735078

research-article2017

NCPXXX10.1177/0884533617735078Nutrition in Clinical PracticeTillman and Opilla

Invited Review

Considerations for Fueling an Endurance Athlete With Home Parenteral Nutrition

Nutrition in Clinical Practice Volume XX Number X Month 201X 1­–7 © 2017 American Society for Parenteral and Enteral Nutrition https://doi.org/10.1177/0884533617735078 DOI: 10.1177/0884533617735078 journals.sagepub.com/home/ncp

Emma M. Tillman, PharmD, PhD, BCNSP1; and Marianne Opilla, RN, CNSC2

Abstract The goal of clinicians managing nutrition support for patients with home parenteral nutrition (HPN) is to adapt nutrition needs to best serve the consumers, so they may have the best quality of life despite specialized nutrition needs. Some HPN consumers may desire to participate in endurance athletics, which will require special considerations. This review is intended to outline key nutrition differences in endurance athletes that a nutrition support team should consider when providing HPN. (Nutr Clin Pract. XXXX;xx:xx-xx)

Keywords parenteral nutrition; athletes; exercise; quality of life

Parenteral nutrition (PN) is commonly used in hospitals to provide supplemental or total nutrition support to patients who are unable to maintain nutrition status via the oral or enteral route.1,2 Central venous access techniques were refined in the late 1960s, and long-term PN administration became a reality in the home setting.3 Although there is an estimation of approximately 33,000 home PN (HPN) patients in the United States, the actual statistic is unknown.4 While HPN offers patients independence to live a more normal life outside the hospital, it is a high-risk and complex therapy that is associated with both immediate and long-term complications.5,6 Clinicians caring for patients with HPN are often challenged with how to best support HPN patients living an active and healthy lifestyle while reducing the risk for complications. Typically, nutrition support is first initiated while patients are acutely ill and, most often, in the hospital. As the patients’ health improves, nutrition support teams are challenged with providing nutrition support for patients as they transition back to a healthy lifestyle. Exercise is important for physical as well as psychological well-being.7 Although the benefits of exercise are not in debate, there may be a reluctance to participate in preillness sports or gym classes over concerns about securing and covering tubing or fear of damage to the central venous catheter (CVC). After discussing with their physician, many HPN patients are able to modify exercise to meet their needs and enjoy activities such as organized athletics, dance, and hiking. The amount of time and intensity of exercise that HPN consumers participate in will have a great impact on nutrition needs. To discuss these needs, it is important to define these levels of intensity. For the purpose of this review, we will use categories previously defined with regard to carbohydrate intake in athletes.8 Light exercise would include low-impact, low-intensity, skills-based activities for less than each hour each; moderate exercise would include moderate-intensity

activities for approximately 1 hour each day. High-intensity activity would include an endurance program with moderateto high-intensity exercise for 1–3 hours each day, and very high-intensity exercise would be defined as moderate- to highintensity exercise for 4 or more hours per day. Prior to beginning or resuming an exercise regimen, the patient’s overall heath and weight should be evaluated and the patient’s physician or medical team should provide approval. It is important to begin with light to moderate exercise and allow for a gradual buildup to high-intensity or very high-intensity activity if that is the goal. As intensity is increased, weight and body composition should be carefully monitored and calories should be adjusted accordingly. In a case study, Tillman et al9 reported the strategies employed by an HPN patient to prepare for returning to marathon running. Her strong desire to run again motivated her to closely and scientifically evaluate her endurance, hydration status, urine output, muscle soreness, and postrace fatigue to proactively prepare for adequate intravenous (IV) fluids before and after the race. She was able to successfully complete the 26.2 miles with the assistance of her pharmacy team on the sidelines. To date, this is the only published report discussing the challenges and considerations for PN patients participating in From 1Riley Hospital for Children at Indiana University Health, Indianapolis, Indiana, USA; and 2Nutrishare, Elk Grove, California, USA. Financial disclosure: None declared. Conflicts of interest: None declared. Corresponding Author: Emma M. Tillman, PharmD, PhD, BCNSP, Pharmacy Department, Riley Hospital for Children at Indiana University Health, 705 Riley Hospital Drive, Indianapolis, IN 46202, USA. Email: [email protected]

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Nutrition in Clinical Practice XX(X)

Table 1.  Nutrition Provisions Based on Exercise Intensity.8,13,30,32,46,47 Intensity Light exercise (low-impact, lowintensity, skills-based activities) Moderate exercise (moderateintensity activities) High intensity (moderate- to high-intensity exercise) Very high intensity (moderate- to high-intensity exercise)

Activity Duration

Examples

Calories, kcal/ kg/d

Dextrose, g/kg/d

Protein, g/kg/d 0.8–1

2 weeks, HPN calories should be adjusted based on weight and any change in exercise intensity. Refer to Table 1 for detailed nutrition requirements based on exercise intensity.

Carbohydrate It is now widely accepted that providing energy as carbohydrate prior to and during endurance exercise can improve endurance capacity and increase performance in exercise lasting >2 hours.14 Although the importance of carbohydrate fueling for the endurance athlete is now almost common knowledge, the science behind this has culminated over the past century. Early studies comparing a diet high in carbohydrate with a diet high in fat showed that athletes consuming a high-carbohydrate diet experienced greater ease with exercise and higher respiratory exchange ratios than when they consumed high-fat diets.15 Based on these studies, scientists studied runners in the 1923 Boston Marathon and found that most runners had low postrace blood glucose concentrations, and the investigators hypothesized that the runner’s hypoglycemia was resulting in increased fatigue and decreased athletic

Tillman and Opilla performance. The following year, athletes were supplement with carbohydrate during the race, and both hypoglycemia and running performance improved.16 It was not until the 1960s that the use of muscle biopsy identified the role of glycogen stores in the muscle.17,18 This led to studies that showed a high-carbohydrate diet led to higher glycogen stores and improved exercise performance.17,18 As investigators began to better understand the importance of carbohydrates as part of the diet to promote glycogen stores, the focus of research shifted to the study of the effects of consuming carbohydrates during exercise.19,20 In the past 30 years, numerous studies have been conducted to evaluate carbohydrate as a part of diet and during endurance exercise (mainly cycling or running), and most have resulted in carbohydrate having a positive impact on athletic performance.14 Studies have not shown dramatic differences in performance when athletes were supplemented with 16–75 g of carbohydrate per hour.21–24 It is possible that carbohydrate bioavailability during exercise may be limited to 40 g per hour; thereby, supplementing with higher amounts of carbohydrate would not lead to increased performance.21 It is clear that consuming even small amounts of carbohydrate (16 g per hour) can improve exercise performance, but the optimal dose and timing are still under investigation. Emerging evidence also suggests that a mouth rinse with a carbohydrate-containing fluid has greater effects on athletic performance compared with a non-carbohydrate-containing mouth rinse.25–27 In an athlete who is unable to retain enteral nutrition (EN), it may be beneficial to have the athlete take a drink of a carbohydratecontaining liquid and swish and spit out the liquid. While carbohydrate intake is important for all athletes, the amount and timing of carbohydrate will vary greatly depending on intensity of athletic training. In addition to difference in daily fueling, athletes who engage in moderate-intensity to very high-intensity training should consider amount of carbohydrate prior to activity, during activity, and after activity to achieve maximal performance and ideal recovery. This careful consideration of timing and amount of carbohydrate is not necessary in those engaging in light to moderate activity. If an athlete plans to participate in an athletic event lasting >90 minutes, he or she may benefit from larger glycogen stores.28 This enhanced glycogen storage can be achieved by the athlete consuming 10–12 g/kg/d of carbohydrate for 36–48 hours prior to the event.8 Approximately 1–4 hours prior to the event, the athlete should consume 1–4 g/kg of carbohydrate.8 It is recommended that in activity 3 hours, an athlete should supplement with up to 90 g of carbohydrate per hour of activity.8

3 The ability to quickly and sufficiently consume sufficient amounts of carbohydrate during prolonged activity can be very problematic for an athlete reliant on HPN. The HPN athlete may be able to supplement with an enteral postworkout snack, but some athletes may be solely reliant on HPN; therefore, timing of the workout and HPN infusion should be carefully coordinated for optimal recovery.

Protein Protein has multiple functions; it is essential for cell structure, maturation, remodeling, and growth. Besides being used for energy, amino acids and proteins serve as precursors that are essential for many biological processes.29 The ASPEN guidelines for PN and EN in adult and pediatric patients recommend that a nonstressed patient should sufficiently maintain a positive nitrogen balance with a daily protein intake of 0.8 g/ kg/d, but doses upward of 2 g/kg/d may be necessary to provide a positive nitrogen balance in highly stressed catabolic patients.1 Protein needs can vary greatly among athletes. In endurance athletes, most of the athletes’ energy will be fueled by carbohydrates and fat,30 yet it is also important to supply sufficient amounts of protein for maintenance and repair of muscles. Protein plays a unique role in fueling an endurance athlete as protein is important for the synthesis of aerobic enzymes, building capillaries around muscles, amplifying mitochondrial biogenesis, and synthesizing connective tissue.31 In addition, in the endurance athlete, there may be increased protein synthesis for repair of damaged muscles, tendons, and ligaments due to periods of intense or sustained training.31 Similar to hospitalized patients, protein needs in athletes may vary greatly depending on the daily time spent training, training intensity, and overall fitness level. In order to make sense and general recommendations for protein requirements, athletes are characterized based on intensity and type of activity.30 Protein requirements for resistance training athletes who aim to achieve a lean body composition with high muscle mass will differ greatly from athletes participating in endurance exercise.32 For the purpose of this review, we focus just on protein in endurance sports. Several historic studies have demonstrated that athletes participating in recreational or low-intensity to moderate-intensity endurance exercise show no negative effect on total body protein or amino acids. As long as caloric intake is sufficient, there is an increased utilization of amino acids.33–37 In a study of young men with low to moderate physical exercise (2 sessions of 90 minutes per session at 50% of VO2MAX per day) consuming 1 g/kg/d of protein, achieved a positive nitrogen balance measured by a 24-hour leucine tracer study.38 In modestly trained athletes or those training 4–5 days per week for >1 hour, protein requirements may be increased by 20%–25%.39–41 In a study of middle-aged men consuming dietary protein at 3 amounts (0.61, 0.92, and 1.21 g/kg/d), no difference in nitrogen balance with the 3 protein doses was

4 found.41 Alternatively, a study in men and women endurance athletes consuming the Canadian recommended daily protein intake of 0.86 g/kg/d for 10 days had a negative nitrogen balance.39 In addition, a study of male and female athletes consuming 1 g/kg/d of protein during moderate training resulted in a negative nitrogen balance.40 Collectively, these studies suggest that providing the recommended dietary allowance of protein will not be sufficient in athletes training at a moderate intensity. As training intensity increases to the elite level with athletes training at a high intensity for several hours per day most days per week, protein requirements will also be increased. In elite cyclists, such as those competing in the Tour de France, protein requirements have been estimated at 1.5–1.8 g/kg/d to maintain a positive nitrogen balance.42 There are few data evaluating the effects of protein supplementation during endurance exercise, but the consensus is that when adequate carbohydrate is supplemented, adding protein does not enhance performance.32 Consuming additional protein after periods of intense endurance exercise, however, may suppress the rise in plasma proteins linked to myofibrillar damage and reduce the feeling of muscle fatigue and soreness.32 When considering protein dose for an HPN athlete, the amount of training and intensity should be considered.

Fat Fat is a necessary part of all diets but is 1 macronutrient that is often restricted by athletes seeking to lose weight or reduce the percentage of total body fat.43 Conversely, some emerging evidence suggests that low-carbohydrate, high-fat (LCHF) diets can induce metabolic changes that may enhance endurance performance.44 Athletes consuming this LCHF diet can reach the maximal fat oxidation rate of approximately 1.5 g per minute, with a lower carbohydrate oxidation rate and similar muscle glycogen content and resynthesis rate compared with those consuming high-carbohydrate, low-fat (HCLF) diets, yet this adaptation may take several months for an athlete to see the benefit.44 Although the adaption that the body can make in response to low-carbohydrate fueling is interesting and may be useful for some athletes, there are not strong data to support this strategy for improved athletic performance in most endurance athletes.45 It is recommended that endurance athletes consume 20%–35% of total dietary calories as fat.46

Hydration Hydration is often a challenge in patients with intestinal failure (IF) because of increased gastrointestinal (GI) losses and the inability to tolerate enteral hydration. Hydration is significantly more challenging in athletic patients, in whom GI losses may be increased, and exercise may increase fluid loss by sweat and insensible losses due to increased CO2 consumption. Even seasoned athletes without significant health problems may struggle

Nutrition in Clinical Practice XX(X) with hydration in the face of vigorous and/or long durations of exercise with varying hydration. As little as a 1% decrease in body weight due to fluid losses can put unnecessary stress on the cardiovascular system.47 This will not only hinder athletic performance but also put an athlete at risk for serious adverse events. As fluid losses increase, the risk of stress on the athlete also increases. Conversely, overhydration can also put undue stress on an athlete and lead to hyponatremia.48 The International Marathon Medical Directors Association has developed guidelines for fluid replacement during endurance running.49 Sweat rate during endurance running is used to determine a hydration strategy.49 This strategy was used and presented in a case report of a consumer who desired to run a marathon with parenteral hydration. To calculate sweat rate and estimate hydration volume needed during the marathon, the consumer was instructed to record weights (pre/post run), ambient temperature, running distance, and duration of time during her marathon training.9 Based on sweat rate calculations during training runs, ambient temperature was a significant factor influencing sweat rate, and this was used to predict hydration needs during the marathon, with sweat rate (x) plotted against temperature (y), which resulted in a slope of y = 0.0406x + 34.291. The estimated temperature for the marathon was 65°F; therefore, the athlete would have an estimated sweat rate of approximately 750 mL/h.9 While this technique is labor intensive and requires an athlete to be very vigilant, this is an excellent technique to use to estimate fluid requirements and fluid replacements after the workout.

Timing and Type of Nutrition Timing of nutrition is very important in relation to exercise. Athletes typically schedule snacks and meals around workout and training sessions. In the athlete receiving HPN, this may be a challenge. Depending on the amount of EN an athlete can tolerate, the majority of nutrition may be provided via HPN, and this is typically provided as a once-daily continuous infusion cycled over 8–24 hours per day. The advantage of a long cycle duration is that patients will receive continuous nutrition to fuel exercise throughout the day. However, this strategy is not appealing to many HPN patients because this would necessitate being connected to IV tubing and carrying a bag with hydration, pump, and PN, which could greatly hinder mobility, range of motion, and comfort during exercise. Timing of PN infusion with regard to time of day and workout time could be very important. Typically, HPN patients will infuse PN overnight while asleep. This norm is due to convenience, as many patients do not want to carry their PN around during the day. Many patients work in a setting where coworkers are unaware of PN dependence and choose not to share this part of their life with others. While there are currently no published studies evaluating PN infusion during the day compared with nocturnal PN, anecdotal reports from patients suggest that they have more energy when they infuse PN during the day, but

Tillman and Opilla this has not been scientifically evaluated. Physiologically, it would make sense that a patient would have a sense of increased energy when receiving continuous hydration and nutrients compared with a long period of fasting. During the day while awake, the patient would be consuming more energy compared with fueling up at night while sleeping. Athletes consuming a typical enteral diet will consume a variety of foods to achieve a balanced diet. Some athletes may also supplement with sports drinks, gels, and bars and the addition protein supplements to achieve goal nutrition.13 One might wonder if providing an athlete’s goal nutrition substrate via PN would be equal to fueling with a caloric-equivalent and nutrient-equivalent enteral omnivorous diet comprising fruit, vegetables, meat, and dairy. Although no studies have evaluated athletic performance in athletes receiving PN compared with a standard diet, some studies have evaluated performance associated with a vegetarian diet. A systematic review concluded that consuming a vegetarian diet did not improve or hinder athletic performance compared with an omnivorous diet.50 These data would suggest that providing adequate protein, carbohydrate, fat, electrolytes, fluids, minerals and vitamins, and calories regardless of the food origin would have equal results on athletic performance.

Monitoring for Athletes With HPN Weight can be a valuable tool in monitoring both fluid balance and lean body mass. Many patients with IF struggle maintaining adequate hydration status in addition to nutrition. Athletes who require parenteral hydration may benefit from weighing themselves prior to and after a workout. The weight difference can then be interpreted to estimate the amount of fluid volume that should be supplemented to return to baseline hydration status. Careful attention should be paid to changes in urine output, stool output, and sweat rate that could also affect hydration status. All HPN consumers benefit from having a set monitoring plan that should be incorporated into the HPN care plan.51 The HPN athlete’s monitoring plan should be targeted toward potential complications that could result from endurance exercise. It is recommended that standard biochemical and anthropometric measurements be closely monitored until stable and then may be spaced to less frequent monitoring.51 Monitoring of trace elements and vitamins should be completed at intervals of 6–12 months.52,53 There is some debate on the effects of supplemental dietary antioxidants on athletic performance. Some data suggest that N-acetylcysteine may improve performance and decrease muscle fatigue.54 These supplements may have some short-term benefits on performance, but chronic antioxidant supplementation may have a harmful overall effect on athletic performance.54 It is not recommended to provide more than standard multivitamins in HPN for athletes. Iron studies should also be assessed every 6–12 months in HPN patients, but this may need to be addressed more frequently in endurance athletes. The ACSM, Academy of

5 Nutrition and Dietetics, and DC recommend iron supplementation to prevent anemia, bone mineral density loss, immunosuppression, and other symptoms that could hinder athletic performance.55 Athletes with HPN may require IV iron supplementation more frequently than HPN patients not engaged in athletics. Bone mineral density assessment is recommended at baseline and periodic intervals thereafter for standard HPN patients, but this may need to be monitored more frequently in athletes if complications arise.1,52 Daily assessments of CVC function and CVC site should also be completed by the HPN athlete.51

Injuries and Potential Complications Suboptimal nutrition can make any athlete vulnerable to injury. The athlete unable to maintain adequate nutrition via an enteral route is reliant on PN and is at especially high risk for nutrition-related injury; these may include muscular skeletal injuries such as muscle strains, tears, and tendon rupture. In addition, if an HPN patient recklessly engages in endurance athletics without proper planning for hydration, he or she may have dehydration that could also result in electrolyte abnormalities, rhabdomyolysis, cardiovascular collapse, and even death.56–59 In addition to athletic-related injuries and complications, athletes receiving HPN will have a CVC. Athletes may have increased sweating, requiring more frequent dressing changes. The actual CVC may undergo more friction or stress due to repetitive movements depending on the placement of the CVC. The actual type of CVC and exit site location should be extensively discussed with an athlete receiving HPN. A single-lumen tunneled CVC is preferred for HPN and should be recommended for all HPN patients unless multiple therapies that are not compatible with coinfusion dictate additional lumens.60,61 Single-lumen CVCs have been shown to have a lower risk of infection, thrombus, and occlusion compared with multilumen CVCs. Multilumen CVCs will have a larger overall diameter, increasing the risk of thrombus, and each lumen diameter will be smaller, increasing the risk of luminal occlusion.61 Because type of CVC device may affect quality of life, the patient and/ or caregiver should be included in determining selection of the most appropriate device. Peripherally inserted central catheters are appropriate for HPN62 but would likely not be the best choice for an athlete due to the location, the lack of a Dacron cuff in a patient prone to increased sweating, and soiling of the dressing. Infusion ports may also be considered for HPN in certain patient populations. Those with a very active lifestyle or only on HPN 2–5 days per week are most appropriate. The need to access with a noncoring needle may require home health nursing indefinitely, unless the patient can learn to self-access. Infusion ports generally last 3–5 years depending on access frequency and septum viability. This type of CVC may be preferred in an athlete, but the risk of infection should be carefully

6 weighed against the aesthetic preference and flexibility of the HPN consumer. The type and intensity of athletics should be strongly considered when determining the most appropriate type of CVC for each patient. Swimming with a CVC is controversial among HPN patients, patients’ parents, and the healthcare team. Generally, immersion of the CVC in any body of water is not advised due to the potential risk of site or bloodstream infection, although there is scarce, if any, research to confirm the actual risk. In an effort to answer this quality-of-life question, Miller et al63 conducted a literature search and identified 45 articles on swimming, bodies of water, and bacteria counts in recreational water. In addition, 25 HPN programs were contacted about swimming recommendations. They concluded that a firm decision on the safety of swimming with a CVC could not be made due to the limited research available and lack of consensus among programs. HPN patients should use caution and carefully weigh the risk vs benefit of this activity with their medical team. Effort should be made to protect the CVC with waterproof covers and perform a dressing change immediately if the CVC site becomes wet. In patients who wish to swim, an infusion port may be preferred as this type of CVC can easily be deaccessed and therefore, although theoretically unproven, should have a lower infection risk compared with a tunneled CVC. In contrast, an infusion port would not be a desired CVC for patients requiring IV hydration and/or nutrition during activity. Ports can easily become de-accessed or dislodged during activity, and excessive sweating around the Huber needle could increase bacterial flora on the skin to contaminate the port.

Conclusions Endurance athletes who are not able to maintain their weight and nutrition status via an enteral route due to underlying GI disease necessitate careful consideration and management. Athletes will have higher caloric requirements compared with nonathletes. Doses of protein, carbohydrate, and fat should be adjusted based on the athletes’ training and athletic performance. Athletes and clinicians should be very diligent with fluid and electrolyte management to prevent complications. While not every HPN consumer will participate in endurance athletics, many of the considerations discussed in this review can be applied to HPN consumers who strive to live an active life.

Statement of Authorship E. Tillman and M. Opilla contributed to the conception/design of this manuscript, participated in the analysis or interpretation of published data to formulate this review, drafted the manuscript, critically revised the manuscript, agree to be fully accountable for ensuring the integrity and accuracy of the work, and authors read and approved the final manuscript.

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Considerations for Fueling an Endurance Athlete With Home Parenteral Nutrition.

The goal of clinicians managing nutrition support for patients with home parenteral nutrition (HPN) is to adapt nutrition needs to best serve the cons...
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