© 2001 American Heart Association, Inc.
Atherosclerosis and Lipoproteins |
Energy Restriction and Weight Loss on Very-Low-Fat Diets Reduce C-Reactive Protein Concentrations in Obese, Healthy Women
From the Department of Physiology (L.K.H.), Adelaide University, and CSIRO Health Sciences and Nutrition (L.K.H., M.N., P.M.C.), Adelaide, South Australia.
Correspondence to Leonie Heilbronn, CSIRO, Health Sciences and Nutrition, PO Box 10041, Adelaide BC, SA 5000, Australia. E-mail leonie.heilbronn{at}hsn.csiro.au
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Abstract |
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Abstract—C-reactive protein (CRP) is an inflammatory-response protein that is a strong, independent predictor of cardiovascular mortality. CRP is positively associated with body mass index (BMI). In this study, we investigated the effects of dynamic weight loss on CRP in 83 healthy, obese women (mean BMI, 33.8±0.4 kg/m2; range, 28.2 to 43.8 kg/m2). Subjects were placed on very-low-fat, energy-restricted diets (5700 kJ, 15% fat) for 12 weeks. Weight, waist and hip circumferences, plasma lipids, glucose, and CRP were measured at baseline and after 12 weeks. CRP was positively associated with BMI (r=0.281, P=0.01) and waist circumference (r=0.278, P=0.01) but was not related to other atherosclerosis risk factors. BMI was significantly different between groups split above or below the median for CRP (34.8±0.6 kg/m2 vs 33.0±0.5 kg/m2, P=0.02). After 12 weeks, weight loss was 7.9±0.3 kg. CRP was significantly decreased by 26% (P<0.001), and a correlation was observed between weight loss and the change in CRP (r=0.309, P=0.005). The variance in the change in CRP was partly explained by initial CRP (13.6%), energy intake (5.4%), and percentage weight loss (4.6%, P=0.001). This study confirms recent observations that BMI is associated with CRP, a marker for low-grade systemic inflammation. Furthermore, we observed that CRP was lowered in proportion to weight loss.
Key Words: C-reactive protein • obesity • weight loss • moderate energy restriction
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Introduction |
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Atherosclerosis has been recognized as an inflammatory process. C-reactive protein (CRP) is an inflammatory-response protein that is elevated several hundred-fold in response to infection and is generally considered to be a good marker for inflammation. CRP usually exists at very low concentrations in plasma, with 90% of individuals having a CRP <3.0 mg/L.1 Epidemiological studies suggest that CRP is a valuable risk marker for cardiovascular disease and that the addition of CRP to a plasma lipid level–based diagnosis may provide an improved method of identifying persons at risk for future cardiovascular events.2 However, it is unclear whether CRP is only a marker for disease progression or whether it is directly involved in the pathogenesis of atherosclerosis and whether reducing inflammation decreases the risk of myocardial infarction or stroke. However, the anti-inflammatory agent aspirin reduces CRP and the risk of myocardial infarction.3
Longitudinal studies in which apparently healthy men and women were followed up for 3 to 8 years have shown that CRP, even at low plasma concentrations, is associated with a risk of cardiac events that is independent of lipid levels, smoking status, and body mass index (BMI).2 3 This finding suggests that inflammation is involved in the initiation of atherosclerosis. Men in the highest quintile of CRP (>2.11 mg/L) had a 3-fold higher risk of myocardial infarction and a 2-fold increased risk of stroke compared with subjects in the lowest quintile of CRP (<0.55 mg/L).3 CRP has also been positively associated with glucose, insulin resistance, total cholesterol, and triglyceride concentrations in men and women.4 5 6
CRP is also strongly associated with BMI.5 6 7 In a study that investigated >16 000 individuals, it was found that CRP was elevated (>2.2 mg/L) in 60% of subjects with a BMI >30 kg/m2 compared with 35% of subjects with a BMI of 25 to 29.9 kg/m2 and 20% of subjects with a BMI <25 kg/m2.7 Weight loss improves more traditional risk factor profiles for atherosclerosis, such as hypertension and hyperlipidemia.8 In this study, we examined CRP concentrations in obese women before and after 12 weeks of energy restriction and weight loss to determine whether CRP could be reduced by weight loss.
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Methods |
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Subjects
Subjects were recruited by public advertisement that sought healthy women with a BMI >28 kg/m2. Subjects all had normal fasting plasma glucose and lipid profiles (Table 1
). Most subjects were sedentary at baseline and were
requested to maintain their usual exercise habits throughout the study.
This was assessed by an activity questionnaire each month. Twenty-eight
women were postmenopausal, 13 of whom were taking hormone
replacement therapy (HRT). Subjects gave written, informed consent to
participate in the study, which was approved by the Human Ethics
Committee of CSIRO, Health Sciences and
Nutrition.
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Diets
Subjects were prescribed a 6.0-MJ diet that was
restricted for fat intake (15% of total energy). Subjects were given
detailed instructions for recording dietary intake and were
required to complete detailed, 3-day dietary food records every 2
weeks. Dietary counseling and weight checks were also performed every 2
weeks. Overall, reported energy consumption was 5700±60 kJ/d. The
macronutrient composition of the diet was 61.4±0.3% carbohydrate,
14.2±0.2% fat (saturated fat 5.9±0.1%), and 22.8±0.2% protein.
Alcohol consumption was not allowed during the
study.
Design
Eighty-three nonsmoking, healthy, obese women (mean
BMI, 33.8±0.4 kg/m2; range, 28.2 to 43.8
kg/m2) completed 12 weeks of energy
restriction and were tested for CRP concentrations in serum before and
after weight loss. During the study, subjects were required to visit
the clinical research unit for 2 consecutive visits at baseline and
every 4 weeks thereafter for 12 weeks after a 12-hour fast. On these
occasions, weight was recorded and blood was taken for measurement
of plasma glucose, serum total cholesterol, HDL
cholesterol (HDL-C), and triglyceride
concentrations by commercially available kits (Roche
Diagnostica). LDL-C was calculated from a modification of
the Friedewald equation.9
Serum CRP concentrations were measured in duplicate at baseline and at
week 12 with an ultrasensitive ELISA (Alpha Diagnostica).
Waist and hip measurements were taken before and after dietary
intervention. Waist circumference was measured as the smallest
dimension between the lower rib margin and the iliac
crest.
Statistical Analysis
Statistical analysis was performed with
SPPS for Windows, version
10 (SPSS, Inc). Significance was found by using a repeated-measures
general linear model for weight-loss effects at weeks 0 and 12
and a 1-way ANOVA for all other tests. Correlations were performed by
using Pearson’s correlation coefficient. All results are given as
mean±SEM. Significance was set at
P<0.05.
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Results |
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Characteristics of the population are described in Table 1
. BMI ranged from 28.2 to 43.8
kg/m2. At baseline, subjects had
concentrations of total cholesterol,
triglyceride, HDL-C, LDL-C, and glucose that were within
normal healthy ranges
(Table 2). CRP was elevated (mean, 5.5 mg/L; range, 0.24 to
15.76 mg/L), with 74% of subjects having CRP concentrations >3.0
mg/L. CRP was associated with BMI at baseline
(r=0.281,
P=0.01) and abdominal fat
distribution as assessed by waist circumference
(r=0.278,
P=0.01) but not hip
circumference or waist-hip ratio. The population was dichotomized into
low and high CRP concentrations based on the median CRP (5.8 mg/L).
Subjects with a low CRP had a significantly lower BMI at baseline
compared with those with a high CRP (33.0±0.5 vs 34.8±0.6
kg/m2,
P=0.02). BMI explained 7.7% of
the variance in initial CRP
(P=0.01).
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No association was found between CRP and fasting plasma lipids or glucose concentrations at baseline. Furthermore, no significant differences were found in CRP at baseline between premenopausal (5.88±1.62 mg/L) and postmenopausal (5.01±1.12 mg/L) women, and adjusting for HRT did not affect these results.
After 12 weeks of energy restriction, total weight loss was
7.9±0.3 kg. Total cholesterol (-10%), LDL-C (-11%),
HDL-C (-6%), and triglyceride (-14%) concentrations
were significantly reduced. CRP was also significantly decreased from
baseline (P<0.001,
Table 2). The reduction in CRP was positively correlated
with weight loss (r=0.270,
P=0.013), percentage weight
loss (r=0.309,
P=0.005), and initial CRP value
(r=0.347,
P=0.001). No correlation was
found between the change in CRP and reported energy intake
(r=0.213,
P=0.056). The variance in the
change in CRP was explained by initial CRP (13.6%), energy intake
(5.4%), and percentage weight loss (4.6%).
After weight loss, CRP was highly correlated with BMI (r=0.375, P=0.001) and indexes of fat mass (waist circumference [r=0.412, P=0.001] and hip circumference [r=0.379, P=0.001]). Furthermore, triglyceride and CRP concentrations were highly correlated (r=0.287, P=0.009), but total cholesterol, LDL-C, HDL-C, and glucose levels were not associated with CRP before or after weight loss. The change in CRP was also correlated with the change in total cholesterol (r=0.240, P=0.03) but not with the change in glucose, LDL-C, or HDL-C.
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Discussion |
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CRP is predictive of cardiac events,2 3 is associated with BMI in obese women, and is significantly reduced with moderate energy restriction and weight loss, suggesting that weight loss may reduce atherosclerotic risk.
In this study, baseline concentrations of CRP were higher than previously reported2 3 and may be reflective of the high level of obesity in this study group. Many studies have shown a strong, positive association between BMI and CRP.5 6 7 One previous study10 that examined CRP in 14 obese women reported concentrations of CRP (6.3 mg/L) similar to those in this study. The reason for the increased production of CRP in obesity is most likely due to interleukin-6 (IL-6). Il-6 is a cytokine that activates the production of CRP from the liver. Recent reports indicate that Il-6 is also produced by the adipocyte in vivo in proportion to fat mass.11 Thus, excess adiposity could increase expression of IL-6 and may increase CRP expression. Obesity-associated elevations in CRP may not, therefore, be related to higher inflammatory states or atherosclerotic progression. CRP has, however, been highly associated with the risk of cardiac events, independent of BMI,2 3 12 but the effects of CRP alone on cardiac events in obese populations have not been investigated.
We examined women only in this study, and women may have higher CRP concentrations in plasma than do men.13 14 The reason for the sex differences is unclear, although this could also be due to a higher percentage of body fat in women. This concept has not been investigated directly, because specific fat measurements were not taken. Garcia-Moll and colleagues13 found that even though CRP was higher in women, cardiac death rates were not different between the sexes.
We did not find any difference in CRP between premenopausal
and postmenopausal women. This result has been supported by a larger
study that investigated 186
women.5 However, a number of
studies have found that CRP concentrations are 
2-fold higher in
postmenopausal women on HRT compared with postmenopausal women not on
HRT.13 15 We did
not observe this association in postmenopausal women; however, only 13
women in the current study were using HRT.
CRP was reduced by 26% after moderate weight loss and energy restriction, indicating a possible reduced risk of atherosclerosis. However, CRP concentrations were not normalized. This may have been due to the fact that more than half of the subjects were still classified as obese at week 12. CRP may have been reduced as IL-6 production from adipose tissue was reduced. The correlation between weight loss and the change in CRP supports this view. Bastard et al10 found that IL-6, but not CRP, was reduced by weight loss after a very-low-calorie diet had been imposed for 3 weeks, although a trend toward reduced CRP was noted in that study. This difference in results could reflect differences in the composition of the weight-loss diets (very-low-calorie diet for 3 weeks [3.9 MJ/d] vs a moderate energy restriction for 3 months [5.7 MJ/d]) or be related to the smaller number of subjects investigated in that study (n=14).
This study was not designed to test whether reductions in CRP were associated with decreased atherosclerosis risk. However, atherosclerosis progression is reduced in morbidly obese subjects after weight-reducing gastroplasty.16 The progression rate of the carotid bulb intima-media thickness in weight-reduced obese subjects followed up after 4 years and a 22-kg weight loss was similar to that in lean controls, whereas the obese control group had a progression rate that was 3 times higher than that of the weight-reduced group. Furthermore, statin therapy reduces CRP17 18 and subsequent cardiac events by eliminating the increased mortality seen across increasing CRP tertiles.18 Aspirin therapy has also been shown to reduce the risk of myocardial infarction in apparently healthy men.3
In summary, CRP is associated with BMI and waist circumference in obese women and was significantly reduced with weight loss, energy restriction, and a very-low-fat diet, indicating that the risk of cardiac events is reduced. However, further investigation into whether reductions in CRP are maintained during energy balance and prospective trials investigating weight loss, inflammatory state, and atherosclerotic disease progression are required.
Received December 20, 2000; accepted February 26, 2001.
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T. You, D. M. Berman, A. S. Ryan, and B. J. Nicklas Effects of Hypocaloric Diet and Exercise Training on Inflammation and Adipocyte Lipolysis in Obese Postmenopausal Women J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1739 - 1746. [Abstract] [Full Text] [PDF]
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C. J. Hukshorn, J. H. N. Lindeman, K. H. Toet, W. H. M. Saris, P. H. C. Eilers, M. S. Westerterp-Plantenga, and T. Kooistra Leptin and the Proinflammatory State Associated with Human Obesity J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1773 - 1778. [Abstract] [Full Text] [PDF]
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E. S. Ford, W. H. Giles, A. H. Mokdad, and G. L. Myers Distribution and Correlates of C-Reactive Protein Concentrations among Adult US Women Clin. Chem., March 1, 2004; 50(3): 574 - 581. [Abstract] [Full Text] [PDF]
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 J. M Backes, P. A Howard, and P. M Moriarty Role of C-Reactive Protein in Cardiovascular Disease Ann. Pharmacother., January 1, 2004; 38(1): 110 - 118. [Abstract] [Full Text] [PDF]
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M. Raitakari, T. Ilvonen, M. Ahotupa, T. Lehtimaki, A. Harmoinen, P. Suominen, J. Elo, J. Hartiala, and O. T. Raitakari Weight Reduction With Very-Low-Caloric Diet and Endothelial Function in Overweight Adults: Role of Plasma Glucose Arterioscler Thromb Vasc Biol, January 1, 2004; 24(1): 124 - 128. [Abstract] [Full Text] [PDF]
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 G.M. Hirschfield and M.B. Pepys C-reactive protein and cardiovascular disease: new insights from an old molecule QJM, November 1, 2003; 96(11): 793 - 807. [Abstract] [Full Text] [PDF]
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L. K Heilbronn and E. Ravussin Calorie restriction and aging: review of the literature and implications for studies in humans Am. J. Clinical Nutrition, September 1, 2003; 78(3): 361 - 369. [Abstract] [Full Text] [PDF]
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J. S. Volek, M. J. Sharman, A. L. Gomez, T. P. Scheett, and W. J. Kraemer An Isoenergetic Very Low Carbohydrate Diet Improves Serum HDL Cholesterol and Triacylglycerol Concentrations, the Total Cholesterol to HDL Cholesterol Ratio and Postprandial Lipemic Responses Compared with a Low Fat Diet in Normal Weight, Normolipidemic Women J. Nutr., September 1, 2003; 133(9): 2756 - 2761. [Abstract] [Full Text] [PDF]
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H.P. Kopp, C.W. Kopp, A. Festa, K. Krzyzanowska, S. Kriwanek, E. Minar, R. Roka, and G. Schernthaner Impact of Weight Loss on Inflammatory Proteins and Their Association With the Insulin Resistance Syndrome in Morbidly Obese Patients Arterioscler Thromb Vasc Biol, June 1, 2003; 23(6): 1042 - 1047. [Abstract] [Full Text] [PDF]
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 K. Esposito, A. Pontillo, C. Di Palo, G. Giugliano, M. Masella, R. Marfella, and D. Giugliano Effect of Weight Loss and Lifestyle Changes on Vascular Inflammatory Markers in Obese Women: A Randomized Trial JAMA, April 9, 2003; 289(14): 1799 - 1804. [Abstract] [Full Text] [PDF]
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T. McLaughlin, F. Abbasi, C. Lamendola, L. Liang, G. Reaven, P. Schaaf, and P. Reaven Differentiation Between Obesity and Insulin Resistance in the Association With C-Reactive Protein Circulation, December 3, 2002; 106(23): 2908 - 2912. [Abstract] [Full Text] [PDF]
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T.S. Church, C.E. Barlow, C.P. Earnest, J.B. Kampert, E.L. Priest, and S.N. Blair Associations Between Cardiorespiratory Fitness and C-Reactive Protein in Men Arterioscler Thromb Vasc Biol, November 1, 2002; 22(11): 1869 - 1876. [Abstract] [Full Text] [PDF]
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G. Davi, M. T. Guagnano, G. Ciabattoni, S. Basili, A. Falco, M. Marinopiccoli, M. Nutini, S. Sensi, and C. Patrono Platelet Activation in Obese Women: Role of Inflammation and Oxidant Stress JAMA, October 23, 2002; 288(16): 2008 - 2014. [Abstract] [Full Text] [PDF]
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K. Esposito, A. Pontillo, M. Ciotola, C. Di Palo, E. Grella, G. Nicoletti, and D. Giugliano Weight Loss Reduces Interleukin-18 Levels in Obese Women J. Clin. Endocrinol. Metab., August 1, 2002; 87(8): 3864 - 3866. [Abstract] [Full Text] [PDF]
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M. J. Jarvisalo, A. Harmoinen, M. Hakanen, U. Paakkunainen, J. Viikari, J. Hartiala, T. Lehtimaki, O. Simell, and O. T. Raitakari Elevated Serum C-Reactive Protein Levels and Early Arterial Changes in Healthy Children Arterioscler Thromb Vasc Biol, August 1, 2002; 22(8): 1323 - 1328. [Abstract] [Full Text] [PDF]
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D. C. Chan, G. F. Watts, P. H. R. Barrett, L. J. Beilin, and T. A. Mori Effect of Atorvastatin and Fish Oil on Plasma High-Sensitivity C-Reactive Protein Concentrations in Individuals with Visceral Obesity Clin. Chem., June 1, 2002; 48(6): 877 - 883. [Abstract] [Full Text] [PDF]
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D. J. Freeman, J. Norrie, M. J. Caslake, A. Gaw, I. Ford, G. D.O. Lowe, D. St. J. O'Reilly, C. J. Packard, and N. Sattar C-Reactive Protein Is an Independent Predictor of Risk for the Development of Diabetes in the West of Scotland Coronary Prevention Study Diabetes, May 1, 2002; 51(5): 1596 - 1600. [Abstract] [Full Text] [PDF]
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A. Tchernof, A. Nolan, C. K. Sites, P. A. Ades, and E. T. Poehlman Weight Loss Reduces C-Reactive Protein Levels in Obese Postmenopausal Women Circulation, February 5, 2002; 105(5): 564 - 569. [Abstract] [Full Text] [PDF]
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R. P. Tracy Is Visceral Adiposity the "Enemy Within"? Arterioscler Thromb Vasc Biol, June 1, 2001; 21(6): 881 - 883. [Full Text] [PDF]
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