Tuesday, October 28, 2008

Book Review: The Jungle Effect, by Daphne Miller, M.D.

Our local library recently began advertising a talk by Dr. Daphne Miller, author of The Jungle Effect. The essential concept of the book is to examine epidemiological "cold spots" for various modern diseases, such as diabetes, heart disease, depression, and cancer. These cold spots are areas notably low in the incidence of said diseases. Dr. Miller visited each area and studied the local cuisines, with the idea that food is a driving force behind development of these diseases which often show the highest incidence amongst those eating a modern Western diet.

I was quite excited when I first read about The Jungle Effect. One reviewer went so far as to dub Dr. Miller the modern equivalent of Weston Price. I'm a big fan of Price's work as a shining example of the application of the scientific method and what can be discovered with limited resources and a determined rational mind. I also believe cultural wisdom that has stood the test of time deserves to be weighed along with more "scientific" evidence, and of course am in favor of whole, nutrient-dense foods (who isn't?). As I read The Jungle Effect, however, my enthusiasm waned and frustration set in. While I do believe that the foods put forth by Dr. Miller would constitute a much healthier diet than eaten by most in modernized society, the scientific rationale falls well short, and I believe leads to confusion and complication that is both unnecessary and unjustified.

Let's start with the good. First and foremost, Dr. Miller is an excellent writer, and clearly passionate about helping people improve their health. The Jungle Effect covers five different traditional cuisines associated with disease cold spots:
  • Copper Canyon, Mexico (the Tarahumara): Diabetes
  • Crete: Heart Disease
  • Iceland: Depression
  • Cameroon: Bowel Trouble
  • Okinawa: Breast and Prostate Cancer
Dr. Miller's descriptions of these cultures and their cuisines are vivid and fascinating. Many of the recipes sound very tasty, and despite the often relatively high carbohydrate content (often from honey, sugar, or maple syrup) are probably considerably more healthy than the average Western diet. Indeed, the patients for which she "prescribed" these diets apparently saw positive results, e.g. in reducing blood sugar, blood pressure, weight, depression symptoms, etc. So there is clearly some upside here, at least compared with the diet and health of the average American.

But in the end, The Jungle Effect suffers from some fundamental flaws. My criticisms here are meant to be constructive. As noted in the last post, sharing information is important if we hope to understand and sort out differences in our beliefs. Dr. Miller's approach is "traditional" not only in searching out elements of indigenous cuisines, but also in adhering to the nutritional orthodoxy. She obviously received the usual medical training, and consulted a nutritionist while writing the book. But many of you reading this realize that widely-held beliefs about the health effects of various foods are constructed on evidence that is weak at best, with contradictory evidence often being ignored. This results in some clear cognitive dissonance. For instance, Dr. Miller briefly discusses the Inuit (Eskimos) and the high level of health maintained on their traditional diet consisting almost entirely of high-fat meat. Yet much of the rest of the book warns against the dangers of red meat and too much fat, particularly saturated fat. I suspect there's also some confirmation bias at work in her selection of which cultures to study. One wonders why she didn't visit the Inuit, Masai, or for that matter the Namgis tribe featured in the excellent documentary My Big Fat Diet. The latter case is particularly interesting, as the Namgis who returned to a traditional high-fat diet experienced rapid and major health improvements, considerably more dramatic than those described for Dr. Miller's patients. Evidence modifies beliefs, but our beliefs should not cause us to filter the evidence.

Dr. Miller does briefly attempt to explain away the apparent Inuit "paradox" by noting the wild animals traditionally eaten themselves eat nutrient dense food, and pass that nutrition along to predators. But then the best one could say is that it isn't meat per se that is unhealthy, just meat fed an unnatural diet (Dr. Miller generally recommends very low meat intake, particularly red meat, usually without distinguishing the source). Give her credit for singing the praises of nutrient-dense organ meats. She also gets some points for not invoking genetics as the root of the apparent paradox. If you ever feel the urge to do this, then you should undertake the following procedure:
  1. Find a friend with some heavy boots.
  2. Have them kick you in the backside.
  3. After each kick, say the following: "I will not blame the observed failure of my hypothesis on unobserved genetic factors."
  4. Repeat 2-4 until rationality sets in.
The Jungle Effect would have benefited from deeper critical thinking, rather than absolute reliance on consensus (see Galileo quote at the top of the page). One aspect of this would be a broader sample of indigenous cuisines, including those high in animal products. It would also have been nice to see some integrative analysis of the different diets. Weston Price studied a wide variety of indigenous cultures, and was able to distill some common nutritional factors resulting in robust health, even so far as to discover a new fat soluble vitamin (which he called Activator X, now thought to be Vitamin K2). I would like to know, for example, how the health of the various cultures compared across the spectrum of diseases. Cameroon may have low incidence of colon cancer, but how do their rates of diabetes, heart disease, etc. compare to the other cultures described in the book? For that matter, one would like to compare traditional Inuit on that basis as well, to include the full spectrum of dietary macronutrient compositions.

Indeed, Dr. Miller notes that the Tarahumara, while notably free of diabetes, are not particularly healthy otherwise. Following Weston Price's cue, I looked for information on Tarahumara dental health, the idea being that dental health is a reflection of overall health, certainly of the status of vitamins involved in immune support and mineral metabolism. I'd be interested in getting Dr. Miller's view, since she was on the spot and got to observe the Tarahumara. I did find this article, which implies that the traditional Tarahumara suffer from significant dental disease, though it's pretty thin on details. We might also compare visually them with a hunter-gatherer. Here's a photo of an indigenous Tarahumaran, who according to Dr. Miller subsists largely on corn, beans, squash, and relatively little meat. Compare with a Kalapalo tribesman, who eats a lot of fish (they don't hunt animals) and jungle fruits and vegetables. Draw your own conclusions. Personally, I wish I had some Kalapalo biceps.

The nutritional context could also have been expanded in time. Modern indigenous diets do not necessarily represent the evolutionary diet of humans. Those sampled by Dr. Miller all relied heavily on agriculture, yet those foods available through agriculture have been part of the human diet for a very short time, evolutionarily speaking. The paleo-anthropological evidence certainly indicates that the pre-agricultural diet often relied heavily on meat from large mammals, and there are some clear markers of health decline at the agricultural boundary (decreased skeletal stature and skull size, evidence of mineral deficiencies, tooth decay). The modern indigenous diets likely evolved from other influences beyond evolution: extinction of large prey animals, geopolitical forces, changing climate, etc. Over time, these cultures may have identified the healthiest combinations of whatever foods were available, but that doesn't mean the available foods are the healthiest as defined by human evolutionary heritage. So again, it's necessary to consider all available evidence, not just that which agrees with our preconceptions.

Let's discuss some of the key nutritional beliefs that underpin Dr. Miller's arguments. Despite being widely held, a critical examination shows that the actual scientific evidence for many of these beliefs is thin at best, and often contradictory. Gary Taubes' Good Calories, Bad Calories (GCBC) gives a broad critical examination of the evidence, so there's no need to go into depth here (I suspect Dr. Miller has not read GCBC - if I can catch up with her at the talk this Sunday, I'll offer her a copy). Start with saturated fat. Obviously it is generally thought that saturated fat is a causal factor in many diseases, from diabetes to cancer to heart disease. Dr. Miller cites Ancel Keys work as evidence for this, but the problems with Keys' studies are well documented in GCBC and in many other places. The biggest one, of course, is that epidemiological research such as the Seven Countries Study can only show statistical associations, not causation, and are susceptible to counfounding from the large number of uncontrolled variables. Other epidemiological studies (like Framingham) have shown the opposite of Keys' conclusions, and to my knowledge there are few (if any) controlled studies that illustrate any causal connection between saturated fat and disease. Stephan is starting a new series at Whole Health Blog on this topic, which I recommend.

Apart from experimental evidence, one would also like to have a plausible mechanism by which saturated fat causes disease. As I discussed here, despite a half-decade of research, nobody has any idea how it is that saturated fat leads to heart disease. "Experts" continue to pound on the health evils of saturated fat, despite evidence that is weak at best and generally contradictory. Dr. Miller calls out saturated fat as a pro-oxidant food "known to cause oxidative stress". Again, we see uncritical acceptance of the consensus. Saturated fats are LESS susceptible to oxidation than unsaturated fats, particularly polyunsaturated fats from vegetable oils, flax, etc. From simple chemistry, one expects polyunsaturates to induce substantially more oxidative stress (credit Dr. Miller with recommending limited vegetable oil intake, though I don't agree with her recommendations for taking flax oil). And of course the human body preferentially manufactures saturated fat from excess sugars, likely an evolutionary response. Were saturated fat to actually increase oxidative stress, one would have to hypothesize some mechanism by which the body preferentially oxidizes it, or by which saturated fat induces some other biological response that leads to oxidative stress. How or why an organism would evolve such responses escapes me, and I'm not aware that any have been experimentally or even theoretically identified.

Let's compare the utter lack of hypotheses tying saturated fat to heart disease with an alternative: athersclerosis is at least partially caused by excess sugar and polyunsaturated fat. Here's the rationale (discussed in several places on the web):
  • Fats are transported in the blood in lipoproteins.
  • Lipoproteins tend to embed themselves at places where arteries sustain damage, such as branches (veins, under considerable lower pressure, do not exhibit atherosclerosis).
  • Macrophages have specific receptors for LDL that has been damaged by oxidation or glycation, but no receptor for undamaged LDL. Oxidized/glycated LDL is consumed by the macrophages, which can lead to accumulation of "foam cells" forming the atherosclerotic plaque.
  • Consumption of polyunsaturated fat promotes oxidation of LDL. Lipoproteins consist of a large protein coat, interspersed with phospholipids (two fatty acids on a phosphate backbone). If the phospholipid contains a polyunsaturated fatty acid, it is more susceptible to oxidation.
  • Increased blood sugar, either via consumption of large amounts of refined carbohydrates or due to metabolic dysfunction (e.g. insulin resistance) increase the potential for glycation damage of LDL, where the sugar binds to the protein and alters its structure in a manner similar to oxidation.
  • So, PUFA + sugar = damaged LDL = inflammatory response = atherosclerosis.
Now, I'm not saying this is the answer, but it at least makes logical sense, follows currently accepted beliefs about chemistry and human biology, and I would guess explains the epidemiological evidence at least as well as the saturated fat hypothesis (which never was particularly clear to start with). It's certainly better than "we have no idea", as put forth in textbooks and by "experts". More research is needed to really nail things down, but I think we can see that the PUFA/sugar hypothesis, which has some basis in accepted science, should receive a greater weight than the saturated fat hypothesis, which has no basis whatsoever.

Another issue is dietary fiber. Dr. Miller is a big fan for the usual reasons: fiber makes you feel full, scrapes the inside of your colon, etc. The satiety argument requires a very narrow view of appetite regulation, as I discuss here and here. It is true that the mechanical distension of the stomach contributes to satiety, probably both via nervous system signals and suppression of ghrelin secretion. But those are two of many other nervous and hormonal signals indicating the macronutrient and energy content of food, energy availability in the body, etc. Fiber has no effect on these other aspects. That's to be expected - otherwise we'd be able to eat only highly fibrous food with little energy content, feel full, and wind up starving to death. Not a very good evolutionary strategy.

Dr. Miller discusses the origins of the fiber hypothesis, from Denis Burkitt's work in Africa. Taubes gives a more detailed history in GCBC. It is interesting to note that Burkitt's hypothesis originated from Peter Cleave's "saccharine-disease hypothesis", namely that refined carbohydrates were at the root of a host of modern diseases. Burkitt was initially impressed with Cleave's work, noting that Cleave possessed "perceptive genius, persuasive argument and irrefutable logic." But over time he modified the argument to accent the absence of fiber rather than the presence of refined carbohydrates. Now, there's nothing wrong with this hypothesis per se, but one must be aware that testing refined vs. unrefined carbohydrate in the diet does not distinguish between these hypotheses: unrefined carbohydrate has more fiber. And there is other evidence that absence of fiber is not the health issue it's made out to be. Says Taubes:

Burkitt and Trowell called their fiber hypothesis a "major modification" of Cleave's ideas, but the never actually addressed the reasons why Cleave had identified refined carbohydrates as the problem to begin with: How to explain the absence of these chronic diseases in cultures whose traditional diets contained predominantly fat and protein and little or no plant foods and thus little or no fiber - the Masai and the Samburu, the Native Americans of the Great Plains, the Inuit? And why did chronic diseases begin appearing in these populations only with the availability of Western diets, if they weren't eating copious fiber prior to this nutrition transition? Trowell did suggest, as Keys had, that the experience of these populations might be irrelevant to the rest of the world. "Special ethnic groups like the Eskimos," he wrote, "adapted many millenia ago to special diets, which in other groups, not adapted to these diets, might induce disease." Trowell spent three decades in Kenya and Uganda administering to the Masai and other nomadic tribes, Burkitt had spent two decades there, and yet that was extent of the discussion.

Sounds like Keys, Burkitt, and Trowell could all use the boot treatment I described above. Taubes' discussion highlights another related hypothesis, namely that red meat is bad, for which the argument at least partially stems from the fiber hypothesis. We can't distinguish between the unrefined carbohydrate and fiber hypotheses by exchanging refined for unrefined carbohydrates, but we can distinguish between red meat vs. fiber hypothesis by exchanging red meat for whole fruits, vegetables, and grains. Taubes addresses this as well:

By the end of the 1990s, clinical trials and large-scale prospective studies had demonstrated that the dietary fat and fiber hypotheses of cancer were almost assuredly wrong, and similar investigations had repeatedly failed to confirm that red meat played any role* (*Those clinical trials that tested the dietary-fat-and-fiber hypotheses of cancer, as we discussed earlier, replaced red meat in the experimental diets with fruits, vegetables, and whole grains. When these trials failed to confirm that fat causes breast cancer, or that fiber prevents colon cancer, they also failed to confirm the hypothesis that red-meat consumption plays a role in either.) Meanwhile, cancer researchers had failed to identify any diet-related carcinogens or mutagens that could account for any of the major cancers. But cancer epidemiologists made little attempt to derive alternative explanations for those 10 to 70 percent of diet-induced cancers, other than to suggest that overnutrition, physical inactivity, and obesity perhaps played a role.

Long story short: when scientists looked specifically for a causal link between fiber and cancer prevention or red meat and cancer causation, they found diddly-squat. Since these hypotheses were originally generated by weak epidemiological evidence, the contradictory evidence from more controlled trials weakens the hypotheses further. The refined carbohydrate hypothesis, on the other hand, provides considerable explanatory power and consistency with known biological properties of cancer, such as the necessity for cancer growth to be driven by insulin and a ready supply of glucose. The refined carb hypothesis also explains all of Dr. Miller's epidemiological observations. Given the above, it certainly seems more likely that, for instance, the absence of colon cancer in Cameroon has less to do with the presence of fiber than the absence of refined carbohydrates.

Finally, Dr. Miller appears to be significantly misinformed as to what is considered a "low carbohydrate diet". She generally uses the term "high protein diet", which underscores the root of the misunderstanding. The term "high protein diet" presumably indicates that it is low in both carbohydrates AND fat, which is problematic to health. One of my favorite books (which The Jungle Effect has inspired me to re-read) is Marvin Harris' Good to Eat. Harris notes that indigenous cultures never get the bulk of their calories from lean protein. Energy is invariably provided by fat and/or carbohydrate, with the amount of protein being remarkably constant across cultures. Dr. Miller correctly notes the underlying reason for this: protein is "dirty" fuel. Not being a pure hydrocarbon like sugar or fat, the conversion of protein to energy essentially results in pollution from nitrogen and other substances, which our kidneys then need to filter. A high-protein diet can overload the body's ability to dispose of these toxins, leading to sickness and ultimately death, even though plenty of food is provided. Dr. Miller relates experiences of some of her patients on high protein diets, that they basically felt unsatisfied and craved carbohydrates. This matches nicely with the phenomenon of rabbit starvation, where pioneers would feast on extremely lean rabbit meat, only to still be hungry. After some time they would eat 3 to 4 pounds of rabbit at a sitting, yet ultimately would waste away and essentially starve to death with full stomachs. It is no surprise that a high protein diet (as defined by restriction of both carbohydrate and fat) is doomed to failure.

But "low carbohydrate" does not necessarily imply "high protein". Indeed, had Dr. Miller read any of the large number of books on low carbohydrate diets, Googled the topic, or consulted with any number of experts, she would have found the recommendations are generally for high fat. This is at odds with the idea that fat is unhealthy, of course, so it may not be surprising that those adhering to current nutritional dogma would infer that any healthy diet must be low fat, so lowering carbohydrate leaves only raising protein. As discussed in the last post, our beliefs are always conditioned on other beliefs, and obviously placing undue weight on some supporting hypothesis leads to poor inferences. Even a moment's consideration of the Inuit diet, for example, would indicate the true nature of a healthy low carbohydrate diet.

Anyway, I could spend many more paragraphs discussing The Jungle Effect (I made a ton of notes while reading - something that the Kindle, for all its flaws, is good for). But I think you get the point. Hopefully Dr. Miller takes the time to read this review in the intended spirit, which is not to bash her work. I think some of what she espouses has value, and I love the idea of studying indigenous diets, provided it's done in an appropriately broad context. But the conclusions one draws from this study need to be consistent with the all of the actual relevant scientific evidence, not just the arbitrary socially-driven beliefs that form "consensus". Otherwise you risk coming to unjustifiable and/or inconsistent conclusions and sub-optimal recommendations, forcing the addition of ad hoc hypotheses, artificial dietary rules, etc. As I've said, changing lifestyles is hard enough without a lot of extra rules to follow. A healthy diet should be easy. Making it hard and motivated by inconsistent rationales just reduces the chances that people will actually make the change and improve their health.


Stephan Guyenet said...

Nice post. I think I will skip this book.

The problem with your theory of atherosclerosis is it makes too much sense. You need to come up with something wackier like carrots cause atherosclerosis, then maybe you can have a chance of getting it accepted.

By the way, I recently read the book "The Great Cholesterol Con" by Anthony Colpo (there are two books out there with the same title). Despite the sensationalist title, it's a great overview of the data on heart disease, cholesterol/saturated fat/total fat, other factors and health. It's more comprehensive than GCBC. He has several awesome tables that sum up the results of epi and intervention trials on fat/saturated fat. He is clearly very well read. I highly recommend it.

Dave said...

Thanks Stephan.

(-: Everyone knows carrots *prevent* atherosclerosis, because if you feed bunnies carrots, they don't develop heart disease. Of course, when eating their natural diet of lions and tigers, it's plaque galore. :-)

I read Colpo's book some time back, and agree that it is a great review of the evidence, probably the best I've seen. My only problem with it was that I remember Colpo being a bit over-enthusiastic, and not applying the same standard of evidence to his own hypotheses as applied to others'. Definitely worth reading, though.

Stephan Guyenet said...

That's exactly how I felt about it! He roasted his opponents for using epi data to support their conclusions, then he used it himself to support the stress link. Still a great book though. I'd pay the $15 just to get the tables in it.

Anonymous said...

My belief in the diet-heart hypothesis (dietary saturated fat and cholesterol cause atherosclerosis) took a serious hit when Dr. George Bray didn't even bother to defend it in his review of Taubes' book, GCBC.

As I recall, he wrote something like, "you decide for yourself."

That's good advice, but how many of us have the time?

Dave said...

Hi Steve. I've asked several experts to provide any sort of rationale for the diet-heart hypothesis, and have come up with a big zero. People are firmly convinced of its truth, but when asked to supply supporting evidence it doesn't get much farther than the Seven Countries Study. The evidence from controlled studies as well as other epidemiological studies seems to equivocal (some show positive correlation, some negative, some none). The only hypothesis consistently supported by these results is that dietary saturated fat has no effect on CHD development, and that any significant observed correlation is probably due to correlation of saturated fat intake with some other causal variables in the particular dataset.

Suppose one removed the saturated fat nonsense and started from scratch. The development of atherosclerotic lesions is much more well understood today than when the diet-heart hypothesis got its start. Starting with that knowledge, combined with what is known about lipoprotein metabolism and the inflammatory response to oxidized/glycated LDL, I suspect most people would come up with a very different version of the diet-heart hypothesis. The erroneously high weight placed on the saturated fat hypothesis effectively blinds people. It's a great example of "pseudo-logic": starting from evidence that is assumed correct, one follows rational thinking to a hypothesis. The problem is that far too much weight was placed on the original evidence, so the hypothesis, while following "logically", actually carries much less weight than is presumed.

I'm still waiting for anybody to mount any sort of reasonably coherent response to Taubes' book. All of those I've seen so far amount to "He must be wrong, because we're right".

The Jungle Effect gives a good example of how pseudo-logical reasoning pollutes what otherwise would have been a clean scientific process. Dr. Miller started with a reasonable hypothesis: diet may be responsible for disease, thus in populations show low incidence of some disease, they are either protected by some food or by the absence of causative food(s) in diseased populations. So, for example, she puts a pre-diabetic patient on the Tarahumaran diet, and presto, the problem fixes itself. Several similar examples are given in the book, all of which support the core hypothesis. Great scientific method, right? The problem is that she then tries to explain all of this in terms of a bunch of other nutritional hypotheses (like diet-heart), and winds up with a mess of contradictions and paradoxes. Had she stuck with the actual evidence she had, the whole thing would have been nicely self-contained and consistent.

Anonymous said...

LOVED this post. I just finished reading Uffe Ravnskov's book The Cholesterol Myths. He pretty much dismantles the "evidence" on the diet-heart hypothesis. One wonders how scientists like Dr. Miller and Ancel Keyes can be so convinced of the "truth" of ideas that have no basis in science. Such is the power of belief, whether in reason or dogma.

Dave said...

Thanks Ellen.

What I find usually happens is that people are too quick to listen to the "voice of authority". Ancel Keys had some kind of agenda, if only to advance his own career and standing in the scientific community (for which he was quite successful). Others like Dr. Miller assume that Keys position is authoritative, if only because he is supported by the weight of *opinion*. What's lacking is any sort of critical thinking about the evidence, particularly when confronted by apparent contradictions. "The Jungle Effect" would have been far more compelling had Dr. Miller simply stuck to the actual evidence she had: when people changed to the diet she recommended, they experienced improvements in health. Trying to reconcile that with the rest of nutritional dogma is pointless, because the existence of the nutritional dogma (right or wrong) changes the observations of how health improves with these dietary changes.

BTW, I believe that the results Dr. Miller saw are nicely explained by the hypothesis of how food affects hormones (or the effects of hormones) like insulin. This hypothesis also encompasses the results seen for low-carbohydrate diets (not "high protein diets", where Dr. Miller seems to be confused). I have yet to see any evidence contradicting the food/hormone hypothesis.

Anonymous said...

I agree. One of the reasons I loved the Colpo and Ravnskov books was because the authors actually read the studies they quoted.

It seems to me that most doctors and journal editors don't do that much, and the result is that researchers are able to write summary statements that don't reflect the actual data. Thus begins the lie of "authority".

It's mind boggling to me that medical professionals don't have the time or inclination to really look at the data on which they base patient treatment.

It's also clear to me that the food/hormone hypothesis is the strongest, and Taubes book can only be ignored for so long. He has said he is going to write a "layman's version" and I hope once the American public really understands the relationship between food, insulin, blood sugar and health, they will begin to question the advice of the mainstream medical establishment in mass. I'm hoping for a revolt at the grass roots level..

Unknown said...

Love your blog!


Dave said...

Thank you.

Diet said...

Hi Dave,
My english is poor, so I read over 2 hours but It was very interesting. Thanks