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Plant Monoterpenes Do Not Raise Plasma High-Density-Lipoprotein Concentrations in Humans1–3

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Plant Monoterpenes Do Not Raise Plasma High-Density-Lipoprotein Concentrations in Humans1–3 Plant monoterpenes do not raise plasma high-density-lipoprotein concentrations in humans1–3 C Justin Cooke, M Nazeem Nanjee, Peter Dewey, Jacqueline A Cooper, George J Miller, and Norman E Miller Downloaded from https://academic.oup.com/ajcn/article/68/5/1042/4648608 by guest on 30 September 2021 ABSTRACT Diets high in saturated fat, cholesterol, or alcohol have been Background: Low plasma concentrations of HDLs are associ- shown to raise HDL-cholesterol concentrations (11–13), ated with an increased risk of coronary artery disease. Two whereas diets high in trans fatty acids have the opposite effect uncontrolled studies suggested that plant monoterpenes may have (14). Long-chain cis fatty acids have only small effects on HDL substantial HDL-cholesterol-elevating activity in humans. Each cholesterol, except in diets of extreme composition (15–17). study used a proprietary mixture of 6 monoterpenes in olive oil. Dietary fiber also has little effect (18). We reported that dietary Objective: The present study was undertaken to test more rigor- phytochemicals with cytochrome P-450–inducing activity ously the hypothesis that monoterpenes raise HDL concentra- (indoles, eugenol) had no effect on HDL-cholesterol or apo A-I tions in men with hypoalphalipoproteinemia. concentrations in healthy young men (19). However, the effects Design: A double-blind, placebo-controlled crossover design of other phytochemicals, and the overall contribution of diet to was used. Twenty-four men aged 58–68 y (–x: 62.3 y) with the determination of the HDL concentration, are not known. plasma HDL cholesterol <1.1 mmol/L, plasma triacylglycerols Monoterpenes are a family of cyclic hydrocarbon oils that are <3.5 mmol/L, and plasma total cholesterol <5.5 mmol/L at widely distributed in plants. Common dietary items rich in recruitment were randomly assigned to 6 capsules daily of a pro- monoterpenes include citrus fruit, peppermint oil, chickpeas, prietary mixture of 6 monoterpenes in olive oil or 6 capsules ginger, rosemary, thyme, sage, bergamot, and caraway. Two daily of olive oil alone for 24 wk, followed by a washout period papers described major increases in HDL-cholesterol concentra- of 8 wk, and then the alternative capsules for 24 wk. tions when subjects with low HDL cholesterol were given a Results: Five men dropped out. In the others, compliance was dietary supplement of monoterpenes. Each study used a propri- excellent as judged by capsule counts and urinary menthol glu- etary monoterpene preparation (Rowachol; Rowa Ltd, Bantry, curonide concentrations. No significant effects were observed on Ireland) that had been reported to reduce atherosclerosis in cho- plasma HDL-cholesterol or apolipoprotein A-I concentrations, lesterol-fed rabbits (20). Each capsule of this monoterpene nor on plasma triacylglycerol, LDL-cholesterol, or apolipopro- preparation contains 32 mg menthol, 6 mg menthone, 17 mg tein B concentrations. pinene, 5 mg borneol, 5 mg camphene, and 2 mg cineole in olive Conclusions: Plant monoterpenes have no HDL-elevating activ- oil. Hordinsky and Hordinsky (21) reported a 2-fold increase in ity of potential value for coronary artery disease prevention. mean HDL-cholesterol concentrations when 10 subjects with Am J Clin Nutr 1998;68:1042–5. hyperlipidemia and low HDL cholesterol were given the monoterpene capsules for 6 wk. Although the subjects were also KEY WORDS Apolipoprotein A-I, apolipoprotein B, low- given a diet low in saturated fat and cholesterol, this could not density lipoprotein, LDL, high-density lipoprotein, HDL, tria- have explained the rise in HDL cholesterol (11, 12). Bell et al cylglycerols, monoterpenes, cholesterol, men (22) subsequently studied 14 subjects with low initial HDL cho- lesterol, including 3 with hypertriglyceridemia. The monoter- pene preparation appeared to increase plasma HDL cholesterol INTRODUCTION Plasma HDL-cholesterol concentrations are negatively corre- lated with the incidence of coronary artery disease (CAD) (1, 2). 1 From the Department of Cardiovascular Biochemistry, St Bartholomew’s Several studies have shown that this relation is independent of and the Royal London School of Medicine and Dentistry, London; the Rowett the positive association of LDL-cholesterol concentrations with Research Institute, Aberdeen, United Kingdom; and the MRC Epidemiology CAD risk (2). A direct antiatherogenic effect of HDLs has been and Medical Care Unit, Wolfson Institute of Preventive Medicine, London. 2 Supported by the British Heart Foundation. shown in animals through human apolipoprotein (apo) A-I gene 3 Address reprint requests to CJ Cooke, Department of Cardiovascular transfer (3, 4), HDL-raising drugs (5), and intravenous infusion Biochemistry, St Bartholomew’s and the Royal London School of Medicine of HDLs (6). This may reflect the function of HDLs in the trans- and Dentistry, Charterhouse Square, London EC1M 6BQ, United Kingdom. port of cholesterol from tissues (7), inhibition of LDL oxidation E-mail: [email protected]. (8), suppression of adhesion molecule expression (9), or inhibi- Received April 1, 1998. tion of platelet aggregation (10). Accepted for publication June 17, 1998. 1042 Am J Clin Nutr 1998;68:1042–5. Printed in USA. © 1998 American Society for Clinical Nutrition MONOTERPENES AND PLASMA HDL 1043 progressively with time: on average by <85% after 16 wk and by assay of menthol glucuronide as a measure of compliance. >100% after 6 mo. In contrast, plasma total cholesterol and tria- Records were kept of the numbers of unused capsules. cylglycerol concentrations were unchanged. On the basis of prospective epidemiologic data (12, 23–25), increases in HDL Laboratory procedures cholesterol of such magnitude might be associated with 40–90% All laboratory analyses were carried out in duplicate in a single reductions in CAD risk. However, because both studies were batch at the end of the trial. Plasma cholesterol and triacylglycerol uncontrolled and unblinded, these results must be confirmed in a concentrations were measured by enzymatic colorimetric proce- study with a better trial design. We describe a randomized, dou- dures (27). HDL cholesterol was measured after precipitation ble-blind, placebo-controlled crossover trial of the effect of the (>96% apo B and <5% apo A-I precipitated) of other lipoproteins monoterpene preparation on HDL-cholesterol and apo A-I con- with polyethylene glycol 6000 (28). LDL cholesterol was calculated centrations in men with hypoalphalipoproteinemia. as described by Friedewald et al (29). The concentrations of apo A- I and apo B, the major protein components of HDLs and LDLs, respectively, were assayed by rocket immunoelectrophoresis using SUBJECTS AND METHODS polyclonal antisera (International Immunology Corporation, Muri- Downloaded from https://academic.oup.com/ajcn/article/68/5/1042/4648608 by guest on 30 September 2021 etta, CA) (30). Within-assay CVs were ≤2% for plasma triacylglyc- Clinical procedures erols and total cholesterol, ≤6% for HDL cholesterol, 4–11% for Monoterpene (Rowachol) and placebo capsules were obtained apo A-I (at 0.28–1.38 g/L) and 6–12% for apo B (at 0.18–0.92 g/L). from Rowa Ltd. The placebo capsules contained only olive oil. Urinary menthol glucuronide concentrations were measured by gas- Twenty-four men aged 58–68 y, all clinically without CAD, were liquid chromatography (31), with geraniol as an internal standard. recruited from a general medical practice (St Andrews Health Cen- ter, Fife, United Kingdom), one of several centers participating in Statistical analyses the Medical Research Council Northwick Park Heart Study II, a Plasma triacylglycerol concentrations were log transformed prospective survey of cardiovascular disease (26). The subjects rep- before statistical analysis. Differences between the placebo and resented all men in that practice who had been found to have a monoterpene periods in plasma concentrations of lipids and plasma total cholesterol concentration below the 40th percentile apolipoproteins at baseline, in their concentrations during treat- and a plasma triacylglycerol concentration below the 90th per- ment, and in changes in their concentrations over time were tested centile for the baseline population on each of 5 annual examina- by using paired t tests. The data were also analyzed by the non- tions, and a plasma apo A-I concentration below the 50th percentile parametric Wilcoxon matched-pairs signed-rank test and by (measured on a single occasion). All were shown to have an HDL- repeated-measures analysis of variance with inclusion of the inter- cholesterol concentration <1.1 mmol/L at the time of recruitment. action terms (treatment 3 smoking and treatment 3 time) to study No subjects were taking lipid-lowering, antihypertensive or antico- effects of current smoking on the response to treatment and differ- agulant therapy or had liver, kidney, or endocrine disease; active ences in responses to treatment over time. A value of P < 0.05 (two malignancy; or a history of alcohol abuse. The sample size used tail) was taken to indicate statistical significance. Data were ana- was sufficient to demonstrate a 10% increase in HDL cholesterol lyzed with SPSS version 6.1.3 (SPSS Inc, Chicago). during the monoterpene period with an a of 0.05 and a power of 90%. The study was approved by the local ethics committee. Subjects were randomly assigned over 2 wk to treatment with RESULTS monoterpenes, 3 capsules twice daily for 24 wk, followed by the Of the 24 subjects who started the study, 5 subsequently placebo capsules in the same dose for an additional 24 wk, or to dropped out because of their unwillingness to continue attending the same agents in the reverse order. The 2 treatment periods the follow-up visits. Their results were omitted from the statisti- were separated by a washout period (no capsules) of 8 wk. Each cal analysis. No subject reported side effects during either the subject was asked to maintain his habitual diet, alcohol intake, monoterpene or the placebo period. Among 6 cigarette smokers, smoking habit, and level of physical activity. Compliance with no significant changes occurred in the number of cigarettes this request was reinforced during the trial.
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