http://t-nation.com/readTopic.do?id=659666
The Top 10 Post Workout Nutrition Myths
by Dave Barr
The Revolution has come, are you ready?
The world of strength training is obviously full of contradiction and confusion. Just pick up any standard bodybuilding magazine and you’ll see different people with drastically diverse views, all telling you that they have the one method to help you achieve your goals. But through all of this crap, every now and then we find certain principles that we can take to the grave and apply universally.
Examples include: "lift heavy weights and you’ll get big," "cardio helps with weight loss," and "Canadian men are hung like moose."
Another such principle is the post workout nutrient window, which states that during the time immediately post workout, our bodies are in a state of shock and physical disarray, resulting in an opportunity for enhanced nutrient absorption and accelerated recovery. In fact, it’s pretty safe to say that since its inception a decade ago, this scientifically "proven" idea has revolutionized the way we look at nutrition.
Unfortunately, this principle has become so engrained in our subculture that much of it has mutated and become dogmatic in scope. While the general principles remain, many of the studies on which they are based were done on populations that aren’t completely applicable to us, such as animals or endurance athletes.
Despite the emergence of new, more applicable science, we’ve had a very difficult time in adapting our thinking to these current and better-suited ideas.
Making the situation worse is the fact that everyone seems to have their own input about what post workout nutrition should be! This stems from what I like to call the "telephone-chain effect" (derived from the lesson-yielding children’s game), which illustrates how easily messages can change when passed through a chain of people.
How it works is that one person will dictate something to another, who in turn tells this same information to someone else, who then repeats it to another, and so on. By human nature, each person will subtly alter the message, by leaving out some parts, embellishing others, etc. to the extent that by the time you get to the tenth person, the original statement of "Hey sugar, could you mop up the mess in the pantry with the Swiffer?" becomes warped to something like "Shugart is a messed up panty sniffer."
True as it may be, obviously the point of the latter statement does not even remotely resemble the original.
But since this article is not entitled "The Top Ten Things Wrong With Our Post Workout Information," let’s get to the myths that have developed, and the current reality.
1. Replenishing Glycogen Needs to be a Focus of PWO.
I’m not just suggesting that glycogen resynthesis is not important following exercise, I’m flat out saying that for strength training it’s not even a concern! This is because it’s just really easy to get our glycogen levels back up, and timing is generally not an issue.
Although one study showed that following endurance exercise, glycogen levels were replenished more rapidly when carbohydrates were consumed shortly after the exercise (Ivy, 1988), this is really of little concern to most of us. Unless we’re subscribers to Runners World, athletes in competition, or doing 2 a day workouts, why do we care so much about rapid glycogen restoration? After all, we’re mostly concerned with muscle growth, fat loss, and getting stronger.
The most common argument is that the subsequent cellular hydration and swelling will have an anticatabolic effect on muscle. I don’t believe that this is possible because cellular hydration to the extent that we get with creatine supplementation has little effect on muscle protein synthesis or breakdown in healthy men or women (Louis et al., 2003).
Then there’s the suggestion that if we don’t replenish post exercise glycogen right away, we’ll miss a window of opportunity to do so. This is largely hyperbole, exploded from bits and pieces of endurance training studies, and a perfect example of the telephone game effect.
Surprisingly, one study showed that consuming carbohydrates after strength training only increased muscle glycogen by 16% more than when water was consumed (Pascoe et al., 1993)! With this information and the huge amount of carbs that we consume on a daily basis, we should have little doubt that glycogen levels will be maximized within 24 hours of the workout.
Now these may be irrelevant points, because in the effort of keeping our focus where it ought to lie—on maximizing protein synthesis— we’re going to quickly stimulate our glycogen restoration anyway. This is because we consume rapidly absorbed carbohydrates along with our protein and amino acids, which has been shown to enhance muscle protein anabolism (Rasmussen et al., 2000).
In other words, muscle glycogen will be restored whether we make it a priority or not. This way, even those who can’t escape the dogma of having to rapidly restore glycogen get their fix, while at the same time, unknowingly assisting with muscle protein recovery.
2. Pre workout Nutrition will divert blood flow away from muscles during the workout.
One of a plethora of excuses made in an attempt to resist preworkout nutrition; this myth actually makes a lot of sense…until you become familiar with the physiology of hormones. Looking deeper, we can find that the insulin stimulated by food intake, actually enhances blood flow and subsequent nutrient delivery to muscles (Coggins et al., 2001).
Applying this principle, liquid pre workout meal consumption dramatically increases muscle blood flow and protein synthesis (Tipton et al., 2001). This elevation in muscle growth is at least twice that observed with the same drink taken post workout (Tipton et al., 2001)! In fact, this effect even lasts for an hour after the workout, so it’s like having 2 drinks for the price of 1! If you want more detail on this topic check out the article on Arginine blood flow stimulators.
Fortunately, early resistance to this research is falling by the wayside, and people are finally starting to reap the benefits that this practice has to offer. While "pre workout nutrition" just doesn’t sound as sexy as "post workout nutrition," actually doubling our muscle growth should seem pretty damn sexy to everyone!
3. The post workout meal is the most important meal of the day.
I have to admit that with all the hype on post-workout meals over the past few years, I got tangled up in this myth, too. Realistically though, as great as they are, a single post-workout meal will have minimal impact compared to what can happen if your nutrition is completely optimized. Of course it’s heresy to say that these days, but that’s a result of the myth building on itself more than any factual data. For example, as discussed in the myth #2, pre-workout meals can be 200% more effective for stimulating muscle growth compared to post-workout (Tipton et al., 2001).
Perhaps even more important than the pre-workout meal is the old standard: breakfast. No this article isn’t part of a conspiracy by MABB (Mom’s Against Bad Breakfasts) to promote the importance of this meal. Just think about it: being essentially fasted for 8-10 hours is incredibly destructive for muscle -yes even if you eat cottage cheese before bed.
This is especially true in trained individuals like us, because we have higher rates of muscle breakdown (Phillips et al. 2002) The faster we can stop this catabolism once we wake up, the better. In fact, one could even argue that the amount of muscle protein spared from this first meal would be equal to, or even greater, than that gained by a post workout meal.
Also, consuming a high quality slow protein before bed, like Low-Carb Grow! with micellar casein, will largely mitigate the catabolic effect induced by nocturnal fasting. Taking this one step further, nighttime eating will actually put your muscle into anabolic overdrive, by supplying even more amino acids to stimulate this metabolic process.
Finally, a second post workout meal can be even better for protein synthesis than the first, but I’ll get to that one in a bit.
Mini-Summary: Nocturnal feedings, breakfast, preworkout meals, and multiple post workout meals can be more beneficial for muscle growth than a single post workout meal.
4. There’s a one-hour window of opportunity for protein synthesis following a workout.
You may be wondering: is this a myth because the real window is half an hour? Two or 3 hours? Maybe 6 hours? Sadly, in the past 2 weeks I’ve read different articles, all suggesting that the "window" is one of the above lengths of time.
It’s not surprising that with this type of inconsistency that this is probably the most pervasive myth in bodybuilding today! Worse yet, it stems directly from the scientific research itself. The most often cited research on the protein synthetic post workout window, used elderly subjects (Esmark et al., 2001) and cardio exercise findings (Levenhagen et al., 2001) to make their predictions. While this is a completely acceptable practice when these are the only data we have to go on, there are a couple noteworthy problems.
Elderly individuals digest and absorb protein differently than healthy adults. In fact, they digest and absorb whey protein in a similar manner as they do casein (Dangin et al., 2003); in other words they have slow digestion and absorption for whey. Elderly also benefit from having 80% of their daily protein consumed at a single sitting (Arnal et al., 1999), in contrast to the benefits of our multiple feedings.
Additionally, the traditionally referenced Esmark et al. (2001), study showed that consuming the post workout meal just 2 hours after working out actually prevented any improvements induced by the training! Figure that one out and you get a prize.
Secondly, with regards to cardio…well, let’s just say that there’s an obvious difference between how our muscles respond to the two forms of exercise. Bear in mind that with regard to carbohydrate metabolism following a workout, there might not be much of a difference—we just don’t know, but certainly the long-term protein metabolism differences can be seen.
So now what are we supposed to base our nutrition on? Enter the most underrated scientific paper in the last 5 years. Tipton and colleagues (2003) examined responsiveness of protein synthesis for a day after a workout, and found it to reflect a 24 hour enhanced level. That’s right folks, a FULL DAY! This means that having a morning shake will have the same impact on muscle protein synthesis as one consumed following the workout!
These results shouldn’t be too surprising because we’ve known for over a decade that postworkout protein synthesis is jacked up for this long (MacDougall et al., 1995), but if you’re discovering this for the first time, then it’s pretty exciting!
Some research suggests that even 48 hours after the workout our protein synthesis levels can be elevated by ~33% (Phillips et al., 1997), giving us an even longer period during which we can maximize our muscle growth with protein drinks.
Strike one for the one hour post workout window.
5. Consuming the drink immediately following the workout will elicit the greatest protein synthesis.
It’s amazing to see how more advanced, and often experienced, people behave in the gym when it comes to getting their post workout meal. Some guys even sit there, right after their last set, and slug back a drink! In fact I’ve even heard "as soon as the weight hits the floor" touted as the war cry for the hardcore. While this is actually a sub-optimal practice for muscle growth and recovery, not to mention borderline obsessive compulsive, it’s good to see their heart is the right place.
Comparing research that used drinks consumed immediately after a workout (Tipton et al., 2001) versus those ingested an hour after training (Rasmussen et al., 2000), the results are surprising: it seems that post workout meal ingestion actually results in 30% lower protein synthesis rates than when we wait! So every time we thought that we were badass for drinking "as soon as the weight hit the floor, we were actually short changing ourselves. Not a big deal, that’s why we read T-Nation. Let’s just learn, adapt, and move on.
Strike two for the one hour post workout window.
6. The best meal to consume following a post workout meal is a good SOLID meal.
This is where we can start to apply some of the novel information presented above. While we know that our post workout window (is it really even a window any more? 24 hours is more like a giant garage door) lasts for at least 24 hours, we can’t assume that the responses to repeated meals will all be the same.
This is where research by Borsheim and pals (2002) comes in. This landmark research shows that the best thing to consume after our post workout meal is… another protein shake! In fact, if we time it right, we’ll get the same huge increase in protein synthesis. Talk about a double whammy for our muscle growth! Now considering how crazy people get when it comes to a single post workout meal, imagine how they’ll react when you tell them that they can double that effect!
Also, for those who have a hard time accepting the reality explained in myth #5, you’ll get an even bigger response from the second drink, compared to what you get from the first.
7. Insulin sensitivity is enhanced for an hour following a resistance training bout.
The term insulin sensitivity gets thrown around in the strength-training world, as only the most vague of concepts. From here on, lets universally define it as: the inverse of the quantity of insulin required for an effect of a given magnitude. In other words, high insulin sensitivity requires low levels of insulin to do the job. Make sense? Now that we have a working definition, we need to destroy the myth of the one-hour post workout window once and for all!
We know that both endurance exercise and strength training will enhance insulin sensitivity in the long term. This is a good thing. Unfortunately, with all of the hype surrounding the post workout window, people have started throwing out numbers related to how long insulin sensitivity is altered. While we know that heavily damaging eccentric exercise will actually reduce insulin sensitivity (Asp et al., 1996), this should be an extreme condition and not our regular response. So if you’ve overdone it a bit, back off and heal up!
The more common response to strength training is an increase in insulin sensitivity (Fujitani et al., 1998; Miller et al, 1984), and brand new data show even the acute effect from a single bout lasts for over 24 hours (Koopman et al., 2005). So while we’ll have an enhanced whole body insulin sensitivity following resistance training, this effect is even greater for 24 hours following exercise!
Steeerike THREE for the one hour post workout window!
8. Whey is a "fast" protein, ideal for post workout.
Back when it first came out, whey protein was pretty kick ass because it was discovered to be very high quality. Then research came out that made it even more kick ass, because we could classify it as a "fast" digesting protein compared to casein (Boirie et al., 1997).
You know what? This research stands today, because compared to casein, whey protein really is fast! Then again, a tortoise is also fast compared to a snail, but that doesn’t mean we want to take a tortoise to a greyhound park. In other words, we’ve been considering whey a "fast" protein only because we’ve been comparing it to something incredibly slow. When we compare the digestibility of whey to the gold standard of amino acids, on which we base nearly all of our post workout nutritional data, whey flat out sucks.
This is incredibly frustrating because all of the ways to maximize protein synthesis we’ve been discussing have used amino acids. So we need to either use pure amino acids or use something that closely resembles their absorptive properties. This is where whey protein hydrolysate comes in. The protein is already broken up into large peptides, so we get a rapid absorption with peak levels reaching the blood at around 80 minutes (Calbet and MacLean, 2002), compared to 60 minutes for pharmaceutical grade amino acids (Borsheim et al., 2002).
Unfortunately, even the highly touted whey isolate is completely useless for our timing purposes here, because it just takes too long to get taken up by the gut (Dangin et al., 2002). This is all discussed in more detail in the official product review of Surge, complete with graphs of blood amino acid profiles: [Link niet meer beschikbaar]
In light of these data and the growing body of literature contradicting the versatility and usefulness of whey protein, it should henceforth be classified as "moderate" or "intermediate" speed protein, with only whey hydrolysate and amino acids existing as truly "fast."
It may be difficult to adjust our thinking, but this is simply more dogma that needs to be destroyed in order to bring us up to date with the proper application of research.
9. Using antioxidants post workout enhances recovery.
Here’s another myth that just makes sense: we work out, cause all kinds of damage to our bodies, then we use antioxidants to help clean up the mess. Simple and sweet. The reality? Neither simple or sweet. In fact, it may not surprise you to find that there is a clear lack of data on antioxidant supplementation following exercise.
Taking a step back to look at the basis for the theory, it’s been shown that damaging eccentric exercise didn’t change the normal levels of our body’s antioxidants (Child et al., 1999). In other words, our body has a natural antioxidant defense capability, and this was not stressed at all despite the exercise and the subsequent muscle damage.
This is contradicted by other data showing that there is an impact of exercise on natural antioxidant levels (Lee et al., 2002; Goldfarb et al., 2005), but clearly the case is not closed. With this conflicting research, you’d have to wonder if antioxidant supplementation would have any effect at all! Oh it does, my oxidized friend, but the effects are not what we’d expect!
Once again, here’s one of the most underrated research papers of the last 5 years—take note folks because this is one of those studies you need to know about. This groundbreaking research by Childs and buddies (2001) examined the impact of post workout antioxidant supplementation on subsequent muscle damage and healing.
You’ll be shocked to know they found that this practice actually increased muscle damage and delayed recovery! That’s right, the microtrauma experienced by the muscle cells was exacerbated by the antioxidants. With this, the greater the damage, the more time it takes to repair.
It seems that there are pro-oxidant effects happening here, meaning that the "antioxidants" actually started causing the damage they were meant to clean up! While this effect is thought to occur with excessive antioxidant use, it’s surprising that these effects were seen at a Vitamin C dosage of ~1100mg and ~900mg N-Acetyl Cysteine per day, for a 200 lb guy, neither of which are all that incredibly high. To my knowledge, this is the only study to investigate antioxidant supplementation after strength training. This makes the findings incredibly powerful because they are directly applicable to us!
On a personal note, I was pretty blown away when I read this paper because I’d been using Vitamin C post workout for years. While these data aren’t strong enough to make me swear off antioxidants altogether, they clearly show that we can overdo it quite easily with these supplements. More importantly, these data help us rethink the post workout window dogma.
10. Aspirin and ibuprofen are good anti-inflammatories for muscle recovery.
The topic of muscle inflammation is pretty hot these days because it’s thought that minimizing this natural response will enhance recovery. By allowing us to hit the gym or get back on the field quicker, we can once again stimulate our bodies with a hard training session.
While the theory holds some water, we need to be careful how far we take it. For example, the use of traditional pain relievers, like aspirin and ibuprofen, has been increasingly common, because most people just don’t like the feeling of muscle soreness (T-Nation readers excepted because we’re hardly "most people").
A common effect of these pain relievers is that they exert a powerful anti-inflammatory effect. This fact has excited some budding pseudo-scientists, because they reason that using these common drugs will reduce muscle inflammation and enhance recovery. Great theory, poor applicability.
Early research showed that post workout use of these drugs inhibited our natural production of a chemical necessary for muscle growth and repair (Trappe et al., 2001). Further investigation showed that sure enough, muscle protein synthesis was completely shut down when these drugs were combined with strength training (Trappe et al., 2002). As a final kick in the teeth, using these drugs resulted in no effect on either inflammation (Peterson et al., 2003), or muscle soreness (Trappe et al., 2002).
Essentially we get the worst of all worlds when combining nonsteroidal anti-inflammatory drugs (NSAIDS) like aspirin and ibuprofen, with strength straining. Having said that, it is important to note that there are several different ways of affecting inflammation, some may be good, others are clearly bad. Keep in the back of your mind that limiting inflammation is a good idea, but certainly be aware that it is not universally beneficial.
Ten Take Home Points
—glycogen restoration is all too easy to achieve and may not be as critical as once thought
—protein synthesis needs to be the focus of our recovery intervention
—pre-workout meals actually enhance muscle blood flow and nutrient delivery during exercise
—pre-workout meals, nocturnal feeding, and multiple post workout drinks are more beneficial than a single post workout drink
—the "post workout window" lasts at least 24 hours
—consuming a protein shake immediately after training hinders optimal results
—strength training acutely enhances insulin sensitivity for at least 24 hours
—whey protein is generally only moderate speed, while whey hydrolysate and pure amino acids are "fast"
—antioxidants taken after exercise may increase muscle damage and delay recovery
—aspirin and ibuprofen can prevent the exercise-induced elevation in muscle protein synthesis thus hindering growth and prolonging recovery
Five Frequently Asked Questions
FAQ: If we don’t care about glycogen, then why would we use high glycemic carbs post workout?
A: Don’t forget that the main goal is to maximize protein synthesis, which is likely accomplished using quickly absorbed carbohydrates and greatly elevating insulin.
FAQ: In the study with the pre workout drink, what did they consume and when did they drink it?
A: Pure amino acids and sucrose were consumed immediately before training started.
FAQ: Doesn’t consuming carbs before a workout cause a blood sugar crash during the workout?
A: Usually no, our catecholamine response seems to keep out blood sugar elevated without problems. But if you’re just starting to try this, consume carbs during the workout or have them ready just in case.
FAQ: If there is a 24-hour post workout window, why do we care about consuming multiple drinks?
A: The multiple drink method is still the best way to maximize our anabolic response following training. We take advantage of this "window" by spiking our blood amino acid level as often as we can.
FAQ: If there is a 24-hour post workout window, why do we care about fast or intermediate speed proteins?
A: The multiple drink method can only be used when fast proteins or amino acids are consumed. It just doesn’t work with intermediate speed proteins.
CONCLUSIONS
It’s safe to say that we’ve been brought up to date with the current research regarding strength training and nutrition. Perhaps more importantly it’s clear that the post workout dogma has been destroyed. Unfortunately, with all of this destruction going on, there is a knowledge gap that needs to be filled, which will allow us to apply these new findings.
In other words, we need to figure out what all of this science stuff means, and how we can best use it to our advantage. In an upcoming article, I’ll introduce the Anabolic Index: a detailed blueprint for making use of this latest information, allowing us to maximize our anabolic potential.
Until then, Raise the Barr!
Thanks to: Nathan Devey, Nathan Dewsbury, Tan Huaiyu, Jonathan Boyle, my Phrenologist Dr. Ryan Smith, and everyone who helped review this document.
Dave can be reached via e-mail at
DBMuscle@Hotmail.com.
References
1. Arnal MA, Mosoni L, Boirie Y, Houlier ML, Morin L, Verdier E, Ritz P, Antoine JM, Prugnaud J, Beaufrere B, Mirand PP. Protein pulse feeding improves protein retention in elderly women. Am J Clin Nutr. 1999 Jun;69(6):1202-8
2. Asp S, Daugaard JR, Kristiansen S, Kiens B, Richter EA. Eccentric exercise decreases maximal insulin action in humans: muscle and systemic effects. J Physiol. 1996 Aug 1;494 ( Pt 3):891-8.
3. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrere B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14930-5.
4. Borsheim E, Tipton KD, Wolf SE, Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab. 2002 Oct;283(4):E648-57.
5. Calbet JA, MacLean DA. Plasma glucagon and insulin responses depend on the rate of appearance of amino acids after ingestion of different protein solutions in humans. J Nutr. 2002 Aug;132(8):2174-82.
6. Child R, Brown S, Day S, Donnelly A, Roper H, Saxton J. Changes in indices of antioxidant status, lipid peroxidation and inflammation in human skeletal muscle after eccentric muscle actions. Clin Sci (Lond). 1999 Jan;96(1):105-15.
7. Childs A, Jacobs C, Kaminski T, Halliwell B, Leeuwenburgh C. Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after an acute muscle injury induced by eccentric exercise. Free Radic Biol Med. 2001 Sep 15;31(6):745-53.
8. Coggins M, Lindner J, Rattigan S, Jahn L, Fasy E, Kaul S, Barrett E. Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes. 2001 Dec;50(12):2682-90.
9. Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, Ballevre O, Beaufrere B. The digestion rate of protein is an independent regulating factor of postprandial protein retention Am J Physiol Endocrinol Metab 280: E340-E348, 2001
10. Dangin M, Guillet C, Garcia-Rodenas C, Gachon P, Bouteloup-Demange C, Reiffers-Magnani K, Fauquant J, Ballevre O, Beaufrere B. The rate of protein digestion affects protein gain differently during aging in humans. Physiol. 2003 Jun 1;549(Pt 2):635-44.
11. Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol. 2001 Aug 15;535(Pt 1):301-11.
12. Fujitani J, Higaki Y, Kagawa T, Sakamoto M, Kiyonaga A, Shindo M,
Taniguchi A, Nakai Y, Tokuyama K, Tanaka H. Intravenous glucose tolerance test-derived glucose effectiveness in strength-trained humans. Metabolism. 1998 Jul;47(7):874-7.
13. Goldfarb AH, Bloomer RJ, McKenzie MJ. Combined antioxidant treatment effects on blood oxidative stress after eccentric exercise. Med Sci Sports Exerc. 2005 Feb;37(2):234-9.
14. Ivy JL, Katz AL, Cutler CL, Sherman WM, Coyle EF. Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J Appl Physiol. 1988 Apr;64(4):1480-5.
15. Koopman R, Manders RJ, Zorenc AH, Hul GB, Kuipers H, Keizer HA, van Loon LJ. A single session of resistance exercise enhances insulin sensitivity for at least 24 h in healthy men. Eur J Appl Physiol. 2005 May;94(1-2):180-7.
16. Lee J, Goldfarb AH, Rescino MH, Hegde S, Patrick S, Apperson K. Eccentric exercise effect on blood oxidative-stress markers and delayed onset of muscle soreness. Med Sci Sports Exerc. 2002 Mar;34(3):443-8.
17. Levenhagen DK, Gresham JD, Carlson MG, Maron DJ, Borel MJ, Flakoll PJ. Postexercise nutrient intake timing in humans is critical to recovery of leg glucose and protein homeostasis. Am J Physiol Endocrinol Metab. 2001 Jun;280(6):E982-93.
18. Louis M, Poortmans JR, Francaux M, Berre J, Boisseau N, Brassine E, Cuthbertson DJ, Smith K, Babraj JA, Waddell T, Rennie MJ. No effect of creatine supplementation on human myofibrillar and sarcoplasmic protein synthesis after resistance exercise. Am J Physiol Endocrinol Metab. 2003 Nov;285(5):E1089-94.
19. MacDougall JD, Gibala MJ, Tarnopolsky MA, MacDonald JR, Interisano SA, Yarasheski KE. The time course for elevated muscle protein synthesis following heavy resistance exercise. Can J Appl Physiol. 1995 Dec;20(4):480-6.
20. Miller WJ, Sherman WM, Ivy JL. Effect of strength training on glucose tolerance and post-glucose insulin response. Med Sci Sports Exerc. 1984 Dec;16(6):539-43.
21. Pascoe DD, Costill DL, Fink WJ, Robergs RA, Zachwieja JJ. Glycogen resynthesis in skeletal muscle following resistive exercise. Med Sci Sports Exerc. 1993 Mar;25(3):349-54.
22. Peterson JM, Trappe TA, Mylona E, White F, Lambert CP, Evans WJ, Pizza FX. Ibuprofen and acetaminophen: effect on muscle inflammation after eccentric exercise. Med Sci Sports Exerc. 2003 Jun;35(6):892-6.
23. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol. 1997 Jul;273(1 Pt 1):E99-107.
24. Phillips SM, Parise G, Roy BD, Tipton KD, Wolfe RR, Tamopolsky MA.
Resistance-training-induced adaptations in skeletal muscle protein turnover in the fed state. Can J Physiol Pharmacol. 2002 Nov;80(11):1045-53.
25. Rasmussen, BB, Tipton KD, Miller SL, Wolf SE, and Wolfe RR. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol 88: 386-392, 2000
26. Tipton KD, Rasmussen BB, Miller SL, Wolf SE, Owens-Stovall SK, Petrini BE, Wolfe RR. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Am J Physiol Endocrinol Metab. 2001 Aug;281(2):E197-206
27. Tipton KD, Borsheim E, Wolf SE, Sanford AP, Wolfe RR. Acute response of net muscle protein balance reflects 24-h balance after exercise and amino acid ingestion. Am J Physiol Endocrinol Metab. 2003 Jan;284(1):E76-89.
28. Trappe TA, Fluckey JD, White F, Lambert CP, Evans WJ. Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J Clin Endocrinol Metab. 2001 Oct;86(10):5067-70.
29. Trappe TA, White F, Lambert CP, Cesar D, Hellerstein M, Evans WJ.
Effect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab. 2002 Mar;282(3):E551-6.
---------- Post added vr 10 jun 2011 at 08:38 ----------
nog relevanter:
[Link niet meer beschikbaar]
Part I: Carb Nightmare?
Lonnie Lowery, PhD Cndt
You see it first! Some pretty disturbing EARLY data revealing the struggle your body undertakes just to deal with dietary carbohydrates while in a sore state. You punish your body with intense exercise but you're certainly no runner. The bottom line is, you shouldn't have to rely on high carb recommendations that stem from research on endurance athletes! Well, you don't have to anymore...
(This is the printer-friendly version.)
Do you get muscle soreness regularly from your lifting? If you train intensely, using eccentric contractions ("negatives") you're probably no stranger to the pain that comes from muscle damage. By "muscle damage" we mean the microscopic trauma that causes weakness and soreness while your body struggles to recover. Experienced lifters and physiologists know that the actual time spent in the gym is destructive, not constructive; that is, maximal growth comes only after some stress is placed upon a muscle and some damage is done. But many do not realize that if a large enough amount of muscle tissue is stressed, their ability to take-up and metabolize blood glucose is considerably worsened. That's right. Worsened.
A disease that is similar to (but more severe than) this state of poor glucose tolerance is Type II diabetes. Type II diabetics suffer from bodily tissues that are chronically unresponsive to insulin. The carbohydrates they eat enter their bloodstream (as glucose) but tend to stay there, gumming-up (glycosylating) other blood constituents and casing the pancreas to dump insulin in an effort to drive it in. About 90% of them are obese and have other problems related to hyperinsulinemia. Although many bodybuilders actually use insulin injections to aid muscle growth and recovery (dangerous and not recommended!), Type II diabetes is definitely "too much of a good thing". You see, having excess insulin in one's circulation can cause a number of problems, not the least of which is excess body FAT.
Enter exercise. It's a great way to get muscles to take-up blood glucose independent of insulin. Endurance training and weight training are a critical part of American Diabetes Association guidelines. But spending 30 minutes on a universal machine lifting two plates is a far cry from having 315 on one's back for six sets of ten! This is one thing we've been discovering lately in the Human Nutrition Lab (HNL) at Kent State University. Place enough load on large muscle groups using negatives - as many athletes do - and glucose intolerance can result! It's not as severe as that seen in diabetics but it appears to be enough to dampen recovery. You see, muscles need to turn blood glucose into glycogen (stored carbs) to stay full and energetic... but it can't get into a damaged muscle very well. It's a "catch-22" situation. Eccentric contractions induce superior growth4 but result in long recovery periods and poor carbohydrate efficiency.1,2,3,6,7 With regards to glucose intolerance, it's a scenario similar in appearance to Syndrome X, a condition rampant in western societies characterized by obesity and hypertension - presumably due to poor glucose handling. Even without intense lifting nearly 10% of men are hyperglycemic (have abnormally high blood glucose)5.
Taking a look at the above graph that's hot off the presses from the HNL at Kent State, we see that early results suggest hampered glucose tolerance in all subjects from muscle damage. This bodes poorly for maximal recovery. The lines come from an oral glucose tolerance test (OGTT) performed before and 24 hours after an intense workout. An OGTT is simply a series of blood draws, taken before and immediately after ingestion of 75 g of glucose (fast-acting sugar). Blood glucose commonly goes up about 40 points (mg/ dl) between 30-60 minutes, then insulin drives it back down. We didn't expect blood glucose to be this affected by the intense (eccentric) lifting. You see, the body's control over circulating glucose is necessarily TIGHT. We hypothesized (guessed) that subjects' pancreases would have to dump extra insulin to keep the glucose down in the face of all this "trauma", but not this actual hyperglycemic response; wow! The exercise bout consisted of six sets of six repetitions at 80% of the subjects' one rep max. Both bench press and squatting were performed in this manner on a Smith machine, using a four-count to lower the bar. The exercise session was designed to affect a maximal amount of skeletal muscle but also to mimic a state that is common to weight lifters.
Of course data is still coming in, but we are able to share some numbers on the first five subjects. By analyzing the data, we find that (with a fancy statistical test) we have high statistical power, meaning that we will end up with significant results by the end of the study (20 subjects). Yes, stats can turn us into veritable "swamis", allowing us to "see into the future" and not waste time on worthless studies. How many supplement investigators do that?! It's another benefit of having strong researchers at the HNL. We've got evidence to be pretty excited about the possibility of actually changing current nutrition recommendations for lifters, which is why I'm sharing this info now. I have to reserve final judgment, however, for the date my associates and I complete the study.
It's also important to realize that we need to validate that the large muscle groups of the shoulder girdle and lower body were actually damaged to some extent from the exercise. To do this we took some of the blood from the OGTT, spun it down in a centrifuge and tested the serum for creatine kinase (CK), alanine aminotransferase (ALT), aspartate aminotransferase (AST) and lactate dehydrogenase (LDH). These enzymes (notice the -ase suffix on each word; that denotes an enzyme) are "spilled" from muscle tissue for a period of 3-7 days after hard eccentric exercise.6 They suggest muscle trauma and our subjects were, in fact "traumatized". Check out the elevation in CK from an example subject:
The relatedness (or correlation) between fasting blood glucose and CK, for example, was tested on two separate post-workout occasions, revealing significant relationships (r = 0.54 to 0.75). These are moderate to strong relationships between muscle damage and poor glucose usage. In other words, when muscles are damaged, dietary carbs don't leave the blood stream very well (and enter the muscle tissue). Muscle soreness measurements add to the evidence, also suggesting that damage was done (have YOU ever gotten really sore from training?). They correlated moderately to highly with the CK results.
Clearly runners and cyclists need to replenish carb stores; they exhaust their glycogen almost daily. Hence the high dietary carb recommendations. And although many weight trainers insist carbs make them fat, they do need some for similar reasons. But for most of us it's really about growth as opposed to say, boosted performance and if we're not getting them into our sore muscles, where are they going?
One answer could be adipose tissue. Yep, body fat is another recipient of blood glucose. When insulin levels are high, fat cells grab up the blood borne glucose - even more so than sore muscles, presumably. And what happens to glucose once in a fat cell? You guessed it, fat building (lipogenesis). So now we see a "double whammy" scenario when muscles are just too rocked to accept blood glucose efficiently: First, they can't recovery rapidly, failing to optimally replenish their glycogen stores (and creating muscle fullness); Second, the left over circulating glucose likely goes where it can, into body fat.
What can be done about this problem that appears to be specific to weight trainers? Well, one thing is to report it to the scientific community so "experts" tone-down their "high carbs for all athletes" recommendations. Another is to give some preliminary suggestions to athletes as to when to eat plenty of carbs and when it might be better to reduce them. Finally, we can search for nutrients that may help glucose tolerance so bodybuilders can continue to induce muscle growth via "negatives" AND recover maximally. THAT, my friends, is what we're working on in the HNL right now! Stay tuned for Part Two of "High Carbs for Everyone?" to get practical suggestions and to see which compounds we're testing and what they're doing for glucose metabolism!
Editors' Note: Remember, data on graphs above are preliminary, using available data as it comes-in and representative case examples. It's important to wait for the completion of these studies for more comprehensive conclusions. Virtual Muscle shares this information in an effort to get it to those who matter, the ATHLETES, as soon as possible!
REFERENCES
Doyle, J., et al. (1993). J Appl Physiol 74(4): 1848-1855.
Friden, J., et al. (1983). Int J Sport Med 4: 170-176.
Gibala, M., et al. (1995). J Appl Physiol 78(2): 702-708.
Hortobagyi, T., et al. (1996). J Appl Physiol 80(3): 765-772.
Lowe, L., et al. (1997). Diabetes Care 20 (1): 163-175.
Lowery, L., et al. (2001). Doctoral dissertation. Kent State University.
Sherman, W. (1992). Int J Sport Nutr 2(3): 251-259.
---------- Post added vr 10 jun 2011 at 08:39 ----------
Part II: Data Accumulates
the VM Editors
This article is for those of you who want hard facts to help your supplement buying decisions and training recovery! It shows relationships between exercise-induced muscle damage and hampered carb use. It also updates everyone on the effects of a new herbal blend that may help. If you lift to the point of muscle soreness you need to stay abreast of this series of studies! Knowledge is power, baby. Show me the data!
Having printer issues? Want a more easily printed version of this article? Right-click here.
Hormone Havok
The alarm goes off in its usual rude tone: Beep! Beep! Beep! “Time to make the donuts”, thinks professor Lowery jokingly as his feet hit the cool hardwood floor. It’s six o’clock AM on a Sunday. Lonnie Lowery, director of the Human Nutrition Laboratory (HNL) at Kent State University, might be a bit salty at this hour but he rushes to the shower nonetheless. “Today’s the day,” he anticipates. “We’ll finally get our insulin measurements and know the whole picture…”
Why is this man excited – especially at this hour? Because he knows that a picture is becoming clearer as his research continues. The picture involves resistance trained athletes and their ability to recover from intense lifting. It's starting to look as if current high dietary carbohydrate recommendations may be overstated. Thirty minutes away, his colleague, Dr. Ron Mendel is already getting in his car to leave for the Lab. Ron, too knows that they may be on the verge of something big.
The campus is a ghost town on this frigid Sunday morning but already the Lab is percolating to life. As the coffee brews down in the office, the two men are joined by Dr. Tim Ziegenfuss, who’s made the drive down to lend a hand with the hormone assays.
“Hmm…” mutters Lonnie as the results are spit out of the ELISA machine. “It looks as if the hypothesis was correct; these subjects are not handling carbohydrates well at all when they’re sore. Look at those insulin levels.” For the past few months these researchers have been hypothesizing (guessing) that intensely training bodybuilders may be at least partly justified in their insistence that “carbs make them fat”. [Editors’ note: See “Carb Nightmare” in the Virtual Muscle online archives.] There has been indirect evidence of this in the past but a primary goal of HNL is to provide direct evidence straight to those who matter: the athletes. Look how strong the relationships are between muscle damage (from exercise) and poor dietary carb use:
The above graphs show how the body produces additional insulin after a "meal" to try and compensate for damaged muscles. They also indicate that dietary carbs appear to stay in the blood of sore athletes. The muscle damage, as indicated by CK in the blood (described more below) and perceptions of soreness, apparently r*tard muscles' ability to take up blood sugar (glucose). That is, subjects with more damage are the ones who exhibit worse "glucose tolerance". The more severe the damage, the worse the glucose intolerance. The pancreas won't stand for high blood sugar and attempts to hammer-home the glucose by dumping lots of insulin. If you've read earlier VM pieces on insulin and muscle building, you know that, although highly anabolic, insulin is a "Jeckyl and Hyde" hormone. Too much can be counter productive to the physique athlete by building fatty tissue (lipogenesis).
The problem here is that athletes need to rebuild muscle carbohydrate stores (glycogen) in order to recover - but can't ...at least not when they use heavy weights and "negatives" to induce additional growth. Are we hard lifters relegated to limiting our workouts to less than once per week?
Supplement Savior?
The following information refers to a "double blind" study: a type of research in which supplement bottles are simply labeled by a letter (rather than the type of supplement). For example, subjects will get "A" or "B" - but neither they nor the researchers know what's what during the study. Only one outside person knows the code and breaks it for the researchers at the end. This ensures objectivity and eliminates bias until the end of the study...
And yet these men are not content to simply acknowledge a problem. They’ve set out to do something about it with the help of Bodyonics Pinnacle and Phoenix Labs. With the financial commitment of these forward-looking companies and some compelling evidence on particular herbs from the scientific literature, it’s time to see if bodybuilders will have a legal alternative to insulin use. [Editors’ note: See “Bodybuilding and the Insulin Enigma” in the Virtual Muscle online archives.]
The second in their series of studies on muscle recovery and insulin focused upon the acute (immediate) effects of a blend containing glucosol, inzitol, and known nutrients like chromium and lipoic acid. Would this combination reduce blood sugar after consuming carbohydrates? Would the effects be similar to those of insulin? Based on existing data from studies on diabetics and muscle cells in culture (in vitro studies), Mel Rich, product formulator (and pharmacist) for Pinnacle thinks so.
The Human Nutrition Lab is now humming with hormone analyzers and overheating computers as data are created and analyzed. “Look at this,” says Dr. Mendel as Lonnie peers over his shoulder. “We’ve got three subjects done in each group and it looks as if a picture is emerging here.” Ron Mendel is looking closely at a blood (actually serum) marker of muscle damage called creatine kinase (CK). "First, we knew from your and Traci's data that CK was related to poor glucose tolerance1 (above) and now we know even more. Check it out... there’s a nearly significant decline in CK after four weeks of ingesting the capsules in group D; this wasn't expected, eh? Could the supplement protect subjects from a session THAT intense? Meanwhile the other group looks just as damaged as ever from the lifting session. I bet that's the placebo group. If it’s Insulene protecting the damage-resistant subjects then we may be onto something..."
“Hey guys,” inquires Tim as he returns from the biochemistry lab. “How’s the data analysis coming?”
“Well Z, Ron’s seeing some pretty interesting findings regarding improved muscle recovery… and check this out… after four weeks of the supplementation, there’s a trend toward lower fasting glucose levels in group D as well.”
"Mel is definitely going to be interested in this,” muses Tim. All that digging in the scientific literature seems to be paying-off for him. And for Pinnacle. There’s very little chance that it's the placebo group that's improving after just a month, wouldn’t you agree? If only we knew right now! I'm telling ya, I can't wait to finally break the code and know for sure the reason for these recovery-boosting effects.
Will these researchers’ hunch be right? Will the unique combination of insulin potentiating compounds pan out to be the reason for the improved ability to handle dietary carbs and recover better? The data won’t lie, so tune in next month when these guys finally wrap-up this study and ask colleague Dr. Karen Lowry-Gordon to unlock the “double blind” code.
Only then will the Virtual Muscle editors start pestering Pinnacle executives for discounts on this fascinating supplement.
Editors' Note: Remember, data on graphs above are preliminary, using available data (currently three to nine subjects per analysis) as it comes-in. It's important to wait for the completion of these studies for more comprehensive conclusions. Virtual Muscle shares this information in an effort to get it to those who matter, the ATHLETES, as soon as possible!
REFERENCES
Sexton, T. and Lowery, L. (2001). Oh J Sci (Medicine and Biology), 101 (1): 13.
---------- Post added vr 10 jun 2011 at 08:39 ----------
Part III: Lessons From a Year of Research
by Drs. Lonnie Lowery, Ron Mendel and Tim Ziegenfuss
This article is an update in a series. It's meant for those of you who have been following the whole research process at the Human Nutrition Lab since last Fall. After collecting and analyzing data on a total of 12 subjects, we have new findings to share. If you lift to the point of muscle soreness you should review this series of studies. Knowledge is power, baby. Show me the data!
Also see Carb Nightmare Part I and Carb Nightmare Part II.
Insulin Inquiry
How is a dietary supplement evaluated? How do we assess if it "works"? If you've ever thought about such things, good for you. Knowing how and why dietary substances work help keep you from getting conned. There is a fairly consistent research process and it starts with asking the right questions. In the case of the new generation of herbs that aid humans' ability to handle dietary carbohydrate, called "insulin potentiators", a specific question came to mind: Can we overcome power athlete's difficulties in using dietary carbs? It's become rather well established that sore muscles don't take up carbs well (See Parts I and II). We've only recently shown this for the first time specifically in resistance-trained athletes.1 Well, guess what ? We at the Human Nutrition Lab (HNL) are resistance trained athletes... and we seem to always be sore. Are you? If so, your ability to recover and grow is probably compromised. And training like a wimp, avoiding soreness is not the answer. Soreness is a sign of progress.
Dr. Lowery (Lonnie) has been examining post-exercise muscle soreness in the lab for about three years. But he knows soreness is just the tip of the iceberg. It's a symptom of something much deeper. A whole series of biological events take place over about four days after an intense workout. Lengthening contractions, called "eccentric" contractions or, in the weight room, "negatives", induce muscle damage, immune reactions and metabolic disturbances collectively referred to as the acute phase response.3 Believe it or not, it's the same response your body has to infection and trauma! Nutrition support is called for.
One disturbance is glucose intolerance. Dietary carbohydrates don't enter muscle tissue well in this state. It could be due to hormonal alterations or perhaps damaged muscle tissue itself. It's particularly problematic for us athletes because we need carbs from our diets to form glycogen in our liver and muscles to optimally recover. Without replenished glycogen storage, athletes get fatigued, break down bodily protein and can't perform as well.1,2
Over countless discussions in the lab we've wrestled with ways to handle this dilemma. Before conclusions could be made, however, we needed to observe and record various phenomena. That's part of what science is. Our first observation was that the current high-carb recommendations (up to 70 percent of kcal intake!) for all athletes stem from data on endurance athletes who aren't chronically sore. Perhaps this was why bodybuilders insist that "carbs make them fat". Our second observation came early this year with the confirmation that bodybuilders do, in fact, need help recovering...from a carb usage perspective. We confirmed this by looking carefully at insulin and blood glucose levels 24 hours after an intense whole-body workout using negatives. Here it is:
Smith machine bench press:
6 sets of six negative reps at 80% of 1 RM*
Smith machine squat:
6 sets of six negative reps at 80% of 1 RM*
If this looks tough to you, you're pretty astute. It was. In fact, we used the Smith machine not only to remove skill differences in the exercises, but for safety reasons. Think how you'd feel after 36 slow, lowering reps (four-count) in the bench AND squat! Research can be rough on subjects as well as researchers! Check out the video.
This type of data collection is a long, sometimes difficult, expensive, and somewhat invasive process. If you've been contaminated with the wild claims like "2000% better than D-bol !" that pervade our industry, it's time to smell the coffee. Let's get real. Dietary supplements are typically more mild than drugs (this can be good and bad, we suppose). Being as honest and straight forward as possible helps athletes. It is ultimately even the best long-term approach for supplement marketers. Supplement sales don't last if marketing claims don't live up to their hype. Our funding sources at the HNL know this and thus have few concerns with us sharing the presently mild effects (compared to insulin, for example) of a herbal blend called Insulene.
Design Difficulties
Since our last update, we've discovered that "group D" in our protocol was, in fact, the blend of "glucose control agents" and "group C" was, in fact, a placebo. Unfortunately, the effects regarding creatine kinase and glucose reduction were lost after adding a few additional subjects. What does this mean? Well, when analyzing four out of seven subjects, improved recovery was probable but as things now stand, the effect is not significant. Power analyses (see Carb Nightmare Part I) have their limitations when performing expensive, relatively invasive research on just a few subjects.
To be more certain that any recovery effects are real, we've decided to look deeper. The nutrients within the Insulene supplement are too promising to ignore. Glucosol, Inzitol, lipoic acid and "insulin-potentiating" minerals are all backed by evidence that they could help athletes. Several companies now sell some or all of these substances in various products and athletes are raving. But please recognize that these nutrients must be documented by science. Next month we hope to perform what's called a "crossover" design, bringing placebo subjects back into the lab to try Insulene for one month. Of course, they won't know what they're taking. Likewise, we'll be asking Insulene subjects to come back for a month on the placebo. This way we can avoid genetic differences that we believe are confounding (messing up) our data. It's a longer process, to be sure, but it will allow for very tightly controlled research.
We're here for you, the consumer, and, thus, need your support. Email your thoughts to Virtual Muscle! It's either that or you can continue to spend your hard-earned cash based on bullsh*t claims and marketing hype! The companies working with us at the Human Nutrition Lab agree that there's a better way. If you insist on hard data, stay tuned!
New Bodybuilder-Specific Data!
Our research is not only about dietary supplements. We've learned a ton about how bodybuilders recover and metabolize carbohydrates. Want to learn and grow as a result? Read on.
After bringing in additional subjects (since our last update), we still found relationships between muscle damage and poor glucose use. We also looked carefully to see if our research protocols were producing results that one would expect. They did. For example, we found direct relationships between blood glucose and insulin levels after administering sugar beverages (for you research enthusiasts: r=0.63, p=0.028 to r=0.73, p=0.007). One would expect this: higher blood sugar brings about higher blood insulin levels. We also found correlations between our various markers of muscle damage, including soreness and serum enzymes coming from damaged tissues (p<0.05). Okay, so the expected relationships were there, but anything else interesting?
Well, we learned that fat-free mass (largely muscle tissue) tended to correlate negatively with fasting blood glucose (r=-0.59, p=0.055) as well as "gummed-up red blood cells", known as "glycosylated hemoglobin" (r=-0.52, p=0.10). In this case, the negative correlation shows that subjects with higher fat free (muscle) mass had lower blood glucose levels over time. This suggests that adding muscle mass gives athletes more tissue to store glucose as glycogen (when they're not sore) and thus reduces potential "diabetes-like" problems (e.g. bodyfat). Cool. In other words, get big and recover properly to help stay lean.
Additionally, we learned - as one might expect - that the heaviest squatters did more damage to themselves than weaker ones. This was observed despite setting everyone at 80 percent of their maximum squat for the workout (above). It makes sense that our strongest squatter (max = 525 pounds, workout at 420 lb.) self-inflicted more damage than the weaker ones who only worked out with about 135 pounds (even though they, too, were at 80 percent of their max).
Alrighty then, to summarize what we know from this past year, specific to bodybuilders:
Adding muscle appears to be a good thing regarding glucose usage and body fat reduction - if adequate recovery is present.
Damaged sore muscles, however, are related to poor dietary carb use; one MUST recover to make progress.
It makes sense to eat plenty of carbs on days when soreness is low / gone, especially in the morning.
Strong guys can self inflict more damage in the weight room and may actually need nutrition support even more than beginning lifters.
The time frame for unaided recovery from eccentric training can be approximately five days.
Difficulties with dietary carb use occur in as little as 24 hours after lifting.
We're already using this data to make ourselves better. Will you? Until next update from the lab, keep sending your feedback. It helps us form hypotheses towards better research!
Editor's Note: Remember, data on graphs above are still preliminary, using available data (currently up to twelve subjects per analysis) as it comes in. It's important to wait for the completion of these studies for more comprehensive conclusions. Virtual Muscle shares this information in an effort to get it to those who matter, the ATHLETES, as soon as possible!
REFERENCES
Hargreaves, M. (1991). J Sports Sci. 9 Spec No:17-28.
Lemon, P. and Mullin, J. (1980). J Appl Physiol. 48(4): 624-9.
Lowery, L., et al. (2001). Doctoral dissertation. Kent State University.
Sexton, T. and Lowery, L. (2001). Oh J Sci (Medicine and Biology), 101 (1): 13.