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Nutritional Methodology

The Fatty Acid Profile of Buccal Cheek Cell Phospholipids Is a Noninvasive Marker of Long-Chain Polyunsaturated Fatty Acid Status in Piglets^{1 ,2}

U.S. Department of Agriculture/ARS Children’s Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030-2600

³To whom correspondence should be addressed. E-mail: alapillo{at}bcm.tmc.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The fatty acid pattern of cheek cell phospholipids has been proposed as a noninvasive marker of long-chain polyunsaturated fatty acid (PUFA) status. However, the cheek cell phospholipid fatty acid pattern has been compared only with that of plasma and erythrocytes. The objective of this study was to assess the extent to which the fatty acid profile of cheek cell phospholipids reflects that of tissue phospholipids. Piglets (n = 31; 6 d old) were fed five formula diets differing in total fat and fatty acid composition. After 14 d of consuming the assigned diets, cheek cell plasma, erythrocyte, liver, muscle, adipose tissue, retina and brain samples were collected for determination of the phospholipid fatty acid patterns. There were significant correlations between the cheek cell phospholipid content of most PUFA and the content of these fatty acids in tissue phospholipids (r = 0.509–0.951, P < 0.01). The cheek cell phospholipid content of most of the PUFA, except 20:4(n-6), reflected that of other tissue phospholipids as well as, or nearly as well as the contents of plasma and/or erythrocyte phospholipids. The correlations between the 22:6(n-3) contents of cheek cell, plasma, or erythrocyte phospholipids and those of brain and retina phospholipids were relatively poor (r = 0.596–0.737, P < 0.001). We conclude that the fatty acid pattern of cheek cell phospholipid can be used as a noninvasive marker of PUFA status, but it is not a better index than the pattern of plasma or erythrocyte phospholipids, particularly for assessing the fatty acid pattern of organs with slow fatty acid incorporation and/or turnover rates.

KEY WORDS: • brain • buccal mucosa • fatty acids • liver • pigs

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Analytical measurements of fatty acid intakes are useful for validating the dietary intakes of subjects participating in epidemiologic and interventional studies as well as for evaluating essential fatty acid status. Most clinical trials have used either plasma or erythrocyte lipid profiles to document compliance and/or to assess tissue fatty acid status (1 ). Some studies in adults have used the fatty acid pattern of adipose tissue for these purposes (2 –4 ). However, a less invasive marker is preferred, particularly for longitudinal studies requiring repetitive tissue sampling and studies in infants, in whom the type, amount, and frequency of tissue sampling is often restricted. For such studies, the fatty acid pattern of cheek cell lipids is an attractive alternative (5 ,6 ).

Three recent studies have shown that the polyunsaturated fatty acid (PUFA)⁴ profile of cheek cell phospholipid correlates significantly with that of plasma and red blood cell (RBC) phospholipids (7 –9 ). It also has been postulated that the cheek cell fatty acid pattern is a reliable index of tissue fatty acid status (8 ), particularly that of neural tissues, and one study showed a significant association between cheek cell docosahexaenoic acid content and visual function of infants (9 ). Nonetheless, the extent to which the fatty acid pattern of cheek cell phospholipid correlates with the fatty acid pattern of tissue phospholipids is not known.

We hypothesized that the fatty acid pattern of cheek cell phospholipids reflects the phospholipid fatty acid pattern not only of plasma and erythrocyte phospholipids but also of organs such as liver, skeletal muscle, adipose tissue, retina, and brain. This hypothesis was addressed by a study in piglets, which respond similarly to human infants with respect to changes in plasma phospholipid fatty acid content in response to diet (10 –13 ). The objectives of the study were as follows: 1) to assess the extent to which the fatty acid content of cheek cell phospholipids reflects the fatty acid content of the phospholipids of other tissues (i.e., liver, skeletal muscle, adipose tissue, retina, and brain); 2) to compare the fatty acid pattern of cheek cell phospholipids (i.e., proposed new marker) to that of plasma and erythrocyte phospholipids (i.e., currently used markers) as indicators of the fatty acid pattern of tissue phospholipids.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Animal and diets.

The study involved crossbred male piglets (n = 31; Large White x Hampshire x Duroc) purchased from the Texas Department of Criminal Justice (Huntsville, TX). The pigs had been suckled for a minimum of 48 h before arrival at the laboratory. Upon arrival, they consumed a liquid milk replacer (LitterLife, Merrick’s, Middleton, WI) ad libitum until 5 d of age. On d 6 of life, they were assigned to one of five formulas (n = 5–7 per group), which were fed exclusively from d 6 to 20 of life at a rate of 840 kJ [200 kcal]/(kg·d). The experimental diets were designed for another study concerning the effects of type and amount of (n-3) PUFA on gene expression. The diets were fed at a rate of 50 g dry matter/(kg·d). The energy and protein content/kg dry matter was 1680 kJ and 250 g, respectively. The five formulas had identical amounts of energy (1680 kJ/kg dry matter), protein (250 g/kg dry matter), and vitamins and minerals⁵ . Formulas A and C contained 25% of energy as fat (low fat), whereas Formulas B, D, and E contained 44% of energy as fat (high fat); these diets were made isocaloric to Formulas A and C by lowering lactose content (300 g/kg vs. 500 g/kg dry matter). The fat blends and the fatty acid compositions of the diets differed (Table 1 ). Formulas A and B were enriched with corn oil [high 18:2(n-6) concentration], Formulas C and D were enriched with flaxseed oil [high 18:3(n-3) concentration], and Formula E was enriched with fish oil [high 20:5(n-3) and 22:6(n-3) concentration]. The protocol was approved by the Animal Care and Use Committee of Baylor College of Medicine and was conducted in accordance with the NRC’s Guide for the Care and Use of Laboratory Animals.

At 20 d of age, 5 mL of blood was withdrawn from the jugular vein into a tube containing 150 g/L potassium EDTA solution (Vacutainer, Becton Dickinson and Company, Franklin Lakes, NJ). Plasma and erythrocytes were separated by centrifugation at 2000 x g for 15 min. The erythrocyte pellet was washed three times by suspension in PBS containing 1 mmol/L EDTA, pH 7.4 (8 parts buffer; 1 part erythrocytes). Plasma and washed erythrocytes were stored at -70°C until used for analysis.

As the blood sample was being processed, the piglets were killed by intracardiac injection (1 mL/4.5 kg) of a commercially available euthanasia solution (Beuthanasia-D, Schering-Plough Animal Health, Kenilworth, NJ) and liver (left lobe), muscle (gastrocnemius), adipose tissue (subcutaneous shoulder fat), eyes, and brain were rapidly removed. Liver, muscle and adipose tissue were cleaned of blood with PBS/1 mmol/L EDTA buffer and samples were frozen immediately in liquid nitrogen. Brain and eyes were kept on ice until processed further. The mouth cavity of the piglets was flushed with 10 mL of water to remove residual food and cheek cells were collected by gentle, repeated ( 4 times) rubbing of the mucosal membrane lining the inside of both cheeks with two sterile cotton swabs per cheek (Pur-Wraps, Hardwood Products, Guilford, ME). The cotton swabs, with the majority of the wooden applicator stick removed, were then placed in a clean glass tube and frozen at -70°C until analysis.

The whole brain was cut to expose ventricular spaces, washed with excess PBS/1 mmol/L EDTA buffer and frozen at -70°C. Eyes were converted to eyecups by removal of the anterior region (cornea, iris, and lens) and the vitreous humor. Eyecups were incubated for 15 min at room temperature in Hank’s balanced salt solution (HBSS) containing 2 mmol/L EDTA, pH 7.4, and the retinas were removed by detachment from the underlying retinal pigment epithelium/choroid plexus and optic nerve junction using jeweler’s forceps (14 ). Retinas were washed by gentle flotation in HBSS/2 mmol/L EDTA buffer and frozen at -70°C.

Total lipid extraction.

Samples (1–2 g) of liver, brain, muscle, and adipose tissue were homogenized in PBS containing 40 mmol/L EDTA, pH 7.4 (5 mL/g tissue), using an electric homogenizer equipped with a sawtooth generator (Polytron, Brinkmann Instruments, Westbury, NY). Retinas from both eyes were homogenized into 1 mL of HBSS/2 mmol/L EDTA buffer, using a vortex mixer. Lipids were extracted from 1 mL of each tissue homogenate (liver, muscle, brain, adipose tissue, and retina), 0.4 mL plasma, the entire erythrocyte pellet, the cotton swabs used to collect cheek cells and 0.1 mL of the formulas using a modification of the methods of Folch et al. (15 ) and Bligh and Dyer (16 ). Before the extraction, 1 µmol of heptadecanoic acid (17:0), as di-17:0 L--phosphatidylcholine (Sigma, St. Louis, MO) dissolved in chloroform/methanol (2:1, v/v) was added to the sample as an internal standard for later quantification of fatty acids.

Separation of phospholipids, preparation of fatty acid methyl esters (FAME) and gas chromatography (GC) analysis.

Phospholipids of all specimens were separated by TLC as described by Kupke and Zeugner (17 ). The TLC plate was dried, sprayed with 0.5g/L 2,7-dichlorofluorescein in methanol and visualized under UV light to mark the exact position of the lipid bands. The band, which remained at the origin and is assumed to contained mainly phospholipids, was scraped from the TLC plate and converted to FAME as described by Morrison and Smith (18 ).

FAME (2 µL) were separated by GC on a 30 m x 0.25 mm i.d., 0.25-µm film, DB-225 capillary column (J&W Scientific, Folsom, CA), using a Hewlett-Packard 5890 gas chromatograph (Hewlett Packard, Atlanta, GA) equipped with a hydrogen flame ionization detector. Individual fatty acids were identified by comparison with the retention times of FAME standards (Nu-Chek-Prep, Elysian, MN). The temperature gradient for elution of the FAME was 160°C initially, ramped at 1°C/min to 220°C (60 min total), and held at 220°C for 5 min before reinitialization.

The method for collecting the cheek cells as described above did not allow quantification of the concentration of fatty acids. Therefore, all results were expressed as mol/100 mol total fatty acids, which were calculated from chromatograms using a proportional comparison of fatty acid peak areas after each was normalized against the fatty acid’s molecular mass and flame ionization response factor. In the absence of a detectable peak for a fatty acid, a value of 0.05 mol/100 mol of fatty acids, the limit of detection of the GC, was assumed. GC analyses were performed in duplicate and the data averaged.

Assuming that the mass of cheek cells collected from each piglet was similar, the fatty acid content of each cheek cell sample (nmol/sample) was estimated by comparing fatty acid peak areas to the correspondingly area of the 17:0 internal standard. A greater fatty acid content per sample was found in pigs fed 44% of energy as fat compared with those fed 25% energy as fat (146.5 ± 47.1 vs. 68.8 ± 32.8 nmol/sample, P < 0.0001). The cheek cell fatty acid content per sample was approximately similar to that of 100 µL of plasma diluted 1:4. When dealing with small samples, even minimal contamination during the determination of the fatty acid pattern is likely to lead to inaccurate results. Thus, to test the effect of dilution on accuracy, we compared the fatty acid patterns of a 1:4 dilution of plasma to that of the nondiluted plasma. The (n-3) and (n-6) fatty acid contents were similar, but the 16:1(n-9) content of all diluted plasma samples was higher, presumably reflecting contamination from the TLC plate itself. Because the monounsaturated fatty acids contents were questionable, only PUFA contents of the cheek cells are reported.

Statistical analysis.

Equality of variance for each variable was tested using Bartlett’s and Levene’s tests. One-way ANOVA followed by Fisher’s test, or the Kruskal-Wallis test followed by the Mann-Whitney test were used when appropriate to determine significant differences among groups in mean content of each fatty acid. The relationships between the cheek cell phospholipid content of a given fatty acid (mol/100 mol total fatty acids) and that of other tissues were examined by regression analysis. Correlations were expressed as the Pearson product moment correlation coefficient (r). Differences among significant correlation coefficients were assessed by Fisher’s Z transformation. Differences with a P value < 0.05 were considered significant.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The groups of piglets differed in the fatty acid contents of cheek cell phospholipids (Table 2 ) as well as plasma, erythrocyte, liver, skeletal muscle, adipose tissue, retina, and brain phospholipids contents (results not shown). These differences in cheek cell as well as other phospholipid contents mirrored the PUFA intakes of the piglets.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Measuring the content of cheek cell fatty acids is a very attractive method for assessing fatty acid intake, including the compliance of subjects with a specific experimental diet. Our data, obtained in piglets, show that the PUFA contents of cheek cell phospholipids mirror the dietary content of these fatty acids. This finding, combined with the results of three recent studies in infants fed diets differing less dramatically in PUFA (7 –9 ), demonstrate that the fatty acid pattern of cheek cell phospholipid can be used to monitor compliance with diets enriched with PUFA.

These data are the first to examine the relationship between the fatty acid profile of cheek cell phospholipids and that of other organs. The major goal in designing the diets was not to mimic fatty acid composition of infant formulas but to ensure significant differences in tissue fatty acid profiles within a relatively short period of time (i.e., 2 wk). The fatty acid profile of cheek cell phospholipid reflected that of liver, skeletal muscle and adipose tissue with a reasonable degree of confidence. Indeed, the PUFA content, except that of 20:4(n-6), correlated significantly and strongly (r > 0.7; P < 0.001) with that of cheek cell phospholipids. Further, correlations between the liver or muscle phospholipid fatty acid profile and the profile of cheek cell phospholipid were either minimally lower or not different from the correlations between the fatty acid profiles of plasma or erythrocyte phospholipid and those of liver and muscle phospholipids.

Prediction of the 22:6(n-3) content of brain is of particular interest. Some animal studies show that the correlation between the brain content of this fatty acid and the 22:6(n-3) content of plasma or erythrocyte phospholipids is weaker than the correlation between the 22:6(n-3) content of other tissues (e.g., liver) and that of plasma and erythrocytes (10 ,11 ). In addition, a postmortem study of human infants showed a significant correlation between the 22:6(n-3) content of brain phospholipids and that of erythrocyte phospholipids but not between the contents of retina and erythrocyte phospholipids (19 ). In the present study, the correlations between the 22:6(n-3) content of cheek cell phospholipids and that of brain and retina phospholipids were significant but relatively poor. These correlations, however, are similar to those between the brain and retinal phospholipid contents of 22:6(n-3) and the contents of plasma and the erythrocyte phospholipids. Phospholipid content of 20:4(n-6) in the brain does not reflect the content of this fatty acid in plasma, erythrocyte or cheek cell phospholipids. Thus, these data do not support the use of cheek cell fatty acid pattern over that of plasma or erythrocytes as a better index of the brain and retina fatty acid composition.

A potential drawback to the use of the cheek cell phospholipid fatty acid pattern is the small amount of material (i.e., lipids) collected. The amount of cheek cell phospholipid fatty acids collected in this study was 25% as much as in 100 µL of plasma. The small amount of material collected increases the chances of error because of contamination. In addition, the concentrations of long-chain PUFA [i.e., 20:4(n-6), 20:5(n-3), and 22:6(n-3)] in cheek cell phospholipid are only 5–25% of their concentrations in plasma phospholipid. Therefore, the low 20:4(n-6) content of cheek cell phospholipid is a reasonable explanation for the absence of a significant correlation, or a poor correlation, between cheek cell phospholipid 20:4(n-6) content and the 20:4(n-6) content of other tissue phospholipids in both piglets and infants (7 ,9 ).

Tissues that interact directly with the bloodstream or are nurtured by easily permeable barriers would be expected to show changes in response to diet more quickly and extensively than tissues that are nurtured by diffusion through highly selective barriers (20 ). If the major origin of fatty acids in cheek cell phospholipids is the plasma, the fatty acid pattern of cheek cell phospholipids and plasma phospholipids should be similar, just as the patterns of plasma, erythrocyte and liver phospholipids are similar. In addition, the rapid turnover of cheek cells (5 d) makes them relatively sensitive to diet-induced changes and, hence, more likely to reflect the fatty acid composition of organs with rapid fatty acid incorporation and turnover rates (e.g., liver) than that of organs with slower fatty acid incorporation and turnover rates (e.g., brain and retina) (21 ).

In summary, the data reported here show that the cheek cell phospholipid content of most of the PUFA reflects that of liver, skeletal muscle, and adipose tissue phospholipids as well as or nearly as well as the contents of plasma and/or erythrocyte phospholipids. However, the fatty acid pattern of cheek cell phospholipids is not a better marker of the pattern of brain or retinal phospholipids than the pattern of plasma and erythrocyte phospholipids. Thus, the fatty acid pattern of cheek cell phospholipids is a reasonable, noninvasive marker of PUFA status but it is not a better index than the pattern of plasma or erythrocyte phospholipids.

	ACKNOWLEDGMENTS

 
The authors thank O’Brian E. Smith and J. Kennard Fraley for statistical advice, Harry J. Mersmann for technical help, and Leslie A. Loddeke for editorial assistance (USDA/ARS Children’s Nutrition Research Center, Houston, TX).

	FOOTNOTES

 
¹ This work is a publication of the U.S. Department of Agriculture/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organization imply endorsement by the U.S. Government.

² Supported by federal funds from the U.S. Department of Agriculture, Agricultural Research Service, under Cooperative Agreement No. 58–6250-6001 and by grant IRO1-HD37133. Alexandre Lapillonne was supported in part by the Association de Nutrition, Santé et Charcuteries, France.

⁴ Abbreviations: FAME, fatty acid methyl esters; GC, gas chromatography; HBSS, Hank’s balanced salt solution; PUFA, polyunsaturated fatty acid.

⁵ Mineral concentration (/100g): calcium, 0.05 g; copper, 20 mg; iron, 11.9 mg; phosphorus, 0.83 g; sodium, 1.08 g, zinc, 11.9 mg. Vitamin concentration (IU/100 g): vitamin A, 5997; vitamin D, 550; vitamin E, 38.

Manuscript received 26 February 2002. Initial review completed 16 March 2002. Revision accepted 29 April 2002.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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