≥2�1 m2 underestimated.

The Bland–Altman plots (Fig. 3) visualize the agreements

between BSA determined by CT scans and those calculated by

the predicted formulae. If the individuals are divided into the

Table 2 BSA values obtained from CT scans and calculated using predictive equations.

Equations according to references

BSA (m2) Pearson’scorrelation

coefficient (r)

Average differencesfrom CT scans (m2) t-test

Mean BSA SD Mean (%) T P

CT scans 1�873 0�171 – – – –DuBois & DuBois (1916) 1�866 0�185 0�970* 0�006 (0�3) 0�046 0�995 0�324Boyd (1935) 1�860 0�191 0�970* 0�013 (0�7) 0�049 1�907 0�062Gehan & George (1970) 1�874 0�199 0�968* �0�002 (0�1) 0�055 �0�228 0�821Haycock et al. (1978) 1�868 0�205 0�967* 0�004 (0�2) 0�059 0�550 0�585Shuter & Aslani (2000) 1�839 0�183 0�971* 0�034 (1�8) 0�045 5�615 <0�001Livingston & Lee (2001) 1�854 0�223 0�947* 0�019 (1�0) 0�082 1�697 0�096Tikuisis et al. (2001) 1�858 0�182 0�971* 0�014 (0�7) 0�044 2�424 0�019Yu et al. (2003) 1�782 0�189 0�970* 0�091 (4�9) 0�048 14�016 <0�001Yu et al. (2010) 1�868 0�179 0�969* 0�005 (0�3) 0�045 0�801 0�427

This table shows the BSA (mean, SD), average differences (mean and SD), correlation coefficients and t-test results from comparison between BSAvalues from CT scans and BSA values calculated using predictive equations.*P < 0�001.

Figure 2 Scatter plots of BSA from CT scans (y-axis) and BSA from the predictive equations (x-axis), with line of equality.

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al.4

BMI groups (underweight, normal-weight and overweight),

presented by increasing size of the circles, the differences are

obvious. As mentioned above, the BSA values calculated from

our CT scans are very closely correlated in the far majority of

moderately underweight and normal-weight subjects with val-

ues calculated by the other formulae mentioned above. In

other words, most of the formulae work well for average BSA

values. But regression analyses show that with a as the inter-

cept and b as the slope, all nine equations have intercepts

above (0;0) and slopes less than 1�0 (Table 3). This suggests

that very low BSA values, that is BSA of children, could be

overestimated and high BSA values probably underestimated

with other formulae if our determinations are correct. The

BSA values in the four overweight subjects are near or actually

outside the statistical limit of agreement (>mean � 2SD), sug-

gesting that BSA is overestimated by the predictive formulae.

The plot comparing the difference between our CT scans

and the calculations using the formula by Livingston & Lee

(2001) demonstrates that our underweight cadavers are signif-

icantly underestimated using their formula. Furthermore, the

regression analysis and the t-test both show that the formula

by Yu et al. (2003) deviates most from our CT results. The

visual impression from some of the plots in Fig. 2 also shows

a clear trend of a positive intercept and a reduced (<1) slope.

Figure 3 Bland–Altman plots of the difference in BSA as a function of the mean BSA based on CT scans and BSA based on the predictive equations.The solid line indicates the mean difference, and the two dotted lines indicate mean � 2SD. BMI groups are reflected in the size of the points.

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al. 5

Discussion

This study provides the first comparison between BSA

obtained from post-mortem CT scans and BSA calculated by

predictive formulae reported in the literature, based on

different techniques including linear geometry, coating, trian-

gulation and more recent techniques like 3D surface scanning.

We found close agreement between the BSA values

determined in the adult male cadavers examined with our CT

scannings with Mimics software analyses, and values calculated

from the height and weight of the cadavers using existing for-

mulae, giving average differences of about 1% or less. As also

previously suggested (Livingston & Lee, 2001; Sardinha et al.,

2006; Verbraecken et al., 2006; Daniell et al., 2012), we

observed that BSA in the few overweight individuals is appar-

ently overestimated (Table 3). Livingston & Lee (2001)

developed a formula to improve the accuracy of overweight

subjects based on a population of 81 overweight or obese

subjects individuals. However, their formula did not improve

the accuracy of our four overweight subjects. On the contrary,

our determinations suggest significant disagreement with the

formula by Livingston & Lee (2001) both in overweight and

underweight subjects (Fig. 3), in line with the analysis of

Daniell et al. (2012), who found a similar discrepancy

between BSA values calculated by the Livingston and Lee

equation versus their 3D surface scanning.

The comparison between calculations from our CT scans

and the formulae of DuBois & DuBois (1916), Gehan &

George (1970) and Haycock et al. (1978), respectively, shows

very strong correlations and very low average differences

(0�3% or lower). Once again, in spite of the extremely limited

number of nine subjects examined in their study, the present

investigation confirms that the formula by DuBois and DuBois

produces accurate BSA values in normal-weight, male subjects.

Interesting is the comparison between the BSA generated

from the most recent techniques, that is the CT and the laser

scanners that may be anticipated to quantify BSA in a more

accurate way. We tested three formulae and found statistically

significant differences (P<0�05) between the BSA means for

two of the methods. Using the formula of Tikuisis et al.

(2001), BSA is underestimated in many subjects. The differ-

ences with the predictive formula reported by Tikuisis et al.

(2001) in their laser scanner study are very similar to our

results: they found an average difference of 0�32% with

DuBois & DuBois (1916), 0�54% with Boyd (1935) and

0�02% with Gehan & George (1970). Furthermore, in agree-

ment with our results they found an average difference of

around 1�6% with Shuter and Aslani’s formula. They reported

that their technic could be less accurate in some areas of the

body, including the upper arm, between the thighs and

around the ear, leading to an underestimation of BSA. The

lowest agreement was found with Yu et al. (2003); they

developed their formula also by laser surface scanning in a

Chinese population. The discrepancies between our data and

the values calculated from their formula were not unexpected

because high differences between BSA from surface scanner

and the predictive formulae were also reported by the authors

in relation to other predictive formulae: 3% with DuBois &

DuBois (1916), 2�1% with Shuter & Aslani (2000), 2�6% with

Boyd (1935), 5�7% with Gehan & George (1970) and 5�3%with Haycock et al. (1978). These differences could be due to

methodological differences in ancestry composition, resulting

in a significantly smaller mean body BMI and BSA. In a more

recent study, Yu and other colleagues (Yu et al., 2010) devel-

oped another formula based on Taiwanese subjects using a

more sophisticated laser scanner system and found an average

difference of 0�39% with DuBois and DuBois formula. We

also found much better agreement with the more recent study

and difference of 0�3%.Using whole-body CT scans, only one pilot study was

performed (Martinez-M€oller et al., 2007); the authors used the

whole-body CT of nine living subjects and reported,

differently from our results, a higher percentage of average

differences with DuBois and DuBois (2�2%) and Gehan and

George (2�5%). This may be due to their small sample size.

The use of the CT scans to calculate BSA has several advan-

tages compared with a surface scanner. The CT scanning does

not present any difficulty in areas where fat deposits artificially

enclose the space, like the regions between thighs or under

the upper arms: these areas can be easily corrected. Moreover,

no surfaces of the body cannot be properly scanned by a CT

scanner, nor is there any need to restore gaps in certain criti-

cal areas in the 3D models. These problems were reported by

Tikuisis et al. (2001) for areas such as ears, hands and feet

using a laser scanner.

Unfortunately, a true gold standard is very complicated to

create for BSA determination except by the hard and original

Table 3 CT scan as a function of the different formulae.

Estimate SE

DuBois & DuBois (1916) Intercept (a) 0�197 0�059Slope (b) 0�898 0�031

Boyd (1935) Intercept (a) 0�260 0�056Slope (b) 0�867 0�030

Gehan & George (1970) Intercept (a) 0�315 0�056Slope (b) 0�831 0�030

Haycock et al. (1978) Intercept (a) 0�367 0�055Slope (b) 0�806 0�029

Shuter & Aslani (2000) Intercept (a) 0�207 0�058Slope (b) 0�906 0�031

Livingston & Lee (2001) Intercept (a) 0�523 0�064Slope (b) 0�728 0�034

Tikuisis et al. (2001) Intercept (a) 0�175 0�058Slope (b) 0�914 0�031

Yu et al. (2003) Intercept (a) 0�306 0�055Slope (b) 0�879 0�031

Yu et al. (2010) Intercept (a) 0�143 0�062Slope (b) 0�926 0�033

CT scan = a + bx, a being the intercept, b the slope and x the valuecalculated from the different formulae.

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al.6

way of DuBois & DuBois (1916). In our opinion, the surface

area measurement from the CT scanner is very accurate: CT

scanning can easily detect the edge of the body; the thin slice

thickness gives detailed information of the body surface; and

modern postprocessing software can easily create 3D of the

body, based on the differences of HU values between the air

and the skin. In addition, we think it is reasonable to assume

the errors of the CT scanner and the software are negligible.

In fact, BSA values in normal-weight subjects calculated in 3D

models from CT scans are very similar to those calculated with

other techniques. However, in the extremes cases (overweight

individuals), we find some fairly consistent trends suggesting

that the predictive formulae in the literature (including DuBois

& DuBois) may give erroneous results, a point of view that

has been repeatedly expressed in the literature. Thus, our

study strongly supports the need of modified formulae for

small and large BMI values.

Clinical impact of BSA calculations

The clinical importance of BSA estimations is obvious in

different areas of clinical medicine, such as standardization of

physiologic parameters like cardiac output and renal glomeru-

lar filtration rate, calculation of drug dosages and many other

areas including transplantation medicine, burn injuries and

critical care medicine.

Cardiac volumes, both cardiac output, stroke volume, and

end-diastolic and end-systolic chamber volumes, have been

normalized as the preferred parameter to body surface area

over several decades (Taylor & Tiede, 1952). Even left atrial

volume index has been shown and used as an important

prognosticator, for example in dialysis patients (Ozdogan

et al., 2010). A more recent interest has developed in sports

medicine for comparison of different types of training and

athletes regarding cardiac and left ventricular performance

assessed by normalized cardiac output and left ventricular vol-

umes (Erz et al., 2013). But obviously, the normalization may

be complicated by extreme BSA values in this population, as

recently discussed in a study on cardiac morbidity in obese

patients (Adler et al., 2013), where the authors conclude that

‘cardiac and stroke indices can be misleading relative to the

underlying raw values as a result of distortion by widely used

BSA formulae’. The same message is concluded by Adler et al.,

(2012) in their editorial about inappropriately indexed hemo-

dynamic measurements of body surface area extremes. In the

other end of the scale, that is in children, the same problems

have long been recognized, and they may get even worse in

obese children and adolescents (Ingul et al., 2010).

Accurate determination of renal function by measurement

of glomerular filtration rate (GFR) is important in several

clinical conditions such as optimal dosing of many drugs

including several cytostatic drugs, evaluation of renal disease

in children, determination of the need of dialysis in renal

insufficiency, etc. It is generally recommended to use a BSA

normalized plasma clearance measurement of a radionuclide

tracer (99mTc-labelled DTPA or 51Cr-EDTA) for accurate

determination (Fleming et al., 2004), but many attempts have

been carried out to replace the more cumbersome plasma

clearance measurement by determination of some plasma con-

centration for an estimated GFR (eGFR). Although less reliable

for a correct assessment of renal function, it has recently been

demonstrated that the clinical value of different eGFR formu-

lae is also significantly improved by normalization to BSA

(Mocroft et al., 2014). GFR normalized to BSA is furthermore

a strong predictor of development of cardiotoxicity of trastu-

zumab-based chemotherapy, independent of original cardiac

function (Russo et al., 2012). Again BSA has its shortcomings

in the extremes of the BSA curves, that is <1�6 m2 and

>2�0 m2, as recently shown (Redal-Baigorri et al., 2014). A

specific and unresolved normalization problem is related to

determination of children’s GFR, as discussed in several stud-

ies (e.g. reviewed by Filler et al., 2014).

The significance of BSA in cytostatic treatment is widely

accepted and repeatedly documented (e.g. Buzdar et al.,

2013), also for the introduction of new drugs or protocols

(e.g. Floquet et al., 2014). This has also been shown in

children (Camaione et al., 2013).

BSA is successfully applied in other areas as, for example

transplantation medicine, where both the donor and the

recipient BSA values were successfully included in the calcula-

tion of transplanted organ size (Fukazawa et al., 2013). In

anaesthesiology and critical care, medicine estimation of BSA

is frequently needed for determination of functions related to

body metabolism including ventilation, fluid requirements,

extracorporeal circulation and drug dosages (Current, 1998).

Also, for the treatment of burn injuries, BSA calculations

including the fraction of total burned surface areas are widely

used (Baryza et al., 2013).

Limitations

The sample used in our analysis was composed only of male

subjects of Caucasian origin. This means that the results

cannot be applied to women, to other ethnic groups, or to

children, without additional examinations. Indeed, Tikuisis

et al. (2001) found differences in BSA between sexes propos-

ing sex-based equations, and we found statistically, highly

significant differences with the formula developed from

Chinese population (Yu et al., 2003).

As in most other studies, we could include only few sub-

jects with high BMI. CT scanners, like MRI scanners, cannot

be used in many overweight and obese individuals, because

the typical 70 cm gantry diameter does not allow inclusion of

a total circumference of more than 58 cm, which is exceeded

in the majority of those individuals. Other techniques like a

laser scanner may be easier to use in subjects with a

BMI > 30.

If cadavers are subjected to decomposition processes, the

body surface could deviate from that of living subjects. We

carefully excluded subjects in whom putrefaction was

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al. 7

moderately advanced since that produces gas, which may

enlarge the abdomen and the scrotum. None of the cadavers

examined showed signs of putrefaction.

Finally, the surface of the hands was not determined in

each cadaver. Instead, we predicted the hand surface from the

determinations of ten subjects (as outlined in Material and

Methods). We found that the surface of two hands measured

close to 5% of the remaining body surface. Exactly, the same

percentage was reported by Tikuisis et al. (2001) and Yu et al.

(2010). In particular, the surface of the hands was accurately

measured by Yu et al. (2010) using an advanced laser scanner.

The maximum error due to this estimation of the surface of

the hands appears to be 1% of the total BSA, a small error

compared to the inaccuracy of a clinical BSA estimation based

on body height and weight.

In conclusion, we believe that our CT-based BSA calcula-

tions are more accurate than previous BSA determinations due

to the detailed information obtained of the body contour and

the well-documented software computation of the body sur-

face data. Nevertheless, we did not create a new formula, as

in agreement with several other groups, we found that the

widely employed DuBois and DuBois’ equation (1916) can

still be used quite accurately for the clinical determination of

BSA in normal-weight, Caucasian, male subjects. However,

our data suggest that BSA may be underestimated in under-

weight men and overestimated in overweight men. We do

not recommend the use of the modified formula developed

by Livingston & Lee (2001). New sex-specific formulae may

be needed, this demands further examinations in female pop-

ulation groups. New formulae should probably be developed

for overweight and obese subjects and for children.

Given the mechanical limitations of CT scanners in over-

weight subjects, surface laser scanning may be the best way to

generate new data in overweight subjects, although a signifi-

cant limitation of this method is related to the sometimes

large areas where fat deposits create closed spaces. Post-mor-

tem CT scanning may be an accurate technology to obtain sur-

face data in children and severely underweight adults and for

the examination of the influence of sex and different ethnics.

Acknowledgments

The authors would like to thank the Forensic Technicians at

the Section of Forensic Pathology (University of Copenhagen)

for helping with the data collection.

Conflict of interest

The authors have no conflict of interests.

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Appendix

1Dem

ograph

icinform

ationof

the54

Caucasian,malecadavers

(sex,age,

nation

ality,

height,weigh

t,BM

IandBM

Igrou

p)andBSA(from

CTscansandusingpredictive

equation

s)of

each

subjectinclud

edin

thestud

y.

IDSex

Age

(years)Nationality

Height

(cm)

Weight

(kg)

BMI

(kgm

�2)

BMI

groups

Bodysurface

areacalculatedusing

CT

scans

DuBois

&DuBois

(1916)

Boyd

(1935)

Gehan&

George

(1970

)

Haycock

etal.

(1978

)

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Aslani

(2000)

Livingston&

Lee

(2001)

Tikuisis

etal.

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53

(con

tinu

ed)

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al.10

Appendix

1(con

tinu

ed)

IDSex

Age

(years)Nationality

Height

(cm)

Weight

(kg)

BMI

(kgm

�2)

BMI

groups

Bodysurface

areacalculatedusing

CT

scans

DuBois

&

DuBois

(1916)

Boyd

(1935)

Gehan&

George

(1970

)

Haycock

etal.

(1978

)

Shuter&

Aslani

(2000)

Livingston&

Lee

(2001)

Tikuisis

etal.

(2001)

Yuetal.

(2003)

Yuetal.

(2010)

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53

© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd

Body surface area from CT scans, C. Villa et al. 11