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Original Articles: Nutrition

Red Meat Consumption and Serum Lipids and Fatty Acids in Toddlers: Secondary Outcomes of a Randomized Controlled Trial

Szymlek-Gay, Ewa A.; Gray, Andrew R.; Heath, Anne-Louise M.; Ferguson, Elaine L.§; Skeaff, C. Murray

Author Information
Journal of Pediatric Gastroenterology and Nutrition: September 2018 - Volume 67 - Issue 3 - p 395-400
doi: 10.1097/MPG.0000000000002018

Abstract

What Is Known

  • Lean red meat is recommended for toddlers because it is rich in iron.
  • Red meat also contributes saturated fat and cholesterol to toddlers’ diets.
  • The effects of increasing red meat consumption on serum cholesterol and fatty acids in toddlers have not been investigated.

What Is New

  • An ∼3-fold increase in lean red meat intake, from ∼10 to ∼30 g/day, does not change serum lipid concentrations or fatty acid composition among healthy toddlers.
  • Approximately 30 g/day of lean red meat, to a total of ∼40 g/day of all meat, can be incorporated into toddlers’ diets without adverse effects on their serum lipids or fatty acids.

Up to 40% of young children in high-income countries have iron deficiency (1–6). Lean red meat is rich in bioavailable iron and its inclusion in toddlers’ diets is recommended to maintain adequate iron status (7–9).

In a 20-week randomized controlled trial we found that a diet with increased amounts of red meat prevented the decline in toddlers’ iron stores observed when the usual diet was consumed (10). Amongst parents of toddlers in the trial, a barrier to increasing the amount of red meat in their children's diet was a concern that it would adversely affect their child's blood cholesterol (11). Serum cholesterol in children responds to changes in saturated fat and cholesterol intake (12–14), and red meat contributes saturated fat and cholesterol to toddlers’ diets (15). Therefore, in designing the study, a secondary outcome was to examine the effects of increased red meat consumption on serum cholesterol.

Red meat also contains docosahexaenoic acid (DHA), a very-long-chain n-3 polyunsaturated fatty acid (PUFA) that plays a role in neurological development (16). Fish is the richest dietary source of DHA. When fish intake is low, meat can provide a significant proportion of total DHA intake (15,17), and has been shown to increase DHA composition of plasma or platelet lipids in adults (18,19).

This study examined, in toddlers, the effects of promoting increased red meat consumption on serum total and high-density lipoprotein (HDL) cholesterol concentrations, and serum fatty acid composition.

METHODS

Participants and Study Design

Study details have been published previously (10) and only essential elements are presented here. This 20-week parallel randomized controlled trial investigated the effects of providing lean red meat on micronutrient status in healthy 12 to 20-month-old New Zealand toddlers (10,20,21). The sample size was based on detecting a reduction in the prevalence of low iron status (10). An exclusion criterion pertinent to this article was a parent unwilling to encourage their toddler to consume the study foods. On enrollment, parents completed a self-administered sociodemographic questionnaire, and child weight and length were measured (22,23). The University of Otago Human Ethics Committee approved this trial (03/141); the parent or legal guardian of each toddler (referred to as the “parent” throughout the article) provided informed written consent.

Toddlers were randomized to red meat (n = 90) or control (n = 90) groups (10). The result of the primary outcome, which was improved iron status, has been published previously (10). This article focuses on the secondary outcomes of serum lipids and fatty acids.

Intervention

Parents were provided with preprepared portions of toddler-friendly meat dishes (red meat group) or powdered cow's milk (control group; standard instantized whole milk powder with required A and D added; Fonterra, Auckland, New Zealand; control milk). The meat dishes were designed to contain 0.25 mg of absorbable iron per portion. Sixteen meat dishes included beef (14 dishes based on 94% lean ground beef and 2 based on 92% lean blade steak), 4 lamb (93% lean short-cut leg), and 1 dish included lamb's liver (91% lean) and pork bacon (92% lean); all visible fat was removed before preparation of the dishes. The red meat group was encouraged to consume 2 portions/day of the study dishes for 20 weeks. Each cooked portion of the study dishes provided on average 28 g of red meat, 428 kJ of energy and 5.2 g of fat (Table, Supplemental Digital Content 1, http://links.lww.com/MPG/B381). The control group was advised to replace the milk normally consumed with the study milk. When reconstituted, the powdered cow's milk contained 278 kJ of energy and 3.6 g of fat per 100 g.

Adherence to the intervention was assessed by parents recording the weight of study dishes or powdered cow's milk consumed daily during weeks 2, 7, 11, 15, and 19.

Dietary Assessment

Daily intakes of energy, nutrients, red meat, all meat, and milk were calculated from 3-day weighed food records (Vista Electronic Kitchen Scale, model 3010, Salter Housewares; precision ±1 g) (24,25) collected at baseline, weeks 4 and 20.

Biochemical Assessment

Nonfasting venipuncture blood samples were collected at baseline and week 20, immediately refrigerated, and processed within 2 hours; serum was stored at −80°C.

Serum total cholesterol was measured on a Cobas Mira Plus autoanalyzer using Cholesterol CHOD-PAP enzyme kits (Roche Diagnostics, Mannheim, Germany). HDL cholesterol was measured in the supernatant after precipitation of apolipoprotein B–containing lipoproteins with phosphotungstic acid/magnesium chloride solution (26). The cholesterol measurements were validated through participation in the Royal Australasian College of Pathologists Quality Assurance Program. The coefficient of variation was 1.8% for total cholesterol and 4.3% for HDL cholesterol.

For serum fatty acid analysis, lipids were extracted along with an internal standard (triheptadecanoyl-glycerol) and fatty acid methyl esters prepared using 6% H2SO4 in methanol. Individual fatty acids were separated by gas-liquid chromatography and detected by flame ionization. The gas chromatography column was a DB-225 megabore column (30 m length, 0.25 mm internal diameter, 0.25 μm film thickness; J & W Scientific, Deerfield, IL). The fatty acid results are reported as molecular percentage (mol%). Pooled serum was used to assess the precision of the fatty acid analysis; 9 pooled samples in total were analyzed, 1 for every 40 experimental samples. The coefficient of variation was <5% for fatty acids contributing >1 mol%, and 4% to 10% for fatty acids contributing ≤1 mol%.

A limited volume of serum was available for each participant and priority was given to measuring the primary study endpoints of biochemical iron status. Therefore, some participants had either no or insufficient sample remaining from the baseline or week 20 blood samples for the analysis of serum lipids and fatty acids. The number of serum lipid and fatty acid samples analyzed are reported in the tables.

Statistical Analysis

Analyses were conducted using modified intention to treat principles (using all available data and according to the assigned study group irrespective of compliance). Baseline values for age, sex, ethnicity, education, breast-feeding status, income, and z scores were described and then compared between participants with and without the measurements of serum lipids or fatty acids; Student's t tests were used for continuous variables providing residuals were normally distributed; and Chi-square tests were used for categorical variables providing expected cell counts were ≥5 in ≥80% of cells.

Linear mixed models with a random participant effect were used to compare changes in energy and nutrient intakes (week 0–20), and serum lipids and serum fatty acid composition (week 0– 20) between the groups. Differences in change between the groups were assessed using a group-by-time interaction and differences in adjusted means were used to estimate effects. In all models, adjustments were made for sex, breast-feeding status at weeks 0 and 20, and baseline age. Conditional residuals from all models were examined and the outcome variables were log-transformed where this improved their normality and/or homoscedasticity. Where log-transformations were used, results are shown as ratios of geometric means.

The analyses of red meat, all meat, and milk intake at all 3 time points are described elsewhere (10).

Analyses were performed with Stata (version 13.1; Stata Corp) or SAS (version 9.1.2; SAS Institute Inc, Cary, NC). No adjustments were made for multiplicity and marginally significant results should be interpreted with caution. Statistical significance was determined by 2-sided P < 0.05.

RESULTS

Of the 180 participants, 87 (97%) in the red meat group and 85 (94%) in the control group completed the study (no evidence of a difference in these percentages: Fisher's exact P = 0.720).

The participants’ mean age at baseline was 17.2 (standard deviation 2.8) months, 57% were boys, and 80% were white (Table, Supplemental Digital Content 2, http://links.lww.com/MPG/B382). The characteristics of participants for whom serum lipids or fatty acids were measured did not differ from those of participants for whom they were not measured (all P ≥ 0.057).

The red meat group consumed a mean of 0.7 portions/day of study meat dishes (range: 0.0–2.3 portions/day). Seventy-six (84.4%) children in the control group adhered fully to the intervention and replaced all their regular milk with the control milk.

Compared to the control group, mean intakes of red meat and all meat increased in the red meat group by 19.4 g/day (95% confidence interval [CI]: 14.9, 23.8 g/day) and 9.7 g/day (95% CI: 4.3, 15.1 g/day), respectively, and milk intake decreased by 89.7 g/day (95% CI: −133.4, −45.9 g/day; Table 1).

TABLE 1
TABLE 1:
Reported red meat, all meat, and milk intakes of toddlers at week 0 and during the intervention

In the red meat group, relative to the control group, the mean energy intake decreased by 278 kJ/day (95% CI: −547, −9 kJ/day), total fat decreased by 3% of energy (95% CI: −5, −1%), saturated fat decreased by 2% of energy (95% CI: −3, −1%), monounsaturated fat decreased by 1% of energy (95% CI: −2, −0%), cholesterol decreased by 23% (95% CI: −32, −12%), and carbohydrate increased by 3% of energy (95% CI: 1, 5%; Table 2).

TABLE 2
TABLE 2:
Reported energy and nutrient intakes of toddlers at week 0 and week 20

There was no evidence of intervention effects on serum lipids (Table 3), or serum fatty acid composition except for pentadecanoic acid (15:0) which marginally decreased in the red meat group relative to the control group (−0.0 mol%; 95% CI: −0.1, −0.0 mol%; Table 4).

TABLE 3
TABLE 3:
Serum lipids of toddlers at week 0 and week 20
TABLE 4
TABLE 4:
Serum total fatty acid composition of toddlers at week 0 and week 20

DISCUSSION

This first randomized controlled trial to investigate the effects of promoting increased lean red meat consumption on serum total and HDL cholesterol, and serum fatty acids in toddlers found that an ∼3-fold increase in daily lean red meat intake during 20 weeks, from ∼10 to ∼30 g/day, resulted in no consistent evidence of change in serum lipids or fatty acids.

The finding that serum cholesterol did not change is not unexpected. Evidence from adults suggests that lean red meat can be included in cholesterol-lowering diets without attenuating the cholesterol-lowering effects of the diet (27–29). In the present study, the meat dishes were prepared from lean red meat (<10% fat) and were consumed as part of the toddlers’ usual diet so would not be expected to affect serum cholesterol. Interestingly, the intervention did result in significant reductions in the intakes of saturated fat and cholesterol in the red meat group, but these dietary changes were not sufficient to change serum lipid concentrations. Although the reductions in the intake of saturated fat and cholesterol per 1000 kJ in the red meat group were similar to those reported previously in Finnish children in whom a diet lower in saturated fat and cholesterol in infancy and toddlerhood led to a decrease in serum total cholesterol concentrations (12,13), the contribution of saturated fat to total energy intake (ie, 17%–18%) appeared higher and the polyunsaturated to saturated fat ratio (∼0.17) was considerably lower in the red meat group compared to that reported for the children in the Finnish study (at 24 months, energy from saturated fat was ∼12% and polyunsaturated to saturated fat ratio was ∼0.52) (13). The 19.4 g/day higher red meat consumption in the red meat group may seem modest, but the response to the dietary intervention is probably at the upper end of changes achievable in the general population given that participants received intensive advice and support to increase red meat intake, and were provided with free-of-charge ready-to-heat pretested red meat meals.

Although meat is a source of long- and very-long-chain n-3 PUFAs (30), an increase in lean red meat intake to ∼30 g/day and all meat to ∼40 g/day for 20 weeks did not appear to affect their serum composition in our study. As the New Zealand food composition database does not provide information on the individual fatty acid content of all foods in the database, we were unable to assess their intakes. We, however, estimated that, based on the amount of animal tissue consumed by the toddlers and the fatty acid composition of meat, poultry, and fish (30), the red meat group would have increased intakes of long- and very-long-chain n-3 PUFAs from animal tissue by at least 2-fold up to 35 to 50 mg/day; these amounts were clearly insufficient to effect a change in serum fatty acid composition. In contrast, consumption of 67 g/day of red meat from grass-fed animals (addition of 15 mg/day of long- and very-long-chain n-3 PUFAs) (18) or 49 g/day of kangaroo meat (addition of 80 mg/day of very-long-chain n-3 PUFAs) (9,19,31) resulted in a significant increase in alpha-linolenic, eicosapentaenoic, docosapentaenoic, and DHA composition of plasma or platelet lipids in adults. Although the energy intake in these studies was only twice as high as that of the toddlers in our study, due to the types of meat consumed, the long- and very-long-chain n-3 PUFA intakes were several-fold greater (18,19) than those estimated in our study. The 89.7 g/day decrease in milk consumed by the red meat group is unlikely to have affected intakes or serum composition of long- and very-long-chain n-3 PUFAs because bovine milk is a poor dietary source of these fatty acids (32).

Our results may be generalizable to other populations of healthy 12 to 24-month-old children because toddlers residing in high-income countries have red meat intakes (33–37) and total meat intakes (33,35–38) strikingly similar to those reported at baseline by children in our study.

The study's strengths include excellent participant retention rates. Blood samples were, however, not available for all participants, and the increase in red meat intake in the red meat group was relatively small (19.4 g/day) despite parental efforts to offer more than this. These results suggest that the toddlers’ appetite for red meat was the limiting factor.

In conclusion, these data suggest that ∼30 g/day of lean red meat, to a total of ∼40 g/day of all meat, can be recommended to toddlers within high-resource settings to improve their iron intake and status (10), with no adverse effects on their serum lipids or fatty acids.

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Keywords:

alpha-linolenic acid; docosahexaenoic acid; docosapentaenoic acid; eicosapentaenoic acid; high-density lipoprotein cholesterol; total cholesterol

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