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Article

Physical Activity, Dietary Patterns, and Glycemic Management in Active Individuals with Type 1 Diabetes: An Online Survey

by
Sheri R. Colberg
1,*,
Jihan Kannane
2 and
Norou Diawara
2
1
Department of Human Movement Sciences, Old Dominion University, Norfolk, VA 23508, USA
2
Department of Mathematics & Statistics, Old Dominion University, Norfolk, VA 23529, USA
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2021, 18(17), 9332; https://doi.org/10.3390/ijerph18179332
Submission received: 11 June 2021 / Revised: 18 August 2021 / Accepted: 31 August 2021 / Published: 3 September 2021
(This article belongs to the Special Issue Diabetes in Sports and Exercise Medicine)
Browse Figures
Review Reports Versions Notes

Abstract

:
Individuals with type 1 diabetes (T1D) are able to balance their blood glucose levels while engaging in a wide variety of physical activities and sports. However, insulin use forces them to contend with many daily training and performance challenges involved with fine-tuning medication dosing, physical activity levels, and dietary patterns to optimize their participation and performance. The aim of this study was to ascertain which variables related to the diabetes management of physically active individuals with T1D have the greatest impact on overall blood glucose levels (reported as A1C) in a real-world setting. A total of 220 individuals with T1D completed an online survey to self-report information about their glycemic management, physical activity patterns, carbohydrate and dietary intake, use of diabetes technologies, and other variables that impact diabetes management and health. In analyzing many variables affecting glycemic management, the primary significant finding was that A1C values in lower, recommended ranges (<7%) were significantly predicted by a very-low carbohydrate intake dietary pattern, whereas the use of continuous glucose monitoring (CGM) devices had the greatest predictive ability when A1C was above recommended (≥7%). Various aspects of physical activity participation (including type, weekly time, frequency, and intensity) were not significantly associated with A1C for participants in this survey. In conclusion, when individuals with T1D are already physically active, dietary changes and more frequent monitoring of glucose may be most capable of further enhancing glycemic management.

1. Introduction

In 2021, a full century has passed since the 1921 discovery of insulin [1], a hormone that must be replaced in individuals with type 1 diabetes (T1D), all of whom have lost the ability to produce it as the result of primarily autoimmune destruction of the pancreatic β-cells [2]. Since its discovery, replacement insulin has evolved greatly with numerous types and delivery methods now possible, along with use of better glycemic management and tracking tools that can assist individuals in preventing acute and chronic diabetes-related health complications. In fact, most people with T1D can expect to experience near normal longevity with a high quality of life, particularly if glycemic management and cardiovascular health are maintained [3].
When undertaken by individuals of all ages with T1D, physical activity is associated with many well-established health benefits, including improved cardiovascular fitness, lower cardiovascular risk, better quality overall health, and enhanced psychological well-being [4,5]. One of the major factors linked with their long-term survival is the absence of features of the metabolic syndrome and, more specifically, the presence of insulin sensitivity [6]. Physical activity of all types has been associated with greater insulin sensitivity [7,8,9]. In adults with T1D, being regularly active improves cardiometabolic risk profile [10] and is associated with increased longevity [6,11]. Individuals with T1D of all ages are capable of engaging in a wide variety of physical activities and sports, ranging from recreational to Olympic-level (12), and many choose to be physically active to achieve unique goals related to athletics and/or health. However, these individuals must contend with the continuous challenges associated with being physically active with T1D, including monitoring glucose levels, managing dietary choices and intake, adjusting insulin doses, and adapting daily regimens to account for other factors that impact glycemia [12,13,14,15]. Physical activity acutely can lead to hypoglycemia and hyperglycemia [15,16,17,18,19,20], either of which may become a medical emergency if not adequately managed.
Numerous physical activity training patterns and regimens are possible with T1D, and each individual must choose to follow the one that works uniquely best, although that may vary with the type, intensity, frequency, and timing of activities, among other variables [18,19,21,22]. High-intensity training as well as competition can substantially increase glucose output from the liver, potentially leading to hyperglycemia both before and during activity [19]. Resistance exercise is associated with less of a decline in blood glucose than aerobic [18,23] and can provide a protective effect against glycemic declines if performed prior to aerobic exercise [24]. Even the timing of exercise can impact outcomes, with exercise before breakfast resulting in less hypoglycemia than the same bout of aerobic or resistance activity undertaken later in the day [18,23,25]. An appropriate dose of rapid-acting insulin can be used to treat hyperglycemia after morning exercise of any type without inducing hypoglycemia post-exercise [26]. In addition, exercise glycemic management strategies often vary within sporting events [27,28] and afterward [20,28].
In addition, nutrition and dietary patterns are one of the more controversial topics related to athletic performance in all individuals, as well as to glycemic management in T1D and overall health [12,13,29,30,31]. Whether individuals are participating in sports and activities recreationally or aiming for competitive levels of athletic achievement, their performance can be positively or negatively impacted by a number of nutritional factors, such as intake and timing of macronutrients, availability of micronutrients, hydration status and electrolyte balance, and exercise training practices [12,13,14]. In particular, carbohydrate consumption to fuel the exercise bout and/or for hypoglycemia prevention is an important cornerstone to maintain performance and avoid hypoglycemia [31,32].
Use of some of the insulin delivery systems, glucose monitoring devices, algorithms, other glucose-focused technology and tools may also improve how well activity can be managed [26,33,34,35]. Recent technological advances, such as insulin pumps and continuous glucose monitoring (CGM) devices, have greatly advanced the ability of individuals to manage glucose levels around physical activity by allowing for almost real-time changes in insulin delivery and feedback on glycemic responses [36,37]. When using continuous subcutaneous insulin infusion (i.e., an insulin pump), active individuals can reduce or suspend basal insulin infusion at the start of exercise [38], or even starting 30–60 min before exercise [39], in order to mitigate declines in blood glucose. Likewise, CGM devices have been shown to improve glycemic management [40,41,42], even in individuals with T1D with lower A1C (a measure of overall blood glucose over the last 2–3 months) values already [43]. However, CGM measure glucose in interstitial spaces, and a time lag exists between blood glucose (measured via finger stick) and CGM glucose levels (measured via CGM) [36,44,45], making it unclear whether use of such devices can benefit glycemic management with physical activity. Finally, integrated insulin pump and CGM systems have shown promise with regard to ameliorating glycemic management in individuals with T1D [35,46,47,48], but their successful use around exercise remains more limited [49,50,51,52,53,54].
Thus, the purpose of this study was to ascertain which variables related to the diabetes management of physically active individuals with T1D have the greatest impact on overall blood glucose levels (via A1C) in a cohort of active adults and adolescents with T1D in a real-world setting. Given the complexity of managing blood glucose levels when exogenous insulin must be precisely balanced with food intake for any physical activity, we hypothesized that both physical activity (total weekly time, frequency, intensity, and/or type) and dietary patterns (particularly carbohydrate intake) would potentially impact overall blood glucose management in these active individuals, along with the use of the latest diabetes technologies (e.g., insulin pumps and CGM devices).

2. Materials and Methods

2.1. Subject Recruitment

An online survey conducted in English was advertised in 2018 by investigators on diabetes-focused social media platforms and distributed to various professional contacts via email. Participation was completely voluntary with no incentives offered, and the survey was open to all physically active individuals with diabetes of any age during a month-long period. The survey itself was completed through a separate online platform and contained no questions that could be used to identify personal data or characteristics by the investigators. Data collection methods were considered exempt from requiring participant consent by our university due to the online anonymous and voluntary nature in which all survey responses were obtained and recorded.
A total of 220 participants (109 male, 111 female, age range of 13 to 84 years) who had been diagnosed with T1D for varying lengths of time were included in the study. Their distributions by age and years with T1D are shown in Figure 1.

2.2. Online Survey and Data Collection

The online survey included a broad array of questions that participants could choose to complete with none being mandatory. Self-reported data about each participant included the following variables: age, sex, diabetes type, latest A1C value, usual insulin regimen (including insulin pumps), use of other medications, glucose self-monitoring practices (i.e., frequency and use of CGM devices), typical dietary patterns and estimated carbohydrate intake, physical activity patterns, target blood glucose ranges for exercise, regimen changes for physical activity, and typical treatments for exercise-related hypoglycemia or hyperglycemia. Any A1C values that were reported in mmol/mol (all coming from respondents outside the United States) were converted to equivalent % values before analysis, and only self-reported insulin users were included in the analyses.

2.2.1. Physical Activity Participation and Categorization

Physical activity participation was assessed with questions about typical frequency, intensity, time, and type. Their usual intensity was self-categorized as light, moderate, vigorous (hard), very hard, or maximal using drop-down selections found in the survey. Total physical activity time per week was calculated as a product of self-reported days of activity per week and the typical amount of time spent exercising per day regardless of the activities undertaken. Additional open-ended responses related to participants’ individualized diabetes regimen changes were collected for over 165 different sports and activities, which were largely used for other purposes [55]. Responses to these physical activity and other related, open-ended questions were not directly analyzed and only included in terms of whether participants reported engaging in various activities.
Participants’ self-reported activities were placed into one or more of five categories: fitness, endurance, endurance-power, power, and outdoor. The designation of each sport was determined by the investigators and primarily based on the energy systems engaged during the activity itself (aerobic vs. anaerobic ones) [56], although some overlap among categories exists for certain sports and activities. Once participants answered “yes” for a category, numerous examples of activities and sports in each category were provided in the survey as drop-down selections to steer them to select representative ones. Some examples of selections in each category included, but were not limited to, the following:
  • Fitness activities: fitness walking, aerobic conditioning machines, resistance training, aerobics classes, Pilates, kettle ball training, dancing, agility training, balance training, stretching, yoga, indoor climbing, martial arts, tai chi, physical activity classes;
  • Endurance activities/sports: running and jogging, swimming, cycling, marathons, biathlons, triathlons, cross-country running or skiing, ultra endurance training;
  • Endurance-power sports: basketball, soccer, golf, tennis, hockey, football, tennis, indoor racquet sports, intermediate-distance track events, CrossFit, high-intensity interval training;
  • Power sports: baseball, bodybuilding, Olympic weight lifting or power lifting, sprinting, field events (shot put, pole vault, high jump, etc.), volleyball or beach volleyball;
  • Outdoor activities/sports: kayaking, downhill skiing, curling, waterskiing or wakeboarding, kiteboarding, hiking and backpacking, horseback riding, rock or ice climbing, adventure racing, trail running, hunting, fishing, gardening, etc.

2.2.2. Dietary Patterns and Carbohydrate Intake

The usual dietary patterns of participants were assessed with specific questions about whether they ingested carbohydrate for physical activity, their preferred sport-specific carbohydrate choices, and their usual dietary treatments for hypoglycemia, along with more open-ended questions about their typical dietary patterns. Some responded with definitive dietary patterns from which carbohydrate intake could be easily estimated, such as “keto diet” [57] or “Dr. Bernstein diet” [58,59], whereas others gave actual daily carbohydrate estimates or stated that they were vegan or vegetarian, ate a meat-based diet, consumed a plant-based whole foods diet, or avoided/limited their intake of starches or other food categories. These carbohydrate intake/dietary pattern data have been reported for a larger cohort of individuals with T1D or type 2 diabetes previously [12,13]. All of their responses to nutrition-related or dietary questions were considered together by the investigators, along with typical calorie requirements for active adults and adolescents [60], when estimating participants’ generalized daily carbohydrate intake and placing them into one of four categories for analyses:
  • Normal (unrestricted): >200 g/day;
  • Moderate: 100–200 g/day;
  • Low-carbohydrate: 40–99 g/day;
  • Very low-carbohydrate: <40 g/day.

2.3. Statistical Analyses

For this study, descriptive variables are presented as mean, standard error of the mean (SE), median, minimum, and maximum. A generalized linear model (GLM) approach was used to measure and quantify association between A1C and predictor variables. Using GLM, the equation for these associations was formulated as:
y i = β 0 + β 1 x 1 i + β 2 x 2 i + … + β p x p i + e i ,  
where y i represents the response of the ith participant’s A1C, for i = 1 , … , n , with x 1 , x 2 , … , x p representing other predictors like biological sex, usual carbohydrate intake, use of CGM devices, and other collected variables. Predictor variables were either discrete or continuous. In the model equation, the term β 0 served as the model intercept and β i referred to the slope associated with the i t h predictor variable, with the errors e i   independent   and   identically   distributed   ~ N ( 0 ,   σ 2 ) and σ 2 with the model variance. In order to minimize variance and satisfy model assumptions, a transformation of the A1C to a natural log scale was applied.
Due to a gap in self-reported A1C values, the natural log values (log A1C) were found to be closer to the normal distribution than the A1C itself. Consequently, log A1C values were used for further analyses in the GLM (see Appendix A for a detailed justification of the transformation to natural log and results of statistical tests). Significance for all such analyses was set as p < 0.05.

3. Results

3.1. Participant Characteristics and Survey Responses

The demographic factors of participants included their A1C, age, and years living with diabetes, as shown in Table 1, along with responses to other quantifiable and categorical questions from the online survey. The majority of the 220 respondents were from the United States (68%), with others from Europe (13%), Canada (7%), Australia (6%), Eastern Europe (3%), and the rest (3%) from Mexico, South Africa, Iran, India, and the Philippines. Data from another 30 participants with T1D were excluded due to incomplete or missing responses related to A1C and other relevant variables.
As a whole, the participants’ latest A1C mean and median values (Table 1) were well within commonly recommended ranges of less than 7% [61]. Almost 70% self-reported having an A1C within this recommended range, although values ranged from 4.2% to 10.5%. About 25 individuals reported using a second diabetes medication besides insulin, with the majority of them using either metformin or a sodium-glucose transport protein 2 (SGLT2) inhibitor. As none of these medications impacts exercise-associated blood glucose levels, they were not included in any further analyses.

3.2. AIC and Its Predictors

3.2.1. A1C Prediction with Physical Activity Variables

The total weekly time spent being physically active was estimated based on participant responses to both frequency (number of days per week) and usual time spent exercising on active days. The total hours per week were calculated as a product of the two, and the distribution of participant time is shown in Figure 2. The nature of the survey did not allow for any differentiation among time spent doing different types of activities.
When total physical activity time per week was further categorized into whether participants’ met the recommended minimum (at least 150 min, or 2.5 h, of aerobic activity) or engaging in less than 150 min [62,63], total time was not significantly predictive of log A1C values regardless of whether or not participants met weekly physical activity recommendations (Figure 3). Total time, however, included all types of activities in this survey.
The number of days of activity per week ranged from 2 to 7 (Figure 4), demonstrating that all participants were physically active. However, frequency of physical activity was not a significant predictor of A1C.
The usual intensity of physical activity engaged in by participants ranged from light to maximal, depending on the sport or activity (Figure 5). However, intensity also failed to predict differences in A1C values.

3.2.2. A1C Prediction with Categorical Responses to Selected Survey Responses

Survey responses related to participation in each category of physical activity or sports and carbohydrate ingestion for activity are shown in Figure 6 and Figure 7. No significant associations were found between these categorical responses and log A1C for any of these.

3.2.3. A1C Prediction Based on CMG Use and Dietary Patterns

CGM device use and whether participants experience activity-related low and high blood glucose values are shown in Figure 8. No significant associations were found between these yes/no categorical responses and log A1C for these variables.
With all variables considered within our model, the only significant predictors of participants’ log A1C values ended up being their use of CGM devices (p = 0.02) and their typical carbohydrate intake (p < 0.0001). These associations remained strong when analyzing either A1C or transformed natural log A1C (analyses shown in Appendix A). However, the variance was significantly reduced when the prediction model used log A1C given the gap evident in the distribution of participants’ A1C values (see Figure A1). The overall associations between A1C and usual carbohydrate intake categories are shown in Figure 9, and the relative percentages of participants falling into each carbohydrate intake category are shown in Figure 10.

3.2.4. A1C Prediction Based on Attainment of Recommended Ranges

An even more precise prediction emerged when participants were separated into one of two groups based whether their A1C values fell into the recommended range (<7%) or above (≥7%). A very-low carbohydrate intake was significantly associated with the lowest log A1C values when in recommended ranges (p < 0.0001), but CGM use was not predictive in that case (p = 0.90). When log A1C was in ranges above recommended, the most significant predictor was CGM wear (p < 0.01), with users of the devices having significantly lower values even though they failed to meet A1C recommendations, although carbohydrate intake failed to be predictive when A1C was higher (p = 0.16).

4. Discussion

As the aim of this online survey study was to ascertain which variables related to the diabetes management have the greatest impact on overall blood glucose levels, the outcomes were focused around achievement of A1C values in a recommended range. The primary findings were that in this cohort of free-living, physically active individuals with T1D of various ages, lower A1C values (within the recommended range of <7%) were best predicted by following a very-low carbohydrate dietary pattern, whereas using a CGM device was associated with better A1C values when A1C was higher than recommended. Contrary to our expectations, participants’ self-reported physical activity levels were not predictive of A1C values, even when they engaged in recommended amounts of total weekly activity of any type, and consideration of frequency, intensity, type, or total time did not increase the predictive value. However, most participants were already very active when compared to the population as a whole, which likely impacted these findings.
Reliance on physical activity participation to better manage overall blood glucose in individuals with T1D has shown mixed outcomes, although recent results are more promising (21). Participants in our online survey reported a fairly wide range of A1C values, demonstrating that being physically active alone does not guarantee optimal glycemic management, although the majority of values (70%) fell in the recommended range of <7% and would be considered well-managed. These results concur overall with many other studies showing that unless other glycemic variables are effectively balanced at the same time—such as food intake, insulin doses, and physical or mental stress—individuals with T1D do not necessarily experience improvements in overall glucose values when regularly active, with some studies demonstrating benefits [64,65,66] and others finding no improvement in A1C following aerobic or resistance training [67,68]. Our participants were engaging in myriad activities, though, making interpretation more difficult compared to those studies and others in which activities were more controlled and uniform. Moreover, our survey respondents engaged in physical activity 2 to 7 days per week, with over 93% of them reportedly engaging in more than the minimal recommended time. Some were training up to 42 h of weekly as competitive athletes and only five participants were active less than 100 min per week. This level of participation is far more than in the population overall [69,70] and for most with diabetes [71]. While our survey was not capable of discerning time spent in aerobic (as recommended 150 to 300 or more minutes a week) versus other types of activities, others have shown that total exercise volume and time spent being physically active doing any type of activity may matter more to cardiovascular and metabolic health than participation in specific bouts of moderate-to-vigorous aerobic activities by themselves [72,73,74,75]. Engaging in muscle-strengthening activity ≥2 times/week may provide additional benefits among insufficiently active adults [76]. With these observations in mind, we felt comfortable categorizing our participants as meeting or failing to meet the recommended total activity time with all types of activities considered together, not just aerobic ones.
Being physically active with T1D increases an individual’s risk of activity-related hypoglycemia [77,78,79] and hyperglycemia [80,81], and fear of activity-related hypoglycemia has often been a deterrent of regular participation for insulin users of all ages [82,83]. Conversely, since all of our participants were engaging in regular physical activity, they likely had already adapted their diabetes management strategies to better manage their glycemic variations while minimizing any fear of hypoglycemia associated with being active; in fact, out of 220 participants, only 10 reported A1C values of 8% or higher and only two of those were above 9%. Their regular participation may also at least partly explain why their total activity was not predictive of overall glycemic management since the vast majority were already exceeding recommended levels of activity and had A1C values that were well-managed compared to the majority of individuals with T1D as a whole [41,42]. Thus, it is likely that the glycemic impact of being active was already reflected in their having better A1C values than most individuals with T1D.
Another challenge associated with attempting to achieve better A1C values with physical activity is the unpredictability of glucose responses even to similar bouts of exercise. Active individuals completing our online survey frequently expressed frustrations with maintaining glycemic balance while doing a variety of physical activities under free-living conditions [55]. A recent study conducted on 12 adults with T1D reported that three identical cycling sessions completed on separate days under controlled conditions resulted in varying values for glucose measured either with a finger-stick (capillary blood) blood glucose monitor or a CGM device, even though glucose declined in all three trials [78]; these results indicated low reproducibility at the participant level and remained unchanged after adjustment for baseline glucose values. Likewise, in adolescents with T1D, while greater intrasubject reliability and repeatability of blood glucose responses to prolonged exercise was shown to be possible, this result occurred only when pre-exercise meal, exercise, and insulin regimens were kept constant [84], which is not always feasible in real life. However, recent technological advances, improvements in insulin regimens, newer insulins, and a better understanding of the physiology of various types of exercise may help limit such unpredictability for similar activities and, at the same time, lessen the fear of hypoglycemia by facilitating hypoglycemia prevention [82]. With proper management around activities, athletes with T1D at all levels have been shown to be capable of undertaking and performing well even in long endurance training, high-intensity sports, and other types of events [27,29,85,86].
With regard to dietary patterns, in the current study a very-low carbohydrate intake was surprisingly most predictive of achieving recommended glycemic levels overall (i.e., an A1C < 7%), regardless of differing levels and types of physical activity participation. Many endurance athletes with and without T1D have claimed to perform well with a lower, or at least moderate, intake of this macronutrient [57,87] and to maintain a better glycemic balance [31], although the consensus remains that carbohydrates are necessary to perform well at higher intensities and durations of activity [12,88,89]. However, the active individuals in our study who stated that they ingest carbohydrates during physical activity had similar A1C values to those who claimed to refrain from carbohydrate supplementation. In fact, supplementing with carbohydrates has been shown to potentially be superior to bolus insulin reduction for prevention of hypoglycemia during physical activity, as was demonstrated in a group of adults with T1D engaging in moderate-intensity cycling for 45 min in one study [90]. In our survey, however, both strategies (i.e., carbohydrate ingestion and insulin reduction) were used by most participants to prevent hypoglycemia with activity; in many cases, active individuals with T1D must employ a combination of both in order to maintain glycemic balance during and after training or events [12,15,29].
Nowadays, daily carbohydrate intake alone is usually not predictive of A1C values for most with T1D, and consuming carbohydrates can be feasible, which may be reflective of individuals’ use of faster-acting insulin analogues for meal boluses. In fact, a single mealtime bolus of insulin has been shown to cover a range of carbohydrate intake without deterioration in postprandial glycemia [91]. Even dietary fat, protein, and the glycemic index of ingested carbohydrates are associated with insulin dosing needs and impact postprandial glucose excursions [92,93], making glycemic predictions and insulin dosing based on grams of carbohydrate intake alone inadequate. Carbohydrate counting is fraught with complications given the complexities in digestion and absorption rates of that macronutrient and challenges related to proper estimation of the amount ingested by individuals [94,95,96]. With regard to our survey participants, most of whom already had optimal blood glucose management, it may be that they simply were able to tighten it slightly further by restricting their carbohydrate intake. Avoiding greater fluctuations in blood glucose after meals and during activity can improve overall glycemia [97]. In our survey, for individuals with higher-than-recommended A1C values, carbohydrate restriction was not predictive of better glycemic management, suggesting that other variables are impacting glycemia more in their case.
Although trials are undergoing, to date low- and very low-carbohydrate diets have not been extensively studied in the management of T1D [13], with available studies examining glycemic outcomes from such diets being largely cross-sectional and lacking validated dietary data or control subjects [32,98]. Many of the participants in such studies can be described as highly motivated individuals who follow intensive insulin management practices, including frequent blood glucose monitoring and additional insulin corrections to meet tight glycemic targets. While athletes may still perform adequately when following such restricted diets [32,99,100], some potential negative health consequences of ketogenic and other low-carbohydrate diets have been noted [101,102], and longer term studies are needed to determine how feasible these dietary patterns are for most individuals with T1D [103]. Thus, much work remains to be done to fully determine the extent of the impact of dietary carbohydrate restriction on glycemic outcomes and optimal intake levels, particularly in physically active individuals with T1D.
Finally, the use of the latest diabetes technological advances, such as insulin pumps and CGM devices, has greatly advanced the ability to manage glucose levels around physical activity [36,37]. While 60% of our participants used an insulin pump, an even larger percentage (77%) used a CGM. Having access to either one or both devices potentially can allow users to make more informed choices to manage glycemia around exercise [104]. For our survey participants, using a CGM device was predictive of lower A1C values (specifically when above recommended levels) although insulin pump use was not predictive. This is unsurprising given that other studies have shown that CGM can be beneficial for all individuals with T1D [40,41,42], even for those who have already achieved recommended A1C at <7.0% [43]. Despite the demonstrated time lag between blood glucose (measured via finger stick) and interstitial glucose levels (measured via CGM) [36,44,45], having closer to real-time feedback on the impact of any activity likely makes glycemic management easier, especially when activities can vary so widely in their effects. For instance, a recent systematic review and meta-analysis that included 12 studies using CGM devices to examine the delayed impact of engaging in various physical activities reported that intermittent exercise (i.e., most endurance-power or power sports) actually increases the time spent in hypoglycemia and lowers mean glycemic values via CGM, with no differences in time spent in hyperglycemia or the number of hypoglycemic events [105]. Hypoglycemia risk was also lower for activities performed in the morning rather than in the afternoon, even with a 50% rapid-acting insulin reduction prior to later-day exercise. While our participants did not indicate their usual time of day for activities, CGM use has the potential to provide feedback that allows users to take corrective actions to manage glycemia in a timelier manner.
Although not a survey question, some of our participants noted employing various exercise strategies with use of hybrid closed-loop systems (i.e., Medtronic 670G), which involve integration of an insulin pump, CGM, and algorithm control system to manage insulin delivery in response to real-time glucose levels with minimal user input. Although some input is usually still required (such as announcement of meals or exercise), hybrid systems have recently been found to improve time-in-range (typically defined as 70–180 mg/dL, or 3.9–10.0 mmol/L) around physical activity [106]. Users of such systems with a lower intake of daily carbohydrates have also experienced better glycemic management [107], likely due to the ability of such systems to make adjustments in response to the slower glucose fluctuations resulting from dietary protein and fat [97,108].
The limitations of this survey research localize mainly around our inability to collect more quantifiable and directly verifiable data, since all of it was self-reported and many of the survey questions were more open-ended. This is particularly an issue for dietary considerations including estimating carbohydrate intake, total calories, macronutrient distribution, and micronutrient adequacy, among other considerations. The authors used their best judgment when placing the participants into dietary categories for carbohydrate intake based on the data collected. However, it is possible that their interpretation of some responses was flawed or that participants failed to report or recognize all the carbohydrate sources in their diets, including those in high-fat, low-carbohydrate foods (e.g., olives, avocados, and nuts); in foods, drinks, or sports supplements taken during activities; and in rapid hypoglycemia treatments. A dietary recall questionnaire would have enhanced the reliability of these data around dietary patterns, total calorie intake, and macronutrient distribution. Likewise, although participants responded to questions around insulin use, types, and delivery methods, our interpretations are limited. More information related to actual dosing, timing, and other insulin-related data, particularly around physical activity and glycemic management would have provided more definitive results. Finally, relying on self-reported data in any research study has its limitations and can be problematic [109,110]; this is particularly true when it comes to data related to physical activity. Our survey participants reported engaging in a wide array of physical activities, many of which have varied glucose responses even within a specific category, especially “outdoor activities and sports”. Our data collection and interpretation would have been enhanced by use of a more standardized physical activity questionnaire, quantifiable data that could be converted into objective total exercise volume measures (such as MET-min/week) and, of course, controlled laboratory conditions.
Much remains to be studied related to physical activity in individuals with T1D, especially given the large number of variables that must be simultaneously balanced to maintain normal or near normal glycemic levels. Future research likely should include the potential implications of carbohydrate-restriction and other dietary patterns on physical activity performance and glycemic balance in this population. Another area to pursue is the glycemic benefits of using the latest technologies related to insulin delivery, glucose monitoring, and physical activity trackers and other devices. Such technologies can provide immediate feedback to users and allow them to make optimal and real-time diabetes regimen adjustments before, during, and after physical activity.

5. Conclusions

In conclusion, when individuals with type 1 diabetes of any age are already physically active and their blood glucose is well-managed, a greater focus on lowering carbohydrate intake may improve glycemic management. In addition, active individuals may benefit from using continuous glucose monitoring to lower overall glycemia, especially when their A1C values are higher than recommended. Nevertheless, all individuals can benefit from being physically active on a regular basis, especially when the myriad variables affecting glucose responses can be adequately managed to prevent hypoglycemia or hyperglycemia.

Author Contributions

Conceptualization, S.R.C.; methodology, S.R.C., J.K. and N.D.; formal analysis, J.K. and N.D.; investigation, S.R.C.; data curation, S.R.C. and J.K.; writing—original draft preparation, S.R.C., J.K. and N.D.; writing—review and editing, S.R.C., J.K. and N.D.; visualization, J.K. and N.D. All authors have read and agreed to the published version of the manuscript.

Funding

This study received no external funding.

Institutional Review Board Statement

The study was conducted anonymously online through voluntary participation. Ethical review and approval were waived for this study given that participant names and identifying data were not collected on the survey.

Informed Consent Statement

Patient consent was not required due to the anonymous and voluntary nature in which all survey responses were obtained and recorded. This research was considered “exempt” by the Institutional Review Board of Old Dominion University.

Acknowledgments

We greatly appreciate the willingness of the hundreds of active individuals with diabetes around the world to complete our online questionnaire. In addition, we acknowledge the helpful editing and feedback provided by Alexander R. Ochs, student at the University of Washington (Seattle, WA, USA).

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Multiple selection methods used revealed that the participants’ usual carbohydrate intake (“CarbIntake”) and use of CGM devices (“CGM”) factors were strong predictors of their A1C values (Table A1). The corresponding model variance in the case of the parsimonious simplified model (with CarbIntake and CGM use only) showed an estimate of the model variance of σ ^ 2 = 0.7098177 (Table A2).
Table
Table A1. A1C with CGM and CarbIntake as independent variables.
Table A1. A1C with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM13.926065533.926065535.530.0196
CarbIntake316.966673955.65557987.97<0.0001
Table
Table A2. GLM with A1C as dependent variable.
Table A2. GLM with A1C as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model422.23151035.55787767.83<0.0001
Error215152.61080780.7098177
Corrected Total219174.8423182
R-SquareCoeff VarRoot MSEA1C Mean
0.12715212.851110.8425076.555909
To minimize that variance, a transformation of the A1C to natural log (base e) was considered. When this log A1C was used, the same significant predictors (i.e., CGM and CarbIntake) were still obtained from the data (Table A3), but the parsimonious model variance was reduced. The variance of the log A1C was σ ^ 2 = 0.0162 (Table A4), which was more than 44 times smaller than the variance of the model with untransformed A1C. With the reduced variance, the model precision increased.
Table
Table A3. Log A1C with CGM and CarbIntake as independent variables.
Table A3. Log A1C with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM10.069101700.069101704.240.0407
CarbIntake30.453761790.151253939.28<0.0001
Table
Table A4. GLM with log A1C as dependent variable.
Table A4. GLM with log A1C as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model40.552087980.138021998.47<0.0001
Error2153.503785200.01629668
Corrected Total2194.05587317
R-SquareCoeff VarRoot MSELog A1C Mean
0.1361216.8223300.1276581.871185
Thus, the histogram and boxplots of log A1C with respect to the same predictors (e.g., sex, CarbIntake, insulin pump use, CGM, physical activity categories) were created. The histogram plot showed of A1C data exhibited a gap, which led log A1C to have a narrower distribution closer to a normal one than A1C (Figure A1).
Ijerph 18 09332 g0a1 550
Figure A1. Histogram plots of A1C (a) and log A1C (b) distributions.
Figure A1. Histogram plots of A1C (a) and log A1C (b) distributions.
Ijerph 18 09332 g0a1
A classification of the A1C was suggested around current clinical recommendations, leading to equivalent log A1C values to be put into one of two categories: in recommended ranges (low, or <7%) or higher than recommended (high, or ≥7%). At that point, the data were asymmetric, and options were considered. One option was to consider using a regression model to predict A1C based on each category, but the data were mainly limited and exhibited an imbalance with 154 and 148 participants in low A1C and high A1C, respectively. Use of the GLM technique with the transformed, categorized data led to the observation that the imbalanced proportions were not too acute, and the expectation was that the separate models with selected predictor(s) would reduce biases.
We observed that when the A1C was low (<7%), the model variance went from 0.3367 (Table A5) to 0.0101 (Table A6), an almost 33-fold reduction in variance. Moreover, the most significant predictor under GLM for the A1C or its log was CarbIntake (Table A7 and Table A8).
Table
Table A5. GLM with A1C < 7% as dependent variable.
Table A5. GLM with A1C < 7% as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model47.018695911.754673985.210.0006
Error14950.162862530.33666351
Corrected Total15357.181555844
R-SquareCoeff VarRoot MSEA1C Mean
0.1227449.4535520.5802276.137662
Table
Table A6. GLM with log A1C < 1.95% (log < 7% equivalent) as dependent variable.
Table A6. GLM with log A1C < 1.95% (log < 7% equivalent) as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model40.244122920.061030736.020.0002
Error1611.631140200.01013131
Corrected Total1651.87526312
R-SquareCoeff VarRoot MSELog A1C Mean
0.1301815.5332380.1006541.819086
Table
Table A7. A1C < 7% with CGM and CarbIntake as independent variables.
Table A7. A1C < 7% with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM10.012722450.012722450.040.8461
CarbIntake36.798968052.266322686.730.0003
Table
Table A8. Log A1C < 1.95% with CGM and CarbIntake as independent variables.
Table A8. Log A1C < 1.95% with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM10.000188870.000188870.020.8916
CarbIntake30.242810200.080936737.99<0.0001
When the A1C was high (≥7%), the model variance went from 0.3440 (Table A9) to 0.0055 (Table A10), a substantial almost 62-fold reduction. Moreover, the most significant predictor under GLM for the A1C or its log was CGM use (Table A11 and Table A12, respectively).
Table
Table A9. GLM with A1C ≥ 7% as dependent variable.
Table A9. GLM with A1C ≥ 7% as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model46.873754831.718438714.990.0015
Error6120.989426990.34408897
Corrected Total6527.86318182
R-SquareCoeff VarRoot MSEA1C Mean
0.2466977.7881720.5865917.531818
Table
Table A10. GLM with log A1C ≥ 1.95% (log ≥ 7% equivalent) as dependent variable.
Table A10. GLM with log A1C ≥ 1.95% (log ≥ 7% equivalent) as dependent variable.
SourceDFSum of SquaresMean SquareF ValuePr > F
Model40.073113330.018278333.290.0181
Error490.271838790.00554773
Corrected Total530.34495212
R-SquareCoeff VarRoot MSELog A1C Mean
0.2119523.6666960.0744832.031341
Table
Table A11. A1C ≥ 7% with CGM and CarbIntake as independent variables.
Table A11. A1C ≥ 7% with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM14.271503744.2715037412.410.0008
CarbIntake32.883698010.961232672.790.0478
Table
Table A12. Log A1C ≥ 1.95% with CGM and CarbIntake as independent variables.
Table A12. Log A1C ≥ 1.95% with CGM and CarbIntake as independent variables.
SourceDFType III SSMean SquareF ValuePr > F
CGM10.053929630.053929639.720.0030
CarbIntake30.0310580400.010526801.900.1423

References

  1. Gerstein, H.C.; Rutty, C.J. Insulin Therapy: The Discovery That Shaped a Century. Can. J. Diabetes 2021, S1499-2671(21)00066-6. [Google Scholar] [CrossRef]
  2. American Diabetes Association. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes—2021. Diabetes Care 2021, 44 (Suppl. 1), S15–S33. [Google Scholar] [CrossRef] [PubMed]
  3. Colom, C.; Rull, A.; Sanchez-Quesada, J.; Pérez, A. Cardiovascular Disease in Type 1 Diabetes Mellitus: Epidemiology and Management of Cardiovascular Risk. J. Clin. Med. 2021, 10, 1798. [Google Scholar] [CrossRef] [PubMed]
  4. Chimen, M.; Kennedy, A.; Nirantharakumar, K.; Pang, T.T.; Andrews, R.; Narendran, P. What are the health benefits of physical activity in type 1 diabetes mellitus? A literature review. Diabetologia 2012, 55, 542–551. [Google Scholar] [CrossRef] [Green Version]
  5. Brazeau, A.S.; Leroux, C.; Mircescu, H.; Rabasa-Lhoret, R. Physical activity level and body composition among adults with Type 1 diabetes. Diabet. Med. 2012, 29, e402–e408. [Google Scholar] [CrossRef]
  6. Distiller, L.A. Why do some patients with type 1 diabetes live so long? World J. Diabetes 2014, 5, 282–287. [Google Scholar] [CrossRef] [PubMed]
  7. Knudsen, J.R.; Steenberg, D.; Hingst, J.R.; Hodgson, L.R.; Henriquez-Olguin, C.; Li, Z.; Kiens, B.; Richter, E.A.; Wojtaszewski, J.; Verkade, P.; et al. Prior exercise in humans redistributes intramuscular GLUT4 and enhances insulin-stimulated sarcolemmal and endosomal GLUT4 translocation. Mol. Metab. 2020, 39, 100998. [Google Scholar] [CrossRef]
  8. Ryan, B.J.; Schleh, M.W.; Ahn, C.; Ludzki, A.C.; Gillen, J.B.; Varshney, P.; Van Pelt, D.W.; Pitchford, L.M.; Chenevert, T.L.; Gioscia-Ryan, R.A.; et al. Moderate-Intensity Exercise and High-Intensity Interval Training Affect Insulin Sensitivity Similarly in Obese Adults. J. Clin. Endocrinol. Metab. 2020, 105. [Google Scholar] [CrossRef] [PubMed]
  9. Marcinko, K.; Sikkema, S.R.; Samaan, M.C.; Kemp, B.E.; Fullerton, M.D.; Steinberg, G.R. High intensity interval training improves liver and adipose tissue insulin sensitivity. Mol. Metab. 2015, 4, 903–915. [Google Scholar] [CrossRef]
  10. Leroux, C.; Gingras, V.; Desjardins, K.; Brazeau, A.-S.; Ott-Braschi, S.; Strychar, I.; Rabasa-Lhoret, R. In adult patients with type 1 diabetes healthy lifestyle associates with a better cardiometabolic profile. Nutr. Metab. Cardiovasc. Dis. 2015, 25, 444–451. [Google Scholar] [CrossRef] [PubMed]
  11. Sekercioglu, N.; Lovblom, L.E.; Bjornstad, P.; Lovshin, J.A.; Lytvyn, Y.; Boulet, G.; Farooqi, M.A.; Orszag, A.; Lai, V.; Tse, J.; et al. Risk factors for diabetic kidney disease in adults with longstanding type 1 diabetes: Results from the Canadian Study of Longevity in Diabetes. Ren. Fail. 2019, 41, 427–433. [Google Scholar] [CrossRef] [Green Version]
  12. Riddell, M.C.; Scott, S.; Fournier, P.A.; Colberg, S.R.; Gallen, I.W.; Moser, O.; Stettler, C.; Yardley, J.E.; Zaharieva, D.P.; Adolfsson, P.; et al. The competitive athlete with type 1 diabetes. Diabetologia 2020, 63, 1475–1490. [Google Scholar] [CrossRef]
  13. Colberg, S.R. Nutrition and Exercise Performance in Adults with Type 1 Diabetes. Can. J. Diabetes 2020, 44, 750–758. [Google Scholar] [CrossRef] [PubMed]
  14. Yardley, J.E.; Colberg, S. Update on Management of Type 1 Diabetes and Type 2 Diabetes in Athletes. Curr. Sports Med. Rep. 2017, 16, 38–44. [Google Scholar] [CrossRef] [PubMed]
  15. Riddell, M.C.; Gallen, I.W.; Smart, C.E.; Taplin, C.E.; Adolfsson, P.; Lumb, A.N.; Kowalski, A.; Rabasa-Lhoret, R.; McCrimmon, R.J.; Hume, C.; et al. Exercise management in type 1 diabetes: A consensus statement. Lancet Diabetes Endocrinol. 2017, 5, 377–390. [Google Scholar] [CrossRef] [Green Version]
  16. Lespagnol, E.; Bocock, O.; Heyman, J.; Gamelin, F.-X.; Berthoin, S.; Pereira, B.; Boissière, J.; Duclos, M.; Heyman, E. In Amateur Athletes with Type 1 Diabetes, a 9-Day Period of Cycling at Moderate-to-Vigorous Intensity Unexpectedly Increased the Time Spent in Hyperglycemia, Which Was Associated with Impairment in Heart Rate Variability. Diabetes Care 2020, 43, 2564–2573. [Google Scholar] [CrossRef]
  17. Steineck, I.I.K.; Ranjan, A.G.; Schmidt, S.; Norgaard, K. Time spent in hypoglycemia is comparable when the same amount of exercise is performed 5 or 2 days weekly: A randomized crossover study in people with type 1 diabetes. BMJ Open Diabetes Res. Care 2021, 9, e001919. [Google Scholar] [CrossRef]
  18. Yardley, J.E.; Kenny, G.P.; Perkins, B.A.; Riddell, M.C.; Balaa, N.; Malcolm, J.; Boulay, P.; Khandwala, F.; Sigal, R.J. Resistance Versus Aerobic Exercise: Acute effects on glycemia in type 1 diabetes. Diabetes Care 2012, 36, 537–542. [Google Scholar] [CrossRef] [Green Version]
  19. Yardley, J.; Mollard, R.; MacIntosh, A.; MacMillan, F.; Wicklow, B.; Berard, L.; Hurd, C.; Marks, S.; McGavock, J. Vigorous Intensity Exercise for Glycemic Control in Patients with Type 1 Diabetes. Can. J. Diabetes 2013, 37, 427–432. [Google Scholar] [CrossRef]
  20. Yardley, J.E.; Sigal, R.J. Exercise Strategies for Hypoglycemia Prevention in Individuals with Type 1 Diabetes. Diabetes Spectr. 2015, 28, 32–38. [Google Scholar] [CrossRef] [Green Version]
  21. Yardley, J.E.; Hay, J.; Abou-Setta, A.M.; Marks, S.D.; McGavock, J. A systematic review and meta-analysis of exercise interventions in adults with type 1 diabetes. Diabetes Res. Clin. Pract. 2014, 106, 393–400. [Google Scholar] [CrossRef]
  22. Yardley, J.E.; Sigal, R.J.; Riddell, M.C.; Perkins, B.A.; Kenny, G.P. Performing resistance exercise before versus after aerobic exercise influences growth hormone secretion in type 1 diabetes. Appl. Physiol. Nutr. Metab. 2014, 39, 262–265. [Google Scholar] [CrossRef] [PubMed]
  23. Turner, D.; Luzio, S.; Gray, B.; Dunseath, G.; Rees, E.D.; Kilduff, L.P.; Campbell, M.; West, D.J.; Bain, S.C.; Bracken, R. Impact of single and multiple sets of resistance exercise in type 1 diabetes. Scand. J. Med. Sci. Sports 2014, 25, e99–e109. [Google Scholar] [CrossRef]
  24. Yardley, J.E.; Kenny, G.P.; Perkins, B.A.; Riddell, M.C.; Malcolm, J.; Boulay, P.; Khandwala, F.; Sigal, R.J. Effects of Performing Resistance Exercise before versus after Aerobic Exercise on Glycemia in Type 1 Diabetes. Diabetes Care 2012, 35, 669–675. [Google Scholar] [CrossRef] [Green Version]
  25. Gomez, A.M.; Gomez, C.; Aschner, P.; Veloza, A.; Muñoz, O.; Rubio, C.; Vallejo, S. Effects of Performing Morning Versus Afternoon Exercise on Glycemic Control and Hypoglycemia Frequency in Type 1 Diabetes Patients on Sensor-Augmented Insulin Pump Therapy. J. Diabetes Sci. Technol. 2015, 9, 619–624. [Google Scholar] [CrossRef] [Green Version]
  26. Turner, D.; Luzio, S.; Gray, B.; Bain, S.C.; Hanley, S.; Richards, A.; Rhydderch, D.C.; Martin, R.; Campbell, M.D.; Kilduff, L.P.; et al. Algorithm that delivers an individualized rapid-acting insulin dose after morning resistance exercise counters post-exercise hyperglycaemia in people with Type 1 diabetes. Diabet. Med. 2015, 33, 506–510. [Google Scholar] [CrossRef]
  27. Yardley, J.E.; Zaharieva, D.P.; Jarvis, C.; Riddell, M.C. The “ups” and “downs” of a bike race in people with type 1 diabetes: Dramatic differences in strategies and blood glucose responses in the Paris-to-Ancaster Spring Classic. Can. J. Diabetes 2015, 39, 105–110. [Google Scholar] [CrossRef]
  28. Scott, S.N.; Christiansen, M.P.; Fontana, F.Y.; Stettler, C.; Bracken, R.; Hayes, C.A.; Fisher, M.; Bode, B.; Lagrou, P.H.; Southerland, P.; et al. Evaluation of Factors Related to Glycemic Management in Professional Cyclists with Type 1 Diabetes Over a 7-Day Stage Race. Diabetes Care 2020, 43, 1142–1145. [Google Scholar] [CrossRef] [Green Version]
  29. Scott, S.N.; Fontana, F.Y.; Cocks, M.; Morton, J.P.; Jeukendrup, A.; Dragulin, R.; Wojtaszewski, J.F.P.; Jensen, J.; Castol, R.; Riddell, M.C.; et al. Post-exercise recovery for the endurance athlete with type 1 diabetes: A consensus statement. Lancet Diabetes Endocrinol. 2021, 9, 304–317. [Google Scholar] [CrossRef]
  30. Wong, K.; Raffray, M.; Roy-Fleming, A.; Blunden, S.; Brazeau, A.-S. Ketogenic Diet as a Normal Way of Eating in Adults with Type 1 and Type 2 Diabetes: A Qualitative Study. Can. J. Diabetes 2021, 45, 137–143.e1. [Google Scholar] [CrossRef]
  31. Scott, S.N.; Anderson, L.; Morton, J.P.; Wagenmakers, A.J.M.; Riddell, M.C. Carbohydrate Restriction in Type 1 Diabetes: A Realistic Therapy for Improved Glycaemic Control and Athletic Performance? Nutrients 2019, 11, 1022. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Scott, S.; Kempf, P.; Bally, L.; Stettler, C. Carbohydrate Intake in the Context of Exercise in People with Type 1 Diabetes. Nutrients 2019, 11, 3017. [Google Scholar] [CrossRef] [Green Version]
  33. Cichosz, S.L.; Frystyk, J.; Hejlesen, O.; Tarnow, L.; Fleischer, J. A Novel Algorithm for Prediction and Detection of Hypoglycemia Based on Continuous Glucose Monitoring and Heart Rate Variability in Patients with Type 1 Diabetes. J. Diabetes Sci. Technol. 2014, 8, 731–737. [Google Scholar] [CrossRef]
  34. Wadwa, R.P.; Laffel, L.M.; Shah, V.N.; Garg, S.K. Accuracy of a Factory-Calibrated, Real-Time Continuous Glucose Monitoring System During 10 Days of Use in Youth and Adults with Diabetes. Diabetes Technol. Ther. 2018, 20, 395–402. [Google Scholar] [CrossRef] [Green Version]
  35. Woldaregay, A.Z.; Årsand, E.; Walderhaug, S.; Albers, D.; Mamykina, L.; Botsis, T.; Hartvigsen, G. Data-driven modeling and prediction of blood glucose dynamics: Machine learning applications in type 1 diabetes. Artif. Intell. Med. 2019, 98, 109–134. [Google Scholar] [CrossRef]
  36. Moser, O.; Riddell, M.C.; Eckstein, M.L.; Adolfsson, P.; Rabasa-Lhoret, R.; Boom, L.V.D.; Gillard, P.; Nørgaard, K.; Oliver, N.S.; Zaharieva, D.P.; et al. Glucose management for exercise using continuous glucose monitoring (CGM) and intermittently scanned CGM (isCGM) systems in type 1 diabetes: Position statement of the European Association for the Study of Diabetes (EASD) and of the International Society for Pediatric and Adolescent Diabetes (ISPAD) endorsed by JDRF and supported by the American Diabetes Association (ADA). Diabetologia 2020, 63, 2501–2520. [Google Scholar] [CrossRef]
  37. Zaharieva, D.P.; McGaugh, S.; Pooni, R.; Vienneau, T.; Ly, T.; Riddell, M.C. Improved Open-Loop Glucose Control with Basal Insulin Reduction 90 Minutes Before Aerobic Exercise in Patients with Type 1 Diabetes on Continuous Subcutaneous Insulin Infusion. Diabetes Care 2019, 42, 824–831. [Google Scholar] [CrossRef]
  38. Franc, S.; Daoudi, A.; Pochat, A.; Petit, M.; Randazzo, C.; Petit, C.; Duclos, M.; Penfornis, A.; Pussard, E.; Not, D.; et al. Insulin-based strategies to prevent hypoglycaemia during and after exercise in adult patients with type 1 diabetes on pump therapy: The DIABRASPORT randomized study. Diabetes Obes. Metab. 2015, 17, 1150–1157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Heinemann, L.; Nosek, L.; Kapitza, C.; Schweitzer, M.-A.; Krinelke, L. Changes in Basal Insulin Infusion Rates with Subcutaneous Insulin Infusion: Time until a change in metabolic effect is induced in patients with type 1 diabetes. Diabetes Care 2009, 32, 1437–1439. [Google Scholar] [CrossRef] [Green Version]
  40. Beck, R.W.; Riddlesworth, T.; Ruedy, K.; Ahmann, A.; Bergenstal, R.; Haller, S.; Kollman, C.; Kruger, D.; McGill, J.B.; Polonsky, W.; et al. Effect of Continuous Glucose Monitoring on Glycemic Control in Adults with Type 1 Diabetes Using Insulin Injections: The DIAMOND Randomized Clinical Trial. JAMA 2017, 317, 371–378. [Google Scholar] [CrossRef]
  41. Pratley, R.E.; Kanapka, L.G.; Rickels, M.R.; Ahmann, A.; Aleppo, G.; Beck, R.; Bhargava, A.; Bode, B.W.; Carlson, A.; Chaytor, N.S.; et al. Effect of Continuous Glucose Monitoring on Hypoglycemia in Older Adults with Type 1 Diabetes: A Randomized Clinical Trial. JAMA 2020, 323, 2397–2406. [Google Scholar] [CrossRef]
  42. Laffel, L.M.; Kanapka, L.G.; Beck, R.W.; Bergamo, K.; Clements, M.A.; Criego, A.; DeSalvo, D.J.; Goland, R.; Hood, K.; Liljenquist, D.; et al. Effect of Continuous Glucose Monitoring on Glycemic Control in Adolescents and Young Adults with Type 1 Diabetes: A Randomized Clinical Trial. JAMA 2020, 323, 2388–2396. [Google Scholar] [CrossRef] [PubMed]
  43. Juvenile Diabetes Research Foundation Continuous Glucose Monitoring Study Group. The effect of continuous glucose monitoring in well-controlled type 1 diabetes. Diabetes Care 2009, 32, 1378–1783. [Google Scholar] [CrossRef] [Green Version]
  44. Zaharieva, D.P.; Turksoy, K.; McGaugh, S.M.; Pooni, R.; Vienneau, T.; Ly, T.; Riddell, M.C. Lag Time Remains with Newer Real-Time Continuous Glucose Monitoring Technology During Aerobic Exercise in Adults Living with Type 1 Diabetes. Diabetes Technol. Ther. 2019, 21, 313–321. [Google Scholar] [CrossRef] [Green Version]
  45. Zaharieva, D.P.; Riddell, M.C.; Henske, J. The Accuracy of Continuous Glucose Monitoring and Flash Glucose Monitoring During Aerobic Exercise in Type 1 Diabetes. J. Diabetes Sci. Technol. 2019, 13, 140–141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Zisser, H.; Renard, E.; Kovatchev, B.; Cobelli, C.; Avogaro, A.; Nimri, R.; Magni, L.; Buckingham, B.A.; Chase, H.P.; DoyleIII, F.J.; et al. Multicenter Closed-Loop Insulin Delivery Study Points to Challenges for Keeping Blood Glucose in a Safe Range by a Control Algorithm in Adults and Adolescents with Type 1 Diabetes from Various Sites. Diabetes Technol. Ther. 2014, 16, 613–622. [Google Scholar] [CrossRef]
  47. Dassau, E.; Brown, S.A.; Basu, A.; Pinsker, J.; Kudva, Y.C.; Gondhalekar, R.; Patek, S.; Lv, D.; Schiavon, M.; Lee, J.B.; et al. Adjustment of Open-Loop Settings to Improve Closed-Loop Results in Type 1 Diabetes: A Multicenter Randomized Trial. J. Clin. Endocrinol. Metab. 2015, 100, 3878–3886. [Google Scholar] [CrossRef] [Green Version]
  48. Brown, S.A.; Breton, M.D.; Anderson, S.M.; Kollar, L.; Keith-Hynes, P.; Levy, C.J.; Lam, D.W.; Levister, C.; Baysal, N.; Kudva, Y.C.; et al. Overnight Closed-Loop Control Improves Glycemic Control in a Multicenter Study of Adults with Type 1 Diabetes. J. Clin. Endocrinol. Metab. 2017, 102, 3674–3682. [Google Scholar] [CrossRef] [Green Version]
  49. Ekhlaspour, L.; Forlenza, G.; Chernavvsky, D.; Maahs, D.M.; Wadwa, R.P.; DeBoer, M.D.; Messer, L.H.; Town, M.; Rn, J.P.; Kruse, G.; et al. Closed loop control in adolescents and children during winter sports: Use of the Tandem Control-IQ AP system. Pediatr. Diabetes 2019, 20, 759–768. [Google Scholar] [CrossRef]
  50. Riddell, M.C.; Pooni, R.; Fontana, F.Y.; Scott, S. Diabetes Technology and Exercise. Endocrinol. Metab. Clin. N. Am. 2020, 49, 109–125. [Google Scholar] [CrossRef]
  51. Viñals, C.; Beneyto, A.; Martín-SanJosé, J.-F.; Furió-Novejarque, C.; Bertachi, A.; Bondia, J.; Vehi, J.; Conget, I.; Giménez, M. Artificial Pancreas with Carbohydrate Suggestion Performance for Unannounced and Announced Exercise in Type 1 Diabetes. J. Clin. Endocrinol. Metab. 2021, 106, 55–63. [Google Scholar] [CrossRef] [PubMed]
  52. Breton, M.D. Handling Exercise During Closed Loop Control. Diabetes Technol. Ther. 2017, 19, 328–330. [Google Scholar] [CrossRef] [PubMed]
  53. Jayawardene, D.C.; McAuley, S.A.; Horsburgh, J.C.; La Gerche, A.; Jenkins, A.; Ward, G.M.; MacIsaac, R.J.; Roberts, T.J.; Grosman, B.; Kurtz, N.; et al. Closed-Loop Insulin Delivery for Adults with Type 1 Diabetes Undertaking High-Intensity Interval Exercise Versus Moderate-Intensity Exercise: A Randomized, Crossover Study. Diabetes Technol. Ther. 2017, 19, 340–348. [Google Scholar] [CrossRef]
  54. Biagi, L.; Bertachi, L.R.B.S.; Quirós, C.; Giménez, M.; Conget, I.; Bondia, J.; Vehí, J. Accuracy of Continuous Glucose Monitoring before, during, and after Aerobic and Anaerobic Exercise in Patients with Type 1 Diabetes Mellitus. Biosensors 2018, 8, 22. [Google Scholar] [CrossRef] [Green Version]
  55. Colberg, S. The Athlete’s Guide to Diabetes: Expert Advice for 165 Sports and Activities; Human Kinetics: Champaign, IL, USA, 2020; 382p. [Google Scholar]
  56. Wells, G.D.; Selvadurai, H.; Tein, I. Bioenergetic provision of energy for muscular activity. Paediatr. Respir. Rev. 2009, 10, 83–90. [Google Scholar] [CrossRef]
  57. McSwiney, F.; Wardrop, B.; Hyde, P.N.; Lafountain, R.A.; Volek, J.S.; Doyle, L. Keto-adaptation enhances exercise performance and body composition responses to training in endurance athletes. Metabolism 2018, 81, 25–34. [Google Scholar] [CrossRef] [PubMed]
  58. Lennerz, B.S.; Barton, A.; Bernstein, R.K.; Dikeman, R.D.; Diulus, C.; Hallberg, S.; Rhodes, E.T.; Ebbeling, C.B.; Westman, E.C.; Yancy, W.S.; et al. Management of Type 1 Diabetes with a Very Low-Carbohydrate Diet. Pediatrics 2018, 141, e20173349. [Google Scholar] [CrossRef] [Green Version]
  59. Feinman, R.D.; Pogozelski, W.K.; Astrup, A.; Bernstein, R.K.; Fine, E.J.; Westman, E.C.; Accurso, A.; Frassetto, L.; Gower, B.A.; McFarlane, S.I.; et al. Dietary carbohydrate restriction as the first approach in diabetes management: Critical review and evidence base. Nutrition 2015, 31, 1–13. [Google Scholar] [CrossRef] [Green Version]
  60. Marriott, B.P.; Hunt, K.J.; Malek, A.M.; Newman, J.C. Trends in Intake of Energy and Total Sugar from Sugar-Sweetened Beverages in the United States among Children and Adults, NHANES 2003–2016. Nutrients 2019, 11, 2004. [Google Scholar] [CrossRef] [Green Version]
  61. American Diabetes Association. 6. Glycemic Targets: Standards of Medical Care in Diabetes-2021. Diabetes Care 2021, 44 (Suppl. 1), S73–S84. [Google Scholar] [CrossRef]
  62. Piercy, K.L.; Troiano, R.P.; Ballard, R.M.; Carlson, S.A.; Fulton, J.E.; Galuska, D.A.; George, S.M.; Olson, R.D. The Physical Activity Guidelines for Americans. JAMA 2018, 320, 2020–2028. [Google Scholar] [CrossRef] [PubMed]
  63. Colberg, S.R.; Sigal, R.J.; Yardley, J.E.; Riddell, M.C.; Dunstan, D.W.; Dempsey, P.C.; Horton, E.S.; Castorino, K.; Tate, D.T. Physical Activity/Exercise and Diabetes: A Position Statement of the American Diabetes Association. Diabetes Care 2016, 39, 2065–2079. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Cuenca-García, M.; Jago, R.; Shield, J.P.H.; Burren, C.P. How does physical activity and fitness influence glycaemic control in young people with Type 1 diabetes? Diabet. Med. 2012, 29, e369–e376. [Google Scholar] [CrossRef]
  65. Aouadi, R.; Khalifa, R.; Aouidet, A.; Ben Mansour, A.; Ben Rayana, M.; Mdini, F.; Bahri, S.; Stratton, G. Aerobic training programs and glycemic control in diabetic children in relation to exercise frequency. J. Sports Med. Phys. Fit. 2011, 51, 393–400. [Google Scholar]
  66. Schweiger, B.; Klingensmith, G.; Snell-Bergeon, J.K. Physical Activity in Adolescent Females with Type 1 Diabetes. Int. J. Pediatr. 2010, 2010, 1–6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Ramalho, A.C.; Lima, M.D.L.; Nunes, F.; Cambuí, Z.; Barbosa, C.; Andrade, A.; Viana, A.; Martins, M.; Abrantes, V.; Aragão, C.; et al. The effect of resistance versus aerobic training on metabolic control in patients with type-1 diabetes mellitus. Diabetes Res. Clin. Pract. 2006, 72, 271–276. [Google Scholar] [CrossRef] [PubMed]
  68. Aman, J.; Skinner, T.C.; de Beaufort, C.E.; Swift, P.G.; Aanstoot, H.J.; Cameron, F. Associations between physical activity, sedentary behavior, and glycemic control in a large cohort of adolescents with type 1 diabetes: The Hvidoere Study Group on Childhood Diabetes. Pediatr. Diabetes 2009, 10, 234–239. [Google Scholar] [CrossRef]
  69. Ham, S.; Kruger, J.; Tudor-Locke, C. Participation by US Adults in Sports, Exercise, and Recreational Physical Activities. J. Phys. Act. Health 2009, 6, 6–14. [Google Scholar] [CrossRef]
  70. Crespo, C.J.; Keteyian, S.J.; Heath, G.W.; Sempos, C.T. Leisure-time physical activity among US adults. Results from the Third National Health and Nutrition Examination Survey. Arch. Intern. Med. 1996, 156, 93–98. [Google Scholar] [CrossRef]
  71. Zhao, G.; Ford, E.S.; Li, C.; Mokdad, A.H. Compliance with physical activity recommendations in US adults with diabetes. Diabet. Med. 2008, 25, 221–227. [Google Scholar] [CrossRef]
  72. Schmid, D.; Ricci, C.; Leitzmann, M.F. Associations of Objectively Assessed Physical Activity and Sedentary Time with All-Cause Mortality in US Adults: The NHANES Study. PLoS ONE 2015, 10, e0119591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Wolff-Hughes, D.L.; Fitzhugh, E.C.; Bassett, D.R.; Churilla, J.R. Total Activity Counts and Bouted Minutes of Moderate-To-Vigorous Physical Activity: Relationships with Cardiometabolic Biomarkers Using 2003–2006 NHANES. J. Phys. Act. Health 2015, 12, 694–700. [Google Scholar] [CrossRef]
  74. Loprinzi, P.D.; Sng, E. The effects of objectively measured sedentary behavior on all-cause mortality in a national sample of adults with diabetes. Prev. Med. 2016, 86, 55–57. [Google Scholar] [CrossRef]
  75. Boyer, W.R.; Wolff-Hughes, D.L.; Bassett, D.R.; Churilla, J.R.; Fitzhugh, E.C. Accelerometer-Derived Total Activity Counts, Bouted Minutes of Moderate to Vigorous Activity, and Insulin Resistance: NHANES 2003–2006. Prev. Chronic Dis. 2016, 13, E146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Zhao, G.; Li, C.; Ford, E.S.; Fulton, J.E.; Carlson, S.A.; Okoro, C.A.; Wen, X.J.; Balluz, L.S. Leisure-time aerobic physical activity, muscle-strengthening activity and mortality risks among US adults: The NHANES linked mortality study. Br. J. Sports Med. 2013, 48, 244–249. [Google Scholar] [CrossRef] [PubMed]
  77. McCarthy, O.; Deere, R.; Churm, R.; Dunseath, G.J.; Jones, C.; Eckstein, M.L.; Williams, D.M.; Hayes, J.; Pitt, J.; Bain, S.C.; et al. Extent and prevalence of post-exercise and nocturnal hypoglycemia following peri-exercise bolus insulin adjustments in individuals with type 1 diabetes. Nutr. Metab. Cardiovasc. Dis. 2021, 31, 227–236. [Google Scholar] [CrossRef]
  78. Notkin, G.T.; Kristensen, P.L.; Pedersen-Bjergaard, U.; Jensen, A.K.; Molsted, S. Reproducibility of Glucose Fluctuations Induced by Moderate Intensity Cycling Exercise in Persons with Type 1 Diabetes. J. Diabetes Res. 2021, 2021, 1–8. [Google Scholar] [CrossRef]
  79. Aljawarneh, Y.M.; Wardell, D.W.; Wood, G.L.; Rozmus, C.L. A Systematic Review of Physical Activity and Exercise on Physiological and Biochemical Outcomes in Children and Adolescents with Type 1 Diabetes. J. Nurs. Sch. 2019, 51, 337–345. [Google Scholar] [CrossRef] [PubMed]
  80. Aronson, R.; Brown, R.E.; Li, A.; Riddell, M.C. Optimal Insulin Correction Factor in Post–High-Intensity Exercise Hyperglycemia in Adults with Type 1 Diabetes: The FIT Study. Diabetes Care 2019, 42, 10–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  81. Riddell, M.C.; Zaharieva, D.P.; Tansey, M.; Tsalikian, E.; Admon, G.; Li, Z.; Kollman, C.; Beck, R.W. Individual glucose responses to prolonged moderate intensity aerobic exercise in adolescents with type 1 diabetes: The higher they start, the harder they fall. Pediatr. Diabetes 2018, 20, 99–106. [Google Scholar] [CrossRef] [Green Version]
  82. Martyn-Nemeth, P.; Quinn, L.; Penckofer, S.; Park, C.; Hofer, V.; Burke, L. Fear of hypoglycemia: Influence on glycemic variability and self-management behavior in young adults with type 1 diabetes. J. Diabetes Complicat. 2017, 31, 735–741. [Google Scholar] [CrossRef] [Green Version]
  83. Berkovic, M.C.; Bilic-Curcic, I.; La Grasta Sabolic, L.; Mrzljak, A.; Cigrovski, V. Fear of hypoglycemia, a game changer during physical activity in type 1 diabetes mellitus patients. World J. Diabetes 2021, 12, 569–577. [Google Scholar] [CrossRef]
  84. Temple, M.Y.M.; Bar-Or, O.; Riddell, M.C. The Reliability and Repeatability of the Blood Glucose Response to Prolonged Exercise in Adolescent Boys with IDDM. Diabetes Care 1995, 18, 326–332. [Google Scholar] [CrossRef]
  85. Ferguson, D.; Myers, N. Physical Fitness and Blood Glucose Influence Performance in IndyCar Racing. J. Strength Cond. Res. 2018, 32, 3193–3206. [Google Scholar] [CrossRef]
  86. Scott, S.N.; Cocks, M.; Andrews, R.C.; Narendran, P.; Purewal, T.S.; Cuthbertson, D.J.; Wagenmakers, A.J.M.; Shepherd, S.O. High-Intensity Interval Training Improves Aerobic Capacity Without a Detrimental Decline in Blood Glucose in People with Type 1 Diabetes. J. Clin. Endocrinol. Metab. 2018, 104, 604–612. [Google Scholar] [CrossRef] [PubMed]
  87. Chang, C.-K.; Borer, K.; Lin, P.-J. Low-Carbohydrate-High-Fat Diet: Can it Help Exercise Performance? J. Hum. Kinet. 2017, 56, 81–92. [Google Scholar] [CrossRef] [PubMed]
  88. Kanter, M. High-Quality Carbohydrates and Physical Performance: Expert Panel Report. Nutr. Today 2018, 53, 35–39. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Burke, L.M.; Castell, L.M.; Casa, D.J.; Close, G.L.; Costa, R.J.S.; Desbrow, B.; Halson, S.L.; Lis, D.M.; Melin, A.K.; Peeling, P.; et al. International Association of Athletics Federations Consensus Statement 2019: Nutrition for Athletics. Int. J. Sport Nutr. Exerc. Metab. 2019, 29, 73–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Eckstein, M.L.; McCarthy, O.; Tripolt, N.J.; Müller, A.; Birnbaumer, P.; Pferschy, P.N.; Hofmann, P.; Bracken, R.; Sourij, H.; Moser, O. Efficacy of Carbohydrate Supplementation Compared with Bolus Insulin Dose Reduction Around Exercise in Adults With Type 1 Diabetes: A Retrospective, Controlled Analysis. Can. J. Diabetes 2020, 44, 697–700. [Google Scholar] [CrossRef] [PubMed]
  91. Bell, K.J.; King, B.R.; Shafat, A.; Smart, C.E. The relationship between carbohydrate and the mealtime insulin dose in type 1 diabetes. J. Diabetes Complicat. 2015, 29, 1323–1329. [Google Scholar] [CrossRef]
  92. Bell, K.J.; Smart, C.E.; Steil, G.M.; Brand-Miller, J.; King, B.; Wolpert, H.A. Impact of Fat, Protein, and Glycemic Index on Postprandial Glucose Control in Type 1 Diabetes: Implications for Intensive Diabetes Management in the Continuous Glucose Monitoring Era. Diabetes Care 2015, 38, 1008–1015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Campbell, M.D.; Walker, M.; Ajjan, R.A.; Birch, K.M.; Gonzalez, J.T.; West, D.J. An additional bolus of rapid-acting insulin to normalise postprandial cardiovascular risk factors following a high-carbohydrate high-fat meal in patients with type 1 diabetes: A randomised controlled trial. Diabetes Vasc. Dis. Res. 2017, 14, 336–344. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Bozzetto, L.; Giorgini, M.; Alderisio, A.; Costagliola, L.; Giacco, A.; Riccardi, G.; Rivellese, A.A.; Annuzzi, G. Glycaemic load versus carbohydrate counting for insulin bolus calculation in patients with type 1 diabetes on insulin pump. Acta Diabetol. 2015, 52, 865–871. [Google Scholar] [CrossRef] [PubMed]
  95. Bell, K.J.; Barclay, A.W.; Petocz, P.; Colagiuri, S.; Brand-Miller, J.C. Efficacy of carbohydrate counting in type 1 diabetes: A systematic review and meta-analysis. Lancet Diabetes Endocrinol. 2014, 2, 133–140. [Google Scholar] [CrossRef]
  96. Brazeau, A.; Mircescu, H.; Desjardins, K.; Leroux, C.; Strychar, I.; Ekoé, J.; Rabasa-Lhoret, R. Carbohydrate counting accuracy and blood glucose variability in adults with type 1 diabetes. Diabetes Res. Clin. Pract. 2013, 99, 19–23. [Google Scholar] [CrossRef]
  97. Bell, K.J.; Fio, C.Z.; Twigg, S.; Duke, S.-A.; Fulcher, G.; Alexander, K.; McGill, M.; Wong, J.; Brand-Miller, J.; Steil, G.M. Amount and Type of Dietary Fat, Postprandial Glycemia, and Insulin Requirements in Type 1 Diabetes: A Randomized Within-Subject Trial. Diabetes Care 2019, 43, 59–66. [Google Scholar] [CrossRef] [Green Version]
  98. Seckold, R.; Fisher, E.; De Bock, M.; King, B.R.; Smart, C.E. The ups and downs of low-carbohydrate diets in the management of Type 1 diabetes: A review of clinical outcomes. Diabet. Med. 2018, 36, 326–334. [Google Scholar] [CrossRef]
  99. Nolan, J.; Rush, A.; Kaye, J. Glycaemic stability of a cyclist with Type 1 diabetes: 4011 km in 20 days on a ketogenic diet. Diabet. Med. 2019, 36, 1503–1507. [Google Scholar] [CrossRef] [PubMed]
  100. McSwiney, F.; Doyle, L.; Plews, D.J.; Zinn, C. Impact of Ketogenic Diet on Athletes: Current Insights. Open Access J. Sports Med. 2019, 10, 171–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  101. Heikura, I.; Burke, L.M.; Hawley, J.; Ross, M.L.; Garvican-Lewis, L.; Sharma, A.P.; McKay, A.K.A.; Leckey, J.J.; Welvaert, M.; McCall, L.; et al. A Short-Term Ketogenic Diet Impairs Markers of Bone Health in Response to Exercise. Front. Endocrinol. 2020, 10, 880. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  102. Mckay, A.K.A.; Peeling, P.; Pyne, D.B.; Welvaert, M.; Tee, N.; Leckey, J.J.; Sharma, A.P.; Ross, M.L.R.; Garvican-Lewis, L.A.; Swinkels, D.W.; et al. Chronic Adherence to a Ketogenic Diet Modifies Iron Metabolism in Elite Athletes. Med. Sci. Sports Exerc. 2019, 51, 548–555. [Google Scholar] [CrossRef]
  103. Krebs, J.D.; Strong, A.P.; Cresswell, P.; Reynolds, A.N.; Hanna, A.; Haeusler, S. A randomised trial of the feasibility of a low carbohydrate diet vs standard carbohydrate counting in adults with type 1 diabetes taking body weight into account. Asia Pac. J. Clin. Nutr. 2016, 25, 78–84. [Google Scholar] [PubMed]
  104. Yardley, J.E.; Iscoe, K.E.; Sigal, R.J.; Kenny, G.P.; Perkins, B.A.; Riddell, M.C. Insulin Pump Therapy Is Associated with Less Post-Exercise Hyperglycemia than Multiple Daily Injections: An Observational Study of Physically Active Type 1 Diabetes Patients. Diabetes Technol. Ther. 2013, 15, 84–88. [Google Scholar] [CrossRef] [PubMed]
  105. Valli, G.; Minnock, D.; Tarantino, G.; Neville, R.D. Delayed effect of different exercise modalities on glycaemic control in type 1 diabetes mellitus: A systematic review and meta-analysis. Nutr. Metab. Cardiovasc. Dis. 2021, 31, 705–716. [Google Scholar] [CrossRef] [PubMed]
  106. Eckstein, M.; Weilguni, B.; Tauschmann, M.; Zimmer, R.; Aziz, F.; Sourij, H.; Moser, O. Time in Range for Closed-Loop Systems versus Standard of Care during Physical Exercise in People with Type 1 Diabetes: A Systematic Review and Meta-Analysis. J. Clin. Med. 2021, 10, 2445. [Google Scholar] [CrossRef] [PubMed]
  107. Lehmann, V.; Zueger, T.; Zeder, A.; Scott, S.; Bally, L.; Laimer, M.; Stettler, C. Lower Daily Carbohydrate Intake Is Associated with Improved Glycemic Control in Adults with Type 1 Diabetes Using a Hybrid Closed-Loop System. Diabetes Care 2020, 43, 3102–3105. [Google Scholar] [CrossRef]
  108. Zhong, V.W.; Crandell, J.L.; Shay, C.M.; Gordon-Larsen, P.; Cole, S.R.; Juhaeri, J.; Kahkoska, A.R.; Maahs, D.M.; Seid, M.; Forlenza, G.P.; et al. Dietary intake and risk of non-severe hypoglycemia in adolescents with type 1 diabetes. J. Diabetes Its Complicat. 2017, 31, 1340–1347. [Google Scholar] [CrossRef]
  109. Brener, N.D.; Billy, J.O.; Grady, W.R. Assessment of factors affecting the validity of self-reported health-risk behavior among adolescents: Evidence from the scientific literature. J. Adolesc. Health 2003, 33, 436–457. [Google Scholar] [CrossRef] [Green Version]
  110. Orsini, N.; Bellocco, R.; Bottai, M.; Hagströmer, M.; Sjöström, M.; Pagano, M.; Wolk, A. Validity of self-reported total physical activity questionnaire among older women. Eur. J. Epidemiol. 2008, 23, 661–667. [Google Scholar] [CrossRef]
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Figure 1. Distribution of participants by age (a) and years living with type 1 diabetes (b).
Figure 1. Distribution of participants by age (a) and years living with type 1 diabetes (b).
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Figure 2. Distribution of participants by total hours per week spent doing all physical activities.
Figure 2. Distribution of participants by total hours per week spent doing all physical activities.
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Figure 3. Total physical activity time by recommended amount and association with log A1C values.
Figure 3. Total physical activity time by recommended amount and association with log A1C values.
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Figure 4. Number of days of physical activity per week and association with log A1C values.
Figure 4. Number of days of physical activity per week and association with log A1C values.
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Figure 5. Intensity of physical activity and association with log A1C values.
Figure 5. Intensity of physical activity and association with log A1C values.
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Figure 6. Participation in fitness activities, endurance sports, and endurance-power sports and association with log A1C values.
Figure 6. Participation in fitness activities, endurance sports, and endurance-power sports and association with log A1C values.
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Figure 7. Participation in power sports and outdoor activities and ingestion of carbohydrates for physical activity and association with log A1C values.
Figure 7. Participation in power sports and outdoor activities and ingestion of carbohydrates for physical activity and association with log A1C values.
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Figure 8. Use of CGM and physical activity-related low and high glucose and association with log A1C values.
Figure 8. Use of CGM and physical activity-related low and high glucose and association with log A1C values.
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Figure 9. Usual daily carbohydrate intake and association with log A1C values.
Figure 9. Usual daily carbohydrate intake and association with log A1C values.
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Figure 10. Percentages of usual daily carbohydrate intake by category.
Figure 10. Percentages of usual daily carbohydrate intake by category.
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Table
Table 1. Participant Characteristics and Survey Question Responses.
Table 1. Participant Characteristics and Survey Question Responses.
Characteristic or Survey QuestionNMeanMedianSEMinMax
Latest A1C (%)2206.66.60.14.210.5
Age (years)22042.14011384
Time with T1D (years)22021181180
Total weekly physical activity (minutes)22049836026302520
Total weekly physical activity (hours)2208.360.40.542
Days per week of physical activity (number)2205.250.127
Typical duration of physical activity (minutes) 2209375515720
Carbohydrate intake (1 = normal to 4 = very low)2202.120.114
Ingest carbs if glucose falls with activity (yes/no)2201.0710.021 (yes)2 (no)
Insulin pump use (yes/no)2201.410.031 (yes)2 (no)
Noninsulin diabetes medication use (yes/no)2201.8620.021 (yes)2 (no)
Statin use to lower blood cholesterol (yes/no)2201.7120.031 (yes)2 (no)
Self-monitor blood glucose (yes/no)2201.0510.021 (yes)2 (no)
Continuous glucose monitor use (yes/no)2201.2210.031 (yes)2 (no)
Fitness activities (yes/no)2201.1810.031 (yes)2 (no)
Endurance sports or training (yes/no)2201.2910.051 (yes)2 (no)
Endurance-power sports (yes/no)2201.7520.031 (yes)2 (no)
Power sports or training (yes/no)2201.8620.021 (yes)2 (no)
Outdoor recreational activities (yes/no)2201.5320.031 (yes)2 (no)
Exercise-induced low blood glucose (yes/no)2201.1310.021 (yes)2 (no)
Exercise-induced high blood glucose (yes/no)2201.3210.031 (yes)2 (no)
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Colberg, S.R.; Kannane, J.; Diawara, N. Physical Activity, Dietary Patterns, and Glycemic Management in Active Individuals with Type 1 Diabetes: An Online Survey. Int. J. Environ. Res. Public Health 2021, 18, 9332. https://doi.org/10.3390/ijerph18179332

AMA Style

Colberg SR, Kannane J, Diawara N. Physical Activity, Dietary Patterns, and Glycemic Management in Active Individuals with Type 1 Diabetes: An Online Survey. International Journal of Environmental Research and Public Health. 2021; 18(17):9332. https://doi.org/10.3390/ijerph18179332

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Colberg, Sheri R., Jihan Kannane, and Norou Diawara. 2021. "Physical Activity, Dietary Patterns, and Glycemic Management in Active Individuals with Type 1 Diabetes: An Online Survey" International Journal of Environmental Research and Public Health 18, no. 17: 9332. https://doi.org/10.3390/ijerph18179332

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