Spinal Cord (2008) 46, 494–499& 2008 International Spinal Cord Society All rights reserved 1362-4393/08 $30.00
www.nature.com/sc

ORIGINAL ARTICLE
Serum leptin, abdominal obesity and the metabolic syndrome inindividuals with chronic spinal cord injury
Y Maruyama1,2, M Mizuguchi1,2, T Yaginuma1,2, M Kusaka1,2, H Yoshida2, K Yokoyama2, Y Kasahara3
and T Hosoya2
1
Division of Internal Medicine, Kanagawa Rehabilitation Hospital, Kanagawa, Japan; 2Division of Kidney and Hypertension,
Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan and 3TANITA Body Weight Scientific
Institute, Tokyo, Japan

Study Design: Cross-sectional comparison.
Objective: The mortality rate is higher in individuals with spinal cord injury (SCI), and one major cause
is cardiovascular disease (CVD). In the general population, the metabolic syndrome (MetS) is associatedwith an increased risk of CVD, and abdominal obesity is a major feature. Adipokines, secreted byadipose tissue, contribute to obesity-linked metabolic diseases. The aim of this study is to evaluate theprevalence of MetS, the components of this syndrome, especially body composition, and the relations
between adipokines and body composition, in SCI individuals.
Setting: Kanagawa Rehabilitation Hospital, Kanagawa, Japan.
Methods: Forty-four male SCI individuals (57±13 years and 28 paraplegia) and age-matched ablebodied controls were studied. Body composition was assessed by dual-energy X-ray absorptiometry(DXA) and anthropometry (waist circumference). The visceral fat area (VFA) was measured bycomputed tomography (CT). Plasma adipokine levels, including that of leptin, adiponectin andplasminogen activator inhibitor-1 (PAI-1), were measured.
Results: Overall, 43% of SCI individuals met the criteria for MetS. Total and regional fat mass (FM), as
well as VFA, were higher, whereas total and regional lean mass, except for arm, were lower than ablebodied controls. In the SCI, leptin and PAI-1 levels were positively associated and adiponectin levels
were negatively associated with waist circumference, VFA and trunk FM. In multiple regression models,
only leptin level was independently associated with waist circumference, VFA and trunk FM.
Conclusion: SCI individuals were predisposed to excessive abdominal obesity, and higher leptin levels
were strongly associated with higher prevalence of abdominal obesity in this population.
Spinal Cord (2008) 46, 494–499; doi:10.1038/sj.sc.3102171; published online 22 January 2008
Keywords: abdominal obesity; adipokine; body composition; leptin; metabolic syndrome; spinal cord

injuryIntroduction
The longevity of individuals with spinal cord injury (SCI) has
improved, but the mortality rate is still higher than that of
the general population.1 The most common underlying andcontributing cause of death is cardiovascular disease (CVD),1and the SCI population has a higher incidence of ischemic
heart disease than able-bodied population.2 Recently, thepresence of metabolic syndrome (MetS) has been used to
identify individuals at high risk for CVD in the general
population.3 MetS is characterized by low levels of highdensity lipoprotein cholesterol (HDL-C), elevated fasting
Correspondence: Dr Y Maruyama, Division of Kidney and Hypertension,
Department of Internal Medicine, The Jikei University School of Medicine,
3-25-8 Nishi-shinbashi, Minato-ku, Tokyo 105-8461, Japan.
E-mail: maruyama@td5.so-net.ne.jp
Received 16 April 2007; revised 17 October 2007; accepted 21 October 2007;
published online 22 January 2008

glucose and triglyceride (TG), abdominal obesity and highblood pressure (BP).4
Abdominal obesity is a major characteristic of MetS; it isdefined as an excess accumulation of body fat. Since
measurement of body fat accurately is not conventional ina clinical setting, body mass index (BMI) has been used as asurrogate marker. Increased BMI is associated with anincreased risk of chronic heart disease in the general
population.5 However, BMI measurements of the SCI
individuals may not be sensitive indicators, since individuals
with chronic SCI have a greater fat mass (FM) and a lower fatfree mass per unit BMI than able-bodied controls.6
Fat mass, measured by magnetic resonance imaging (MRI),
computed tomography (CT) or dual-energy X-ray absorptiometry (DXA), is more accurate compared with measurementof BMI. Furthermore, simple anthropometric measurements,

Leptin, body composition and MetS in SCI individuals
Y Maruyama et al495such as waist circumference, can also be used. On the basis ofthese specific markers, several studies have shown that SCI
individuals have a lower total body and regional lean mass(LM), especially in lower limb, and a higher FM thancontrols.7–9
Adipose tissue is an important secretory organ that
produces various bioactive substances known as adipokines,
which include leptin, tumor necrosis factor-a, adiponectin
and plasminogen activator inhibitor-1 (PAI-1); they contribute to obesity-linked metabolic and vascular diseases, aswell as MetS.10 In the SCI population, correlation between
adipokine levels and body composition is assumed to bedifferent from that in general population because ofdifferences in location of adipose tissue. Additionally, it isstill unknown as to which types of the adipokine levels canreflect abdominal obesity in this population.
The primary aims of this study were to evaluate theprevalence of MetS, the components of this syndrome,
especially body composition, and the relations between
adipokine levels and body composition, in SCI individuals.
We hypothesized that the prevalence of MetS, especiallyabdominal obesity, is high, and the strong relationshipbetween adipokine levels and the markers of abdominal
obesity in this population.

square of the height in meters. Total and regional bodycomposition, including LM and body FM, were evaluated by
DXA (DPX-IQ; Lunar Corp., Madison, WI, USA) using Lunarsoftware version 4.6b. Visceral fat area (VFA) was measured
by CT at the umbilical level, using a software program(FatScan; N2system, Osaka, Japan). Waist circumference, VFA
and trunk FM were used as markers of abdominal obesity.

Blood sampling and laboratory analysis
Blood samples were drawn after an overnight fast. The whole
blood samples were centrifuged at 3000 g for 10 min. Levelsof TG, HDL-C and fasting plasma glucose (FPG) were
measured by an automatic analyzer in a clinical laboratory.
Serum insulin was measured using an immunoradiometricassay (SRL Inc., Tokyo, Japan). An estimate of insulin
resistance was calculated on the basis of the homeostasis
model assessment of insulin resistance using the following
formula: FPG (mg dl1)  fasting serum insulin (mU ml1)/
405.11 Plasma leptin levels were measured using a radioimmunoassay kit (Linco Research Inc., St Charles, MO, USA),plasma adiponectin levels were measured using an enzymelinked immunosorbent assay kit (Otsuka Pharmaceutical Co.
Ltd., Tokyo, Japan) and plasma PAI-1 levels were measured
using an enzyme-linked immunosorbent assay kit (Sysmex
International Reagents Co. Ltd., Hyogo, Japan).

Materials and methods
Patients
Forty-four male SCI individuals (an average age of 57±13
years; range, 26–82 years) were studied at the Kanagawa
Rehabilitation Hospital (Kanagawa, Japan). The SCI groupconsisted of 16 tetraplegics and 28 paraplegics with 64%
complete and 36% incomplete injury, respectively. SCI was
due to traumatic injury in 34 individuals (77%), vasculardisease in 3 (7%), infection in 2 (5%), disc disease in 1 (2%),
tumor in 1 (2%) and other causes in 3 individuals (7%).
Duration of injury was 26±15 years (range, 0.5–57 years).
Thirteen (30%) and eight (18%) individuals were on
antihypertensive medication and on medication for hypertriglyceridemia, respectively. None of the individuals had
signs of acute infection and none were treated with insulin.
Two different control groups were enrolled: group A(n ¼ 125) served as controls primarily for BP and laboratory
data, and group B (n ¼ 50) served as controls primarily forbody composition. We extracted the data of control
individuals from two different health examination databases. The Ethics Committee of Kanagawa Rehabilitation
Hospital approved the study protocol, and written informed
consent was obtained from all SCI individuals.
Body composition measurements
In the SCI group, body weight, height and waist circumference at the umbilical level were measured in the supine
position. For individuals who could not extend all joints
fully, the distance from the top of head to the bottom of theheel was measured. In contrast, in the control group, theseparameters were measured in the standing position. BMI was
defined as the body weight in kilograms divided by the

Definition of the MetS
Definition of the MetS was based on the National Cholesterol Education Program Adult Treatment Panel III (NCEP ATPIII),4 and we modified the definition of visceral fat obesity.
The Japanese Society for the Study of Obesity defined visceralfat obesity in Japanese as a VFA 4100 cm2, which corresponds to a waist circumference 485 cm for men and490 cm for women.12 In this study, MetS was defined as
the presence of at least three of the following criteria: VFA
4100 cm2, TG X150 mg dl1 or on medication for hypertriglyceridemia; HDL-C o40 mg dl1 in men and 50 mg dl1
in women; BP X130/85 mm Hg or on antihypertensive
medication and FPG X110 mg dl1 or on medication fordiabetes. BP was measured in the sitting position.

Statistical analysis
Data are presented as mean±s.d. or median and range asappropriate. A P-value of less than 0.05 was considered
statistically significant. For continuous variables, the distribution was tested by the Shapiro–Wilk W-test. Then,Student’s t-test was used for normally distributed variables,
and the Wilcoxon’s rank-sum test was used for skewed
variables. The Spearman correlation coefficient (r) was used
to determine the relationships between clinical parameters.
Nominal variables were tested using the w2-test or Fisher’s
exact test when appropriate. Multiple regression models,
including age, TG, plasma leptin, plasma adiponectin andplasma PAI-1 level, were used to identify the independent
predictors of the body composition markers. Statisticalanalyses were performed using JMP, version 5.1.1 forWindows (SAS Institute Inc., Cary, NC, USA).
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Leptin, body composition and MetS in SCI individuals
Y Maruyama et al496

Results

Table 2 Comparisons of clinical data

The clinical characteristics of the male SCI individuals areshown in Table 1; 43% of SCI individuals met the criteria for
MetS. Mean waist circumference, VFA and trunk FM were
88.1±12.1 cm, 191±79 cm2 and 12 000±5200 g, respectively.
Prevalence of MetS, BMI, waist circumference, VFA, total andtrunk FM, TG, HDL-C and adipokines level were similar
between tetraplegic and paraplegic individuals, whereas
tetraplegic individuals had lower systolic BP (107±15 versus
129±16 mm Hg, Po0.01) and diastolic BP (67±12 versus
76±9 mm Hg, Po0.01) than paraplegic individuals. Furthermore, 12 paraplegics received antihypertensive, whereas only
one tetraplegic received antihypertensive.
Table 2 shows comparisons of clinical data between the
SCI and able-bodied control individuals. Age was similar
between three groups. The SCI individuals had lesser height
as compared with individuals in the two different control
groups (Po0.01). Although body weight tended to be lower
and BMI tended to be higher among the SCI, these did notachieve statistical significance (P ¼ 0.06). The SCI individuals
had lower systolic BP (P ¼ 0.02), diastolic BP (Po0.01) and
HDL-C (Po0.01) as compared with individuals in control
group A. TG and FPG were similar between the individuals of
the SCI group and control group A. Regarding the othermarkers of body composition, waist circumference and arm
LM were similar between the individuals of the SCI groupand control group B. Leg LM (Po0.01), trunk LM (Po0.01)
and total LM (Po0.01) were lower, whereas VFA (Po0.01),
arm FM (Po0.01), leg FM (Po0.01), trunk FM (Po0.01) andtotal FM (Po0.01) were higher in the individuals SCI groupthan those in control group B.

Table 1 Clinical characteristics of the SCI individuals
CharacteristicsnAge (years)
Duration of SCI (years)
Tetra/paraplegia
Complete/incomplete
Prevalence of MetS
Systolic BP (mm Hg)
Diastolic BP (mm Hg)
Height (cm)Body weight (kg)BMI (kg m2)
Waist circumference (cm)
Visceral fat area (cm2)
Trunk FM (g)TG (mg dl1)
HDL-C (mg dl1)
FPG (mg dl1)
Plasma leptin (ng ml1)
Plasma adiponectin (mg ml1)
Plasma PAI-1 (ng ml1)
HOMA-IR

Value
44
57±13
26 (0.5–57)
16/28
28/16
19 (43%)121±1873±11164±1164.4±13.2
24.1±4.888.1±12.1
191±7912 000±5200
124±5344±12103±195.4 (1.8–16.4)
7.24 (2.91–37.2)
20.9±7.4
2.49 (0.71–6.71)

Abbreviations: BMI, body mass index; BP, blood pressure; FM, fat mass; FPG,
fasting plasma glucose; HDL-C, high-density lipoprotein cholesterol; HOMAIR, the homeostasis model assessment of insulin resistance; MetS, metabolic
syndrome; PAI-1, plasminogen activator inhibitor-1; SCI, spinal cord injury;
TG, triglyceride.
Mean±s.d. or median (range).

Spinal Cord

SCI

Control A

Control B

Pa

n
44
125
50
Age (y)
57±13
57±9
57±17
0.99
Height (cm)
164±11
168±6
168±7
o0.01
Body Weight (kg)64.4±13.2 65.0±9.6
68.9±10.2
0.06
BMI (kg m2)
24.1±4.8 23.1±3.0
24.3±3.2
0.06
Systolic BP (mm Hg)
121±18127±14NA
0.02
Diastolic BP (mm Hg)
73±11
78±8
NA
o0.01
TG (mg dl1)
124±53138±116NA
0.29
HDL-C (mg dl1)
44±12
59±16
NA
o0.01
1
FPG (mg dl )103±19102±18
NA
0.81
Waist
88.1±12.1NA85.7±7.8
0.33
circumference (cm)
VFA (cm2)
191±79NA
135±70o0.01
Arm FM (g)1940±850NA
1370±507 o0.01
Arm LM (g)5030±1450NA5420±663
0.11
Leg FM (g)6350±2600
NA
4650±1810 o0.01
Leg LM (g)9530±2750
NA
16 900±2870 o0.01
Trunk FM (g)12 000±5200
NA9120±3960 o0.01
Trunk LM (g)20 700±3330
NA
23 500±2580 o0.01
Total FM (g)22 200±8890
NA
16 000±5910 o0.01
Total LM (g)38 500±6380
NA49 600±5420 o0.01
Abbreviations: BMI, body mass index; BP, blood pressure; FM, fat mass; FPG,
fasting plasma glucose; HDL-C, high-density lipoprotein cholesterol; LM, leanmass; NA, not applicable; SCI, spinal cord injury; TG, triglyceride; VFA, visceralfat area.
Mean±s.d. or median (range).
aComparison between SCI and control group individuals.

Figure 1 shows comparisons of the markers of abdominal
obesity. The individuals with SCI had higher VFA (191±79
versus 135±70 cm2, Po0.01) and higher trunk FM(12 000±5200 versus 9120±3960 g, Po0.01). However,there was no significant difference in waist circumference(88.1±12.1 versus 85.7±7.8 cm, P ¼ 0.33) between the twogroups.
The results of the Spearman correlation tests are summarized in Table 3. All markers of body composition, including
BMI, waist circumference, VFA and trunk FM, were closelyinterrelated (Po0.01). Plasma leptin levels, plasma PAI-1
levels and homeostasis model assessment of insulin resistance were positively associated with these parameters ofbody composition (Po0.05). In contrast, plasma adiponectinlevels were associated only with VFA (r ¼ 0.38, Po0.01). TG
levels were positively associated with all of these markers,
except for VFA, whereas HDL-C levels were not associatedwith any marker.
Table 4 shows the results of the multiple regression models
that included age, TG, plasma leptin, plasma adiponectin
and plasma PAI-1. Most of these variables showed relationship to the markers of abdominal obesity in univariate
analyses. Only plasma leptin levels were independently
associated with waist circumference (total adjusted
R2 ¼ 0.475, Po0.01), VFA (total adjusted R2 ¼ 0.379,
Po0.01) and trunk FM (total adjusted R2 ¼ 0.554, Po0.01).

Discussion
One of the chief purposes of this study is to evaluate theprevalence of MetS and the components of this syndrome,Leptin, body composition and MetS in SCI individuals
Y Maruyama et al497
especially body composition in SCI. In the present study,
43% of male SCI individuals met the criteria for MetS as
defined by the modified NCEP definition. The original NCEP
ATP III definition includes a cut-off for abdominal obesity(waist circumference, 4102 cm for men and 489 cm for
women) that has been shown to be inappropriate for Asian
populations;13 therefore, Japanese Society for the Study ofObesity defined the cut-off point of visceral fat obesity inJapanese as a VFA 4100 cm2, which corresponds to a waist
circumference 485 cm for men and 490 cm for women.12
Although we did not have age-matched controls who met
the criteria for MetS in the control group, the prevalence of
MetS, especially in SCI men, appeared to be higher than that

P=0.33
Waist circumference [cm]

120
100
80
60
40
20
0
P<0.01Visceral fat area [cm2]400

Table 4 Multiple regression model for each marker of body composition

300

Independent
variable2000
P<0.01

Trunk fat mass [g]P

Dependent variable: visceral fat area (total adjusted R2 ¼ 0.379, n ¼ 43,
Po0.01)Age0.644
2.29–1.01
0.43
TG0.1600.603–0.283
0.47
Leptin9.01
3.77–14.2
o0.01
Adiponectin
3.15
6.29–0.015
0.05
PAI-1
2.86
0.294–6.02
0.07

20000
15000
10000
5000
0
SCI

Control

Figure 1 Comparisons of the markers of abdominal obesity,
including waist circumference, VFA and higher trunk FM, between
the SCI and control groups. FM, fat mass; SCI, spinal cord injury;
VFA, visceral fat area.

Table 3

95% confidence
interval

Dependent variable: waist circumference (total adjusted R2 ¼ 0.475, n ¼ 42,
Po0.01)Age0.087
0.321–0.146
0.45
TG
0.013
0.047–0.074
0.66
Leptin2.03
1.31–2.75
o0.01
Adiponectin
0.3500.779–0.080
0.11
PAI-1
0.038
0.470–0.395
0.86

100

25000

Regression
coefficient

Dependent variable: trunk fat mass (total adjusted R2 ¼ 0.554, n ¼ 43,
Po0.01)Age43.5
134–47.3
0.33
TG
11.5
12.9–35.9
0.35
Leptin885
596–1170
o0.01
Adiponectin
62.6
235–110
0.47
PAI-1
45.3
129–2190.60
Abbreviations: PAI-1, plasminogen activator inhibitor-1; TG, triglyceride.

Spearman correlation coefficient (r) between each clinical parameter in SCI individuals

BMI
Waist
VFA
Trunk FMTG
HDL-C
LeptinAdiponectin
PAI-1
HOMA-IR

BMI

Waist

VFA

Trunk FM

TG

HDL-C

LeptinAdiponectin

PAI-1

HOMA-IR10.71ww
0.49ww
0.79ww
0.36w
0.12
0.62ww
0.19
0.32w
0.41ww

1
0.64ww
0.90ww
0.38w
0.23
0.67ww
0.30
0.39w
0.49ww

1
0.66ww
0.20
0.14
0.59ww
0.38w
0.44ww
0.36w

10.45ww
0.11
0.80ww
0.27
0.50ww
0.57ww

1
0.27
0.28
0.41ww0.52ww
0.40w

1
0.08
0.35w
0.16
0.31

1
0.07
0.34w
0.42ww1
0.48ww0.40ww

1
0.38w

1

Abbreviations: BMI, body mass index; FM, fat mass; HDL-C, high-density lipoprotein cholesterol; HOMA-IR, the homeostasis model assessment of insulin
resistance; PAI-1, plasminogen activator inhibitor-1; SCI, spinal cord injury; TG, triglyceride; VFA, visceral fat area; waist, waist circumference.
w
Po0.05.
ww
Po0.01.

Spinal Cord

Leptin, body composition and MetS in SCI individuals
Y Maruyama et al498
reported in general Japanese workers (19.5% in men and7.9% in women).14 Further studies with a greater number ofindividuals are needed to confirm the higher prevalence of
MetS in SCI individuals.
Abdominal obesity per se is a risk factor for CVD. In thegeneral population, as reflected in the 5881 participants of
the Framingham Heart Study, Kenchaiah et al.5 reported thatthe risk of heart failure increased by 5% in men and 7% in
women for each unit increment in the BMI. Since bodyweight does not distinguish between FM and fat-free mass,
the BMI would appear to be a poor surrogate marker ofobesity in SCI individuals. Buchholz et al.15 found that the
30 kg m2 BMI cut-off level had a 100% specificity and only a
20% sensitivity in distinguishing obese from non-obese
individuals with paraplegia. Indeed, in the present study,
the BMI was not significantly different between the SCI
group and able-bodied controls.
Thus, more accurate ways to measure visceral fat in the SCI
population are needed. In this study, waist circumference,
VFA determined by CT and trunk FM determined by DXA
were used as markers of abdominal obesity. As expected,
these three parameters were closely interrelated. Leg LM,
trunk LM and total LM were lower, whereas arm FM, leg FM,
trunk FM and total FM, as well as VFA and waist
circumference, were higher in the SCI group. These results
are consistent with previous reports. Spungen et al.7 reported
that total body and regional LM were lower and FM washigher in male SCI individuals using DXA. Modlesky et al.8
reported that the skeletal muscle mass of the mid-thighdetermined by MRI and the fat-free soft tissue mass of the
mid-thigh determined by DXA were lower in the male SCI
population. However, to the best of our knowledge, this is
the first report to demonstrate abdominal obesity in the SCI
population based on the VFA on CT.
The other chief finding of the present study was that, on
multiple regression analyses, plasma leptin level was anindependent determinant of the markers of abdominal
obesity, including waist circumference, VFA and trunk FM.
A range of soluble products, the so-called adipokines,
secreted by adipose tissue, which is a highly active endocrineorgan, plays an important role in the creation of abdominal
fat. Leptin, the product of the adipose-specific ob gene,
regulates food intake and energy expenditure. Furthermore,
leptin induces high BP and tachycardia via increased
adrenergic activity; this suggests that leptin may be an
important link between obesity, increased sympathetic
activity and hypertension.16 Among SCI individuals, several
univariate analyses have shown that leptin levels are
positively associated with BMI and FM.17 Additionally,
Mamoun et al.17 reported that the leptin levels increased
gradually from week 24 after injury. Although in the present
study, plasma adiponectin, plasma PAI-1 and homeostasis
model assessment of insulin resistance were related toabdominal obesity, only the plasma leptin level was anindependent determinant of abdominal obesity in multiple
regression models.
There are several limitations of this study. First, thenumber of the SCI individuals was relatively small. Additionally, we used two separate control groups for different
Spinal Cord

comparisons. We obtained the data of control individuals
from two different health examination databases; one wasmainly for laboratory data and the other was mainly forbody composition, including CT, DXA and anthropometry.
Hence, we could not compare all measures against the same
control group, and could not assess the prevalence of MetS
among able-bodied controls. Second, selection bias wasinevitable. All SCI individuals were hospital-based, whilemost of the laboratory data of the able-bodied controls wereobtained during routine physical examination. Third, we did
not monitor physical activity, which was reported toattribute an increased FM in the SCI.18 Fourth, we used thesame criteria of MetS as for general population. The criteriaof abdominal obesity might be different, because of differences in location of adipose tissue in the SCI.
In conclusion, SCI individuals were predisposed to excessive abdominal obesity represented by waist circumference, VFA and trunk FM. The strong relationship between
serum leptin and abdominal obesity suggests that thishormone can be used as a surrogate marker of the MetS in
SCI individuals. Since the effects of the MetS on CVD in SCI
are still unknown, further studies, particularly longitudinalstudies with more individuals, are needed.

Acknowledgements
We thank Dr Taichi Sekine (Mitsubishi Kagaku Bio-ClinicalLaboratories Inc., Kanagawa, Japan) for technical assistance.

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