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. 2019 Jun;60(6):637–643.

Comparison of the glucose and insulin responses of horses to 2 formulations of corn syrup

Kira Moser 1, Heidi Banse 1,✉
PMCID: PMC6515809  PMID: 31156265

Abstract

The objectives of this study were to compare the insulin and glucose responses of horses to 2 formulations of corn syrup, [Karo Light (Karo) available in the United States, and Crown Lily White (Crown), available in Canada]. Horses were evaluated under both fed (n = 14) and fasted (n = 10) conditions. Using a randomized crossover design, each horse underwent an oral sugar test using Karo or Crown syrup. There were no significant differences in insulin or glucose time of maximum concentration (Tmax), maximum concentration (Cmax), or area under the curve (AUC) or in insulin or glucose concentrations at individual timepoints during fed or fasted conditions. Bland-Altman analysis of insulin at 75 minutes indicated a mean bias of 28.7 pmol/L, with 95% limits of agreement from −83.9 to 140.6 pmol/L (fed) and a mean bias of 11.5 pmol/L, with 95% limits of agreement from −78.9 to 101.9 pmol/L (fasted). These findings suggest that Karo and Crown syrup produce similar glucose and insulin responses in horses.

Introduction

Insulin dysregulation in horses is characterized by hyperinsulinemia, excessive response to oral carbohydrates, and/or tissue insulin resistance (1,2), and is broadly associated with an increased risk for laminitis (3–5). A diagnostic test for insulin dysregulation is a valuable tool to identify horses at risk for endocrinopathic laminitis, in order to allow for implementation of management strategies to reduce risk. Multiple tests have been developed for the diagnosis of insulin resistance in horses, including the frequently sampled intravenous glucose tolerance test (FSIGTT), the euglycemic hyperinsulinemic clamp (EHC), the combined glucose-insulin tolerance test (CGIT), and the insulin tolerance test (6–9). However, many of these tests are expensive and/or impractical outside of a hospital or research setting. Furthermore, by design, these tests do not include assessment of the intestinal tract in insulin regulation, and a growing body of literature supports the role of incretin hormones and intestinal nutrient absorption in development of insulin dysregulation (10–12). An oral sugar test (OST) is a more recently developed, practical field test for diagnosis of insulin dysregulation in horses (13) that includes evaluation of the entero-insular axis. Therefore, the OST may be useful in the early identification of horses with an excessive response to oral sugar, which may more closely reflect the clinical situation of pasture-associated laminitis than tissue insulin resistance alone (10,14).

The OST was developed using Karo Light (Karo) (ACH Food companies, Memphis, Tennessee, USA) corn syrup and most data on the OST in horses have used this corn syrup formulation (13,15–18). However, Karo syrup is not commercially available in Canada (or other countries), and it is unclear whether any available corn syrups have an equivalent carbohydrate composition. Differences in carbohydrate composition between the 2 formulations could impact insulin responses and thus interpretation of the OST. Therefore, a comparison of the OST using the standard Karo corn syrup versus an available Canadian formulation is warranted, to determine whether each formulation results in a similar insulin response in horses.

The purpose of this study was to compare the insulin and glucose responses of horses to 2 formulations of corn syrup, Karo Light and Crown Lily White (ACH Food companies, Memphis, Tennessee, USA), a formulation available in Canada. Since fasting is not always feasible during field testing, horses were tested under both fed and fasted conditions.

Materials and methods

Experiment I

This study was approved by the University of Calgary’s Veterinary Sciences Animal Care Committee (AC 17-0081). Fourteen seemingly healthy adult horses were included. Nine horses were sourced from a veterinary school teaching herd and 5 were recruited from clients of the University of Calgary’s Distributed Veterinary Teaching Hospital after informed client consent was obtained. Two obese horses had a history of laminitis. Signalment and morphometric data are presented in Table 1. Owners were instructed to maintain horses on a consistent diet for the duration of the study. Horses were either tied or kept in a gravel paddock for the duration of each OST. Horses were not fasted, but feed was removed for the duration of the OST. Data collection was performed in May.

Table 1.

Signalment and morphometric data of horses. Normally distributed data are presented as mean ± standard deviation (SD); categorical data and data that were not normally distributed are presented as medians [interquartile range (IQR)].

Parameter Experiment I (fed) (n = 14) Experiment II (fasted) (n =10)
Breed TB (n = 6) TB (n = 6)
QH (n = 6) QH (n = 3)
WB (n = 1) SB (n = 1)
Paint/Appaloosa (n = 1)
Gender 8 M 8 M
6 G 2 G
Age (mean ± SD) 18 ± 7 y 18 ± 3 y
Weight (mean ± SD) 525 ± 66 kg 500 ± 48 kg
Girth:height (mean ± SD) 1.2 ± 0.06 1.2 ± 0.04
Neck:height (mean ± SD) 0.6 ± 0.05 0.6 ± 0.04
Neck circumference (0.50) (mean ± SD) 95.8 ± 6.6 cm 92.8 ± 6.3 cm
Neck height (mean ± SD) 11.1 ± 1.9 cm 11.4 ± 1.7 cm
Body condition score (median, IQR) 5.3 (range: 4 to 7) 5 (range: 4 to 5.5)
Cresty neck score (median, IQR) 2 (range: 1 to 2.25) 1 (range: 1 to 2)
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TB — Thoroughbred; QH — Quarter horse; WB — Warmblood; SB — Standardbred; SD — Standard deviation; IQR — Interquartile range; M — Male; G — Gelding.

Experiment II

Ten horses were included, all sourced from a veterinary school teaching herd. Signalment and morphometric data are presented in Table 1. No horses had a history of laminitis. Horses were kept on pasture for 1 mo before the study and during the washout period. All horses were fasted overnight before the OST. Horses were brought into gravel paddocks and fed 3 flakes of compressed timothy hay at 4 pm the night before each OST. Data collection was performed in July.

Study design

An oral sugar test (OST) was performed on each horse randomly assigned to receive 0.15 mL/kg body weight (BW) of either Karo Light corn syrup (ACH Food Companies) or Crown Lily White corn syrup (ACH Food Companies) syringed by mouth. After a 1-week washout period, the OST was repeated and the other corn syrup formulation was administered. Horses were weighed on the morning of each OST using either an electronic scale (Ezi-Weigh; Mettler-Toledo, Columbus, Ohio, USA) or a mobile equine scale (Tokyo, Horse Weigh; Llandrindod Wells, Powys, UK). A 14-gauge catheter (Angiocath; BD Medical, Sandy, Utah, USA) was placed aseptically into the jugular vein of each horse at least 1 h before obtaining the baseline blood sample. Blood was collected from the jugular catheter at baseline, and at 30, 60, 75, 90, and 120 min post-syrup administration into blood tubes with no anti-coagulant for glucose and insulin analyses. Blood glucose was measured within 2 min of collection using a previously validated handheld glucometer (19) (AlphaTrak; Zoetis, Parsippany, New Jersey, USA). Due to high ambient environmental temperatures (up to 30°C), samples were kept on ice until centrifugation within 2.5 h of collection. Whole blood was allowed to warm to room temperature (~30 min) before centrifuging at 1500 × g for 15 min, serum was stored at −80°C until analysis. Serum was analyzed for insulin concentration via radioimmunoassay (Millipore; Temecula, California, USA) at the Animal Health Laboratory, Guelph, Ontario. All samples were analyzed within 2 mo of collection.

Statistical analysis

Data were analyzed for normality using a Kolmogorov-Smirnov test. Coefficient of variation was calculated for insulin concentrations. As coefficient of variation was not normally distributed for insulin concentrations in the sampled population, median and interquartile range are reported. Insulin concentrations were log-transformed to achieve normality for assessment of changes over time. Glucose and insulin concentrations over time were compared between formulations using a 2-way analysis of variance (ANOVA) with repeated measures. A Bonferroni post hoc test was carried out to identify any differences between formulations at individual timepoints. A paired t-test was used to compare variables that were normally distributed [glucose area under the curve (AUC), maximum concentration of glucose (Cmax)] and a Wilcoxon signed-rank test was used to compare variables that were not normally distributed [insulin AUC, time of maximum concentration (Tmax) for glucose and insulin, and insulin Cmax]. Differences between insulin concentrations at T60 and T75 were normally distributed, so Bland-Altman analysis was used to determine agreement between formulations in insulin concentrations at 60 and 75 min.

Results

Insulin immunoassay

The samples were measured using 4 kits. The high and low controls were from the same lot number across the study and were measured in duplicate. Mean concentration of the high control was 356 pmol/L (inter-assay CV, 5.9%; intra-assay CV, 4.7% ± 2.8%) and mean concentration of the low control was 122 pmol/L (inter-assay CV 9.3%; intra-assay CV of 5.8% ± 9.1%). Sample intra-assay CV was not normally distributed. Median intra-assay CV of all samples was 4.9% (interquartile range: 2.45% to 8.7%).

Experiment I

One horse had a missing insulin T30 timepoint in 1 OST, so was excluded from insulin AUC, Cmax, and Tmax analyses. Five of 14 horses had changes in management (access to pasture) within 24 to 48 h before the second oral sugar test. Based upon currently recommended insulin cutoff values for insulin dysregulation (20), 1 horse in Experiment I was considered insulin dysregulated with both formulations of corn syrup. All other horses were considered insulin regulated using both formulations of corn syrup. Individual insulin responses over time following oral sugar administration are presented in Figure 1. When evaluating insulin concentrations, there was an effect of time (P < 0.0001) but not treatment (i.e., formulation; P = 0.46), and there was no time by treatment interaction (P = 0.42). Furthermore, there were no differences between formulations in insulin concentrations at individual timepoints (P > 0.99; Figure 2). There was an effect of time (P < 0.001) but not formulation (P = 0.83) on glucose concentrations, and there was no time by treatment interaction (P = 0.96). Furthermore, there were no differences between formulations in insulin concentrations at individual timepoints (P > 0.99). There were also no differences between formulations in insulin or glucose AUC, Tmax, or Cmax (Table 2). When evaluating insulin concentrations at 60 min, Bland-Altman analysis indicated a mean bias of −30 pmol/L, with 95% limits of agreement from −95.7 to 35.7 pmol/L. When evaluating insulin concentrations at 75 min, Bland-Altman analysis indicated a mean bias of 28.7 pmol/L, with 95% limits of agreement from −83.9 to 140.6 pmol/L (Figure 3).

Figure 1.

Figure 1

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Insulin curves for individual (n = 14) horses undergoing an OST with a) Crown and b) Karo syrup in Experiment I (fed).

Figure 2.

Figure 2

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Mean (log-transformed) insulin concentrations over time in Experiment I (fed) with Karo (gray circles, filled line) and Crown (black squares, dashed line) syrup. Error bars = standard deviation. There was a significant effect of time (P < 0.0001) but not treatment (i.e., formulation; P = 0.46) on insulin concentrations and no significant time by treatment interaction (P = 0.42). Furthermore, there were no significant differences between formulations at any timepoint (P > 0.99).

Table 2.

Area under the curve (AUC), Cmax, and Tmax of insulin and glucose responses to corn syrup administration in experiments I (fed) and II (fasted).

Parameter Experiment I (fed) (n = 14) Experiment II (fasted) (n = 10)
Karo insulin AUC (pmol/L/min) 15 908 (10 965 to 24 840) 14 442 (10 112 to 17 753)
Crown insulin AUC (pmol/L/min) 15 360 (9563 to 21 432) 14 194 (13 001 to 17 396)
(median, IQR) P = 0.19 P = 0.28
Karo insulin Cmax (pmol/L) 173 (125.5 to 253.5) 154 (137.5 to 211.5)
Crown insulin Cmax (pmol/L) 172 (115.5 to 234.5) 157 (122.8 to 191.5)
(median, IQR) P = 0.35 P = 0.32
Karo insulin Tmax (min) 60 (30 to 60) 60 (52.5 to 97.5)
Crown insulin Tmax (min) 60 (30 to 67.5) 60 (30 to 63.75)
(median, IQR) P > 0.99 P = 0.38
Karo glucose AUC (mmol/L) 800.5 +/− 133.8 777.9 +/− 91.2
Crown glucose AUC (mmol/L) 805.7 +/− 115.8 804.9 +/− 34.83
(mean ± SD) P = 0.89 P = 0.26
Karo glucose Cmax (mmol/L) 7.6 +/− 1.5 7.2 +/− 0.9
Crown glucose Cmax (mmol/L) 7.7 +/− 1.1 7.6 +/− 0.4
(mean ± SD) P = 0.78 P = 0.20
Karo glucose Tmax (min) 60 (30 to 67.5) 60 (60 to 86.25)
Crown glucose Tmax (min) 60 (45 to 67.5) 60 (30 to 60)
(median, IQR) P = 0.70 P = 0.22
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Tmax — time of maximum concentration; Cmax — maximum concentration.

SD — standard deviation; IQR — interquartile range.

Figure 3.

Figure 3

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Bland-Altman plot of the average and the difference between insulin concentrations at 75 min using Crown and Karo corn syrups in Experiment I (fed). Filled line — bias; dashed lines — 95% limits of agreement.

As it is possible that acute dietary change may have contributed to variation among horses in Experiment I, thus increasing the likelihood of a type II error, data were also evaluated with the 5 horses with diet changes excluded. When removing the variability that may be attributable to acute dietary change, there was an effect of time (P < 0.0001) but not treatment (i.e., formulation; P = 0.49) on insulin concentrations, and there was no time by treatment interaction (P = 0.91). There were no differences in insulin concentrations between formulations at any timepoint (P > 0.99). When evaluating glucose concentrations, there was an effect of time (P < 0.0001) but not treatment (P = 0.73) and no time by treatment interaction (P > 0.99) or differences between formulations at any timepoint (P > 0.99). There were no differences in insulin or glucose Tmax, Cmax, or AUC (P > 0.25).

Experiment II

Based upon currently recommended insulin cutoff values for insulin dysregulation (20), 1 horse was considered insulin dysregulated using both formulations of corn syrup. All other horses were considered insulin regulated using both formulations of corn syrup. Individual insulin responses over time following oral sugar administration are presented in Figure 4. There was an effect of time (P < 0.0001) but not treatment (P = 0.78) and no time by treatment interaction (P = 0.08) on insulin concentrations (Figure 5). Furthermore, there were no differences in insulin concentrations between formulations at any timepoint (P > 0.99). There was an effect of time (P < 0.0001) but not treatment (P = 0.51) and no time by treatment interaction (P = 0.09) on glucose concentrations or differences in formulations on glucose concentrations at individual timepoints (P > 0.4), or on insulin or glucose AUC, Tmax, or Cmax (P > 0.26). For insulin concentrations at 60 min, Bland-Altman analysis indicated a mean bias of 39.2, with 95% limits of agreement from −103.7 to 182.1 pmol/L. For insulin concentrations at 75 min, Bland-Altman analysis indicated a mean bias of 11.5 pmol/L, with 95% limits of agreement from −78.9 to 101.9 pmol/L (Figure 6).

Figure 4.

Figure 4

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Insulin curves for individual (n = 10) horses undergoing an OST with a) Crown and b) Karo syrup in Experiment II (fasted).

Figure 5.

Figure 5

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Mean (log-transformed) insulin concentrations over time in Experiment II (fasted) with Karo (gray circles, filled line) and Crown (black squares, dashed line) syrup. Error bars = standard deviation. There was a significant effect of time (P < 0.0001) but not treatment (P = 0.78) and no significant time by treatment interaction (P = 0.08). Furthermore, there were no significant differences between formulations at any timepoint (P > 0.99).

Figure 6.

Figure 6

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Bland-Altman plot of the average and difference between insulin concentrations at 75 min using Crown and Karo corn syrups in Experiment II (fasted). Filled line — bias; dashed lines — 95% limits of agreement.

Discussion

The OST using Karo syrup provides a practical and cost-effective method of assessing insulin regulation in horses in the United States. However, the limited global availability of Karo corn syrup makes the test in its current form impractical in other countries. In this study, we compared the insulin and glucose responses of horses in an OST using Karo Light (ACH Food Companies) corn syrup and a Canadian formulation of corn syrup, Crown Lily White (ACH Food Companies) corn syrup. As this test is often performed in the field, and housing may preclude complete fasting, horses were evaluated following administration of corn syrup in both a fed and a fasted state. The results of this study suggest that Crown and Karo syrups produce similar glucose and insulin responses in horses when used in an OST, whether horses are in a fed or fasted state.

The OST using Karo syrup has good repeatability when using binary interpretation (i.e., insulin dysregulated or not insulin dysregulated) (16,17). However, based upon the Equine Endocrinology Group cut-off guidelines (20), only 2 horses in the present study were diagnosed as insulin dysregulated, including 1 horse that had an insulin outside cut-off guidelines at T30. Since there was only 1 insulin dysregulated horse in each experiment, evaluating repeatability of the OST using a binary interpretation (insulin dysregulated or not) was of limited value, so agreement between the 2 formulations was evaluated based upon a single timepoint (either 60 or 75 min). In addition, differences in insulin concentrations at each individual timepoint were assessed. The 95% limits of agreement in insulin concentrations between formulations at T60 or T75 in both fed and fasted horses were similar to those found by Frank and Walsh (17) in horses when repeatability was assessed using the same syrup formulation (Karo Light). Furthermore, there were no significant differences between formulations in insulin concentrations at any timepoint, whether horses were fed or fasted. Taken together, these findings suggest that the differences observed between Karo and Crown corn syrup formulations are similar to the differences observed in repeatability studies using Karo Light corn syrup in horses.

In this study, a wide range in insulin Tmax between horses was observed with both formulations, from 30 min to 120 min. This variability presents a challenge in interpreting the OST with a single blood sample. This is in agreement with other studies which have found a difference in insulin Tmax between ponies and horses, and between horses of different body conditions (21–23). Knowles et al (16) found that test agreement improved when 2 samples were taken 30 min apart, rather than at a single timepoint. Thus, perhaps 2 blood samples would improve the sensitivity of the test and increase the probability of obtaining a sample at the Cmax (24). Insulin AUC has been demonstrated to be more repeatable than a single timepoint (15,16). However, this measured outcome would increase the cost and time involved to perform the test, making it a less practical field option. Additionally, it is unclear which measured outcome (insulin AUC, Cmax, or another) is most associated with the risk of developing laminitis. In 1 study, both AUC and insulin at 60 min differentiated between previously laminitic and non-laminitic ponies (15).

Experiment I of the study included 2 horses with BCS of 8/9 and a history of laminitis, thus were highly suspected of being insulin dysregulated. However, they were not diagnosed as insulin dysregulated using either formulation of syrup based on cut-offs recommended by the Equine Endocrinology Group (20). The lack of fasting before the OST in these horses may have altered their insulin response to the OST. The OST was developed under fasted conditions (13), and feeding may decrease the degree of insulin response observed following oral sugar administration (15,25). Furthermore, corn syrup dose or insulin cut-off values may not have been appropriate for diagnosis of insulin dysregulation in those horses. Initially, an insulin concentration > 430 pmol/L using a Coat-A-Count radioimmunoassay (RIA) was proposed as diagnostic for insulin dysregulation at 60 to 90 min post-OST (26). However, initial evaluation of the OST was performed comparing lean, healthy horses to horses with severe insulin dysregulation (most had fasting hyperinsulinemia), suggesting that those horses may have had more severe disease (13). More recently, the Equine Endocrinology Group has proposed an insulin concentration of > 323 pmol/L to be consistent with insulin dysregulation (20). A recent study in a small cohort of ponies suggested that a higher dose of Karo syrup (0.45 mL/kg BW) was better at predicting laminitis than a 0.15 or 0.3 mL/kg BW dose (15), and a cut-off value of 790 pmol/L at 60 min could differentiate previously laminitic from non-laminitic ponies. Although these studies did not all use the same method for insulin measurement, which may influence absolute cut-off values, when taken together, these findings suggest that a lower insulin cut-off value at the 0.15 mL/kg BW dose, or a higher dose of corn syrup, may improve sensitivity of the test for diagnosis of insulin dysregulation. Further investigation of insulin response to the oral sugar test in a larger population of horses with and without laminitis may allow for establishment of appropriate cut-off values.

Label claims suggest that the sugar content of Karo and Crown corn syrups may differ. Karo syrup contains 5 g of sugar per 15 mL, whereas Crown contains 6 g per 15 mL. High performance liquid chromatography has demonstrated that the Karo syrup has 356.3 mg/mL of digestible (i.e., dextrose and maltose) sugars (15). The composition of digestible sugars in Crown syrup is not known, and there may be other sugars present in corn syrup, including inulin and fructose, that lead to differences in insulin response (21,27). However, the expense of high-performance liquid chromatography precluded analysis by this method herein. Furthermore, since horses appeared to have similar insulin and glucose responses to both corn syrup formulations, differences in sugar content may not have been substantial enough to influence results.

Many factors affect insulin response to oral glucose in horses, including diet, age, and breed (28–31). Limitations for the present study include a heterogeneous population of horses (i.e., different breeds, ages, and body conditions) and lack of a controlled diet. Despite directions to barn managers and owners to maintain the same management for horses throughout the study period, in Experiment I, 5 out of 14 horses were inadvertently turned out to pasture during the washout period for 24 to 48 h, which resulted in an acute diet change from hay to pasture. This may have induced variation in the insulin responses of these horses when the repeat OST was performed. Changes in carbohydrate content of the diet can affect expression of glucose transporters, and it has been shown that horses on high carbohydrate diets become less insulin sensitive (29,32,33). Since pasture generally has a higher non-structural carbohydrate (NSC) content than hay, ingestion of pasture may have affected insulin responses. However, no significant differences were apparent between formulations, either with or without these horses included in analysis. In Experiment II, horses were maintained on the same pasture for the duration of the washout period; however, NSC content of pasture can vary with temperature, moisture, as well as diurnally, and this variation has been shown to affect OST results (18,27,34). Thus, variation in NSC content of the pasture over the 6-day washout period may have affected insulin responses in our horses and resulted in some of the individual variation observed in response to the 2 corn syrup formulations. Duration of fasting may also have varied between horses, since they were fed at 4 pm and not monitored for consumption of their feed. However, differences among insulin responses to the OST were not observed in horses when fasting duration was 3, 6, or 12 h (25); thus, a difference in fasting duration was unlikely to have had a substantial influence on our results.

The preliminary work presented here suggests similar insulin and glucose responses are observed in horses whether using Karo or Crown syrup. Furthermore, the variability seen between formulations is similar to the variability seen in repeatability studies using the same formulation of corn syrup. These findings support the use of similar reference ranges for Crown syrup. However, due to the low number of horses diagnosed with insulin dysregulation in this study, no conclusions can be made on agreement between formulations for diagnosing insulin dysregulated horses. Further investigation into agreement between formulations in insulin dysregulated horses is warranted.

Acknowledgment

This study was funded by Boehringer-Ingelheim Animal Health. CVJ

Footnotes

Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.

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