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Journal of the American College of Nutrition, Vol. 22, No. 4, 253-257 (2003)
Published by the American College of Nutrition

Review

Hypothesis: Vitamin E Complements Polyunsaturated Fatty Acids in Essential Fatty Acid Deficiency in Cystic Fibrosis

Lisa G. Wood, PhD, Dominic A. Fitzgerald, MBBS, PhD and Manohar L. Garg, PhD

Discipline of Nutrition and Dietetics, University of Newcastle, Callaghan (L.G.W., M.L.G.), New South Wales, AUSTRALIA
Department of Respiratory Medicine, The Children’s Hospital at Westmead, Sydney (D.A.F.),New South Wales, AUSTRALIA

Address reprint requests to: Manohar L. Garg, PhD, Discipline of Nutrition & Dietetics, University of Newcastle, Callaghan, NSW, 2308, AUSTRALIA. E-mail: ndmg{at}mail.newcastle.edu.au


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 REFERENCES
 
While several studies have demonstrated essential fatty acid (EFA) deficiency in plasma and tissue lipids of cystic fibrosis (CF) patients, the reasons for this deficiency are not well established. It is believed that reduced EFA intake, malabsorption of fat, altered desaturase/lipase activity and defective cystic fibrosis transmembrane conductance regulator (CFTR) altering utilisation of EFA in epithelial cells contribute to the development of EFA deficiency in CF. It is likely that increased metabolism of arachidonic acid to eicosanoids such as leukotrienes, thromboxane and prostaglandins may also be a contributing factor. Evidence is presented that elevated oxidative damage to EFA and impaired antioxidant defences, in particular vitamin E, may contribute to the development of EFA deficiency in CF. Furthermore, antioxidant supplementation in CF may improve EFA status.

Key words: cystic fibrosis, vitamin E, essential fatty acids, antioxidants, oxidative stress

Key teaching points:

• EFA deficiency is common in CF, with oxidative stress being one of several possible contributing factors.

• Vitamin E is the key antioxidant responsible for protecting cell membranes from oxidation.

• Vitamin E concentrations are linked to PUFA status in stable CF patients.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
REFERENCES
 
Normal levels of the essential fatty acids (EFA), linoleic acid (18:2n-6) and {alpha}-linolenic acid (18:3n-3) are difficult to maintain in CF patients. Christophe and Robberecht reviewed a large number of CF studies [1] and report that EFA status is variable, ranging from normal to highly disturbed. Pancreatic sufficient patients have normal or less disturbed blood and tissue lipid profiles, compared to patients who are pancreatic insufficient [2]. Prevalence estimates for EFA deficiency vary, depending on factors such as patient age, dietary management and pancreatic enzyme supplementation. However, it has been estimated that up to 85% of CF patients have an abnormal EFA profile [3]. Clinical features of EFA deficiency can occur, particularly in infants before diagnosis, including desquamating skin lesions, increased susceptibility to infection, poor wound healing, thrombocytopenia and growth retardation. Clinical evidence of EFA deficiency is extremely rare, however, in older CF patients who are adequately treated with nutritional and pancreatic enzyme supplements as appropriate [4].

Modification of the fatty acid profile in CF patients may be due to a number of factors, including reduced intake (malabsorption of fats [5] or inadequate diet), altered activity of desaturases or of hepatic lipase [6, 7], increased metabolism of EFA in undernourished patients [8, 9], increased synthesis of inflammatory mediators [10], defective CFTR altering utilisation of EFA in epithelial cells [11] and oxidative degradation of polyunsaturated fatty acids (PUFA) (thus decreasing proportion of PUFA) [8, 12].

Oxidative stress, caused by toxic reactive oxygen species (ROS), is believed to play an important role in the pathophysiology of cystic fibrosis (CF) [13–15]. Evidence for systemic oxidative stress in CF includes elevated plasma malondialdehyde (MDA) levels [8, 12, 16, 17], elevated breath pentane and ethane [18], elevated plasma levels of hydroperoxides [8, 16], depletion of the major lipoperoxidation substrates, such as linoleic and arachidonic acid [8], and elevated 8-iso-PGF2{alpha} concentrations in plasma [19] and breath condensate [20]. In CF, factors such as neutrophil response to infection [21] and increased metabolic rate [22] increase oxidant burden while, at the same time, CF patients have reduced antioxidant protection. Despite the administration of vitamin and pancreatic enzyme supplements to the 90% of CF patients with pancreatic insufficiency, residual steatorrhea and azotorrhea occur [4], with the potential for ongoing malabsorption of fat soluble antioxidants, namely vitamin E and ß-carotene. Furthermore, the high fat, high-energy diet that is recommended in CF has also been suggested as a cause of altered antioxidant protection. While increased dietary fat intake may increase levels of vitamin E, the intake of dietary antioxidants in foods such as fruits and vegetables (namely vitamin C and ß-carotene) may be limited. Consequently, many different and interacting factors can potentially lead to increased oxidative stress in CF, which may result in oxidative degradation of PUFA and subsequent decreased proportion of PUFA in cell membranes.

As oxidative stress is elevated in CF [19] and has been proposed as a source of modification of EFA status in CF, it is possible that antioxidant supplementation may prove to be beneficial not only for alleviation of oxidative stress, but also for the improvement of EFA status.

Vitamin E Protects PUFA in Erythrocyte Membranes
Our group previously reported low concentrations of vitamin E in stable CF patients (who had not used vitamin E supplements for at least four weeks prior to assessment) compared to age and gender matched healthy controls (Fig. 1) [19]. This agrees with many other reports of vitamin E deficiency in CF patients [6,23–30]. We have undertaken further analysis of blood samples from the groups previously described [19]. The CF patients were found to have elevated proportions of palmitic (16:0) and oleic (18:1n-9) acids and a decreased proportion of linoleic acid (C18:2n-6) in erythrocyte membranes compared to the controls (Table 1). This is in agreement with several other CF studies, in which analysis of blood and tissue lipids has commonly revealed altered FA distribution. Generally elevated proportions of palmitic (16:0), palmitoleic (16:1) and oleic (18:1n-9) acids and decreased proportions of linoleic (18:2n-6) and arachidonic (20:4n-6) acid are reported [5,6,31,32]. The CF patients in our study were well nourished and received adequate pancreatic supplements. Therefore, it is unlikely that malabsorption contributed to low erythrocyte levels of the EFA, linoleic acid.



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  		Fig. 1. Plasma vitamin E concentration in 21 stable CF patients versus 21 age and gender matched healthy controls. None of the participants had used vitamin supplements within the previous four weeks. The figure is based on previously published data [19]. p < 0.001.

 

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  		Table 1. Erythrocyte Membrane FA Composition in CF Patients versus Controls

 
Interestingly, our data also indicated a weak yet significant correlation between plasma vitamin E concentration and %PUFA in erythrocyte membranes, suggesting the hypothesis that vitamin E may have a protective effect on PUFA (Fig. 2). This is a relationship that is seen in CF patients, but not in healthy controls. It has been reported previously that PUFA concentrations are reduced under conditions of oxidative stress [33,34]. It is also well recognised that vitamin E is the major fat soluble antioxidant responsible for preventing oxidative damage to PUFA in membranes [35]. Vitamin E is transported in the blood attached to plasma lipoproteins and is incorporated into the lipid bilayers of biological membranes, where it determines oxidative susceptibility [35]. Our data [19] supports this view, with a correlation between plasma vitamin E and %PUFA in erythrocyte membranes in stable CF patients. This indicates that either the mechanism of fat absorption has led to similar alterations in vitamin E and FA status, or it indicates a protective effect of vitamin E on the loss of PUFA. A similar relationship has previously been observed in CF between LDL vitamin E content and LDL linoleic acid concentrations [30]. Another study involving athletes also demonstrated a similar direct relationship between plasma vitamin E levels and the EFA, eicosapentaenoic acid [36]. Again, in this context, it is hypothesized that vitamin E is protecting PUFA from oxidative stress, which occurs in athletes due to enhanced free radical production resulting from a heightened respiration rate during physical exercise [36]. Furthermore it has been observed that endogenous antioxidants may be upregulated in response to exercise [37,38], which may complement the effect of vitamin E in protecting PUFA.



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  		Fig. 2. %PUFA in erythrocyte membranes versus plasma vitamin E concentration in 21 CF patients. Data is non-parametric and analyzed using Spearman’s rank coefficient. r = 0.427, p = 0.05.

 
Vitamin E Supplementation Improves PUFA Status in CF
The suggestion that vitamin E may protect PUFA from oxidative degradation is further supported by a correlation we observed between the change in ({Delta}) plasma vitamin E and {Delta} plasma PUFA following antioxidant supplementation with 200mg vitamin E (as d-{alpha}-tocopherol) in 22 CF patients (Fig. 3) [39]. While no correlation was observed between {Delta}vitamin E and {Delta}PUFA in erythrocytes in the supplementation trial, this is not surprising, due to the short duration of the trial (eight weeks). It is probable that in time, as erythrocytes turn over and plasma fatty acids are incorporated into cell membranes, the relationship will also be reflected in erythrocyte cell membranes. Thus a role for vitamin E supplementation in improving EFA status in CF is suggested.



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  		Fig. 3. {Delta} plasma PUFA concentration versus {Delta} plasma vitamin E concentration following antioxidant supplementation. Data is normally distributed and analyzed using Pearson’s correlation coefficient. r = 0.544, p = 0.009.

 
Restoring EFA Status in CF
In the past, supplementation with linoleic acid has been recommended to restore EFA status, usually involving enteral feeding with vegetable oils high in linoleic acid. EFA deficiency has improved or resolved using this technique [40–42]. However, linoleic acid is a precursor for arachidonic acid, which is a precursor of several inflammatory mediators including prostaglandins, thromboxanes and leukotrienes (in particular LTB4). N-3 PUFA inhibit desaturation and chain elongation of linoleic acid, resulting in a build up of linoleic acid and a reduction in arachidonic acid levels [43]. This may lead to a reduction in the inflammatory metabolites of arachidonic acid. Thus the use of an n-3 FA has been considered, as this may improve EFA status (in particular linoleic and {alpha}-linolenic acids) while alleviating inflammation by reducing levels of inflammatory mediators [10]. N-3 fatty acids have previously been shown to correlate with lung function in CF [31].

A study by Kurlandsky et al. [44] showed that supplementation of CF patients with eicosapentaenoic acid (EPA) (20:5n-3) and docosahexaenoic acid (DHA) (22:6n-3) resulted in both n-3 fatty acids being absorbed and incorporated into platelet phospholipids. No significant clinical differences or adverse effects were observed following the six weeks of supplementation. Lawrence and Sorrell [45] supplemented nine CF patients with EPA for six weeks in a double-blind, placebo-controlled crossover trial. EPA supplementation was associated with reduced sputum volume, improved pulmonary function and modulation of inflammatory mediators within the lung. While the results are promising, it is difficult to determine if the improvements were due to the EPA or other variables such as increased energy intake that occurred as a result of the intervention.

The benefit of n-3 fatty acid therapy is yet to be confirmed. While supplementation with n-3 PUFA may improve EFA status, it will also increase the proportion of readily oxidizable PUFA in cell membranes. This, while reducing inflammation, may make the patient more susceptible to oxidant injury and subsequent lung damage [46], although this effect is debatable [47]. Studies regarding the effect of increased concentrations of highly polyunsaturated fatty acids on in vivo lipid peroxidation are highly contradictory [48–53]. The data linking vitamin E to PUFA status indicate that a more appropriate therapy may be to increase n-3 FA intake as well as concurrently supplementing with antioxidants, which may protect PUFAs from oxidative degradation (Fig. 4). Augmented antioxidant status has been shown to inhibit the generation of PUFA oxidation products in other circumstances [54,55].



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  		Fig. 4. Factors determining membrane EFA status.

 
Summary
In CF, EFA status is impaired compared to healthy controls. Furthermore, plasma vitamin E concentration is linked to %PUFA in erythrocyte membranes, suggesting that higher concentrations of circulating vitamin E may prevent loss of PUFA due to oxidative degradation in cell membranes. Supplementation with vitamin E results in increased plasma concentrations of vitamin E, which correlate with increased plasma PUFA concentrations. This suggests that administration of antioxidants (in particular 200mg of vitamin E) to CF patients may be a means of maintaining and/or improving EFA status by blocking losses due to free radical induced oxidation, as described in Fig. 4. Thus, antioxidant supplementation should be further considered in the treatment of CF patients with EFA.

Received July 30, 2001. Accepted August 30, 2002.


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