Original Communication

European Journal of Clinical Nutrition (2005) 59, 1423–1428. doi:10.1038/sj.ejcn.1602257; published online 17 August 2005

Plasma coagulation factor VII activity and its correlates in healthy men

Guarantor: AJ Sinclair.

Contributors: DL, AJS and AT initiated the study. DL prepared the drafts of the paper, did laboratory assays, collected data and did the statistical analysis. AJS selected the study site, supervised the project and secured the funding. All investigators contributed to the interpretation of data and to paper preparation.

D Li1, A Turner2 and A J Sinclair3

  1. 1Department of Food Science and Nutrition, Zhejiang University, Hangzhou, China
  2. 2School of Medical Sciences, RMIT University, Melbourne, Victoria, Australia
  3. 3Department of Food Science, RMIT University, Melbourne, Victoria, Australia

Correspondence: D Li, Department of Food Science and Nutrition, Zhejiang University, 268 Kaixuan Road, Hangzhou, Zhejiang 310029, China. E-mail: duoli@zju.edu.cn

Received 29 October 2004; Revised 17 May 2005; Accepted 11 June 2005; Published online 17 August 2005.

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Abstract

Objective:

 

The aim of this study was to investigate the plasma coagulation factor VII activity and its correlates in healthy Australian men.

Design:

 

Cross-sectional study.

Setting:

 

Free living subjects.

Subjects:

 

A total of 139 healthy Australian males aged 20–55 y with widely varying intakes of individual fatty acids.

Outcome measures:

 

The concentration of phospholipid fatty acids and the parameters of biochemistry were analysed by standard methods. Citrated plasma factor VII activity was measured by using the ACL 200 system with commercially available kits.

Results:

 

In the stepwise multiple regression, controlled for age, body mass index and dietary groups, the two most important variables of factor VII activity were selected in the forward entry model with R 2=0.474 and P<0.0001 from 19 independent variables, which were significantly correlated with plasma factor VII activity in age-adjusted bivariate analysis where significance was considered at P<0.01. Plasma factor VII activity was strongly negatively correlated with prothrombin time (PT) (Std. Coeff. -0.550), and significantly positively correlated with plasma phospholipid (PL) stearic acid (Std. Coeff. 0.285).

Conclusions:

 

Increased factor VII activity was associated with shortening of PT. All types of fatty-acid concentrations of PLs were significantly positively correlated with factor VII activity; however, stearic acid was more potent than other fatty acids in healthy Australian men.

Sponsorship:

 

Meat Research Corporation of Australia.

Keywords:

haemostatic factor VII activity, vegetarians, omnivores, stearic acid, plasma PL fatty acids

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Introduction

Epidemiological and clinical studies have provided evidence showing that increased levels of coagulation factors and impairment of the fibrinolysis system are important predictors of cardiovascular disease (CVD) (Aird, 2003; Selwyn, 2003). Coagulation plasma factor VII activity is of particular significance due to its pivotal role in blood coagulation (Ruddock & Meade, 1994; Miller, 1995, 1998; Noto et al, 2002). Plasma coagulation factor VII is a vitamin K-dependent factor which activates both coagulation factors IX and X in the generation of the prothrombin complex. This complex is the precursor of thrombin generation and the resulting fibrin clot. Factor VII activity measured by a functional assay (based on clotting tests) gives a clear indication of its action in vivo in contributing to the haemostatic balance between the extremes of haemorrhage and thrombosis. Increased concentration of zymogen factor VII antigen and especially the activated form of factor VII is a very potent coagulant in the circulation.

Dietary intervention studies showed that all types of fats resulted in an increase in plasma factor VII activity after a single meal (Hunter et al, 2001, Tholstrup et al, 2003), and after 4 weeks of a high unsaturated and saturated fat diets in healthy individuals (Mitropoulos et al, 1994). However, Poppitt et al (2004) reported that there were no significant changes in plasma factor VII activity after a single saturated-, monounsaturated- or polyunsaturated fatty acid meal. Oakley et al (1998) suggested that this may be a dose-dependent effect of lipid loading.

There is no one ideal method to accurately estimate the dietary intake of individual fatty acid from a food frequency questionnaire (FFQ) or weighed food records since the database on the individual fatty acid content of all foods, especially manufactured foods such as biscuits and pastries, or is not up-to-date. As a result of this difficulty, analysis of adipose tissue or plasma lipid fatty acids has been used as an indication of the quality of the dietary fat intake. In this study, we have used plasma phospholipid (PL) fatty acid concentrations as a surrogate marker of dietary intake of fat. We had an opportunity to study whether plasma factor VII activity was different between habitual vegetarians and omnivorous, and what the important correlates of plasma factor VII activity were since we had collected semiquantitative FFQ and blood samples from four groups of men with widely varying intakes of fat and types of fatty acids. We have reported that meat-eaters had a significantly higher cluster of CVD risk factors compared with vegetarians, including plasma factor VII activity (Li et al, 1999). The present paper represents additional and novel multiple regression data. We hypothesized that the long-term high-fat intake from habitual Australian diet would positively influence plasma factor VII activity. The aim of this study was to correlate plasma factor VII activity with the plasma concentrations of PL fatty acids and lipoprotein lipids, physiological, haemostatic and biochemical parameters in healthy Australian men.

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Methods

Subjects

The present study formed a part of a large project investigating the association between diet and cardiovascular risk factors in Australian men (Li et al, 1999). The project was approved by the Human Research Ethics Committee of RMIT University, and all subjects gave written informed consent. In all, 139 healthy male nonsmokers aged between 20 and 50 y were recruited through advertisements in University newsletters and local newspapers. The exclusion criteria for this study were evidence of CVD, hypertension, renal disease, hyperlipidaemia, haematological disorders, diabetes, family history of CVD, excess alcohol intake and drug therapy. According to their habitual dietary intake (based on the semiquantitative FFQ), the subjects were divided into omnivores (n=78, moderate-meat-eaters n=60 and high-meat-eaters n=18) and vegetarian (n=61, 43 ovolacto vegetarians and 18 vegans). A vegan was defined as someone who ate meat and eggs and dairy products less than six times per year. An ovolacto vegetarian was defined as someone who ate meat not more than six times per year but consumed eggs and dairy products freely. For the subjects to be classified into these categories, they had to have been practising their diets for at least 6 months prior to the study.

The dietary intake data of each subject were assessed using the semiquantitative FFQ and calculated using the Diet/1 Version 4 software (Xyris Software, Pty Ltd, Highgate Hill, QLD, Australia) with NUTTAB 95 database based on Composition of Foods, Australia (National Food Authority, 1995).

Blood specimen collections

Subjects attended the RMIT Medical Centre in the morning following an overnight fast. Subjects were allowed to sit relaxed for 10 min, and then venous blood was taken into vacutainers. After blood collection, the subject's weight, height, waist/hip ratio and blood pressure were measured. Plasma samples were prepared by centrifugation, aliquoted into separate tubes and stored at -20°C until analyses were performed.

Full blood examination

A full blood cell count was performed on a Coulter STKR analyser (Coulter Electronics Inc., Hialeah, USA).

Plasma haemostatic factors

Coagulation and fibrinolysis parameters (prothrombin time (PT), fibrinogen (FIB), activated partial thromboplastin time (APTT), factor VII activity (VII), plasminogen and antithrombin III (ATIII)) were determined in citrated plasma using the ACL 200 system with commercially available kits (Coulter/IL Ltd, Italy) as described by Messmore (1983).

Plasma and lipoprotein lipids

Concentrations of triacylglycerol (TAG) and total cholesterol (TC) of fasting EDTA plasma, and HDL-C of pretreated EDTA plasma were determined by standard enzymatic methods on a centrifugal autoanalyser (Hitachi Autoanalyser System 705, Japan) using commercially available kits (Boehringer Mannheim, Sydney, Australia) as reported previously (Li et al, 1999). LDL-C was calculated using the Friedwald equation as developed by DeLong et al (1986).

PL fatty acids

Total lipids of EDTA plasma was extracted with chloroform: methanol 1:1 (v/v) containing 10 mg/l of butylated hydroxytoluene (Labco, VIC, Australia), and 10 mg/l of C17:0 phosphatidylcholine (diheptadecanoyl) (Nu-Chek-Prep, INC., MN, USA) as internal standards as reported previously (Li et al, 1999). The PL fraction was separated by thin-layer chromatography. The methyl esters of the fatty acids of the plasma PL fraction was prepared by saponification using KOH (0.68 mol/l in methanol) followed by transesterification with 20% boron trifluoride (BF3) in methanol. The fatty-acid concentrations of plasma PL were determined by gas–liquid chromatography as described previously (Li et al, 1999).

Statistical analyses

The data analyses were performed using a StatView software program (Abacus Concepts Inc., Berkeley, CA, USA). ANCOVA was used to analyse the differences between the dietary groups for plasma factor VII activity; age and BMI were used as covariates. Linear regressions were employed to determine the relationship between plasma factor VII activity and parameters. Simple linear regression was initially used to identify the bivariate association between plasma factor VII activity and parameters (Cushman et al, 1996). In order to find the independent variables that are most useful in explaining or predicting plasma factor VII activity, the accepted level of statistical significance was an observed significance level of P<0.01 which was used as an independent variable in the stepwise multiple regression, adjusting for age, BMI and dietary groups.

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Results

The original data of dietary intake, physiological characteristics, PL fatty acids and lipoprotein lipids, physiological, haemostatic and biochemical parameters have been reported previously (Li et al, 1999). The age was 34.2plusminus9.4 y for the high meat eaters, 38.3plusminus7.3 y for the moderate meat eaters, 34.9plusminus9.0 y for ovolacto vegetarians and 33.0plusminus7.7 y for the vegans (P=0.034). The mean body mass index (BMI, kg/m2) was 27.0plusminus3.4 kg/m2 for the high meat eaters, 26.4plusminus3.4 kg/m2 for the moderate meat eaters, 23.6plusminus2.8 kg/m2 for ovolacto vegetarians and 23.3plusminus3.5 kg/m2 for the vegans (P<0.0001). Plasma factor VII activity (%) was 98.8plusminus22.0 kg/m2 for the high meat eaters, 102.8plusminus19.3 kg/m2 for the moderate meat-eaters, 96.2plusminus20.4 kg/m2 for ovolacto vegetarians and 89.0plusminus14.3 kg/m2 for the vegans (P=0.186, ANCOVA, adjusted for age and BMI).

Table 1 reports the bivariate correlations between plasma factor VII activity and predictors. Plasma factor VII activity was significantly positively correlated with 19 independent variables: PL concentrations of 14:0, 16:0, 18:0, 20:0, total monounsaturated, total n-3 and total n-6 fatty acids, plasma antithrombin III (AT III) and plasminogen activities, plasma TC, LDL-C, TAG and ratio of TC to HDL-C, white blood cell count (WBC), mean cell haemoglobin concentration (MCHC), BMI, systolic and diastolic blood pressure (P<0.01). Plasma factor VII activity was significantly negatively correlated with PT (P<0.0001).


Figure 1 shows the results of plasma factor VII activity vs fitted plasma factor VII activity in stepwise multiple regression adjusted for age, BMI and dietary groups. Plasma factor VII activity was used as a dependent variable in the stepwise forward selection entry model, and the 19 predictors were used as independent variables; these 19 variables had a significant correlation with plasma factor VII activity in bivariate analysis with a significance of P<0.01. The two most important predictors, plasma PL 18:0 concentration (Std. Coeff. 0.285) and PT (Std. Coeff. -0.550) of plasma factor VII, were selected in the model with R2=0.474 and P<0.0001.

Figure 1.
Figure 1 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Plasma factor VII activity vs fitted factor VII activity in stepwise multiple regression adjusted for age, BMI and the dietary groups.

Full figure and legend (23K)

Regression plots of plasma factor VII activity vs PT and plasma PL 18:0 concentration are shown in Figures 2 and 3.

Figure 2.
Figure 2 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Correlation of plasma factor VII activity with plasma phospholipid stearic acid concentration.

Full figure and legend (22K)

Figure 3.
Figure 3 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Correlation of plasma factor VII activity with prothrombin time.

Full figure and legend (21K)

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Discussion

Elevated plasma factor VII activity is a critical risk factor for fatal CVD (Noto et al, 2002; Selwyn, 2003). The aim of this study was to determine the relationship between plasma factor VII activity and its correlates in healthy Australian men.

We have reported that low plasma factor VII activity in the vegan group corresponded to the long-term low total fat and saturated fat diet of vegans (Li et al, 1999). This result is consistent with the findings of others that have been reported by Haines et al (1980), and currently reviewed by Miller (1998) and Hornstra (2001). The present results indicate that vegan diet has a protective effect against thrombosis tendency because it contributes to a lower plasma factor VII activity compared with an omnivorous diet in this study population.

Plasma PL fatty-acid concentration was used as a marker of fatty acid intake since there is no ideal method to accurately estimate the dietary intake of individual fatty acids from an FFQ or weighed food records. Epidemiological and dietary intervention studies have shown that the fatty acid profiles of platelet and plasma/serum phospholipids reflect an individual's type of dietary fat intake (Riboli et al, 1987; Hunter, 1995; Hornstra, 2001). Cleland et al (2003) found that plasma PL 20:5 n-3 significantly increased in 64 rheumatoid subjects who were advised to take a fish oil supplement for 12 months. Yep et al (2002) reported that plasma PL 20:5 n-3 and 22:6 significantly increased in 10 healthy subjects, aged 21–64 y-old, after they consumed fish oil enriched bread for 3 weeks compared with baseline. A number of studies found that dietary 18:0 was positively associated with plasma PL 18:0 concentration despite that membrane 18:0 can be partly converted to 18:1, which is controlled by the enzyme 9-desaturase (Pala et al, 2001). In the ARIC Study, the proportion of SFA and PUFA in plasma cholesterol ester and PL was well correlated with the dietary intake of these fatty acids as assessed by a semiquantitative FFQ (Ma et al, 1995). Tholstrup et al (1994) found that plasma PL 16:0 significantly increased and 14:0 decreased when 12 healthy men aged 21–26 y consumed a high-16:0 diet for 3 weeks compared with a low-16:0 diet. There was a 22% increase in platelet PL 18:0 after 13 healthy male subjects consumed a high-18:0 diet (6.6% of energy as 18:0) for 4 weeks compared with baseline diet (2.5% of energy as 18:0) (Kelly et al, 2001). Therefore, PL fatty acid concentrations can be used as a surrogate marker of dietary intake of SFA other than n-3 PUFA (Wang et al, 2003).

In the present study, significant positive correlations between plasma factor VII activity and concentrations of plasma PL individual saturated fatty acids, total monounsaturated, n-3 and n-6 polyunsaturated fatty acids, TC, LDL-C and TAG in the bivariate analysis indicated that increased dietary fat intake was associated with an elevated plasma factor VII activity, which is consistent with the literature (Haines et al, 1980; Miller, 1998; Hornstra, 2001).

In the present study, the two most important variables (PT and plasma PL 18:0 concentration) were selected by the stepwise multiple regression forward model. Strong negative correlation between plasma factor VII activity and PT indicates that elevated plasma factor VII activity promotes blood coagulation, and this relationship has also been reported previously (Palmer & Gralnick, 1984; Wright et al, 1997). Plasma factor VII activity had a strong positive correlation with plasma stearic acid (18:0) concentration. Mitropoulos et al (1994) proposed that dietary fat induces changes in activation of plasma factor VII through effects on plasma free 18:0 concentration, based on results obtained from an in vivo dietary intervention study and in vitro incubation of citrated plasma with injected free 18:0 (Mitropoulos et al, 1994). Miller (1998) reported that all types of fats increase factor VII activity, independent of the fatty-acid composition of the fats; however, 18:0 was less effective than 14:0.

There was no significant difference on fasting plasma factor VII activity between different types of fats, in that study, nine healthy young men consumed three diets enriched with 18:0, 18:1 and 18:2 n-6 for 2 weeks for each diet with 5 weeks washout period (Hunter et al, 2000). Kelly et al (2001) found there was no significant difference between 18:0 and 16:0 on plasma factor VII activity after 13 healthy men consumed two diets enriched with 18:0 and 16:0 for 4 weeks with a 7-week wash period between the two diets.

Studies of 18:0 from different sources on postprandial plasma factor VII activity showed discordant results. A recent study reported that all types of fats (saturated, monounsaturated and polyunsaturated) increased postprandial factor VII activity; however, 18:1 resulted in a more significant increase in factor VII activity than 18:0 after 16 healthy young male subjects consumed six high-fat matching meals (1 g fat/kg body weight, 43% from test fatty acid), 16:0+14:0, 16:0, 18:0, 18:1, trans 18:1 and 18:2n-6, with 2 weeks washout period between each test meal (Tholstrup et al, 2003). A randomised crossover design has failed to show that 18:0 enriched meal raises postprandial plasma factor VII activity compared with 18:1cis, 18:1trans and 16:0 in 16 healthy subjects (Sanders et al, 2000). Postprandial plasma factor VII activity was significantly lower after 18:0-rich structured TAG meal compared with cocoa butter and high-18:1 sunflower oil meals in a randomised cross-over study in 17 male and 18 female healthy subjects (Sanders et al, 2001). Sanders et al (2003) also found that plasma factor VII activity was not significantly increased 6 h after a randomised cocoa butter with long-chain saturated fatty acids in the sn-2 position meal, however, factor VII activity was significantly increased after a normal (nonrandomised) stearic-acid-rich cocoa butter with 18:1 in the sn-2 position meal (50 g fat/meal) in 17 healthy young men. This result indicated that different fat sources and fatty acids in sn-2 position of TAG had different effects on factor VII activity.

The 18:0 sources in above dietary intervention studies were plant based, such as liquid formula/complete hydrogenated vegetable oil, 18:0-rich structured TAG, or cocoa butter, which are uncommon major food items especially in large amounts for most people. In habitual diets, cocoa butter (chocolate) and animal fats are the main source of stearic acid. Cocoa butter, visible fat of beef, lamb, pork, chicken, duck and turkey contain 35, 16, 26, 12, 5, 7 and 7% of stearic acid, respectively (Li, 1998). However, the visible fat of beef and lamb is consumed much more frequently (which provides most dietary stearic acid) than is cocoa butter in Australia (National Heart Foundation of Australia, 1994). It is possible that the 18:0 from different sources (plants, animals, synthesised) has a different effect on plasma factor VII activity. It may be caused by the arrangement of stearic acid and other fatty acids among the three available esterification sites present on the backbone of TAG molecules and the other components that are present in fats.

In the present study, the bivariate analysis significant positive correlations between factor VII activity and plasminogen and antithrombin III indicates that humans have an autoregulating system between blood coagulation and fibrinolysis, ie plasma plasminogen and antithrombin III will also be increased when plasma factor VII activity rises. Consistent results have been reported previously for correlations between factor VII activity and other CVD risk factors. For example, plasma factor VII activity was significantly positively correlated with TC, TAG and LDL-C (Vaisanen et al, 1995; Stengard et al, 2001), blood pressure (Prisco et al, 1996; Junker et al, 1998), BMI (De Pergola & Pannacciulli, 2002) and WBC (Cushman et al, 1996).

PL can be found in the different lipoproteins; about 30% of PL is located in HDL (Cenedella, 1994). Not surprising, plasma PL concentration was significantly correlated with plasma PL 18:0 concentration (Std. Coeff. 0.901, P<0.0001) in the present study. Logically, we were expecting significant positive correlations between plasma factor VII activity and HDL; and plasma PL concentration and HDL, however, these did not occur with Std. Coeff. -0.049 and 0.101, P=0.5743 and 0.2430, respectively.

In conclusion, increased factor VII activity is associated with shortening of PT. All types of fatty acids of plasma PL were significantly positively correlated with factor VII activity; however, stearic acid was more potent than other fatty acids in healthy Australian men.

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Acknowledgements

We thank Neil Mann, Fiona Kelly, Lavinia Abedin, Leeann Johnson, They Ng, Alisa Wilson and Sirithon Nakkote for their assistance.

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