Journal of the American College of Nutrition, Vol. 27, No. 1, 168-176 (2008)
Published by the American College of Nutrition
Pre-Operative Modification of Dietary Glycemic Index Improves Pre but Not Post-Operative Indices of Insulin Resistance in Patients Undergoing Coronary Artery Bypass Graft Surgery
Victoria Tully, MSc,
Thomas M.S. Wolever, MD, PhD,
Pauline Darling, PhD, RD,
Lee Errett, MD and
Mary E. Keith, PhD, RD
Division of Cardiovascular and Thoracic Surgery (V.T., L.E.)
Department of Nutrition (P.D., M.E.K.)
St. Michael's Hospital, Department of Surgery (L.E., M.E.K.)
Department of Nutritional Science (T.M.S.W., P.D., M.E.K.), University of Toronto, Toronto, Ontario, CANADA
Address correspondence to: Mary Keith, PhD, RD, Coordinator of Nutrition and Dietetic Education, 6th Floor Cardinal Carter Wing - 6-056d, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario, M5B 1W8, CANADA. E-mail: keithm{at}smh.toronto.on.ca
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ABSTRACT
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Background: Improving insulin sensitivity in coronary artery bypass grafting (CABG) patients may translate into improved glycemic control and postoperative outcomes. The implementation of a low glycemic index (LGI) diet in the pre-operative period may improve insulin sensitivity and subsequently impact on the development of post-operative insulin resistance. The aim of this study was to determine whether a short term LGI diet would reduce postoperative insulin resistance.
Methods: Eleven non-diabetic patients referred for elective CABG surgery were randomized to consume either a high glycemic index (HGI)(5) or LGI (6) diet for three weeks prior to their surgery. Outcomes, including insulin sensitivity (SITT, HOMA), were measured at baseline, preoperatively and postoperatively.
Results: Substitution of HGI or LGI foods resulted in an average 8.6 unit increase, or 11.0 unit decrease, respectively, in glycemic index. Insulin sensitivity (HOMA) improved significantly in the LGI group preoperatively compared to the HGI group (p = 0.018). Insulin sensitivity (SITT) was significantly reduced postoperatively in both groups, but no significant difference was found between groups. There was a trend in the LGI group towards improved glycemic control which warrants further investigation.
Conclusion: A preoperative LGI diet presents a non-invasive cardio-protective opportunity warranting clinical trial.
Key words: glycemic index, diet, coronary artery bypass graft, surgery, outcomes, insulin resistance, glycemic control, inflammation
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INTRODUCTION
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Patients with heart disease are often obese, hypertensive and have dyslipidemia all of which have been related to the presence of insulin resistance and hyperinsulinemia [1]. Sixty percent of individuals with heart disease have been reported to have hyperinsulinemia reflecting insulin resistance [2]. Furthermore, patients with coronary artery disease (CAD) were found to have a significantly higher fasting insulin level when compared with those of patients without CAD [3]. A significant relationship was observed between the severity of the CAD and the degree of insulin resistance [4].
Insulin resistance may be the primary explanation for the transient hyperglycemia witnessed following major surgeries. Increased insulin resistance and hyperglycemia, particularly in the first few days post-operatively have been directly related with adverse clinical outcomes in both diabetic and non-diabetic CABG patients [5]. In a landmark study, aggressive post-operative glycemic control significantly reduced morbidity and mortality in a large cohort of surgical patients [6].
In an effort to improve outcomes, strategies aimed at reducing insulin resistance have been investigated. The provision of a pre-operative infusion of insulin and glucose was associated with a preservation of insulin sensitivity as well as an attenuated stress response in patients undergoing elective hip replacement surgery [7]. In addition, the consumption of a pre-operative carbohydrate beverage has also been found to preserve insulin sensitivity in a variety of elective surgical procedures [8]. The pooled results of these studies suggest that reduced insulin resistance is related to a shortened length of hospital stay [8,9].
The glycemic index approach to carbohydrate-rich food selection may also be an effective strategy to improve insulin sensitivity in surgical patients. A LGI diet has been linked with improved glycemic control, lower insulinemia, increased satiety and improved weight regulation as well as significantly reducing the risk of developing diabetes [10]. Consuming a LGI diet for four weeks in patients with coronary disease resulted in an improved insulin response to an oral glucose load with a significantly reduced incremental area under the insulin curve [11]. Furthermore, adipocytes from those following the LGI diet, collected at surgery, had improved in-vitro glucose uptake reflecting improved insulin sensitivity at the cellular level as well as a sustained effect of the dietary intervention into the surgical period. Therefore, this study aimed to extend these previous observations by investigating not only the potential of short-term substitution of high glycemic index (HGI) or LGI carbohydrates to improve pre-operative insulin sensitivity but also to determine whether the benefits of this intervention extended into the post-operative period resulting in a reduction of insulin resistance, or improved glycemic control and clinical outcomes in CABG patients.
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METHODS
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Study Subjects
This was a prospective, randomized, controlled trial. All elective, non-diabetic patients referred for first-time elective coronary artery bypass graft surgery were considered for entry into the study. Patients with known diabetes or a fasting glucose >7 mmol/L (last two months), a history of hepatic or renal disease, cancer, inability to communicate in English and who had a history of substance abuse were excluded from the study. Subjects on non-cardiac medications known to significantly influence glucose metabolism were also excluded. Eligible subjects were recruited at their first surgical consultation and subsequently met with the investigators on two occasions prior to surgery. Subjects were randomly allocated to follow a HGI or LGI diet using prepared envelopes blinded to the study coordinator. Subjects started the dietary intervention at baseline and continued up until midnight of the night before surgery at which time they fasted as per protocol. Blood samples for outcomes analyses were collected at baseline, preoperatively, approximately 1 hour postoperatively, 24 and 48 hours postoperatively and at discharge, for a total of 6 sampling intervals. Other relevant clinical and demographic data as well as measures of clinical outcomes were collected from the medical record.
Dietary Intervention
A defined dietary protocol adapted from a long-term glycemic intervention trial was adopted [12]. The protocol was designed to replace approximately 40% of dietary carbohydrates with either HGI or LGI foods. All other aspects of the diet remained unchanged. The number of servings of study foods to be consumed daily was determined by the average of habitual intake and estimated requirement. Habitual intake was assessed from a 3-day food record provided at the time of recruitment and returned at baseline. Subjects were then counseled on how to follow the dietary intervention. Total dietary glycemic index was assessed from 3-day food records filled out just prior to the pre-operative appointment. In between, participants filled out diet journals which were simply checklists for the number of servings of study foods consumed. These daily journals allowed participants to track their consumption of study foods and allowed the investigators to tabulate compliance by comparing reported consumption to the number of prescribed servings. We estimated that a compliance of at least 60% would be sufficient to produce a change in dietary glycemic index based on comparison with previous work [11]. Subjects with a compliance of less than 60% were considered non-compliant with the dietary strategy. A folder containing instructions, food journals and records, and a list of the study foods was provided. A selection of appropriate foods were provided to participants at baseline. Follow-up counseling was provided in the form of a weekly telephone call to answer questions and provide feedback. Daily physical activity and medications were also recorded on diet journals. Dietary analysis was performed using the GI software NUTRIPRO-GI, developed and maintained by TMS Wolever at the University of Toronto. The database is based on the 1991 Canadian Nutrient File, with updates from the 1997 Canadian Nutrient File.
Surgical Procedure
All participants underwent conventional coronary artery bypass graft surgery using cardiopulmonary bypass (CPB) and standard operating procedures. The surgeon as well as the anesthetist were blinded to the nature of the pre-operative treatment. General anesthesia, without propofol, was at the discretion of the anesthesiologist and consisted of a combination of midazolam, fentanyl, panuronium, midzolam and/or sufentanil citrate. The CPB circuit consisted of a hollow-fibre membrane oxygenator, heparin coated tubing, arterial line filter and a roller pump for perfusion. The circuit was primed with a combination of 1200 ml plasmalite (Baxter), 500ml pentaspan, 5000 U heparin and 25 milliequivalents of bicarbonate. Heparin was administered prior to initiating CPB (300–400U/kg body weight) to achieve an activated clotting time of at least 480 seconds. Cardiac arrest was initiated with cold blood cardioplegia (high potassium). Mild hypothermic perfusion (33–34°C) was maintained during the period of myocardial ischemia. Myocardial protection consisted of intermittent antegrade cold blood cardioplegia followed by a warm "hot shot" at the end of the procedure. Protamine was administered to reverse the anticoagulation. Non-glucose containing solutions were administered in the OR and CVICU for fluid therapy as well as for the measurement of cardiac index.
Blood Collection
Blood samples were collected by the study physician at baseline and preoperatively (samples 1–2) or by a research nurse post-surgically (sample 3) using one 10ml evacuated serum separating tube without anticoagulant. Samples were taken to the core laboratory immediately following collection and were allowed to clot at room temperature prior to centrifugation of 1500 x g at 4°C for 10 minutes. Serum was then aliquoted and used for in-house tests. Fasting insulin was analyzed using a standard radio-immunologic assay. C-peptide was determined at McMaster Medical Center, Hamilton, Ontario using a competitive immunologic assay (IMMULITE 2000, Diagnostic Products Corporation, Los Angeles, California).
Insulin Sensitivity
All patients underwent a short insulin tolerance test (SITT) at each study visit. Following the collection of baseline fasting blood samples, a small (0.05 U/kg body weight) intravenous bolus of human regular insulin (Humulin® R, Eli Lilly) was injected followed by the collection of serial blood samples at 3, 6, 9, 12, and 15 minutes post insulin injection from an arterialized vein for glucose determination. At 15 minutes post-insulin injection, a finger prick blood glucose reading was made and juice provided if the blood glucose levels had dropped below normal limits (<4 mmol/L). However, this was not required in any of our subjects. Insulin sensitivity was indicated by the first order rate constant for disappearance rate of glucose estimated from the slope of the regression line of the logarithm of blood glucose against time during the first 15 minutes. The KITT was calculated by multiplying the slope of the regression line by 100 [13]. A normal KITT is considered to be >2% per minute and abnormal or insulin resistant <1.5%/minute [14]. The Homeostasis Model Assessment (HOMA) score for insulin resistance and beta cell function was calculated using fasting insulin and glucose levels taken 5 minutes prior to the insulin injection. HOMA scores are based upon a mathematical model of the responses of fasting insulin and glucose values using standardized equations [15].
Markers of Inflammation
Blood samples for the measurement of inflammatory mediators were drawn at baseline, pre-operatively and within one hour post-surgically. Follow-up blood samples were drawn approximately 24 and 48 hours post-operatively, and at discharge. Free fatty acids (FFA) as well as mediators of inflammation (C-reactive protein (hs-CRP), interleukin-6 (IL-6), tumor necrosis factor (TNF-
), and serum amyloid A (SAA) were measured using commercially available kits. Levels of fructosamine were measured at Hamilton General Hospital, Hamilton, Ontario, using a colorimetric method. (Cobas Fara II analyzer, Roche Diagnostic, Mississauga, Ontario, Canada).
Statistical Analysis
Continuous variables are presented as the median (25th, 75th percentile) and were compared using the Mann Whitney U test between groups (HGI vs LGI) and the Wilcoxon Signed Rank Test for paired data. Categorical data are presented as counts and percentages and were compared using the Chi-square test (gender, medication use etc) or the Fisher Exact Test when the count in any cell was less than 5. Differences between dietary groups were also considered as change from baseline (x1-x0) and percent change from baseline ((x1-x0/x0)(100)) between any two time points for a given variable. Due to the small sample size it was not possible to correct the data for the baseline difference in age between the two groups. Relationships between continuous variables were determined using the Spearman's Rank correlation coefficient.
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RESULTS
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Subjects
98 patients were approached over a 10-month period. Of these, 72 patients were not eligible because surgery was imminent (n = 31), distance to the hospital was too far for repeat visits (n = 9), they had insufficient English literacy skills (n = 14), or other (patient undecided, patient doesn't keep appointments, participation in another study etc.)(n = 18). Thirteen patients declined to participate, and 13 patients were enrolled. One elderly participant died after baseline assessment and his data was subsequently excluded from the analysis. Additionally, one subject was excluded due to suspected non-compliance.
Baseline characteristics of study subjects were similar between treatment groups except for age which was significantly higher in the LGI group (Table 1). There were no significant differences in traditional risk classification scores for Canadian Cardiovascular Society (CCS) angina scores, functional ability (New York Heart Association Functional Class (NYHA)) or heart function (left ventricular grade 1–4). The medication profile was also similar between groups (Table 1).
Baseline SITT was not performed in one individual in whom difficulty in placing the cannula was experienced. Other baseline blood work was obtained and the patient continued in the study, completing all remaining tests. Follow-up blood work was missed on two occasions at the request of the participants.
Dietary Intervention
There were no significant differences between dietary groups for the number of dietary carbohydrate servings prescribed or consumed (Table 2). The reported compliance percentage was significantly better in the HGI group in comparison with the LGI group (118 (99, 125) % vs 88 (79, 100) %, p = 0.04). The average GI of study foods consumed differed significantly between groups: HGI (%) 101.6 (96.2, 105.3), LGI (%) 68.8 (67.2, 70.9)(p = 0.01). Energy intake, available carbohydrate, protein and fat did not differ significantly between groups at baseline or preoperatively. The GI of the diet, assessed by 3-day food records recorded at baseline and in the last week preoperatively, was not significantly different at baseline, but was significantly higher preoperatively in the HGI group (percentage: 91.2 (88.4, 96.6)) compared with the LGI group (percentage: 72.6 (70.2, 78.5))(p = 0.01) (Fig. 1).
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Fig. 1. The Glycemic Index of study participants before and after dietary intervention. The change in glycemic index of the dietary groups from baseline to preoperatively. Box boundaries depict the first and third interquartiles, horizontal line the median, and whisker bars 1.5 times the interquartile range.
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Insulin Sensitivity
Insulin sensitivity (KITT and HOMA) at baseline was similar between groups (Table 3). Following three weeks of dietary intervention, insulin sensitivity (KITT) was similar between groups and not significantly different from baseline. In contrast, the HOMA score was significantly increased after dietary intervention in patients following the HGI in comparison with those following the LGI (p = 0.02) (Table 3). Insulin sensitivity (KITT) declined significantly following CABG (baseline to post-op) in both treatment groups (HGI: p = 0.04; LGI: p = 0.04). However, measures of post-operative insulin sensitivity were not significantly different between dietary treatments. The calculated change from baseline for both preoperative and postoperative values were compared between groups, but these were also not significantly different. Similarly, relative insulin sensitivity (IS) (post-op IS/pre-op IS x 100) decreased by 74.6% in the HGI group and 67.6% in the LGI group which was significant within treatments but not between treatments (HGI: p = 0.04; LGI: p = 0.04) (Fig. 2).
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Fig. 2. The relative change in insulin sensitivity after various types of surgeries. The relative insulin sensitivity of patients undergoing various elective surgical procedures including HGI and LGI CABG groups. Patients undergoing CABG have a dramatic drop in relative insulin sensitivity of 67% in LGI and 75% in HGI. (Adapted from Thorell, 1999 [8].)
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Serum insulin and glucose levels were similar between treatment groups at baseline. Following a HGI diet for three weeks resulted in a significant rise in insulin levels in comparison with those following a LGI diet (p = 0.02) (Table 3). Furthermore, three weeks of a LGI diet resulted in a significant decrease in glucose (p = 0.04) which was not observed in the HGI. Post-operatively, the median insulin level of those on the HGI diet was double that of those following the LGI diet but the differences did not achieve statistical significance. Glucose levels also rose significantly following CABG in both treatment groups; however there were no differences between the LGI and HGI diet groups. There were no significant differences between groups for beta-cell function at any point during the study. C-peptide levels post-CABG were significantly higher in both the HGI and LGI diet groups when compared with pre-operative levels. No significant changes in C-peptide or fructosamine were observed between treatments (Table 3).
Analysis of Inflammatory Mediators
No significant differences between dietary treatments were noted for any of the measured inflammatory mediators with the exception of IL-6 (Fig. 3). Il-6 was found to be significantly higher in the LGI compared with the HGI immediately following cardiac surgery (p = 0.05). Percent change from baseline was calculated and showed a trend for higher IL-6 levels in the LGI over the HGI (p = 0.07). Spearman's correlation analysis suggests patterns of release of inflammatory markers are significantly related (SAA and CRP: rs = 0.44, P = 0.01; TNF- and IL-6: rs = 0.63, P < 0.01).
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Fig. 3. Inflammatory mediators over study collection intervals. Figures show means and SD at each interval for each dietary group. HGI (solid line/diamonds), LGI (dashed line/squares). Baseline (1), Preoperative (2), Postoperative (3), Recovery Day 1 (4), Recovery Day 2 (5), Day of Discharge (6). **Change from baseline to postoperative IL-6 levels is significantly different between groups (Mann-Whitney U Test, P = 0.05, n = 11).
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Analysis of Other Clinical Outcomes
There were no significant differences between groups for blood glucose levels measured during the operation, 12 hours after the operation in the CVICU, or throughout the postoperative period (Table 4). Also no differences between groups were noted for the number of vessels bypassed, length of time on mechanical ventilation or the length of CVICU stay. The LGI group spent a significantly longer time on cardiopulmonary bypass (pump time) which was accompanied by a significantly longer aortic cross-clamp time (p = 0.03 and p = 0.05) in comparison with the HGI group. Rates of post-operative complications were similar between LGI and HGI groups (Table 5).
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DISCUSSION
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All of the participants in this study showed evidence of insulin resistance at baseline using the SITT. Following a LGI diet for three weeks pre-operatively did improve insulin sensitivity using the HOMA as well as significantly reducing blood glucose levels. Coronary artery bypass graft surgery resulted in a dramatic reduction in insulin sensitivity in all participants. The magnitude of the drop in insulin sensitivity most likely reflects the degree of surgical trauma as has been suggested by others [8,16]. While not statistically significant, the relative decline in insulin resistance was smaller in the LGI in comparison with the HGI suggesting some benefit of this intervention warranting further investigation. The lack of relationship observed between the KITT and HOMA suggests that these two measures reflect differing physiological constructs. HOMA scores are based on the relationship between fasting glucose and insulin and therefore primarily reflect hepatic efficiency and beta cell functionality. The KITT on the other hand, is primarily a measure of peripheral insulin sensitivity. Since the dietary treatment was found to significantly affect HOMA and not the KITT this suggests that the effect of diet may be predominantly on hepatic insulin sensitivity rather than at peripheral muscle or alternatively, that the KITT was not sensitive enough to detect changes in our population.
The substitution of a high or low glycemic index foods into the habitual diet of patients was well tolerated and compliance was excellent. The diets were well matched with similar macronutrient profiles. The incorporation of LGI foods resulted in drop in GI of 13% with a mean difference of 18.6 GI units between treatments which exceeded that of other dietary strategies shown to successfully improve insulin sensitivity [7,17]. Body weight and levels of physical activity remained constant throughout the study.
Consuming the LGI diet resulted in a significant increase in dietary fibre. Increasing dietary fibre should have resulted in an insulin-sensitizing effect through the modulation of short chain fatty acid production possibly reducing hepatic gluconeogenesis and lipogenesis [18]. However, we observed a significant and unexpected rise in levels of circulating free fatty acids (FFA) in the LGI group after three weeks of dietary treatment. We anticipated that following a LGI diet overtime would reduce insulinemia, improve insulin sensitivity and would avoid post-prandial hypoglycemia and high rebound free fatty acids. However, Patel et al. [19] did not observe changes in FFA levels in a study of non-diabetic CABG patients following a LGI diet for four weeks despite showing improvements in insulin sensitivity. Therefore it has been suggested that changes in circulating fatty acids may not be readily apparent in the fasting state but may require a post-prandial state in order to observe any differences. Furthermore, a study by Kiens et al. [20] reported that circulating levels of FFA rose in healthy individuals following a low glycemic index diet until the third week of diet treatment and was the explanation for the reduction in IS found in the LGI group. Therefore, the higher circulating levels of FFA in the LGI diet group may have influenced our findings.
A limitation of the study was that the LGI group was found to be significantly older than the HGI group. Since insulin sensitivity has been suggested in some studies to decline with advancing age this may have limited the response to the dietary intervention in this group [20–22]. Arguing against the effect of age is a study by Thorell [8] who reported that it was the degree of surgical trauma that had the largest impact on post-operative insulin resistance and that neither age nor body mass index significantly influenced the relative reduction in IS associated with surgery. The lack of any significant correlation between age and insulin sensitivity at baseline supports that age was most likely not responsible for differences in insulin sensitivity observed between groups. The most likely effect of age was related to surgical outcomes. Advanced age has been linked with an increased incidence of post-operative complications and is routinely used to stratify surgical patients [23]. In addition to being older, the LGI diet group appeared to have a larger disease burden with more vessels being bypassed (median 4 vs 3)and a longer time on cardiopulmonary bypass in comparison with the HGI group. This increased disease burden together with more advanced age is more likely the explanation for the observed tendency in this group to use more blood products. Both the duration and surgical technique have been shown to impact the degree of insulin resistance and thus it is possible that these differences negated any significant preservation of IS post-op. The longer cardiopulmonary bypass time would also reflect a larger ischemic time which has also been associated with the increased release of IL-6 as observed in our study in the LGI. [24]. Other changes in inflammatory mediators are consistent with the inflammatory cascade post CABG [25].
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CONCLUSION
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A short-term glycemic index derived diet was successfully adopted by most participants and resulted in a significant difference in dietary glycemic index between groups. Adoption of the LGI diet resulted in increased IS as measured by HOMA, as well as improved glycemic control as seen by reduced glucose and insulin levels in the pre-operative period. Cardiac surgery resulted in a dramatic drop in relative insulin sensitivity that was not shown to be different between LGI and HGI groups. Despite being older with suspected increased disease burden, the decline in relative insulin sensitivity in the LGI group was smaller in comparison with the HGI suggesting that this dietary intervention was successful. Further investigation of the impact of adopting a LGI diet in surgical patients and patients with IR is warranted.
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ACKNOWLEDGMENTS
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Thank you for the assistance of our research nurse, Rose Mokbel, who was critical in the collection of the post-operative blood samples.
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FOOTNOTES
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Supported by a research grant from the Canadian Foundation for Dietetic Research.
V. Tully was supported by a CIHR training grant.
Received March 30, 2006.
Accepted January 25, 2007.
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ABSTRACT
INTRODUCTION
