Jul 2011 01
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Before I discuss the clinical research on carbohydrate intake and thyroid hormone levels, allow me to get a little ‘unscientific’ and report some anecdotal findings noted by myself and others. Rest assured, I’ll tie these observations in with plenty of published research when I’m done.

In 1998, I moved to Melbourne from Adelaide. Not long after this, in 2000, I began a low-carb diet. What followed was a predictable annual cycle, where winter would roll around and I’d freeze my ass off, despite wearing so many layers of clothing I could’ve doubled for the Michelin Man. My hands and nose were often ice cold, and at night I’d throw not one but two heavy quilt covers over my bed to stay warm. To keep my noggin from freezing I acquired enough beanies to fill a backyard pool, and I kept swearing I’d move to Queensland in due course so I wouldn’t have to put up with “this winter crap!” any longer.

Well, I never did move to Queensland, but something did change dramatically around 3 years ago.

In late 2008, I had successfully reduced my serum ferritin (a reliable marker for bodily iron levels) to the average levels of a teenager. Doing so has been shown to cause significant improvements in insulin sensitivity and glycemic control in both diabetic and non-diabetic folks. In my case, the improvements were more than “significant” – after years of having to follow a low-carb diet due to poor carbohydrate tolerance, the results were nothing short of remarkable. Large servings of carbohydrates no longer caused the brain fog and lethargy they once did. I began eating more and more carbs, until my diet was essentially a high-carbohydrate diet.

This development could not have come at a better time, as I’d just bought a single speed bike that I used, not for commuting, posing or pub-crawling, but for hill climbing. I instantly became hooked (trust me, you haven’t lived until you’ve ridden up the steep side of Waverly Road on a 46/16-geared bike…3 times in quick succession lol). Eschewing gears and relying on good old brute force to get up steep hills dramatically increased the intensity of my rides. As such, my muscles needed all the glycogen they could get their hands on and a high-carbohydrate diet became, not an option, but a necessity.

“Look Ma, no gears!” If the east and west sides of your belly are in a frantic race to get as far away from each other as possible, then start racing up hills on one of these. Problem solved.

The improvements were striking. More carbs meant quicker glycogen replenishment, which meant more frequent and intense rides, which meant improved fitness and cadence, which meant continually improving times. Eventually, my ride times would improve to the point where I was doing faster climbs on a heavy-assed steel-framed single speed (purchased for $400) than what I once did on my feather-light, uber-expensive carbon fiber road bike! That folks, is a bloody big difference.

But that wasn’t the only marked change that occurred. When winter again reared its inhospitable head the following year, I hardly noticed. I didn’t need to dress as heavily, I didn’t need as much covering on my bed, my hands didn’t feel cold all the time, and I wasn’t continually fantasizing about relocating to Queensland. Don’t get me wrong, as a certified and lifelong sun-worshipper, I still think winter sucks immensely, but nowadays it isn’t anywhere near as unbearable as it used to be.

So what happened?

Carbs, Meet Thyroid. Thyroid, Meet Carbs.


Levels of the important thyroid hormone T3 are higher on carb-rich diets.

My thyroid status was finally getting some love, in the form of carbohydrates, and giving me back plenty in the form of improved cold tolerance. An active body doesn’t like carbohydrate restriction. While the body views calorie restriction as a stressful response, it gets doubly concerned when carbohydrate availability drops.

As Danforth et al wrote, “…the caloric content as well as the composition of the diet, specifically, the carbohydrate content, can be important factors in regulating the peripheral metabolism of thyroid hormones.”[Danforth 1979]

Before we delve into the science, let me also report the results experienced by some very large men whose livelihoods depend on being able to achieve insanely low body fat levels.

Those of you who follow competitive bodybuilding will no doubt be aware that Jay Cutler and Branch Warren scored first and second place in the 2009 Mr. Olympia, considered the Superbowl of bodybuilding. And those of you who’ve seen the pictures of these guys will know that their condition was mind-blowing: deep cuts, full muscles, and a healthy glow rather than the all-too-common dehydrated and drawn-out appearance. Cutler’s transformation was especially impressive. After having lost his title and being criticized for problematic symmetry and muscle imbalances, he did what no dethroned Olympia winner has ever done before – he came back better than ever and blew away the competition to reclaim his title.

Warren, meanwhile, did what few thought a relative newcomer to the Olympia could do and pulled off a surprise second with his excellent combination of cuts, size and symmetry.

Branch Warren

In fact, the entire contest was characterized by a higher than usual standard of physiques. The contestants seemed to be doing something different.

Was there a stunning new training regime taking the pro-bodybuilding world by storm? Nope.

Had renegade scientists working in clandestine underground labs formulated some super-powerful new steroid? Nope.

The difference appears to have been carbs. Lots of them.

George Farah, the nutrition consultant who guided Branch to his impressive second place in the Olympia, was perplexed at the widespread use of low-carbohydrate diets in bodybuilding. Many bodybuilders and strength athletes had embraced these diets as eagerly as the general population, but needless to say, the nutritional needs of individuals performing intense daily training differ greatly to someone who spends their day staring at a computer in a seated position.

Farah reported he often had clients on very low-carbohydrate diets coming to see him, exhibiting low morning temperatures of 96ºF that quickly rose when he increased their carbohydrate intake. Farah, not surprisingly, is not a fan of low-carbohydrate diets. He had Warren consume as much as 1,000 grams of carb per day in his preparation for the Olympia[Gwartney].

Harry Rambod, the consultant who helped Cutler reclaim his Olympia title in stunning fashion, also shunned the use of low-carb eating and instructed his trainee to eat 750 grams of carbohydrate per day[Gwartney]. The rest is history – on the front cover of its January 2010 issue, popular bodybuilding magazine Muscular Development exclaimed “CARBS ARE BACK!” The prodigal son of bodybuilding nutrition had returned, and with a vengeance.

Of course, in professional athletics, they’d never gone anywhere in the first place. Intakes of up to 900 grams of carbohydrate per day, for example, are par for the course in professional road cyclists during the Tour de France[Saris WHM]. During the 2010 Tour Down Under the Adelaide Hilton, which serves as the base camp for riders and team staff, dished up 3,800 kilograms of pasta, noodles and rice, 3,000 bananas, 10,000 x 300 ml bottles of juice, along with 1,400 kilograms of chicken, fish, beef and pork, and 6,000 eggs[The Advertiser].

While bodybuilding is a somewhat subjective endeavour, professional sports are unmercifully objective. You either cross the line ahead of your competitor, or you don’t. And that’s why low-carbohydrate diets never caught on in the world of athletics; it’s all well and good for armchair Internet gurus to wank on about low-carb diets and “fat adaptation”, but when you’re a pro athlete with thousands and often millions of dollars in prize money and endorsements on the line, you simply can’t afford to have your glycogen-depleted butt being kicked around like a soccer ball by your competitors.

There will be a certain segment of people reading what I’ve just written, the kind that loses bowel control and screams “steroids!!” upon seeing anyone with a neck circumference bigger than a broomstick, that will poo-poo any mention of bodybuilders. Before doing so, they should remember this: bodybuilders tend to be ‘early adopters’ of nutrition trends and the strategies they embrace routinely go on to be widely used by the general population (examples include whey protein, omega-3 fat supplementation, low-GI foods, meal replacement shakes, multiple daily meals). The popularity of low-carb diets has been waning ever since 2004 and the news that those at the highest levels of bodybuilding are abandoning low-carb nutrition does not bode well for the future of this paradigm.

Thyroid Hormone 101

Before we delve into the science, a quick explanation of the key thyroid hormones is in order. The big daddy of thyroid hormones is triiodothyronine, also known as T3. It affects almost every physiological process in the body, including growth and development, metabolism, body temperature, and heart rate. Production of T3 and its prohormone thyroxine (T4) is activated by thyroid-stimulating hormone (TSH), which is released from the pituitary gland. T3 is around four times more potent than T4. Around twenty percent of thyroid hormone produced is T3, whereas 80% is T4.

Reverse triiodothyronine (rT3) is derived from thyroxine (T4). Unlike T3, rT3 does not stimulate thyroid hormone receptors. Instead, rT3 binds to these receptors and blocks the action of T3.

The Research and What it Shows

In the early 1970s, researchers from the University of Vermont published the results of the landmark Vermont experimental obesity studies, in which young men were deliberately overfed for seven months. That these men gained weight, ending up an average of twenty-five percent above their ideal bodyweight, was hardly an earth-shattering finding. What was surprising was that the men required fifty percent more calories to maintain this new heavier weight than they did at their usual lean weights. The researchers later discovered that short-term overfeeding was associated with increased thermogenesis (energy expenditure). Speculating that changes in thyroid function could be responsible, they proceeded to examine the effect of altering calorie and carbohydrate intake on thyroid hormone levels.

The first of these experiments involved closely supervised volunteer inmates from Vermont State Prison. During the overfeeding experiment, one group consumed a hypercaloric mixed (high-carb) diet for 7 months, while another group ate a hypercaloric high-fat diet for 3 months from primarily fat.

Again, that both groups gained weight should come as no surprise. However, the group overfed the mixed diet required more calories (2,625 kcal/m2 per day) to maintain their new heavier weights than did the group overfed fat (1,840 kcal/m2 per day). Baseline differences in metabolism between the two groups were ruled out, as there was no difference in total calories required to maintain initial lean weights.

Before and after the mixed diet overfeeding phase, the volunteers spent four weeks consuming maintenance level high-carbohydrate or low-carbohydrate diets. Thyroid hormone levels were measured at the end of each maintenance period, and after the overeating phase. For an average adult, the amount of carbohydrate consumed during the high- and low-carbohydrate weight-maintenance phases would translate to around 600 and 200 grams daily, respectively.

During maintenance eating, levels of T3 (triiodothyronine) were higher on the high-carb diet. When subjects on the low-carb diet began eating the higher-carb mixed weight gain diet, their T3 levels rose. T3 levels among those who went from the high-carb maintenance diet to the mixed diet remained unchanged. In contrast to T3, serum concentrations of T4 were unchanged by overeating or changes in dietary composition.

In the men overfed fat for 3 months, there was no change in mean T3 levels before and after the diet.

Vermont, Round 2

The second series of experiments involved 17 subjects housed at the General Clinical Research Center of the University of Vermont. These subjects consumed a variety of diets, varying in caloric and macronutrient content, for periods of 1-6 weeks each. Seven moderately overweight subjects even fasted for 7 days, consuming nothing except for water and electrolytes.

During 3-week overfeeding periods, the subjects gained a mean 4.1 kg. Serum concentrations of T3 increased whether the volunteers were overfed with carbs (25% increase), protein (17%), or fat (29%). However, serum concentrations of rT3 decreased when carbs (15%) or protein (23%) were overfed, but no overall change in rT3 concentrations occurred when fat was overfed (meaning the high fat diet still resulted in less T3 actually stimulating their cells than the high-carb or high-protein diets). T4 concentrations did not change after overfeeding.

The differences were much more pronounced when the results for eucaloric and hypocaloric diets were tabulated. When fat was substituted for carbohydrate in a weight maintaining diet for seven days, serum concentrations of T3 fell from 172 to 116 ng/dl, and then returned toward their initial concentrations when carbohydrate was restored to the diet. Serum concentrations of rT3 responded in the opposite direction to those of T3, rising with the low-carbohydrate intakes and falling again on the high carbohydrate diets. T4 levels were unaffected by the changes in diet composition.

In the subjects that fasted for seven days, T3 levels plummeted from a mean 155 to 87 ng/dl, and then rose to 146 with refeeding on a mixed diet. Initial rT3 concentrations were 25 ng/dl, rose with fasting to 57 ng/dl, and then fell again to 24 ng/dl with refeeding.

Another group followed a “protein-supplemented modified fast” for six weeks, eating a low-calorie zero-carb diet consisting of nothing but lean meat, fish, fowl, and vitamin and mineral supplements. During this rather unappetizing diet, T3 concentrations fell steadily and at six weeks were equivalent to those found after 7 days of fasting (88 ng/dl)!

The Vermont findings indicate that during short-term experiments, eucaloric and hypocaloric low-carb diets decrease levels of the all-important thyroid hormone T3. Over longer time frames, this finding may also extend to hypercaloric diets that result in significant weight gain.

Because concentrations of T4 were unaltered in most of the experiments, it appears that higher caloric and carbohydrate intakes increase T3 levels by accelerating the conversion of T4 to the more active T3, rather than directly stimulating secretion of T3 from the thyroid gland [Danforth 1979].

What Have Other Researchers Found?

The Vermont studies were hardly the only ones to find a negative impact of low-carbohydrate intakes on thyroid hormones. Over the years, an abundance of research has gathered to indicate that, for those who wish to maintain optimal thyroid function, very low-carbohydrate diets aren’t a wise idea.

Spaulding et al found that 800-calorie diets containing no carbohydrate (20 percent protein, 80 percent fat) mimicked the fall in T3 found during starvation. Total fasting resulted in a fifty-three percent reduction in serum T3, while the 2-week zero-carbohydrate diets exhibited a similar 47 percent decline in serum T3. In contrast, the same subjects receiving isocaloric diets containing at least fifty grams of carbohydrate showed no significant changes in T3 levels. The decline in serum T3 during the no-carbohydrate diet correlated significantly with blood glucose and ketones, but there was no correlation with insulin or glucagons[Spaulding SW]. As with the Vermont findings, these results would indicate that zero-carbohydrate dieting is an especially stupid endeavour.

In a study by UCLA researchers, six normal weight subjects followed 5 different diets for 5 days each. Three of the diets provided 2100 calories and 104, 202 and 409 grams of carbohydrate daily. Compared to the high-carbohydrate diet, the low carbohydrate diet caused a significant drop in T3 levels. The mean T3 results were 69, 86, and 91 ng/dl on the low-, medium-, and high-carbohydrate diets, respectively. The remaining two diets were hypercaloric, providing 4100 calories daily and 206 and 407 grams of carbohydrate daily. On both diets, the mean T3 level on both the 206- and 407-gram diets was 108 ng/dl. In this study, increasing carbohydrate intake over a range of 104-409 grams daily at eucaloric levels resulted in greater T3 levels, while on the high-calorie diet T3 concentrations were similarly increased with carbohydrate intakes of 206 and 407 grams per day[Davidson MB].

Dr. Fereidoun Azizi took forty-five obese subjects and studied them after 4 days of fasting and then after re-feeding with 800-calorie diets of varying composition. A minority of the subjects were taking T3 or T4, something we’ll discuss more in a minute.

Not surprisingly, T3 levels declined significantly during fasting, the decrease being greater in men than women. Re-feeding with protein or fat failed to restore the low serum T3, but re-feeding with a mixed diet resulted in a progressive rise of serum T3 to pre-fasting values (from 112 ng with fasting to 150 ng after 4 days of re-feeding). The carbohydrate-only diet caused similar increases in T3 (from 104 ng to 150 ng). Serum T4 levels rose after fasting and did not decrease after protein re-feeding, but did return to baseline values after 4 days of re-feeding with mixed dieting.

In an additional experiment, four subjects were again fasted and then re-fed with only 25 grams of carbohydrate daily for 4 days. This small amount of carbohydrate was able to raise fasting levels of T3 from a mean 110 ng to 136 ng. The changes in serum thyroid hormones were not related to the degree of weight loss or initial body weight.

What about the subjects taking thyroid hormones during the experiment? Among subjects administered oral T3, serum T3 levels did not decline during the fast. In the folks taking oral T4, however, levels of T3 still fell markedly during fasting, confirming that impaired conversion from T4 explains much of the decline in T3 levels seen with fasting and severe carbohydrate restriction[Azizi].

French researchers Serog et al examined four isocaloric (mean intake 2800 calories/day) diets lasting 1 week each. In two of these, a standard diet containing 45 percent carbohydrate was consumed. The remaining two diets were either low- or high-carbohydrate, and were consumed by all the subjects in random order between the two standard diet phases.

Average carbohydrate intake in grams was 250 grams on the standard diet, 71 grams on the low-carbohydrate diet, and 533 grams on the high-carbohydrate diet. On the standard and high-carbohydrate diets, T3 levels did not change, ranging from 163.3 to 169.5 ng. They declined on the low-carb diet to a mean 148.6 ng. Mirroring these changes, rT3 rose significantly only on the low-carb diet, while T4 did not change on any of the diets[Serog P].

Fery et al studied the effects of a 4-day isocaloric dietary replacement of carbohydrate by fat in six healthy subjects. The experimental ketogenic diet was preceded and followed by a 3-day period on a mixed diet. During the ketogenic phase, a significant fall in T3 and concomitant rise in rT3 levels was observed, while T4 levels remained unchanged. These changes were accompanied by a significant increases in glucagon and serum ketone levels, and a marked drop in blood glucose and insulin levels. Changes in levels of gluconeogenic amino acids and the branched chain amino acids reflected those seen during the catabolic environment of total fasting[Fery].

Ruth Mathieson and her colleagues from Virginia Polytech and State University placed fourteen obese free-living women on 530-calorie/day diets containing either 44 grams or 94 grams daily of carbohydrate. After four weeks, the group consuming the lower carbohydrate ketogenic diet lost an average of 8.0 kilograms, while the non-ketogenic group lost 6.7 kilograms, which the researchers attributed to greater water loss. There were no differences in RMR, but the ketogenic diet caused a significantly greater decline in T3[Mathieson RA].

Hendler and Bonde admitted seventeen obese but otherwise healthy subjects to the Yale Adult General Clinical Research Center, where they spent one month under close medical supervision. During this time, they spent 3-5 days on a weight maintenance diet then followed one of two extremely-low-calorie diets for 21 days. In this study, both protein intake was also dramatically manipulated. One diet contained 95% protein, 3% fat, and 2% carbohydrate, the other 41% protein, 4% fat, and 55% carbohydrate. Both diets provided 440 calories per day. Total weight lost by the low- and high-protein subjects after three weeks was 8.88 kg and 8.74 kg, respectively. Estimated lean mass loss was slightly lower in the high-protein group but did not reach statistical significance. Both diets caused similar drops in metabolic rate and fasting insulin levels. The high protein group experienced slightly greater decreases in the thyroid hormones T3 and free T3, although in this study the differences were not statistically significant[Hendler].

Dr. Kenneth Burman and colleagues from the Walter Reed Army and National Naval Medical Centers studied obese subjects during consecutive periods of differing diets. These included a mixed diet (40% carbohydrate, 40% fat, 20% protein, mean 1440 calories) for four days, followed by a fast of 7 days, then 5 days of glucose ingestion only (one group consumed 50 grams of glucose daily, the other 100 grams).

In the group given fifty grams of glucose, the mean serum T3 concentration dropped from 137 ng/dl on day 1 to 117 ng/dl on day 4 of the mixed diet, and gradually decreased to 66 ng/dl on the last day of fasting. The administration of 50 grams of glucose after fasting was followed by an increase in mean serum T3 levels to 94 ng/dl. In the subjects given 100 grams of glucose, T3 levels dropped from 149 ng/dl on day 1 to 133 ng/dl on day 4 of the mixed diet, bottomed out at 76 ng/dl on day 7 of fasting, then rose to 110 ng/dl after 4 days of glucose administration. Similar results were obtained in subjects who consumed 100 grams of fructose instead of glucose.

In yet another group, the fasting phase was eliminated and the glucose diet (100 grams) was given immediately after the mixed diet. Despite the extremely low calorie consumption during the glucose-only phase, there was no decline in T3 values. Mean T3 concentrations were 178 ng/dl after five days of the mixed diet, and 179 ng/dl on day 1, 167 ng/dl on day 5, and 184 ng/dl on day 6 of the glucose-only diet[Burman KD].

For six weeks, six moderately obese, untrained subjects ate a zero-carb diet of lean meat, fish, or fowl, supplemented with minerals and vitamins and providing 500-750 calories per day. Serum concentrations of T3 decreased thirty-three percent and rT3 increased 72 percent after one week of the diet. T3 levels continued to decrease slightly, albeit non-significantly, while resting rT3 levels returned toward base line after week six. T4 concentrations were unaffected after the first week but showed a slight though insignificant fall after six weeks[Phinney SD].

Atkins-sponsored Volek et al examined the effect of a low-carbohydrate diet delivering a mean 46 grams of carbohydrate per day on body composition and hormonal responses in normal-weight young men, most of whom were recreational excercisers. Levels of various hormones were measured whilst the men were following their habitual high carbohydrate diet, then during and after six weeks of the carbohydrate-restricted diet. Upon commencement of the low-carbohydrate diet a small calorie deficit and a significant increase in protein intake occurred, resulting in a mean 3.3 kilogram fat loss and a 1.1 kilogram lean mass gain. There was a significant increase in total T4 (+ 10.8%), but for some reason the researchers did not directly measure T3 nor rT3. They instead tested T3 uptake, an indirect measure of thyroxine binding globulin (TBG) in the blood, which tells us little of any real value about changes in actual thyroid hormone levels. The researchers also measured IGF-1, glucagon, total and free testosterone, sex hormone-binding globulin (SHBG), insulin-like growth factor-I (IGF-I), and cortisol. The only significant change noted was a reduction in insulin following the low-carbohydrate diet[Volek].

Protein and the Thyroid

All the abovementioned studies examined the effect of altering carbohydrate intake on thyroid hormone levels. The results are virtually unanimous: decreasing carbohydrate intake to low levels results in diminished levels of T3 and/or increased rT3, something most aspiring fat-burners wish to avoid desperately.

I know this article is focused on carbohydrate’s effect on thyroid hormone levels, but what about the effect of keeping carbohydrate intake constant and only altering levels of protein and fat? Does this have any effect on thyroid hormone levels?

Let’s find out.

The Plot Fattens

Ullrich and colleagues compared two diets of equal carbohydrate content, one containing 35% protein, 30% fat, and 35% carbohydrate, the latter 10% protein, 55% fat, and 35% carbohydrate. Calories were adjusted so that each individual could maintain their weight throughout the study, but each individual consumed at least 200 grams of carbohydrate daily.

The subjects followed the diets in random order for seven days each. Mean T3 levels at baseline were 198 ng/dl; this declined to a significantly greater degree after the high fat diet (113 ng/dl) than the high-protein diet (138 ng/dl). T4 levels did not change significantly[Ullrich IH].

So What Does This All Mean?

Almost everyone assumes that low thyroid function equals excess weight gain, and that if only they could get their thyroid humming along like a Keonig-tuned Ferrari, eternal leanness is theirs for the taking.

It ain’t that simple. The human hormonal network is amazingly intricate, with an endless array of feedback loops that impact upon hormonal output and function in ways that scientists still don’t fully understand. Focusing on the level of just one or 2 hormones is somewhat myopic and often ineffective.

Researchers, for example, have observed almost no difference in various measures of energy expenditure and body composition in obese individuals with normal thyroid function and subclinical hypothyroidism (of the numerous measurements taken, only resting energy expenditure per kilogram of fat free mass was significantly different and lower, and only in the most severely hypothyroid patients)[Tagliaferri].

Which makes it less surprising to learn that treatment of obesity with thyroid hormone has delivered lacklustre results. In a 1984 report, minor weight loss was seen with treatment of subclinical hypothyroidism, but bodyweight gradually returned to pre-treatment levels at 24 months[Hoogwerf].

And lowered T3/raised rT3 does not necessarily equate to measurable differences in metabolic rate. Numerous clinical studies have compared the effect of low-carb and high-carb diets on dietary induced thermogenesis (the increase in metabolism that occurs after a meal) and overall energy expenditure. There is either no detectable difference or a slight increase seen with higher carbohydrate meals and diets (I discuss this in detail in The Great Eades Smackdown, Part 1). However, even when differences are observed they are quite small and unlikely to have any meaningful impact upon weight loss.

Indeed, as explained in great length in The Fat Loss Bible, tightly controlled metabolic ward trials dating all the way back to 1935 repeatedly show no difference in fat-derived weight loss on isocaloric high- and low-carbohydrate diets, no matter what the caloric intake.

However, the longest lasting of these trials is around 2 months, which leaves open the possibility that the changes in thyroid levels seen on low-carb diets could cause unfavourable effects on weight status over the longer term, especially in susceptible subjects.

And remember, there’s a whole lot more to the thyroid story than just fat loss. The thyroid gland and the hormones it secretes have a profound effect on your overall health and energy levels. Any diet that produces untoward changes in thyroid hormone levels should be regarded with great caution – especially so if you are a hard training athlete whose physiology is subject to the added burden of regular and vigorous activity, or if you’ve previously displayed symptoms of low thyroid function (heightened cold intolerance, low morning temperature, clinically diagnosed thyroid dysfunction).

Anthony Colpo is an independent researcher, physical conditioning specialist, and author of the groundbreaking books The Fat Loss Bible and The Great Cholesterol Con. For more information, visit TheFatLossBible.net or TheGreatCholesterolCon.com

References

Danforth E Jr, et al. Dietary-induced Alterations in Thyroid Hormone Metabolism during Overnutrition. Journal of Clinical Investigation, 1979; 64 (5): 1336–1347.

Gwartney D. Carbs make a comeback. Muscular Development, January 2010: 122-126.

Saris WHM, et al. Study on food intake and energy expenditure during extreme sustained exercise: The Tour de France. International Journal of Sports Medicine, 1989; 10 (Suppl 1): S26-S31. http://arno.unimaas.nl/show.cgi?fid=1571

The Advertiser, January 13, 2010: 45.

Spaulding SW, et al. Effect of caloric restriction and dietary composition of serum T3 and reverse T3 in man. Journal of Clinical Endocrinology & Metabolism, Jan, 1976; 42 (1): 197–200.

Davidson MB, Chopra IJ. Effect of carbohydrate and noncarbohydrate sources of calories on plasma 3,5,3′-triiodothyronine concentrations in man. Journal of Clinical Endocrinology & Metabolism, Apr, 1979; 48 (4): 577–581.

Azizi F. Effect of dietary composition on fasting induced changes in serum thyroid hormones and thyrotropin. Metabolism, 1978; 27: 935-942.

Serog P, et al. Effects of slimming and composition of diets on V02 and thyroid hormones in healthy subjects. American Journal of Clinical Nutrition, Jan 1982; 35: 24-35.

Fery F, et al. Hormonal and metabolic changes induced by an isocaloric isoproteinic ketogenic diet in healthy subjects. Diabetes & Metabolism, Dec 1982; 8 (4): 299-305.

Mathieson RA, et al. The effect of varying carbohydrate content of a very-low-caloric diet on resting metabolic rate and thyroid hormones. Metabolism, May, 1986; 35 (5): 394-398.

Hendler RG, et al. Sucrose substitution in prevention and reversal of the fall in metabolic rate accompanying hypocaloric diets. American Journal of Medicine, 1986; 81 (2): 280-284.

Burman KD, et al. Glucose modulation of alterations in serum iodothyronine concentrations induced by fasting. Metabolism, Apr, 1979; 28 (4): 291–299.

Phinney SD, et al. Capacity for moderate exercise in obese subjects after adaptation to a hypocaloric, ketogenic diet. Journal of Clinical Investigation, Nov, 1980; 66 (5): 1152-1161.

Volek JS, et al. Body composition and hormonal responses to a carbohydrate-restricted diet. Metabolism. 2002 Jul; 51 (7): 864-870.

Ullrich IH, et al. Effect of low-carbohydrate diets high in either fat or protein on thyroid function, plasma insulin, glucose, and triglycerides in healthy young adults. Journal of the American College of Nutrition, 1985; 4 (4): 451-459.

Tagliaferri M, et al. Subclinical hypothyroidism in obese patients: relation to resting energy expenditure, serum leptin, body composition, and lipid profile. Obesity Research, 2001 Mar; 9 (3): 196-201.

Hoogwerf BJ, Nuttall FQ. Long-Term Weight Regulation in Treated Hyperthyroid and Hypothyroid Subjects. American Journal of Medicine, June 1984; 76: 963-970.

Copyright © Anthony Colpo.

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