Dietary carnitine intake and carnitine status in endurance-trained males.

Abstract

Background: Carnitine is an integral component of fatty acid transfer into the mitochondria, and also buffers excess intramitochondrial acyl-CoA. It has previously been suggested that athletes may be at risk of low carnitine status and could therefore benefit from carnitine supplementation.

Objective: To report the habitual dietary carnitine intakes of endurance-trained adult males, and to determine whether they are at risk of carnitine insufficiency by measuring plasma and urinary carnitine concentrations.

Methods: Fourteen non-vegetarian endurance-trained males completed a seven-day weighed food record and exercise logs to determine habitual dietary carnitine intake. Resting venous blood samples and 24-hour urine collections were used to determine plasma carnitine concentration and urinary carnitine excretion.

Results: The mean dietary carnitine intake was 64 (range 21-110) mg/day. Mean [+ or -] SD resting plasma total carnitine was 44 [+ or -] 7 [micro]mol/L and acyl: free carnitine ratio was 0.28 [+ or -] 0.11, which were within normal ranges. Urinary carnitine excretion was 437 [+ or -] 236 [micro]mol/day. There was no correlation between dietary carnitine intake or dietary macro- and micronutrients and plasma carnitine or urinary carnitine excretion.

Conclusion: The results of the present study indicate there is no evidence that endurance-trained males consuming a mixed diet are at risk of carnitine insufficiency.

Key words: cyclist, dietary carnitine, endurance-trained, L-carnitine, plasma carnitine, urinary carnitine excretion.

INTRODUCTION

Carnitine is an amino acid derivative whose primary roles in the human body are in transporting long-chain fatty acids into the mitochondria for use as a fuel and buffering excess acyl-CoA accumulation within mitochondria. (1,2) Carnitine is predominantly found in skeletal and cardiac muscle, with the overall content in a 70-kg male of approximately 100 mmol or 18 g. (3,4) Carnitine homeostasis is maintained from two sources: first, endogenous synthesis from the amino acid precursors methionine and lysine, and requiring vitamin [B.sub.6], iron, niacin and vitamin [C.sup.2], estimated to be 1.2 [micro]mol/kg body mass (BM) daily; (5) second, from exogenous dietary carnitine intake (primarily meat products (6)), reported to be 2-135 mg daily, or 2-12 [micro]mol carnitine/kg BM/day in non-vegetarians. (1,2,7) The daily requirement of exogenous carnitine in humans is unknown. (1,7)

Total body carnitine content is tightly regulated by a balance between dietary carnitine uptake, endogenous synthesis and renal reabsorption. (2) For example, although vegetarians have a lower dietary carnitine intake and lower plasma carnitine concentration than omnivores, (8,9) they have not been shown to be either clinically deficient or insufficient in carnitine as the body adapts by reducing renal carnitine excretion and increasing endogenous synthesis. (9) Hence, clinical carnitine deficiencies are predominantly due to enzyme deficiencies rather than dietary insufficiencies, (10) except in cases of severe protein and energy malnutrition. (11,12) Carnitine insufficiency can be diagnosed by measuring plasma and tissue carnitine concentrations. Normal plasma concentration of total carnitine (TC) is 30-90 [micro]M, free carnitine (FC) 26-52 [micro]M and acyl-carnitine (AC) esters 2-10 [micro]M, (13-15) with TC concentrations lower than 20 [micro]M considered indicative of likely carnitine deficiency. (10,16) A normal ratio of AC: FC in the fed state is less than 0.4, and ratios >0.4 are believed to be indicative of a certain degree of limited FC availability. (17) Normal subjects show a large inter- and intra-individual variation in urinary excretion of carnitine (urinary FC 22-291 [micro]mol/day (18,19)).

Athletes have been considered by some to be at risk of carnitine insufficiency, (20) especially as endurance training over several months has been observed to reduce muscle carnitine concentrations. (21,22) Athletes also have higher iron requirements than the general population, (23) and a proportion are vegetarians, which could result in lower dietary protein, carnitine and vitamin [B.sub.6] intakes and lower iron status. (24) Although the suggestion has been made that exercising humans may achieve performance benefits from ingesting supplemental carnitine, (20) their habitual dietary intake of carnitine has not been well documented nor do we know whether endogenous carnitine synthesis, urinary carnitine excretion or dietary requirements for carnitine are altered by regular exercise. Only one report is available, in cross-country skiers, whose habitual dietary intake was estimated to be 50 [+ or -] 4 mg/day (mean [+ or -] SEM) and was not correlated to their resting muscle carnitine content. (25) However, no plasma carnitine concentrations or urinary carnitine excretion were measured in that study so we know little about their total body carnitine homeostasis.

The aim of the present study was to report the habitual dietary carnitine intakes of endurance-trained adult males, and to determine the relationship between habitual dietary intake and baseline plasma and urinary carnitine concentrations.

METHODS

Fourteen non-vegetarian males aged 18-50 years, who were actively involved in endurance training (V[O.sub.2max] > 50 mL/kg/minute), were recruited for a study of four weeks carnitine supplementation and completed seven-day weighed food intake diaries and exercise logs to assess habitual carnitine intake and exercise habits. The subjects' characteristics are shown in Table 1. All experimental procedures were approved by the University of Stirling Ethics of Research Committee, and subjects provided written informed consent and were free to withdraw from the study at any time without obligation.

Food diaries were completed over seven consecutive days and subjects were provided with electronic kitchen scales (CS-2000, Ohaus Corp, Pine Brook, NJ, USA) accurate to the nearest gram (or used an equivalent scale in their own home). Verbal instructions regarding the details required in recording all food and fluid consumed over seven days were provided to subjects by a registered dietitian. Subjects were requested to provide food labels or recipes of non-standard food items consumed. If subjects were unable to use their scales (e.g. eating out at a restaurant), they were instructed to provide details on ingredients and serving sizes using dimensions and standard household measures. The food diaries were checked by the dietitian in the presence of the subject in order to clarify any entries with insufficient documentation. The food diaries were analysed by the same dietitian using a computerised dietary analysis package with a UK food database (Microdiet, University of Salford, Manchester, UK, 1999).

Following analysis of macronutrient and micronutrient intake, a list of all foods/fluid and the total mass consumed per day was generated for each individual on each day. Foods/fluids known to have no, or insignificant, carnitine content were then omitted from the list (e.g. water, spirits, lettuce, ketchup, sugar). For the remaining food/fluid items, the TC content was calculated in mg using a list of carnitine content of foods translated from Gustavsen. (26) This most thorough and up-to-date listing specified cooked and raw product carnitine contents. Where no exact comparison could be made, the food was broken down to approximate raw ingredients that could then be calculated or a food with the most comparative nutrient composition was selected (e.g. rice substituted for cous cous). Any conversions/substitutes made were used as a standard for all other food diaries.

Two weeks following the seven-day food diary, venous blood samples were drawn at rest, three hours following a standard meal of bread and jam. A two-day, non-weighed food record was completed prior to the blood draw to assess similarity of the diet to habitual food intake. Whole blood samples for haemoglobin analysis (1.5 mL) were drawn into an EDTA tube and mixed continuously at room temperature for no more than three hours until measurement spectrophotometrically (Novaspec II, Amersham Pharmacia, Uppsala, Sweden) using the cyanmethaemoglobin method. Samples for carnitine fractions were mixed into lithium heparin tubes and centrifuged immediately at 5000 r.p.m. at 4[degrees]C for 10 minutes. The plasma was extracted in duplicate and frozen at -80[degrees]C until analysis. Plasma carnitine fractions (TC and FC) were determined by radiometric methods using liquid scintillation as outlined by McGarry and Foster. (27) Briefly, FC is first assessed by measuring the CoASH release in a reaction involving acetyl-CoA with carnitine acetyl transferase. TC is then measured using the same reaction after hydrolysis of carnitine esters using potassium hydroxide. Plasma AC is calculated as the difference between TC and FC. Urinary carnitine excretion was determined by means of 24-hour urine collection immediately prior to the blood sample. A 5-mL sample of mixed urine was collected and frozen at -80[degrees]C until analysis, and the total volume of urine excreted over the 24-hour period measured to the nearest millilitre. Urinary TC was subsequently analysed. (27)

Statistics

Dietary macro- and micronutrients and carnitine intake were compared with plasma and urinary carnitine fractions using a two-tailed Pearson's correlation (SPSS version 11.0.0, SPSS, Chicago, IL, USA, 2001). Results are presented as mean [+ or -] SD, and significance was accepted at P [less than or equal to] 0.05.

RESULTS

Dietary intakes

The mean seven-day dietary intake of energy, protein, fat and carbohydrate (CHO) for each subject and the whole group is presented in Table 2. Mean daily macronutrient intakes were 1.4 [+ or -] 0.5 g/kg BM protein, 30 [+ or -] 6% energy from fat and 5.3 [+ or -] 2.0 g/kg BM CHO. Mean daily intake of vitamin C was 184 [+ or -] 129 mg, vitamin [B.sub.6] 3.3 [+ or -] 1.3 [micro]g, niacin 38 [+ or -] 12 mg and iron 22 [+ or -] 9 mg. None of the subjects' protein or micronutrient intakes were below the UK dietary reference values. (28)

The dietary carnitine intake for individuals and the group are presented in Table 2. Calculating that 1 [micro]mol is equivalent to 0.161 mg L-carnitine, the mean daily intake converts to 389 [micro]mol/day, or 5.4 [micro]mol/kg BM/day (range 1.9-9.6 [micro]mol/kg BM/day). There was no correlation between dietary carnitine intake and energy intake (R = 0.04, P = 0.90) or macronutrient intakes (protein: R = 0.15, P = 0.62; fat: R = -0.25, P = 0.39; CHO: R = 0.15, P = 0.61).

Blood and urinary analyses

Mean resting haemoglobin concentration was 15.0 [+ or -] 0.8 g/dL and none of the subjects' haemoglobin was less than 13 g/dL.

Plasma carnitine concentrations were 44 [+ or -] 7 (total), 34 [+ or -] 5 (free) and 9 [+ or -] 4 (acyl) [micro]mol/L, resulting in a mean AC : FC ratio of 0.28 [+ or -] 0.11. Urinary carnitine excretion was 437 [+ or -] 236 (total), 201 [+ or -] 135 (free) and 237 [+ or -] 127 (acyl) [micro]mol/day, resulting in an AC : FC ratio of 1.52 [+ or -] 0.65.

[FIGURE 1 OMITTED]

There was no correlation between dietary carnitine intake and plasma TC (r = 0.13, P = 0.68; Figure 1), FC (0.36, P = 0.23), AC (-0.21, P = 0.50), or AC : FC ratio (-0.30, P = 0.32). There was also no relationship found between dietary energy, protein, fat, CHO, iron, ascorbic acid, niacin, vitamin [B.sub.6], BM or sum of skinfolds and plasma TC concentration or urinary TC excretion (Table 3). There was also no correlation between dietary carnitine intake and urinary carnitine excretion (total -0.05, P = 0.87; free 0.07, P = 0.81; acyl -0.16, P = 0.58).

DISCUSSION

The main finding of the present study was that the dietary intake of our endurance-trained subjects provided carnitine intakes comparable to other adults, and the subjects were not deficient in any dietary precursors to carnitine biosynthesis as assessed by seven-day food diaries. Circulating carnitine concentration and urinary carnitine excretion were within reported normal ranges and no subjects had an AC : FC ratio greater than 0.4. No correlation was found between dietary carnitine intake, dietary macro- or micronutrients, and plasma carnitine or urinary carnitine excretion. Therefore, the trained individuals in the present study showed no indication that they were at risk of carnitine insufficiency.

The overall dietary intakes of the subjects in the present study (1.4 g/kg BM protein and 5.3 g/kg BM CHO) reflect dietary recommendations for athletes (1.2-1.6 g/kg BM protein (29) and >5 g/kg BM CHO (30)). There were no dietary micronutrient deficiencies that would affect their ability to synthesise carnitine, nor were any of them iron-deficient according to haemoglobin status. However, the limitations of data collection methods must be recognised when interpreting dietary intake data, such as potential for poor compliance and distortion of food choices by the subjects, and the skill and precision of the diagnostic tool used. Weighed food records are considered among the most accurate way of assessing of food intake quantitatively, especially when calibrated scales are used. (31) Although records covering longer than three to four days may reduce accuracy of total dietary energy intake, it was believed seven-day recordings were more suitable for representing dietary carnitine intake, as carnitine-rich foods are not necessarily consumed every day The subjects in the present study were provided with detailed feedback on their food intakes in order to maintain compliance over the full seven days. Furthermore, all records were checked and analysed by the same, trained dietitian using local food composition tables. Finally, based on the reported total energy intakes in comparison with estimated requirements calculated from the subjects' exercise logs, it appears as though the subjects were not substantially underreporting. Therefore, the data presented can be considered closely reflective of the habitual dietary intakes of our subjects at the time of the study.

The mean dietary carnitine intake of our subjects (5.5 [micro]mol/kg/day or 64 mg/day) is similar to that reported for other males in Westernised countries of 2-12 [micro]mol/kg/day or 2-135 mg/day, (1,7) and are slightly higher than those reported in a study of cross-country skiers (50 mg/day (25)). Part of the reason for variation in individual daily intakes (4-520 mg/day) is irregularity of red meat consumption. For example, one subject consumed 370 g of beef (raw weight) for his evening meal on one day, however, did not consume red meat other than ham in sandwiches on the other days (range 12-520 mg/day). The lack of correlation between dietary carnitine intake and dietary macro- and micro-nutrients probably reflects the fact that the range of foods with particularly high carnitine concentrations (e.g. red meat) is much more limited than the wide variety of foods consumed in daily life.

The data in the present study indicate that the habitual dietary intakes of our trained subjects provided sufficient carnitine to maintain what would generally be considered normal carnitine status. Plasma carnitine fractions for our subjects under basal conditions are within the reported 'normal' range of 30-90 [micro]M TC, 26-52 [micro]M FC, 2-10 [micro]M AC and plasma AC : FC ratio less than 0.4. (14,15,17) Although Rebouche contends that plasma carnitine is determined to a large degree by dietary carnitine intake, our results indicate that this relationship is not straightforward. (1) Lennon et al. found a correlation between dietary carnitine intake and plasma TC in males, but not in females. (7) They assessed dietary carnitine intake to be 47 mg using the 24-hour recall method that included an eight-hour fast, and may not have been reflective of habitual dietary carnitine intake. The complexity of the relationship between dietary carnitine intake and plasma carnitine concentration is indicated by Rebouche and Chenard who found using tracer studies that urinary excretion was 12-14% higher with habitually high dietary carnitine intakes (111-158 mg/day) compared with low intakes (19-28 mg/day), highlighting the role of renal excretion in the balance of carnitine homeostasis. (32) Hence, although plasma carnitine concentrations may not directly reflect dietary intake in man under normal living conditions because of a tight balance between factors responsible for its availability, utilisation and excretion, (12) plasma carnitine concentrations can be indicative of extremes in dietary intake, such as vegans compared with supplemented individuals.

Normal subjects show a large inter- and intra-individ-ual variation in urinary excretion of carnitine (urinary FC 22-291 [micro]mol/day (18,19)). Mean 24-hour urinary carnitine excretion in our subjects compares well with other reports in non-vegetarian males of 5.5-6.0 (total) and 2.87 (free) [micro]mol/kg/day, (8,33) 175 [+ or -] 80.7 [micro]mol/day FC (19) and 178-541 [micro]mol/day TC. (34,35) Under basal conditions, mean urinary TC excretion (437 [micro]mol/day) was very close to the mean ingested carnitine (389 [micro]mol/day), which could be interpreted as meaning the dietary carnitine intake was fully excreted. However, as mentioned above, this is misleading as the efficiency of the renal reabsorption of carnitine is influenced by dietary carnitine intake. (9) In the current study, the 24-hour urine collections were undertaken separately to the food diaries, and may be more reflective of the previous day's carnitine intake (which was not reported in sufficient detail to assess appropriately) than the reported average weekly intake. The lack of a significant correlation between dietary carnitine intake and urinary carnitine excretion at baseline for the whole group reinforces the conclusion that the similarity between mean intake and excretion of carnitine was coincidental, and that many variables should be considered when interpreting urinary carnitine excretion data.

Some studies have shown that as well as dietary carnitine, dietary macronutrient content influences plasma carnitine concentration and urinary carnitine excretion. Lennon et al. found a significant positive correlation between dietary protein and plasma TC concentration in males. (7) Other data indicate that although habitually high fat intake increases plasma carnitine concentration and urinary carnitine excretion, a low protein or high CHO diet reduces both of these variables. (36,37) The results of the current study show no correlation between dietary carnitine or any macro- or micronutrient and the concentrations of plasma carnitine fractions or urinary carnitine excretion, which is most likely due to a more homogeneous intake within our subject group than the dietary manipulations used by other authors. The data presented in the present study also show no correlation between BM or body fat and plasma carnitine, which supports data published previously in inactive males and females. (18,38)

CONCLUSION

In conclusion, the results of the present study indicate that there is no evidence that endurance-trained males consuming a mixed diet are at risk of carnitine insufficiency There was also no correlation between habitual dietary carnitine intake, dietary macro- or micronutrient composition, and plasma or urinary carnitine fractions under normal, free living conditions.

ACKNOWLEDGEMENT

The authors would like to thank Lonza, Basel for their support of the present research.

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Elizabeth BROAD, Claire BOLGER and Stuart GALLOWAY

Department of Sports Studies, University of Stirling, Scotland, UK

E. Broad, PhD, Sports Dietitian

C. Bolger, MPhil in Exercise Physiology candidate

S. Galloway, PhD, Senior Lecturer in Exercise Physiology

Correspondence: E. Broad, 44 Tallebudgera Creek Road, Tallebudgera, Qld 4228, Australia. Email: [e-mail]

Table 1 Physical characteristics of subjects (mean [+ or -] SD)

Characteristic                          n = 14

Age (years)                              33 [+ or -]    8
Height (cm)                             176.7 [+ or -]  4.5
Body mass (kg)                           72.6 [+ or -]  8.1
V[O.sub.2max] (mL/kg/minute)             64.5 [+ or -] 11.0
Training history (years)                  7.5 [+ or -]  6.5
Current exercise/training (hours/week)    6.2 [+ or -]  3.3
Sum of seven skinfolds (mm)              61.1 [+ or -] 23.1

Table 2 Daily dietary energy, macronutrients and carnitine intake
(average of seven-day weighed food intake analysis)

         Energy
         intake     Protein        Fat      CHO            Carnitine (a)
Subject  (MJ)       (g/kg BM/day)  (g)      (g/kg BM/day)  (mg)

 1       12.8       1.7            100      6.8             57 (22-115)
 2       12.4       1.9             82      5.8             67 (30-121)
 3       11.0       1.4             75      4.8             46 (4-223)
 4       10.6       1.1             95      5.2             21 (14-29)
 5       12.9       1.3             99      5.8             43 (14-98)
 6       13.7       2.5             81      8.3             69 (41-126)
 7       14.4       1.7            104      5.7             61 (17-252)
 8       12.7       1.6            112      7.9             88 (12-520)
 9       14.4       1.2            102      6.5             67 (31-256)
10       12.7       1.4             87      5.5            110 (35-345)
11        9.5       1.1             53      4.4             90 (27-251)
12       10.6       1.3            111      4.1             48 (19-100)
13       11.2       1.3            108      4.3             32 (25-37)
14       10.1       1.3            102      4.3            102 (18-198)
Mean     12.1       1.5             94      5.7             64
Range     9.5-14.4  1.1-2.5         53-112  4.1-8.3          4-520
SD        1.6       0.4             16      1.3             26

(a) Mean (range)
BM = body mass; CHO = carbohydrate.

Table 3 Correlations between dietary carnitine, nutrient intakes and
subject characteristics with plasma total carnitine concentration and
urinary total carnitine excretion (r (P-value))

                                                      Urinary total
Macronutrient                 Plasma total carnitine  carnitine

Dietary carnitine (mg)         0.13 (0.68)            -0.05 (0.87)
Energy. (kj)                  -0.03 (0.92)             0.01 (0.99)
Protein (g/kg)                 0.08 (0.80)             0.36 (0.20)
Fat (g)                       -0.21 (0.49)            -0.16 (0.59)
Carbohydrate (g/kg)            0.07 (0.81)             0.10 (0.73)
Iron (mg)                      0.27 (0.38)            -0.17 (0.56)
Ascorbic acid (mg)            -0.02 (0.95)            -0.45 (0.11)
Niacin (mg)                   -0.13 (0.66)             0.40 (0.16)
Vitamin [B.sub.6] ([micro]g)  -0.13 (0.68)             0.23 (0.44)
Body mass (kg)                -0.12 (0.70)            -0.12 (0.68)
Sum of seven skinfolds (mm)    0.10 (0.75)            -0.33 (0.25)