Home Posts tagged "Fish Oil"

Strength and Conditioning Stuff You Should Read: 7/24/13

Here's this week's list of recommended strength and conditioning reading/viewing:

The Mobility Manifesto - This is a series of free videos Mike Robertson just released to kick off the launch of his new product.  It's top-notch stuff that could be a seminar in itself, so take advantage of this free opportunity to get some great information.

Fish Oil and Prostate Cancer - Dr. Hector Lopez has a great response to the recent (media sensationalized) assertion that fish oil may lead to an increase in prostate cancer risk.

Do You Need to Squat Deeply? - This might be the article of the year at T-Nation, in my eyes.  Dean Somerset did a really good job of answering this question - and the answer is different for everyone.

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Omega-3 Madness: Clarifying Recent Fish Oil “Research”

Today, I have a fantastic guest post from Dr. Hector Lopez, an expert in the world of nutritional supplements.  This post comes in response to a mainstream media report (you can read it here) that called into question the benefits of fish oil.  Hector and I had emailed privately about the concerns he had with this study, and I asked if he'd be willing to share his feelings with a larger audience.  Enjoy! -EC


I have been asked for my professional opinion on the recent attention drawn to the September 2012 systematic review and meta-analysis published in the prestigious Journal of the American Medical Association by Rizos EC et al [1].

As you can imagine, the few days have been very busy answering emails/calls from various stakeholders in the dietary supplement and omega-3 fish oil industries. The stakeholders range from friends and family to fellow scientists and colleagues, to high-level executives and principals of client companies. I have a few things to say about the manner (at times disingenuous) in which the meta-analysis has been misrepresented.

Multiple video segments from major media outlets have even quoted some of their experts as saying, “they would rather the public spend their money elsewhere as the proof is in with this study.” Perhaps they would feel more at ease suggesting the consumption of another box of "whole-grain" yet low fiber, highly processed cereal, "natural fruit juice," or better yet, "linoleate-rich vegetable oils full of omega-6 fatty acids” (hey, they are polyunsaturated too, right)? ☺

I don't mind the media sharing their opinion, but at the very least, they should attempt to educate the very audience that they are obviously trying to persuade. I find it hard to believe that the public would not be interested in some other material facts to allow consumers to make an informed decision:

1. Out of over 3600 clinical studies and citations retrieved, ONLY 20 were used in this "analysis."

2. The absence of statistically significant association in these 20 studies between omega-3 and cardiovascular disease (CVD) endpoints does not prove that a significant reduction of CVD with omega-3 does not occur.

3. These 20 studies were on a diseased population that were already using multiple cardiovascular drugs such as beta-blockers, statins, niacin, fibrates, resins, and anti-thrombotics - all of which clearly confound outcomes/ endpoints of interest to dilute and wash-out effects of long-chain omega-3 polyunsaturated fatty acids (PUFA). Fish oil at this low dose was likely "too little, too late" to show any statistically significant benefit.

4. A similar meta-analysis on secondary prevention was published earlier this year [2].  And, clearly, the older studies showed benefit as these patients were likely not on as many cardio-protective medications. Hence, their was less of a "washout" in effect size.


5. A mean dose of less than 1.4g of EPA + DHA (the fish oils) was used in all 20 studies. This dose is typically far too low to compensate for the overabundance of omega-6 PUFA and imbalance in omega-6:omega-3 consumption in standard western diets. It’s no surprise that previous studies showing benefit of omega-3 fish oil in heart disease have utilized at least 2g of EPA + DHA. Future studies should also take this into consideration. In addition, future studies should attempt to carry out prospective data collection beyond two years.

6. There was no mention, consideration or control for background dietary intake of EPA/DHA or tissue fatty acids profiles. The researchers did not control for this important variable within each individual study included in this meta-analysis, and as a result, there is no way to determine if placebo groups already had sufficient levels of omega-3 in their diet or tissue, which would make it harder to demonstrate treatment effects of fish oil.

7. Clearly, these 20 studies were not adequately powered to detect changes in the CVD endpoints with omega-3 long-chain-PUFA, even if they were in fact present.

8. Interesting, despite all these flaws, based on the Confidence Interval data, there was still a "trend" toward cardioprotection! This was observed in terms of sudden death, myocardial infarction, cardiac and all-cause mortality. In other words, the data in this article still trended toward decreased risk of various cardiovascular disease outcomes. However, the headlines wouldn't be juicy enough, though, so that was clearly glazed over. Hmm...

9. Sure, most Americans should eat more fish (in their whole food diet), but honestly, how many actually do? Where is the press coverage or meta-analyses looking at PCB/ Dioxin/ Persistent Organic Pollutants/Heavy Metal exposure? I suppose that when this omega-3 story dies down, the environmental toxin exposure story can quickly fill that void.

10. The findings of this selective meta-analysis are in direct conflict with the totality of the scientific evidence that demonstrates a cardiovascular benefit from fish oil in healthy populations, as well as in many of the populations with pre-existing CVD [3-10]. Consumers and health care providers alike continue to feel confident in the use of high-quality omega-3 fish oil for not only cardiovascular benefit, but also for supporting the health of just about every organ system in the body. The long chain omega-3 essential fatty acids found in fish oil are critical for everything from the cardiovascular system to the brain and nervous system, immune system, skin, joint and musculoskeletal tissues, to carbohydrate and lipid metabolism and beyond [11-19].

Finally, there is the issue of the potential mega-misrepresentation created by meta-analyses. It is evident that study selection criteria - as well as data extraction/synthesis - may allow researchers to make assumptions of consistency in the design individual studies included in the meta-analysis. As such, these assumptions may lead the authors – or worse, the less discerning media– to drawing erroneous conclusions. These erroneous conclusions then get virally disseminated throughout the general public. Doesn’t this string of events sound eerily familiar?

About the Author
 
Dr. Lopez is recognized for applying his uniquely diverse expertise in spine and sports medicine, endocrinology and metabolism, nutrition & exercise science, and clinical research to improving not only the health and quality of life in his patients, but also athletic performance in recreational and elite athletes. Dr. Lopez received his specialty training at the world-renowned Northwestern University Feinberg School of Medicine-Rehabilitation Institute of Chicago. He is currently a principal and the Chief Medical Officer of the Center for Applied Health Sciences, a multidisciplinary Clinical Research Organization in Ohio, and Supplement Safety Solutions, a Nutravigilance, Quality Assurance/Safety and Regulatory consulting company focused on dietary supplement/nutraceutical industry. An international speaker, author of popular press and peer-reviewed scientific journal articles, product developer, he consults for the nutritional supplement industry and professional athletes from the NFL, NBA, MLB, NHL, and Martial Arts. You can follow him on Twitter at @DrHectorLopez.

Note: You can find references for this entire article in the first post in the comments section below.

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5 Quick and Easy Ways to Feel and Move Better: Installment 1

My "random thoughts" pieces are some of my favorite writings that I've ever published, and today seemed like a good day to throw out some quick and easy ideas on how you can feel better, move better, lose fat, gain muscle, get strong, and - if you're super-motivated - take over the world.  Here goes... 1. Get a good training partner. There are random dudes you meet at the gym who provide a mediocre lift-off on the bench press here and there, and then there are dedicated training partners.  There is a big difference.  A good training partner will tell you to get your act together and train hard when you're slacking off, or even hold you back when your body is banged up, but you're stupidly trying to push through it.  It's guaranteed accountability, motivation, expertise, safety, competition, and all-around awesomeness.  To be honest, I often wonder if most people get the best results working with a trainer/strength coach for these factors more than the actual expertise the fitness professional provides!

2. Make your bedroom a cave. One of the best investments my wife and I made when we bought our new house were reinforced window shades for our bedroom so that very little light could get through when they were down.  They make a dramatic difference in terms of how dark you can make your room at night (especially if you have street lights near your residence) and were 100% worth the extra cost, as compared to regular shades. Even if you don't want to spend the extra few bucks on souped-up shades, though, you can still get some of the benefits of "cave sleeping" by blocking out light from cell phones, alarm clocks, and - if you're a frat boy - bright green neon signs of your favorite beer in your dorm room.  Also, do your best to shut the TV and computer off at least thirty minutes before you hit the sack as well, as it'll give your brain time to wind down and transition to some deep, restful sleep. 3. Take Athletic Greens. I've always been a non-responder to supplements.  As an example, I never gained an ounce when I started taking creatine in 2001, and never noticed a huge difference in sleep quality when I started taking ZMA. Still, I pretty much trust in research and go with these supplements, plus mainstays like fish oil and Vitamin D and assume that they're doing their job.  It's interesting how some of the most essential supplements we take are the ones where we might notice the most subtle difference, isn't it? Anyway, in 2011, I added Athletic Greens to this mix.  I look at it as whole food based "nutritional insurance" use it in place of my multivitamin.  I think it's solid not only as a greens supplement (which, incidentally, doesn't taste like dog crap), but also because it directly improves gut health to improve absorption of micronutrients.  With loads of superfoods, herbal extracts, trace elements, antioxidants, and pre- and probiotics, I could tell that it would be something that would decrease inflammation and improve immunity (something I've viewed as increasingly important with each passing year as life has gotten more stressful with the growth of Cressey Performance).

Interestingly, one of our long-time athletes who is now playing baseball at a highly ranked D1 university, started taking Athletic Greens after we chatted about it this summer, and he sent me this note: Hey Eric, thanks for the recommendation on Athletic Greens. I love the product! I have not gotten sick once since I started taking it 4 months ago, and my body feels better than ever. This is the first semester I haven't gotten sick. Hope all is well!  I guess I'm not the only one who likes it!  Check it out for yourself here. As an aside, they do a pretty cool combination where you can get greens, fish oil, and vitamin D all at once at a great price, and the fish oil is excellent quality. We have several athletes who get everything in this one place for convenience. 4. Go split-stance. Last week, in my popular post, Are Pull-ups THAT Essential?, I included the following video of forearm wall slides at 135 degrees, a great drill we like to use to train upward rotation, as the arms are directly in the line of pull in the lower traps.  With this exercise, we always cue folks "glutes tight, core braced" so that they don't just substitute lumbar extension in place of the scapulae moving into retraction/depression on the rib cage.

Unfortunately, these cues don't work for everyone - particularly those who are super lordotic (huge arch in their lower back).  A great "substitute cue" for these folks is to simply go into a split stance, putting one foot out in front of the other (even if it's just slightly).  As you have probably observed in performing single-leg exercises like lunges and split-squats, it is much harder to substitute lumbar extension for hip extension than it is with bilateral exercises like squats and deadlifts.  Fortunately, the same is true of substituting lumbar extension for scapular movement on the rib cage.  So, if you're struggling with the exercise above, simply move one foot out in front of the other and you should be golden.

5. Get some assessments done. Imagine you were about to embark on a cross country trip with a great vacation in mind in, say, San Diego.  However, I didn't tell you where you were starting the journey.  While you might get to where you want to be (or at least close to it), it'd make the trip a lot more difficult. You'd probably blow a bunch of money on gas, sleep in some nasty motels in the middle of nowhere, pick up an awkward hitchhiked who smells like cabbage, and maybe even spend a night in a Tijuana jail along the way.  Not exactly optimal planning. A strength and conditioning program isn't much different than this cross-country trip.  If you don't know how your body works - both internally and externally - you need to learn before you subject it to serious stress.  Get some bloodwork done to see if you have any deficiencies (e.g., Vitamin D, iron, essential fatty acids) that could interfere with your energy levels, ability to recover, or endocrine response to exercise.  Likewise, consult someone who understands movement to determine whether you have faulty movement patterns that could predispose you to injury.  I think this is one reason why Assess and Correct has been our most popular product ever; it gives folks some guidance on where to start and where to go.  Otherwise, the strength and conditioning program in front of you is really just a roadmap, and you don't know where the starting point is.

These are just a few quick thoughts that came to mind today, but I'll surely have many more in the follow-ups to this first installment.  Feel free to post some of your own ideas in the comments section below, too! Sign-up Today for our FREE Newsletter and receive a four-part video series on how to deadlift!
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Strength and Conditioning Stuff You Should Read: 11/28/11

Here's a list of recommended strength and conditioning reading to kick off the week: 13 Fun Facts About Optimal Shoulder Performance - Because our OSP DVD set is on sale for 15% off until tonight at midnight, I figured it'd be a good chance to highlight a bit about the product and its creators.  (Click here to purchase the DVD, by the way) Trigger Points and a Sympathetic State - This is Patrick Ward's follow-up blog to the one on soft tissue therapy and stress resistance that I mentioned last week.  Part 2 is just as good as Part 1! Flax Oil vs. Fish Oil - This was a well-researched piece by Robert Yang on a topic about which I've had many client inquiries over the years.  It'll be nice to have a resource to which I can send them. Sign-up Today for our FREE Newsletter and receive a four-part video series on how to deadlift!
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Random Friday Thoughts: 6/26/09

1. I'm writing this on Thursday night as Bill Hartman, Mike Robertson, and I collaborate across several states (them in IN, and me in MA) to finalize the plan of attack for the DVD we'll be filming out in Indy on Saturday.  We're really struggling to decide which of the following two costumes we want Mike to wear.

ultimatewarrior014

viking

I supposed we could just dress him up as a viking with tassels and get the best of both worlds.  I guess you'll just have to buy the DVD to find out for yourself.

2. I just read this week that researchers here in Boston are going to be looking into why girls hate guys who listen to techno the role of Vitamin D and fish oil in reducing the risk of cancer, heart disease, and strokes.

3. We are going to be revamping the Cressey Performance website pretty soon, so be sure to keep an eye on it in the weeks to come.

4. Speaking of CP, a huge congratulations goes out to Cressey Performance athletes Sahil Bloom and Justin Quinn, who were both named to the Spring 2009 Boston Globe All-Scholastic Team.

From the write-up: "Bloom was MVP of the Dual County League Small, posting a 6-0 record with 3 saves, a 0.90 ERA, and 61 strikeouts in 46‚ innings. He finished his career 22-6 with a 1.95 ERA."  And, "Quinn was MVP and won the batting title in the Dual County League Large, batting .488 with five home runs. The four-year starter finished his career with a .386 average and 20 home runs."  Nice job, fellas!

5. I absolutely LOVED Alwyn Cosgrove's contribution to the latest Mythbusters article at T-Nation this week.  If you are a treadmill-aholic or know someone who is, definitely give it a read.

6. If I get one more email this week from someone trying to sell me a supplement in a pyramiding scheme, I'm going to flip my s**t.  If you need a pyramiding scheme to sell something, then it's a crap product in the first place.  And, if you have people who know NOTHING about the product they're pushing, then you have an entirely crap business model, too.

Actually, now that I think about it, these supplement pitch emails are amusing.  I might start posting them as blogs to discuss the commonalities of cheeseball supplement pimps - as I began to cover in item #13 HERE.

Off to Indy tonight.  Hopefully those pleasant, patient Midwestern folks can calm me down.  Have a great weekend!

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Birthday Blogging: 28 Years, 28 Favorites

I turn 28 today, so in hopes of distracting myself from the painful realization that I'm starting to go bald, I thought I'd focus on the positives of my existence in contexts that would appeal to you.  Below, you'll find 28 of my favorite things - most of which are at least loosely related to fitness, nutrition, strength and conditioning, and sports. 1. Favorite Nickname: Power Alleys.  This seemed like a good starting point, as power alleys are bald spots.  Credit for this one goes to Mets pitching prospect Tim Stronach. 2. Favorite Thing About Cressey Performance: The camaraderie among the athletes/clients. I think the hard thing to appreciate about our facility without experiencing it first-hand and being there on a regular basis is that it's as much about the environment and attitude as it is about the expertise and programming.  I'm psyched that we've not only created an environment where clients can improve physically, but one in which they can thrive socially, too. 3. Favorite Book I've Read Related to Fitness: Diagnosis and Treatment of Movement Impairment Syndromes, by Shirley Sahrmann.  This book got me thinking more about dysfunction and less about pathology.  Quality of movement is often far more important than anything a MRI or x-ray can ever tell you.

sahrmann

4. Favorite Book I've Read Unrelated to Fitness: This is a top-up between The Tipping Point and A Prayer for Owen Meany.  They might be taken over, however, by one of the gifts I just got for my birthday from CP Client Steph Holland-Brodney.

howdoyoulightafart

5. Favorite DVD I've Watched: The Indianapolis Performance Enhancement Seminar DVD Set.  Bill Hartman's presentation on "Stiff vs. Short" alone makes this a fantastic resource, and the rest is just gravy.  I reviewed it HERE. 6. Favorite DVD I've Co-Created: The Building the Efficient Athlete DVD set.  I think I'm most proud of this resource because it's something that provided something I so desperately wanted - but couldn't get - during my college education.  Effectively, it's a resource that blends book memorization with real-world practice with a focus on functional anatomy, assessments, and troubleshooting common exercises.

btea_set

7. Favorite Seminar I've Attended: The Perform Better 3-Day Functional Training Summit.  Each year, they get better and better.  Check out Chicago or Long Beach this year if you missed Providence. 8. Favorite Athlete of All Time: Barry Sanders.  I can't imagine an guy with better kinesthetic awareness, body control, or ability to turn a complete disaster of a play into a 90-yard touchdown run - while carrying two defensive linemen on his back. 9. Favorite Athlete of All-Time that you've probably never heard of: Jerry Sichting.  He played for the Celtics from 1985 to 1988, and I'll always remember the night Sichting - at a heigh of 6-1 - got in a fight with 7-4 Ralph Sampson during the 1986 NBA Finals.  At the time, I was a five-year old shadow boxing in my living room yelling at the top of my lungs.

schiting_sampson

10. Favorite Place to Visit: Fenway Park 11. Second Favorite Place to Visit: Gampel Pavilion at the University of Connecticut.  It's an incredible environment in which to watch college basketball, and it's also where I spent just about all my time from 2003 to 2005. 12. Favorite Exercise: was this ever in question?

13. Favorite Sites I Visit Just About Every Day: T-Nation.com, MinorLeagueBaseball.com, ESPN.com, Sports.Yahoo.com, WilliamInman.com, 38Pitches.com, ShawnHaviland.Blogspot.com, MetrowestDailyNews.com, StrengthCoach.com, MikeReinold.com, RobertsonTrainingSystems.com, BillHartman.net, AlwynCosgrove.Blogspot.com, DieselCrew.com, PrecisionNutrition.com, BrianStPierreTraining.com, Tony Gentilcore's Blog, Boston.com, BarstoolSports.com, Facebook.com, EricCressey.com.

14. Favorite Kind of Injury to See (weird category, I know): Labral Tears (SLAP lesions), or really any kind of shoulder or elbow pain in pitchers.  You've got so many potential causes that it's kind of fun (for me, not the athlete) to go through a process of elimination to see what combination of factors caused it.  There are all the classic flexibility deficits in pitchers, plus scapular instability, poor thoracic spine mobility, plus faulty mechanics, plus inappropriate training volumes, plus weak lower bodies.  It's kind of like peeling back the layers on an onion to see what shakes free.  It's also a great scenario to illustrate what I talked about with respect to diagnostic imaging in #3 from above.  All of these guys will have labral fraying and rotator cuff partial thickness tears at the very least; it's our job to fix them up and make them work efficiently in spite of these structural deficits in situations where surgery isn't warranted.

15. Favorite Class I Took in School: Gross Anatomy.  Yes, I cherished the semester I spent with a bunch of cadavers.

16. Favorite Healthy Food: Apple-Cinnamon Protein Bars from John Berardi's Gourmet Nutrition Cookbook. Admittedly, I often just eat the batter before it ever gets cooked.  Not good, I know.

17. Favorite Piece of Equipment We Have at CP: Giant Cambered Bar.  Along with the safety squat bar and front squat set-up, this bad boy has allowed me to keep squatting even though my right shoulder decided a long time ago that traditional back squats weren't a good idea.  It's also a great asset for working with overhead throwing athletes who should avoid the externally rotated, abducted position under load.

18. Favorite Thing About Having a Blog: I can write a lot more casually than in my newsletter, which tends to be more geeky.  And, I can post videos of this kid rocking out:

19. Favorite Mobility Drill: Walking Spiderman w/Overhead Reach.  I love this drill because you're covering so many things at once.  You'll get thoracic spine extension and rotation from the reach, and hip flexor and adductor length in the lower body from the lunge angle.  Keep an eye out for more new movements along these lines in the months to come as we film the sequel to the Magnificent Mobility DVD.

20. Favorite Pastime I Had to Give Up: Fantasy Baseball/Basketball.  During my sophomore year of undergrad, I finished fourth in the world in NBA.com's Virtual GM contest.  Long story short, if you want to be really good at fantasy sports with that kind of set-up, you've got to put a lot of time into it - and realize that it won't make girls like you.  You'll also find yourself watching games in which you'd otherwise have absolutely no interest. I couldn't do it half-ass (aside from the CP Fantasy Football League), so I gave it up.

21. Favorite Inedible Toy: Rubber Steak.

ecrubbertoy

Suffice it to say that Fire & Ice wouldn't allow us to eat a birthday cake inside their restaurant on Saturday night in celebration of my awesomeness.  So, in celebration of their suckiness, none of us (16 in all) will ever eat again - and I was reduced to gnawing on dog toys.

22. Favorite Birthday Excitement: Apparently, it's going to be taking my car in to get work done, buying a new laptop, and then coaching 'em upat CP.  There will also be a dominant upper body lift at CP that will undoubtedly feature Kevin Larrabee missing 300...again...and again).

23. Favorite Bench Press Celebration Spectacle: Antwan Harris, post 340 bench press.

24. Favorite Strength and Conditioning Coach Who is Having Surgery on my Birthday: Josh Bonhotal, Chicago Bulls.  I talked with Josh yesterday and he informed me that he was finally having his ACL fixed today in celebration of my birthday.  Nothing says "Happy Birthday, Buddy" like taking a chunk out of your patellar tendon and turning it into an anterior cruciate ligament.  It's kind of like planting a tree on Earth Day.  What a nice gesture.

25. Favorite Article Series I've Written: A New Model for Training Between Starts (Part 1 and Part 2).  These articles were actually picked up by Collegiate Baseball Magazine as front-page features, and I received a lot of great feedback about them.  If there is one thing I do before I retire, it's convincing the world of the evils of distance running for pitchers.  I'd put the Shoulder Savers series in a close second

26. Favorite Supplement: Fish Oil.  It's followed closely by Vitamin D.  You need both - and probably a lot more than you think. I'm a simple guy when it comes to this stuff.

27. Favorite Random Website a Buddy Texted to Me Last Week: www.EasyCurves.com.  This thing is hilarious. A special thanks goes out to Jesse Burdick for making me just a little bit dumber with that.

28. Favorite Sign of Athlete Dedication for the Month: We have two college pitchers up here from Pennsylvania for the month to work on getting bigger, stronger, faster, and more flexible in hopes of a nice velocity jump on the mound, and the obvious injury prevention benefits of such training.  That's all well and good - until you hear that they got an unfurnished apartment in Hudson, MA.  These guys are sleeping on mattresses on the floor, and all they brought were a few lamps, a TV, some books, and a whole lot of enthusiasm and motivation.  That's committment to training - and just the kind of guys we like to have around Cressey Performance.

cp

What kind of sacrifices are you making to get better and move closer to your goals?  I'm not sure that sleeping on a mattress on the floor is necessary, but it says a lot.

With that in mind, I'm not taking today off.  There is work to be done and I love to do it, birthday or not.

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Fishy Advice, Part II

By Eric Cressey

It's time to pick up where I left off last month in Part I.  To "reset" the stage, I'll just say that fish oil is good because it helps with:

Crohn's Disease:

  • Belluzzi et al (1996) found that 2.7 g of fish oil per day for one-year significantly reduced the incidence of relapse in Crohn's patients in remission. Thirty-nine of the patients received the fish oil, while 39 others received a placebo; the relapse rate was 41% lower in the former group. Regression analysis indicated that the positive effects of fish oil were independent of patient age, sex, previous surgery history, disease duration, and smoking status (34).

Ulcerative Colitis:

  • Barbosa et al (2003) hypothesized that omega-3 fatty acids from fish oil tend to exert their anti-inflammatory effects in ulcerative colitis via decreases in plasma oxidative stress, acting as free radical scavengers (35).
  • In a study of eighteen patients with active ulcerative colitis (characterized by diarrhea and rectal inflammation; ain't that a pretty picture?), four months of 5.4 g combined EPA and DHA supplementation (vs. placebo) led to significantly "reductions in rectal dialysate leukotriene B4 levels, improvements in histologic findings, and weight gain (36)." English translation: their rectums looked, felt, and performed better.

Asthma:

  • Nagakura et al (2000) found that ten months of EPA and DHA supplementation lessened asthma symptoms and acetylcholine sensitivity in 29 children with severe bronchial asthma (in collaboration with a controlled environment and diet) (37).
  • Three weeks of 5.4 g combined EPA and DHA markedly blunted exercise-induced asthma in ten elite athletes and improved post-exercise pulmonary function significantly (38).

Cystic Fibrosis:

  • In a study of thirty cystic fibrosis patients that received EPA and DHA supplementation as 1.3% of their total calories for eight months, researchers noted significant decreases in markers of inflammation. Subtle improvements in forced expiratory volume (a measure of pulmonary function) were noted as well. Furthermore, in comparison with the previous eight-month period, the patients (collectively) required much fewer days (392 vs. 721) of antibiotic therapy during the eight months on EPA and DHA (39).

Chronic Obstructive Pulmonary Disease (COPD):

  • Shahar et al (1994) examined the relationship between dietary omega-3 fatty acid intake and COPD in 8,960 smokers, finding that combined EPA and DHA intake was "inversely related to the risk of COPD in a quantity-dependent fashion (40)." In other words, if you're going to smoke, you might as well complement that metallic cough with some fish breath; it'll probably protect you from COPD down the road.
  • Romieu and Trenga (2001) observed that "data also suggest that omega-3 fatty acids may have a potentially protective effect against airway hyperreactivity and lung function decrements" in both children and adults (41).

Sickle Cell Anemia:

  • In patients with sickle cell disease, omega-3 fatty acid supplementation at 0.1 g/kg per day "reduced the frequency of pain episodes requiring presentation to the hospital from 7.8 events during the preceding year to 3.8 events/year." Conversely, subjects receiving dietary olive oil (the control group) experienced 7.1 pain events/year, only slightly less than the 7.6 event average from the previous year. This reduction in pain episodes was likely attributable to the effects of EPA and DHA on reducing prothrombotic activity (42).
  • A study of Nigerian children found that omega-3 fatty acid concentrations were 40-50% lower in the phospholipid membranes of children with sickle cell disease than in those of healthy children. The researchers noted that "the phospholipids of the children with SCD are less fluid relative to those of their healthy counterparts. (43)"

Menstrual Symptoms:

  • In a Danish study, low intakes of omega-3 fatty acids were correlated with more severe menstrual symptoms. Dysmenorrhea correlations were also observed in low omega-3: omega-6 ratios and vitamin B12 deficiencies. The body utilizes omega-3s to create type-3 prostaglandins that are less "aggressive" than those formed from other fatty acids. The net result of utilizing omega-3s as raw materials appears to be milder symptoms. Prostaglandins act like hormones, controlling uterine contractions and pains (44).

Vision/Eye problems (glaucoma):

  • Ninety days of DHA with vitamins E and B significantly improved computerized visual field (CVF) and retinal contrast sensitivity in thirty chronic glaucoma patients. The researchers concluded that such a supplement merits inclusion in an intervention to prevent the progression of glaucoma-related damage (45).

Multiple Sclerosis:

  • Cunnane et al (1989) found that in comparison with their healthy counterparts, MS patients had lower omega-3 fatty acids in their plasma (46).
  • As a follow-up, Gallai and colleagues (1995) found that omega-3 supplementation in MS patients led to decreases in proinflammatory eicosanoids, indicating potential for fish oil in modulating some immune function decrements associated with MS (47).

Prenatal and postpartum support:

  • Supplementation with DHA between the 24th and 28th week of pregnancy significantly increased (by roughly six days on average) the duration of gestation. Birth weight, length, and head circumference all increased slightly as well (48).
  • A study of Norwegian children found that "use of cod liver oil in the first year of life was associated with a significantly lower risk of type 1 diabetes." Regression analysis implied that this effect was independent of the oil's vitamin D content, and was likely due to the omega-3 fatty acids in the oil (49).
  • Malcolm et al (2003) noted an association between "the DHA status of infants at term and early postnatal development of the pattern-reversal VEP [visual evoked potential], indicating that DHA status itself may influence maturation of the central visual pathways" in infants. These assertions were based on results seen in a trial of one hundred women that received either fish oil capsules or a placebo (50).
  • Uauy and colleagues (2003) found not only that long chain polyunsaturated fatty acid supplementation in newborns improved visual acuity at four months, but also there was "a significant relation between the total DHA equivalents provided and effectiveness (51)." In other words, more was better (to a certain point, of course). This effect is likely due to effects on physical properties of the membranes, neurotransmitters, and modulation of gene expression in the retina and brain (52).
  • Because of the crucial role of essential fatty acids as structural components of all cell membranes, profound implications can be seen at the "brain, retina and other neural tissues are particularly rich in long-chain polyunsaturated fatty acids (LC-PUFA) (52)."
  • Uauy et al (2001) asserted that "light sensitivity of retinal rod photoreceptors is significantly reduced in newborns with n-3 fatty acid deficiency, and that docosahexaenoic acid (DHA) significantly enhances visual acuity maturation and cognitive functions (52)." Furthermore, "DHA also has significant effects on photoreceptor membranes and neurotransmitters involved in the signal transduction process; rhodopsin activation, rod and cone development, neuronal dendritic connectivity, and functional maturation of the central nervous system (52)." It beats feeding potato chips to your kids, doesn't it?
  • Data from Dunstan et al (2003) suggests that there may be a role for omega-3 fatty acids in the prevention of allergic disease. In a study of 83 atopic pregnant women receiving fish oil or placebo, the researchers noted that infants from the fish oil group had significantly less severe atopic dermatitis at age one, although no difference in the frequency of the disease was apparent between groups (53).
  • Williams and colleagues (1995) described preeclampsia (affecting pregnant women) as "a systemic disease characterized by diffuse endothelial dysfunction, increased peripheral vascular resistance, coagulation abnormalities, antioxidant deficiency, persistent elevations of maternal leukocyte-derived cytokines, and hyperlipidemia (54)." These researchers conducted a study to examine the relationship between omega-3 fatty acid intake and preeclampsia. Women with the lowest omega-3 levels were 7.6 times more likely than those with the highest levels to have preeclampsia-related complications during their pregnancies. Moreover, "a 15% increase in the ratio of omega-3 to omega-6 fatty acids was associated with a 46% reduction in risk of preeclampsia (54)."

Psoriasis:

  • Psoriatic lesions are characterized by increased concentrations of arachidonic acid. EPA exerts an anti-inflammatory effect that likely works to counteract the pro-inflammatory effects of arachidonic acid and its metabolites. In a study of 83 patients with chronic plaque-type psoriasis, researchers found that omega-3 fatty acid infusions were superior to omega-6 infusions (the placebo) "with respect to change in severity of psoriasis per body area, change in overall erythema, overall scaling and overall infiltration, as well as change in overall assessment by the investigator and self-assessment by the patient (55)."
  • Grimminger et al (1993) observed that high dose intravenous omega-3 fatty acid supplementation exerted a rapid beneficial effect on inflammatory skin lesions in twenty patients hospitalized with acute guttate psoriasis. These effects were most likely mediated through eicosanoid metabolism regulation (56).

Photosensitivity:

  • Hydroa vacciniforme ?also known as photosensitivity ? is a serious skin disorder characterized by blistering (especially on the face) after even the slightest amount of sun exposure; it affects primarily children. In a small study, Rhodes and White reported that three months of fish oil supplementation reduced erythemal sensitivity to UVA and UVB (two types of ultraviolet radiation), and yielded modest improvements in overall symptoms (57).

Diabetes/Insulin Resistance:

  • Increased oxidative stress is a hallmark of type 2 diabetes. Jain et al (2002) sought to determine the effects of very low dose omega-3 fatty acid supplementation (0.6 g combined EPA and DHA) on type 2 diabetics. Even at such a low dose, they found that the patients in the omega-3 group exhibited significantly greater improvements in glycemic status, blood pressure, lipid profiles, and reductions in markers of oxidative stress as compared to a placebo group of type 2 diabetics (58).
  • It's well established that the various types of fatty acids are clearly involved in the onset of chronic conditions (such as insulin resistance and obesity) characterized by inflammation. In overweight subjects, higher concentrations of saturated fats and omega-6 and lower concentrations of omega-3 fatty acids are significantly associated with higher concentrations of circulating interleukin-6 (IL-6), a marker of inflammation. Interestingly, though, these associations are not apparent in lean subjects (59).
  • In a 14-year study of 84,204 female nurses ages 34-59, the risk of type 2 diabetes was significantly positively associated with high consumptions of trans fatty acids and cholesterol, whereas the condition was negatively associated with omega-3 and omega-6 polyunsaturated fatty acids. The investigators estimated that "replacing 2% of energy from trans fatty acids isoenergetically with polyunsaturated fat would lead to a 40% lower risk" of type 2 diabetes (60). I guess it's time to replace the doughnuts in the nurses' lounge with canned salmon. Or, you could contact Krispy Kreme about introducing the chocolate frosted sardine filled doughnut!
  • Chicco et al (1996) found that low-dose fish oil supplementation in rats led to significant reductions in blood lipids and plasma insulin levels without changes in glucose tolerance. The investigators hypothesized that because no changes in pancreatic insulin content were apparent, the lower insulin levels may have been due to improvements in peripheral insulin sensitivity (61).
  • Unfortunately, studies attempting to demonstrate these effects in humans have been less impressive (62-64). In spite of the fact that omega-3 consumption in the form of fish increased HDL cholesterol and improved overall dyslipidemia in overweight patients, Mori et al (1999) found no independent effect of fish consumption on glucose or insulin (62). Others have come to similar conclusions with actual fish oil supplementation (63,64).

Resting Metabolic Rate:

  • Eric Noreen has done extensive work examining the effect of fish oil on resting metabolic rate (RMR). At the 2003 American College of Sports Medicine Annual Conference, Noreen presented the results of a study that compared RMR in subjects supplemented with 9g of safflower oil (predominately omega-6), 3, 6, or 9g of 60% concentrated fish oil. The fish oil groups saw daily RMR increases of 141 to 448 calories, whereas the safflower group's RMR actually decreased. As an added bonus, the fish oil group also lost a little bit of fat mass while gaining some lean body mass. (65)

Body Composition Regulation and Leptin:

  • Leptin is a hormone released by adipocytes that has a great impact on body fat levels. In simple terms, the amount of leptin present in one's body serves as feedback to the brain about whether one is okay as far as nutritional status is concerned. As you get leaner, leptin levels drop; as you get pudgier, they go up. These are important responses, as high leptin concentrations are associated with decreased hunger and food intake and increased energy expenditure, all of which are important factors in getting and staying lean.
  • Unfortunately, as you get leaner, leptin levels drop as your body essentially senses starvation-like conditions; this decrease makes it difficult to get and stay lean. Fish oil may be able to help with this problem, as rats fed high omega-3 diets demonstrate up-regulation in plasma leptin concentrations significantly above what is predicted based on body fat levels (66,67).
  • In an overfeeding study of rats with 42% of their energy intakes as fish oil, safflower oil, olive oil, or beef tallow, the fish oil group had the greater lean body mass gains and the lowest fat mass gains (68). In other words, if you're going to stuff yourself, be sure to include some fish oil in the feast.

Psychological Disorders:

  • Maes et al (1999) observed that there is a significant deficiency in omega-3 fatty acids serum phospholipids and red blood cell membranes in major depression. Furthermore, the deficiency is likely a result of abnormal omega-3 metabolism in depressed patients and may continue in spite of treatment with antidepressants (69). As such, fish oil treatment may serve as an important adjunct to ? or even a replacement for - traditional antidepressant therapy
  • Hibbeln and Salem (1995) proposed that low concentrations of polyunsaturated fatty acids may be related to increased risks of suicide, depression, alcoholism, and post-partum depression (70).
  • Four out of five trials of EPA in the treatment of schizophrenia have demonstrated significant reduction in patient episodes of severe mania and depression following supplementation (71).
  • In an eight-week study of 28 clinically depressed patients receiving either 9.6 g omega-3 fatty acids per day or a placebo, there were significant decreases in scores on the Hamilton Rating Scale for Depression, an evaluative tool on which high scores indicate more severe feelings of depression (72).
  • Zanarini and Frankenburg (2003) studied the effects of 1 g/day ethyl-EPA (or placebo) on thirty females with borderline personality disorder. The ethyl-EPA supplement proved "to be superior to placebo in diminishing aggression as well as the severity of depressive symptoms (73)."
  • Attention-deficit/hyperactivity disorder (ADHD) may be related to an abnormality in polyunsaturated fatty acid metabolism. As such, both Richardson and Puri (2000) and Kidd (2000) have proposed that omega-3 fatty acid supplementation may have merits in the treatment of this condition, although more research is warranted in this regard (74,75).

The Response to Stress:

  • Here's one for the Type A folks out there. Delarue et al (2003) studied seven subjects on two occasions separated by three weeks. In the first session, these seven individuals were subjected to mental stress in the form of mental arithmetic and the Stroop task, and measures of sympathoadrenal activation (plasma cortisol, catecholamines, energy expenditure, and adipose tissue lipolysis) were taken thirty minutes after the stress. After this mental stress challenge, each subject supplemented with 7.2 g fish oil/day for three weeks, at which point they took the battery of tests again. In this second session, plasma epinephrine, cortisol, energy expenditure, and plasma non-esterified fatty acids concentrations, were all significantly lower than in the initial session. The investigators therefore concluded that omega-3 fatty acid supplementation "inhibits the adrenal activation elicited by a mental stress, presumably through effects exerted at the level of the central nervous system (76)." It appears that omega-3 fatty acids are able to partially inhibit the pro-inflammatory response to psychological stress (77). Ever get a racing heart or high blood pressure before a test, presentation, or job interview? Fish oil may be just what you need to get mellow!

Migraine Headaches:

  • In a study of 27 adolescents with chronic migraines, supplementation with fish oil led to reductions of 87% in headache frequency, 74% in headache duration, and 78% in headache severity compared to a period prior to the study. Interestingly, olive oil (the placebo) produced similar results, although they were not quite as favorable (78).

Epilepsy:

  • Many anticonvulsant medications for epileptics have highly undesirable side effects. In light of the profound roles of omega-3 fatty acids in immune and nervous system activities, Rabinovitz and colleagues (2004) compared the effects of carbamazepine (CBZ) and SR-3, a compound with a 1:4 omega-3: omega-6 ratio, on seizure control efficiency, and protection against cognitive impairment and cortisol elevation in rats. While the two treatments were equally effective in controlling seizures, SR-3 proved to be superior on the latter two measures (79). Treating epilepsy with omega-3 compounds is certainly a new frontier, so more research is warranted (especially in human subjects) to determine its true efficacy.

Chronic Fatigue Syndrome (CFS):

  • The exact cause of CFS remains to be determined, but there is speculation that it could involve abnormalities at the immune, neuroendocrine, and autonomic levels. Because fish oil inhibits the production of certain pro-inflammatory substances, many experts believe that it holds great potential in the treatment of CFS. Research is ongoing (80).

Fibromyaglia:

  • Several experts predict a role for omega-3 fatty acids in the treatment of fibromyalgia; anecdotal evidence supports this assertion, and further research is certainly warranted on this front (81).

Cirrhosis:

  • In chronic liver disease, widespread inflammation can cause the liver to become fibrotic. In light of the known anti-inflammatory benefits of omega-3 fatty acids, Hayashi et al (1999) studied the effect of EPA and DHA supplementation on four patients with hepatitis B infection, one with hepatitis C virus cirrhosis, and one with alcohol-related cirrhosis. Subtle reductions were observed in globulin (a marker of liver pathology) with simultaneous increases in HDL cholesterol and various apolipoproteins (protective agents against hepatitis-related liver disease) (82).

Closing Thoughts

If you aren't taking fish oil, you're an idiot. Seriously. Okay, I'll leave you with a bit more practical wisdom instead. The typical fish oil capsule you'll encounter is 1000 mg fish oil; we, however, are more concerned with the EPA and DHA content of that 1000 mg. In most cases, you'll find 180 mg EPA and 120 mg DHA per capsule. A good rule of thumb (especially based on the results of the clinical trials) is to consume 3-6 g combined EPA and DHA per day; at this capsule size, you'd need 10-20 capsules per day. For this reason, liquid fish oil is a great alternative.

A small percentage of people will suffer from fish burps with the EPA/DHA supplementation; if you're one of those individuals, I recommend you take all your fish oil with your last meal of the day. That way, if you have salmon belches, they'll be in your sleep! Another alternative is to just eat fatty fish every day, but that can get old very quickly! Finally, be patient! Read the finer details of all of the studies that I've outlined and you'll realize that the majority of them were at least 6-8 weeks in duration (usually longer). Your body needs time to make good use of these healthy raw materials, so count on a few months before you see noticeable results if you have one of the aforementioned conditions. For the rest of you, you probably won't notice much, but I guarantee that you'll be healthier in the long run. References (continued) 34. Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med. 1996 Jun 13; 334(24): 1557-60. 35. Barbosa DS, Cecchini R, El Kadri MZ, Rodriguez MA, Burini RC, Dichi I. Decreased oxidative stress in patients with ulcerative colitis supplemented with fish oil omega-3 fatty acids. Nutrition. 2003 Oct;19(10):837-42. 36. Stenson WF, Cort D, Rodgers J, Burakoff R, DeSchryver-Kecskemeti K, Gramlich TL, Beeken W. Dietary supplementation with fish oil in ulcerative colitis. Ann Intern Med. 1992 Apr 15;116(8):609-14. 37. Nagakura T, Matsuda S, Shichijyo K, Sugimoto H, Hata K. Dietary supplementation with fish oil rich in omega-3 polyunsaturated fatty acids in children with bronchial asthma. Eur Respir J. 2000 Nov;16(5):861-5. 38. Mickleborough TD, Murray RL, Ionescu AA, Lindley MR. Fish oil supplementation reduces severity of exercise-induced bronchoconstriction in elite athletes. Am J Respir Crit Care Med. 2003 Nov 15;168(10):1181-9. Epub 2003 Aug 06. 39. De Vizia B, Raia V, Spano C, Pavlidis C, Coruzzo A, Alessio M. Effect of an 8-month treatment with omega-3 fatty acids (eicosapentaenoic and docosahexaenoic) in patients with cystic fibrosis. JPEN J Parenter Enteral Nutr. 2003 Jan-Feb;27(1):52-7. 40. Shahar E, Folsom AR, Melnick SL, Tockman MS, Comstock GW, Gennaro V, Higgins MW, Sorlie PD, Ko WJ, Szklo M. Dietary n-3 polyunsaturated fatty acids and smoking-related chronic obstructive pulmonary disease. Atherosclerosis Risk in Communities Study Investigators. N Engl J Med. 1994 Jul 28;331(4):228-33. 41. Romieu I, Trenga C. Diet and obstructive lung diseases. Epidemiol Rev. 2001;23(2):268-87. 42. Tomer A, Kasey S, Connor WE, Clark S, Harker LA, Eckman JR. Reduction of pain episodes and prothrombotic activity in sickle cell disease by dietary n-3 fatty acids. Thromb Haemost. 2001 Jun;85(6):966-74. 43. Glew RH, Casados JK, Huang YS, Chuang LT, VanderJagt DJ. The fatty acid composition of the serum phospholipids of children with sickle cell disease in Nigeria. Prostaglandins Leukot Essent Fatty Acids. 2002 Oct;67(4):217-22. 44. Deutch B. [Painful menstruation and low intake of n-3 fatty acids]. Ugeskr Laeger. 1996 Jul 15;158(29):4195-8. [Article in Danish] 45. Cellini M, Caramazza N, Mangiafico P, Possati GL, Caramazza R. Fatty acid use in glaucomatous optic neuropathy treatment. Acta Ophthalmol Scand Suppl. 1998; (227): 41-2. 46. Cunnane SC, Ho SY, Dore-Duffy P, Ells KR, Horrobin DF. Essential fatty acid and lipid profiles in plasma and erythrocytes in patients with multiple sclerosis. Am J Clin Nutr. 1989 Oct;50(4):801-6. 47. Gallai V, Sarchielli P, Trequattrini A, Franceschini M, Floridi A, Firenze C, Alberti A, Di Benedetto D, Stragliotto E. Cytokine secretion and eicosanoid production in the peripheral blood mononuclear cells of MS patients undergoing dietary supplementation with n-3 polyunsaturated fatty acids. J Neuroimmunol. 1995 Feb;56(2):143-53. 48. Smuts CM, Huang M, Mundy D, Plasse T, Major S, Carlson SE. A randomized trial of docosahexaenoic acid supplementation during the third trimester of pregnancy. Obstet Gynecol. 2003 Mar;101(3):469-79. 49. Stene LC, Joner G; Norwegian Childhood Diabetes Study Group. Use of cod liver oil during the first year of life is associated with lower risk of childhood-onset type 1 diabetes: a large, population-based, case-control study. Am J Clin Nutr. 2003 Dec;78(6):1128-34. 50. Malcolm CA, McCulloch DL, Montgomery C, Shepherd A, Weaver LT. Maternal docosahexaenoic acid supplementation during pregnancy and visual evoked potential development in term infants: a double blind, prospective, randomised trial. Arch Dis Child Fetal Neonatal Ed. 2003 Sep;88(5):F383-90. 51. Uauy R, Hoffman DR, Mena P, Llanos A, Birch EE. Term infant studies of DHA and ARA supplementation on neurodevelopment: results of randomized controlled trials. J Pediatr. 2003 Oct;143(4 Suppl):S17-25. 52. Uauy R, Hoffman DR, Peirano P, Birch DG, Birch EE. Essential fatty acids in visual and brain development. Lipids. 2001 Sep;36(9):885-95. 53. Dunstan JA, Mori TA, Barden A, Beilin LJ, Taylor AL, Holt PG, Prescott SL. Fish oil supplementation in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: A randomized, controlled trial. J Allergy Clin Immunol. 2003 Dec;112(6):1178-84. 54. Williams MA, Zingheim RW, King IB, Zebelman AM. Omega-3 fatty acids in maternal erythrocytes and risk of preeclampsia. Epidemiology. 1995 May; 6(3): 232-7. 55. Mayser P, Mrowietz U, Arenberger P, Bartak P, Buchvald J, Christophers E, Jablonska S, Salmhofer W, Schill WB, Kramer HJ, Schlotzer E, Mayer K, Seeger W, Grimminger F. Omega-3 fatty acid-based lipid infusion in patients with chronic plaque psoriasis: results of a double-blind, randomized, placebo-controlled, multicenter trial. J Am Acad Dermatol. 1998 Apr;38(4):539-47. 56. Grimminger F, Mayser P, Papavassilis C, Thomas M, Schlotzer E, Heuer KU, Fuhrer D, Hinsch KD, Walmrath D, Schill WB, et al. A double-blind, randomized, placebo-controlled trial of n-3 fatty acid based lipid infusion in acute, extended guttate psoriasis. Rapid improvement of clinical manifestations and changes in neutrophil leukotriene profile. Clin Investig. 1993 Aug;71(8):634-43. 57. Rhodes LE, White SI. Dietary fish oil as a photoprotective agent in hydroa vacciniforme. Br J Dermatol. 1998 Jan;138(1):173-8. 58. Jain S, Gaiha M, Bhattacharjee J, Anuradha S. Effects of low-dose omega-3 fatty acid substitution in type-2 diabetes mellitus with special reference to oxidative stress--a prospective preliminary study. J Assoc Physicians India. 2002 Aug;50:1028-33. 59. Fernandez-Real JM, Broch M, Vendrell J, Ricart W. Insulin resistance, inflammation, and serum fatty acid composition. Diabetes Care. 2003 May;26(5):1362-8. 60. Salmeron J, Hu FB, Manson JE, Stampfer MJ, Colditz GA, Rimm EB, Willett WC. Dietary fat intake and risk of type 2 diabetes in women. Am J Clin Nutr. 2001 Jun;73(6):1019-26. 61. Chicco, A., D'Alessandro, M. E., Karabatas, L., Gutman, R., and Lombardo, Y. B. Effect of moderate levels of dietary fish oil on insulin secretion and sensitivity, and pancreas insulin content in normal rats. Ann Nutr Metab 40(2), 61-70. 1996. 62. Mori, T. A., Bao, D. Q., Burke, V., Puddey, I. B., Watts, G. F., and Beilin, L. J. Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr 70(5), 817-25. 1999. 63. Rivellese AA, Maffettone A, Iovine C, Di Marino L, Annuzzi G, Mancini M, Riccardi G. Long-term effects of fish oil on insulin resistance and plasma lipoproteins in NIDDM patients with hypertriglyceridemia. Diabetes Care. 1996 Nov;19(11):1207-13. 64. Woodman RJ, Mori TA, Burke V, Puddey IB, Watts GF, Beilin LJ. Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension. Am J Clin Nutr. 2002 Nov;76(5):1007-15. 65. Berardi, J. The Real World (of Physique Research), Part 3. Testosterone Magazine. 8 Aug 2003. http://www.t-mag.com/nation_articles/273real.jsp. 66. Cha, M. C. and Jones, P. J. Dietary fat type and energy restriction interactively influence plasma leptin concentration in rats. J Lipid Res 39(8), 1655-60. 1998. 67. Peyron-Caso E, Taverna M, Guerre-Millo M, Veronese A, Pacher N, Slama G, Rizkalla SW. Dietary (n-3) polyunsaturated fatty acids up-regulate plasma leptin in insulin-resistant rats. J Nutr. 2002 Aug;132(8):2235-40. 68. Su W, Jones PJ. Dietary fatty acid composition influences energy accretion in rats. J Nutr. 1993 Dec;123(12):2109-14. 69. Maes M, Christophe A, Delanghe J, Altamura C, Neels H, Meltzer HY. Lowered omega3 polyunsaturated fatty acids in serum phospholipids and cholesteryl esters of depressed patients. Psychiatry Res. 1999 Mar 22;85(3):275-91. 70. Hibbeln JR, Salem N Jr. Dietary polyunsaturated fatty acids and depression: when cholesterol does not satisfy. Am J Clin Nutr. 1995 Jul;62(1):1-9. 71. Peet M. Eicosapentaenoic acid in the treatment of schizophrenia and depression: rationale and preliminary double-blind clinical trial results. Prostaglandins Leukot Essent Fatty Acids. 2003 Dec;69(6):477-85. 72. Su KP, Huang SY, Chiu CC, Shen WW. Omega-3 fatty acids in major depressive disorder. A preliminary double-blind, placebo-controlled trial. Eur Neuropsychopharmacol. 2003 Aug;13(4):267-71. 73. Zanarini MC, Frankenburg FR. omega-3 Fatty acid treatment of women with borderline personality disorder: a double-blind, placebo-controlled pilot study. Am J Psychiatry. 2003 Jan;160(1):167-9. 74. Richardson AJ, Puri BK. The potential role of fatty acids in attention-deficit/hyperactivity disorder.Prostaglandins Leukot Essent Fatty Acids. 2000 Jul-Aug;63(1-2):79-87. Review 75. Kidd PM. Attention deficit/hyperactivity disorder (ADHD) in children: rationale for its integrative management. Altern Med Rev. 2000 Oct;5(5):402-28. Review 76. Delarue J, Matzinger O, Binnert C, Schneiter P, Chiolero R, Tappy L. Fish oil prevents the adrenal activation elicited by mental stress in healthy men. Diabetes Metab. 2003 Jun;29(3):289-95. 77. Maes M, Christophe A, Bosmans E, Lin A, Neels H. In humans, serum polyunsaturated fatty acid levels predict the response of proinflammatory cytokines to psychologic stress. Biol Psychiatry. 2000 May 15;47(10):910-20. 78. Harel Z, Gascon G, Riggs S, Vaz R, Brown W, Exil G. Supplementation with omega-3 polyunsaturated fatty acids in the management of recurrent migraines in adolescents. J Adolesc Health. 2002 Aug;31(2):154-61. 79. Rabinovitz S, Mostofsky DI, Yehuda S. Anticonvulsant efficiency, behavioral performance and cortisol levels: a comparison of carbamazepine (CBZ) and a fatty acid compound (SR-3). Psychoneuroendocrinology. 2004 Feb;29(2):113-24. 80. Tamizi far B, Tamizi B. Treatment of chronic fatigue syndrome by dietary supplementation with omega-3 fatty acids--a good idea? Med Hypotheses. 2002 Mar;58(3):249-50. 81.Ernst E. Complementary and alternative medicine in rheumatology. Baillieres Best Pract Res Clin Rheumatol. 2000 Dec;14(4):731-49. 82. Hayashi H, Tanaka Y, Hibino H, Umeda Y, Kawamitsu H, Fujimoto H, Amakawa T. Beneficial effect of salmon roe phosphatidylcholine in chronic liver disease. Curr Med Res Opin. 1999;15(3):177-84.
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Fishy Advice: Part I

By Eric Cressey

If you're even remotely up-to-date on your nutrition-for-health reading, you're well aware of the benefits of fish oil. Moreover, if you're anything like me, you've also gone to great lengths--often to no avail--to convince people that they should be taking it even if it does sound "icky." In an effort to save you and I a lot of future time and energy, I've compiled the following for you to share with your relatives, mailman, proctologist, lunchlady, and anyone else with whom you associate that isn't currently "on da fish." Based on undeniable scientific evidence and anecdotal evidence, I strongly encourage you to incorporate into your diet two specific omega-3 fatty acids: eicosapentaenoic acid (EPA) and docosahexanoic acid (DHA), commonly referred to as fish oils. EPA and DHA deficiencies have been linked to problems that include, but are certainly not limited to heart disease, hypertension, arthritis, cancer, immune disorders, chronic intestinal disorders, growth retardation, liver disorders, skin lesions, reproductive failure, visual problems, kidney disorders, and neurological disorders (1). Dietary alpha-linolenic acid can be converted to EPA and DHA in the body for utilization as important raw materials in healthy cell membranes. Significant amounts of alpha-linolenic acid can be found in the following oils: flaxseed, soybean, hempseed, pumpkinseed, canola, wheat germ and walnut. Products such as margarine and shortening that are derived from these oils also contain modest amounts of alpha-linolenic acid. Some nuts and seeds-- butternuts, walnuts, pumpkinseeds, and flaxseeds-- and vegetables (soybeans) are good sources as well (1). However, the conversion of alpha-linolenic acid to EPA and DHA is quite inefficient; estimates place the conversion rates at less than 5-10% for EPA and 2-5% for DHA (2). Lifestyle factors can also negatively influence these conversions. There is also evidence to suggest that females are more efficient at converting linolenic acid than men; this is likely due to increased demands for EPA and DHA during pregnancy and lactation (3). Even if you eat plenty of the aforementioned foods regularly, you still might come up short on EPA and DHA because the fatty acid quality is often degraded due to the typical overprocessing that occurs in commercial production (4). As such, it is best to get your EPA and DHA directly whenever possible. EPA and DHA are commonly referred to as fish oils because coldwater fish are by far the best sources. Although the terms EPA/DHA and fish oils are substituted for one another in writing and conversation, EPA and DHA are actually just two kinds of fatty acids contained in fish oils (5). These fish include, but are not limited to: salmon, mackerel, bluefish, tuna, mullet, herring, anchovy, and sardines. Infants receive plenty of EPA and DHA from their mothers' milk (1). Certainly, eating fish every day isn't appetizing for most people, and drinking human milk after the age of one is neither feasible nor socially acceptable! Plus, the typical vegetarian diet is extremely low in alpha-linolenic acid, so even if conversion was efficient, these individuals would still be coming up short (clinical studies have proven that vegetarians have insufficient levels of EPA and DHA) (2). Luckily, fish oil supplements in both liquid and softgel form are widely available to ensure that EPA and DHA requirements can be met easily. EPA and DHA exert their most powerful effects in an anti-inflammatory role. Arachidonic acid, which is created out of the omega-6 fatty acids in our diets, serves as the building block for certain eicosanoids that control the synthesis of cytokines that are pro-inflammatory and immunoregulatory; when these cytokines are overproduced, chronic inflammatory diseases (and even septic shock) can result. Omega-3 fatty acids, on the other hand, inhibit the production of arachidonic acid--thus preventing the production of certain mediators of inflammation--and serve as the raw materials for a healthier class of eicosanoids with anti-inflammatory properties (6). Given how out-of-whack the typical diet is in terms of the omega-6: omega-3 ratio, it should come as no surprise that the world is as unhealthy as it is! Here is some pretty impressive data on a variety of fronts: Cardiovascular Health/Atherosclerosis/Hyperlipidemia/Hypertension:

  • An eleven year study of 20,557 male U.S. physicians showed that those who consumed fatty fish at least once per week were 52% less likely to suffer a sudden cardiac death than those who only ate it once per month or less (5).
  • The typical Greenland Eskimo diet is devoid of fruits and vegetables and very high in fats from animal sources: not your traditional "heart healthy diet." However, the Eskimos had far lower instances of coronary heart disease (CHD) than a Denmark population of nearly identical ethnical composition (same ancestors). The Eskimo and Danish diets both consisted of a high percentage of calories from fat (39% and 42%, respectively), so why didn't the Eskimos suffer from such CHD like the Danes and everyone else? The secret lay with the types of fat that the Eskimos were eating. The typical Danish diet consisted of 22% of total calories from saturated fat and less than 1% from omega-3 polyunsaturated fatty acids (PUFAs). Meanwhile, only 9% of total calories in the Eskimo diet came from saturated fat. Perhaps more importantly, 4.2% of the Eskimos' total calories came from omega-3 PUFAs (5). Similar trends are readily apparent in coastal villages of Korea and Japan and throughout Scandinavian countries. Not surprisingly, they all rely extensively on coldwater fish in their everyday lives. Need further proof? A recent comparison of two Japanese villages: one fishing, one farming, found that the farming village had eight times more atherosclerotic plaques than their fishing counterparts (7).
  • In a study of 59 patients with diagnosed heart disease, Durrington et al (2001) monitored the effects of 2 g daily of Omacor, a pharmaceutical grade fish oil concentrate. The researchers found that "there was a sustained significant decrease in serum triglycerides by 20-30% and in very low density lipoprotein (VLDL) cholesterol by 30-40% in patients receiving active Omacor at three, six, and 12 months compared either to baseline or placebo (8)."
  • Not only do fish oils lower serum triglycerides and, in high dosages and combination with dietary modifications, low density lipoprotein (LDL) cholesterol, but they also decrease arterial platelet collection, which can lead to dangerous clots (5).
  • Harper and Jacobsen (2001) reported that randomized clinical trials with fish oils "have demonstrated reductions in risk that compare favorably with those seen in landmark secondary prevention trials with lipid-lowering drugs (5)."
  • Following coronary artery bypass surgery with venous grafts, patients that receive 4 g per day of omega-3 fatty acids have a significantly lower risk of graft occlusion (obstruction/closure) (9).

Hypertension:

  • There are like 80 bizillion studies out there proving that fish oil reduces blood pressure (although you'll obviously derive greater benefits if you eat right and exercise, too). That said, 4 g omega-3 fatty acids per day is the minimum you'll need to see an improvement (9). You can expect not only reduced blood pressure, but also decreased vascular wall thickness (10). I've included a few more references (11-13) for those of you that either don't believe me or have a lot of time on your hands for extra reading.

Cardiac Arrhythmias:

  • There is significant backing for the assertion that fish oils' antiarrhymthic capacity is the most important. Without sufficient EFAs, the body is forced to make cell membranes out of saturated fatty acids, which yield membranes that are far less elastic. When cardiac cells are made from EFAs (and are thus appropriately elastic), the heart has an easier time returning to a resting state. However, the rigid cell membranes made from saturated fatty acids can cause arrhythmias and alter the cardiac muscle cell contraction (5).

Inflammatory Diseases of Joints and Connective Tissues:

  • In patients with degenerative and inflammatory joint diseases, supplementation with omega-3 fatty acids decreases both the "degradative and inflammatory aspects of chondrocyte metabolism, whilst having no effect on the normal tissue homeostasis (14)."
  • Chondrocytes are the building blocks of articular cartilage and work with the extracellular matrix of collagen and proteoglycans to dissipate forces. If the cartilage is constantly eroding due to chondrocyte degradation, the structure tends to soften as its water content increases. Interventions with omega-3 fatty acids are effective in reducing these negative trends and their related symptoms in most patients with osteoarthritis (15,16).
  • In more than two dozen studies, researchers have found that fish oil supplementation reduces fatigue and stiffness in rheumatoid arthritis (RA) afflicted individuals. In fact, some studies found the effects to be dramatic enough to allow for substantial decreases in nonsteroidal anti-inflammatory drug (NSAID) dosages (16-18). Generally speaking, in trials of 3 g combined EPA and DHA (the minimum recommended dose for RA patients), the benefits of fish oil supplementation were not noticeable until the 12-week mark, so be patient! On a microscopic level, the omega-3 supplementation tended to limit the release of leukotrien B(4) and interleukin 1 from neutrophils and monocytes. In plain English, this means that two inflammation-causing factors were present in lesser quantities (17).
  • RA patients that supplemented with Vitamin E and fish oil showed an even greater decrease in NSAID requirements, indicating a synergistic effect between the two (18).
  • Raynaud's Phenomenon is a vascular disorder that falls under the inflammatory diseases of joints and connective tissues. In this condition, tiny blood vessels that feed the skin periodically contract (called a "vasospasm"), limiting blood flow to the skin. As oxygen deprivation sets in, the skin--especially in the hands and feet--turns white and eventually blue. There is speculation that this phenomenon is due to the body's overreaction to cold, as the body excessively vasoconstricts these arteries to conserve heat. However, while cold atmospheres are most likely to cause a vasospasm, emotional stress can be a causative factor as well. Because omega-3 fatty acids "induce a favorable response to vascular ischemia," they have been investigated as a potential treatment for Raynaud's. DiGiacomo et al (1989) found that fish oil supplementation improved cold exposure tolerance and significantly delayed the onset of vasospasm in Raynaud's patients. Furthermore, this cold tolerance improvement was associated with a significantly increased digital systolic blood pressure in a cold atmosphere (20).
  • Systemic lupus erythematosus (SLE) -- better known simply as lupus - is a chronic, autoimmune rheumatic disease with a wide variety of symptoms. Typically, this disease affects women of childbearing age (21). Symptoms include arthritis, skin rash, vascular inflammation, and profound effects on the central nervous, renal and cardiopulmonary systems (22). Mohan and Das (1997) found that concentrations of EPA and DHA were low in the plasma phospholipids of SLE patients; this supported pre-existing data that EPA and DHA supplementation could lead to clinical remission without side effects (22).
  • In cases of pediatric SLE, dyslipoproteinemia -- essentially high triglycerides, low HDL, and high LDL - is often present. Provision of fish oil supplements has proven effective in significantly improving blood lipid profiles (decreased serum triglycerides concentrations) in these patients beyond dietary intervention alone (24).

Osteoporosis:

  • Two short-term studies have found that a lower omega-6 to omega-3 fatty acid ratio (achieved via omega-3 supplementation) attenuates bone loss in patients with osteoporosis. These effects are likely due to decreases in the production of Prostaglandin E2 (PGE2), an eicosanoid widely implicated in bone resorption (25). Overall eicosanoid balance is largely dependent on fatty acid intake; so it's important to consider both the quantity of omega-3s and omega-6s present.

Kidney Disease/Renal Failure:

  • Researchers at the Mayo Nephrology Collaborative Clinic found that fish oils slowed the progression of immunoglobin A nephropathy in patients at a high risk for kidney disease (26).
  • Omega-3s have shown promise in reducing urinary calcium levels in kidney stone patients and preventing blood clots in hemodialysis patients (26).
  • Hemodialysis patients given fish oil required 16% less erythropoietin while experiencing a 3.6% increase in serum albumin levels in comparison to a placebo group (27).
  • The side effects (such as skin lesions and hyperlipidemia) of cyclosporine, a medication often prescribed for kidney transplant patients, are noticeably less significant when patients supplement with fish oil (28)

Prostate Cancer:

  • A longitudinal study of 6,272 Swedish men showed that those who regularly consumed fish were approximately 50% less likely to be diagnosed with prostate cancer and roughly 70% less likely to die from it than those who avoided fish. Three servings per week appeared to be the minimum amount needed to attain such benefits (29).
  • Augustsson et al (2003) validated the Swedish study with a larger sample size of 47,882, and noted that the strongest association also existed between fish consumption and metastatic cancer (meaning that it's extensive and spreads to other parts of the body via the blood vessels or lymphatic system). Those men that ate fish more than three times per week were 24% less likely to be diagnosed with metastatic cancer (30).

Colon Cancer:

  • Collett et al noted that incidences of colon cancer in rats were reduced significantly with DHA supplementation in the form of fish oil (31).

Breast Cancer:

  • In a five-year prospective study of 35,298 Singapore Chinese women ages 45-74, high levels of dietary omega-3 fatty acids (mostly from shellfish) were associated with a significantly reduced (26% lower) risk of breast cancer (32).

Skin Cancer:

  • In animals, omega-3 fatty acids have been proven effective as protection against photocarcinogenesis, likely due to the fatty acids' ability to combat oxidative stress. Rhodes et al studied the effect of 4 g/day EPA supplementation "on a range of indicators of ultraviolet radiation (UVR)-induced DNA damage in humans, and assessed effect on basal and post-UVR oxidative status" in 42 healthy subjects. The control group received oleic acid, a monounsaturated fatty acid, for the three-month study. Sunburn sensitivity was reduced in the EPA group only; likewise, other early markers of skin cancer diminished significantly with EPA supplementation. These results imply that there was protection against acute UVR-induced damage by dietary EPA; the researchers hypothesized that "longer-term supplementation might reduce skin cancer in humans (33)."

That concludes part one; hopefully, you've picked up some valuable information. Next month, I'll besiege you with another 8,471 references supporting my argument on a variety of different fronts. Stay tuned! References 1. Whitney, E.N. & Rolfes, S.R. Understanding Nutrition: (8th ed.). Belmont, CA: Wadsworth Publishing Company, 1999. 2. Davis BC, Kris-Etherton PM. Achieving optimal essential fatty acid status in vegetarians: current knowledge and practical implications. Am J Clin Nutr. 2003 Sep;78(3 Suppl):640S-646S. 3. Burdge GC, Wootton SA. Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br J Nutr. 2002 Oct;88(4):411-20. 4. Colgan, M. Optimum Sports Nutrition. New York: Advanced Research Press, 1993. 5. Harper CR, Jacobson TA. The fats of life: the role of omega-3 fatty acids in the prevention of coronary heart disease. Arch Intern Med. 2001 Oct 8;161(18):2185-92. 6. Calder PC. n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann Nutr Metab. 1997;41(4):203-34. 7. Yamada T, Strong JP, Ishii T, Ueno T, Koyama M, Wagayama H, Shimizu A, Sakai T, Malcom GT, Guzman MA. Atherosclerosis and omega-3 fatty acids in the populations of a fishing village and a farming village in Japan. Atherosclerosis. 2000 Dec;153(2):469-81. 8. Durrington PN, Bhatnagar D, Mackness MI, Morgan J, Julier K, Khan MA, France M. An omega-3 polyunsaturated fatty acid concentrate administered for one year decreased triglycerides in simvastatin treated patients with coronary heart disease and persisting hypertriglyceridaemia. Heart. 2001 May;85(5):544-8. 9. Nordoy A, Marchioli R, Arnesen H, Videbaek J. n-3 polyunsaturated fatty acids and cardiovascular diseases. Lipids. 2001;36 Suppl:S127-9. 10. Engler MM, Engler MB, Pierson DM, Molteni LB, Molteni A Effects of docosahexaenoic acid on vascular pathology and reactivity in hypertension. Exp Biol Med (Maywood). 2003 Mar;228(3):299-307. 11. Passfall J, Philipp T, Woermann F, Quass P, Thiede M, Haller H. Different effects of eicosapentaenoic acid and olive oil on blood pressure, intracellular free platelet calcium, and plasma lipids in patients with essential hypertension. Clin Investig. 1993 Aug;71(8):628-33. 12. Bhatnagar D, Durrington PN.Omega-3 fatty acids: their role in the prevention and treatment of atherosclerosis related risk factors and complications. Int J Clin Pract. 2003 May;57(4):305-14 13. Holm T, Andreassen AK, Aukrust P, Andersen K, Geiran OR, Kjekshus J, Simonsen S, Gullestad L. Omega-3 fatty acids improve blood pressure control and preserve renal function in hypertensive heart transplant recipients. Eur Heart J. 2001 Mar;22(5):428-36. 14. Curtis CL, Rees SG, Cramp J, Flannery CR, Hughes CE, Little CB, Williams R, Wilson C, Dent CM, Harwood JL, Caterson B. Effects of n-3 fatty acids on cartilage metabolism. Proc Nutr Soc. 2002 Aug;61(3):381-9. 15. Curtis CL, Rees SG, Little CB, Flannery CR, Hughes CE, Wilson C, Dent CM, Otterness IG, Harwood JL, Caterson B. Pathologic indicators of degradation and inflammation in human osteoarthritic cartilage are abrogated by exposure to n-3 fatty acids. Arthritis Rheum. 2002 Jun;46(6):1544-53. 16. Cho SH, Jung YB, Seong SC, Park HB, Byun KY, Lee DC, Song EK, Son JH. Clinical efficacy and safety of Lyprinol, a patented extract from New Zealand green-lipped mussel (Perna Canaliculus) in patients with osteoarthritis of the hip and knee: a multicenter 2-month clinical trial. Allerg Immunol (Paris). 2003 Jun;35(6):212-6. 17. Kremer JM. n-3 fatty acid supplements in rheumatoid arthritis. Am J Clin Nutr. 2000 Jan;71(1 Suppl):349S-51S 18. Tidow-Kebritchi S, Mobarhan S. Effects of diets containing fish oil and vitamin E on rheumatoid arthritis. Nutr Rev. 2001 Oct;59(10):335-8. 19. Rennie KL, Hughes J, Lang R, Jebb SA. Nutritional management of rheumatoid arthritis: a review of the evidence. J Hum Nutr Diet. 2003 Apr;16(2):97-109. 20. DiGiacomo RA, Kremer JM, Shah DM. Fish-oil dietary supplementation in patients with Raynaud's phenomenon: a double-blind, controlled, prospective study. Am J Med. 1989 Feb;86(2):158-64. 21. Ioannou Y, Isenberg DA. Current concepts for the management of systemic lupus erythematosus in adults: a therapeutic challenge. Postgrad Med J. 2002 Oct;78(924):599-606. 22. Das UN. Beneficial effect of eicosapentaenoic and docosahexaenoic acids in the management of systemic lupus erythematosus and its relationship to the cytokine network. Prostaglandins Leukot Essent Fatty Acids. 1994 Sep;51(3):207-13. 23. Mohan IK, Das UN. Oxidant stress, anti-oxidants and essential fatty acids in systemic lupus erythematosus. Prostaglandins Leukot Essent Fatty Acids. 1997 Mar;56(3):193-8. 24. Ilowite NT, Copperman N, Leicht T, Kwong T, Jacobson MS. Effects of dietary modification and fish oil supplementation on dyslipoproteinemia in pediatric systemic lupus erythematosus. J Rheumatol. 1995 Jul;22(7):1347-51. 25. Albertazzi P, Coupland K. Polyunsaturated fatty acids. Is there a role in postmenopausal osteoporosis prevention? Maturitas. 2002 May 20;42(1):13-22. 26. Donadio JV. n-3 Fatty acids and their role in nephrologic practice. Curr Opin Nephrol Hypertens. 2001 Sep;10(5):639-42. 27. Vergili-Nelsen JM. Benefits of fish oil supplementation for hemodialysis patients. J Am Diet Assoc. 2003 Sep;103(9):1174-7. 28. Simopoulos AP. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr. 1991 Sep;54(3):438-63. 29. Terry P, Lichtenstein P, Feychting M, Ahlbom A, Wolk A. Fatty fish consumption and risk of prostate cancer. Lancet. 2001 Jun 2;357(9270):1764-6. 30. Augustsson K, Michaud DS, Rimm EB, Leitzmann MF, Stampfer MJ, Willett WC, Giovannucci E. A prospective study of intake of fish and marine fatty acids and prostate cancer. Cancer Epidemiol Biomarkers Prev. 2003 Jan;12(1):64-7. 31. Collett ED, Davidson LA, Fan YY, Lupton JR, Chapkin RS. n-6 and n-3 polyunsaturated fatty acids differentially modulate oncogenic Ras activation in colonocytes. Am J Physiol Cell Physiol. 2001 May;280(5):C1066-75. 32. Gago-Dominguez M, Yuan JM, Sun CL, Lee HP, Yu MC. Opposing effects of dietary n-3 and n-6 fatty acids on mammary carcinogenesis: The Singapore Chinese Health Study. Br J Cancer. 2003 Nov 3;89(9):1686-92. 33. Rhodes LE, Shahbakhti H, Azurdia RM, Moison RM, Steenwinkel MJ, Homburg MI, Dean MP, McArdle F, Beijersbergen van Henegouwen GM, Epe B, Vink AA. Effect of eicosapentaenoic acid, an omega-3 polyunsaturated fatty acid, on UVR-related cancer risk in humans. An assessment of early genotoxic markers. Carcinogenesis. 2003 May;24(5):919-25.

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