Danger of Zero-Carb Diets III: Scurvy

I started low-carb Paleo dieting in late 2005. I ate a lot of vegetables but no starches and hardly any fruit. In retrospect, I would call it a near zero-carb diet. At that time I was 12 years into a chronic illness that got a little worse each year and was quite mysterious to me. Adopting a low-carb diet brought immediate changes: it made what I would much later recognize as a chronic bacterial infection better (in parts of the body, not the brain) and made a chronic fungal infection worse.

Within about a year I had developed scurvy. It took me an embarrassingly long time to figure out what it was. By the time knew what it was, I had 3 cavities; had lost 25 pounds; had developed diverticulitis and an abdominal aorta that visibly swelled with every heartbeat; and had minor skin wounds – scrapes and scratches – that hadn’t healed in 6 months.

Developing scurvy was a surprise, because I was eating many vegetables plus taking a multivitamin containing 90 mg of vitamin C. I had never had any signs of vitamin C deficiency before adopting a low-carb diet.

Four grams a day of vitamin C for two months cured all the scurvy symptoms. It would be several more years before I figured out the infections, but this experience taught me the importance of micronutrition. The experience persuaded me that I needed to research diets and nutrition closely, and started us down the path of writing Perfect Health Diet.

Scurvy on a Ketogenic Diet

My experience is not unique. Here’s one case we mention in the book: the story of a young girl with epilepsy.

KM was a 9-year old girl … diagnosed with epilepsy at six months old. She started a ketogenic diet in October 2003, as her multiple antiepileptic drugs were proving to be less than effective; indeed she was having as many as 12 tonic seizures per day with prolonged periods of non-convulsive status epilepticus. After the diet was prescribed the seizure frequency reduced markedly and there were a number of long periods of time in which she had no seizures.

KM’s mother gave a history of her daughter having had bleeding gums since the beginning of September 2006; she described them as being very dark red, swollen and bleeding. In addition, she explained that her daughter had dry, crusted blood peri-orally. The family’s general dental practitioner had explained that this was probably caused by erupting teeth and instructed her to use 0.2% chlorhexidine gluconate gel and to continue her regular oral hygiene regimen; however this had no effect. About a month later the patient’s right arm became swollen. It was thought that she had sustained a fracture or a dislocation; however she was discharged from the local hospital’s fracture clinic because there was clinical improvement and radiographs showed no callus formation.

In early November KM inhaled a primary molar tooth while she was having her teeth cleaned (Fig. 1). This required an emergency bronchoscopy to retrieve it; at the same time the surgeons extracted her remaining primary teeth in order to avoid a recurrence of the problem….

At that time an appointment was made to attend a paediatric dentistry consultant clinic at the Leeds Dental Institute; however this was never kept as about three weeks after the extractions the patient was admitted to hospital with low grade fever, persistently bleeding gums, oedema of her hands and feet and a petechial rash on her legs. [1]

This girl was eating a typical amount of vitamin C: her dietary intake was calculated at 73 mg/day, well above the US RDA for 9-13 year olds of 45 mg/day. Yet her blood level was only 0.7 µmol/l. Scurvy is diagnosed at levels below 11 µmol/l.

The symptoms of scurvy are sufficiently insidious that it is easy to miss the diagnosis. In KM’s case, it happened that a “senior house officer” – a junior doctor in training – from India recognized the symptoms of scurvy. Otherwise, it might have never have occurred to the doctors to test her vitamin C level. [2]

What Is the Cause of Low-Carb Scurvy?

So what causes scurvy to develop on low-carb diets even with vitamin C intake well above the US RDA?

It seems to be a confluence of two factors:

  • An infection or some other stress (e.g. injury, cancer) leads to the oxidation of extracellular vitamin C; and
  • On a low-insulin or glutathione-deficiency-inducing diet, oxidized vitamin C is not recycled.

Infection and Vitamin C

The immune response to infections generates reactive oxygen species, which oxidize vitamin C. Oxidation removes a hydrogen atom from vitamin C, turning it into “dehydroascorbic acid,” or DHAA. If DHAA remains in the blood, it degrades with a half-life of 6 minutes. [3]

Infections can cause vitamin C deficiency on any diet. During the “acute phase response” to infection or injury, vitamin C often becomes deficient. Here is a nice paper in which French doctors surveyed their hospital patients for scurvy:

We determined serum ascorbic acid level (SAAL) and searched for clinical and biological signs of scurvy in 184 patients hospitalized during a 2-month period.

RESULTS: The prevalence of hypovitaminosis C (depletion: SAAL<5 mg/l or deficiency: SAAL<2 mg/l) was 47.3%. Some 16.9% of the patients had vitamin C deficiency. There was a strong association between hypovitaminosis C and the presence of an acute phase response (p=0.002). [4]

So half were at least depleted in vitamin C and 17% had outright deficiency, which if it persisted would produce scurvy.

We’ve previously written of how important it is to supplement with vitamin C during infections:

I might add here that in sepsis, an extremely dangerous inflammatory state brought on by bacterial infections, intravenous vitamin C reverses some of the worst symptoms. [5] If you have a loved one suffering from a dangerous infection, it might not be a bad idea to get them some vitamin C.

Insulin Dependence of Vitamin C Recycling

DHAA can be recycled back into vitamin C, but only inside cells.

In order to enter cells, DHAA needs to be transported by glucose transporters. GLUT1, GLUT3, and GLUT4 are the three human DHAA transporters; GLUT1 does most of the work. [6]

DHAA transport is crucial for brain vitamin C status. There is no direct transport of vitamin C into the brain, yet the brain is one of the most vitamin C-dependent tissues in the body. The brain relies entirely on GLUT1-mediated transport of DHAA from the blood for its vitamin C supply. Within the brain, DHAA is restored to vitamin C by glutathione.

Supplying DHAA to stroke victims (of the mouse persuasion) as late as 3 hours after the stroke can reduce the stroke-damaged volume by up to 95%:

DHA (250 mg/kg or 500 mg/kg) administered at 3 h postischemia reduced infarct volume by 6- to 9-fold, to only 5% with the highest DHA dose (P < 0.05). [7]

This is a fascinating reminder of the importance of vitamin C for wound repair and protection from injury.

Glucose transporters are activated by insulin. Thus, DHAA import into cells is increased by insulin, leading to more effective recycling of vitamin C [8]:

Insulin and IGF-1 promote recycling of DHAA into ascorbate. Source.

Confirming the role of insulin in promoting vitamin C recycling, Type I diabetics (who lack insulin) have lower blood levels of vitamin C, higher blood levels of DHAA, increased urinary loss of vitamin C metabolites, and greater need for dietary vitamin C. [9, 10]

Now we have a mechanism by which zero-carb diets reduce vitamin C recycling: by lowering insulin levels they inhibit the transport of DHAA into cells, preventing its recycling into vitamin C. Instead, DHAA is degraded and excreted. As a result, vitamin C is lost from the body.

Glutathione and Vitamin C Recycling

Once inside the cell, DHAA is recycled back to ascorbate, mainly by glutathione inside mitochondria:

Dehydroascorbate, the fully oxidized form of vitamin C, is reduced spontaneously by glutathione, as well as enzymatically in reactions using glutathione or NADPH. [11]

A GLUT1 transporter on the mitochondrial membrane is needed to bring DHAA into mitochondria, possibly squaring the effect of insulin on vitamin C recycling.

Since glutathione recycles vitamin C, glutathione deficiency is another possible cause of vitamin C deficiency.

Glutathione is recycled by the enzyme glutathione peroxidase, a selenium-containing enzyme whose abundance is sensitive to selenium status. One difficulty with zero-carb diets is that they seem to deplete selenium levels.

Selenium deficiency is a common side effect of ketogenic diets. Some epileptic children on ketogenic diets have died from selenium deficiency! [12]

So here we have a second mechanism contributing to the development of scurvy on a zero-carb diet. The diet produces a selenium deficiency, which produces a glutathione deficiency, which prevents DHAA from being recycled into vitamin C, which leads to DHAA degradation and permanent loss of vitamin C.

Conclusion

Zero-carb dieters are at high risk for vitamin C deficiency, glutathione deficiency, and selenium deficiency. Anyone on a zero-carb diet should remedy these by supplementation.

These deficiencies are exacerbated by chronically low insulin levels. Insulin helps recycle vitamin C, which supports glutathione status. Lack of insulin increases vitamin C degradation and loss.

The failure of the body to efficiently recycle vitamin C and maintain antioxidant stores on a zero-carb diet is evidence of an evolutionary maladaption to the zero-carb diet.

There was no reason why our ancestors should have become adapted to a zero-carb diet; after, all they’ve been eating starches for at least 2 million years. It seems a risky step to try to live this way.

Related Posts

Other posts in this series:

  1. Dangers of Zero-Carb Diets, I: Can There Be a Carbohydrate Deficiency? Nov 10, 2010.
  2. Dangers of Zero-Carb Diets, II: Mucus Deficiency and Gastrointestinal Cancers A Nov 15, 2010.
  3. Dangers of Zero-Carb Diets, IV: Kidney Stones Nov 23, 2010.

References

[1] Willmott NS, Bryan RA. Case report: Scurvy in an epileptic child on a ketogenic diet with oral complications.  Eur Arch Paediatr Dent. 2008 Sep;9(3):148-52. http://pmid.us/18793598.

[2] Willmott NS, personal communication.

[3] “Dehydroascorbate,” Wikipedia, http://en.wikipedia.org/wiki/Dehydroascorbate.

[4] Fain O et al. Hypovitaminosis C in hospitalized patients. Eur J Intern Med. 2003 Nov;14(7):419-425. http://pmid.us/14614974.

[5] Tyml K et al. Delayed ascorbate bolus protects against maldistribution of microvascular blood flow in septic rat skeletal muscle. Crit Care Med. 2005 Aug;33(8):1823-8. http://pmid.us/16096461.

[6] Rivas CI et al. Vitamin C transporters. J Physiol Biochem. 2008 Dec;64(4):357-75. http://pmid.us/19391462.

[7] Huang J et al. Dehydroascorbic acid, a blood-brain barrier transportable form of vitamin C, mediates potent cerebroprotection in experimental stroke. Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11720-4. http://pmid.us/11573006.

[8] Qutob S et al. Insulin stimulates vitamin C recycling and ascorbate accumulation in osteoblastic cells. Endocrinology. 1998 Jan;139(1):51-6. http://pmid.us/9421397.

[9] Will JC, Byers T. Does diabetes mellitus increase the requirement for vitamin C? Nutr Rev. 1996 Jul;54(7):193-202. http://pmid.us/8918139.

[10] Seghieri G et al. Renal excretion of ascorbic acid in insulin dependent diabetes mellitus. Int J Vitam Nutr Res. 1994;64(2):119-24. http://pmid.us/7960490.

[11] Linster CL, Van Schaftingen E. Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J. 2007 Jan;274(1):1-22. http://pmid.us/17222174.

[12] Bank IM et al. Sudden cardiac death in association with the ketogenic diet. Pediatr Neurol. 2008 Dec;39(6):429-31. http://pmid.us/19027591. (Hat tip Dr. Deans.)

Leave a comment ?

195 Comments.

  1. “These deficiencies are exacerbated by chronically low insulin levels. Insulin helps recycle vitamin C, which supports glutathione status. Lack of insulin increases vitamin C degradation and loss.”

    Ahah! So the important point is that insulin does a lot more than just regulate blood glucose.

  2. Thank God this has never happened to me. Been on Keto for almost 2 years and have never been healthier!

  3. Paul,
    Does this still apply to a “zero carb” diet which is a meat only or an animal product only diet? As you are aware, there are people in both history and current day who have lived on meat only diets for many many years and not developed any illnesses at all?

    Thanks.

    Link:
    https://autoimmunethyroid.wordpress.com/…/why-meat…/

    Text:
    “Vitamin C is required to form collagen in the body, and it does this – despite being described everywhere as an antioxidant – by oxidation. Vitamin C’s role in collagen formation is to transfer a hydroxyl group to the amino acids lysine and proline. Meat, however, already contains appreciable quantities of hydroxylysine and hydroxyproline, bypassing some of the requirement for vitamin C. In other words, your vitamin C requirement is dependent upon how much meat you do not eat.”

  4. Is there any validity to the fears of ascorbic acid as vitamin c. My friend emailed me yesterday with links to websites warning about the dangers of ascorbic acid.

    Thank you,

    • The valid fears are damage to tooth enamel if you take a powder (from acidity), and loose stools and discomfort and disturbance of gut flora if you take too much. I am not sure what other “dangers” you are reading about. Other negative effects are fairly subtle. Ascorbic acid is a fine form of vitamin C.

      Best, Paul

  5. You gave your self an easily preventable disease by choosing to have dangerous and counter-productive eating habits.

    DO NOT give people advice about how to eat.

    You are a reprehensible and deeply misguided man.

  6. I’ve been a keto dieter for 12 years. I’ve always supplemented with C. I recently feel off the wagon and gained 45 lbs in 4 months. I restarted keto 5 weeks ago and forgot to add the C like an idiot. I’m a smoker too, which leaches the C out. The months I was allowing carbs I was not getting C either. So I became instantly ill after restarting the keto and had no idea why. Never occurred to me what I had done. Then it dawned on me after several days in the hospital near death. What an idiot I was. I started dosing with C right away. The doctors didn’t believe it or understand it because it’s not something they see ever. I’m home still trying to recover, taking 500mg 4 x’s/day. The shortness of breath and leg pain is the worst. 4 periods in 25 days. Ugh. 2 weeks later I’m still very ill and weak but not nearly as bad as 2 weeks ago with excruciating chest pain and couldn’t walk. Guess I’ll be far and alive. Size 2 was nice for the last decade. Size 12 or worse will likely be my future though. Can’t go through this again. I should’ve known about the glucose component with c but I didn’t.

    • Hi Nikki,

      Speed up your recovery by taking C to bowel tolerance at least once. At 2 g per day, it could take you months to normalize vitamin C-dependent proteins in the body.

      Glad you figured this out! I had exactly the same thing so I know how hard it is to figure out.

      Best, Paul

      • I began at 1000 mg every 3-4 hours four days after being released from 1 ER with no answers. Four days later I was admitted to another hospital going through the same round of heart tests and so forth. I told them that I suspected scurvy and what I was doing with the C and the doctor freaked out on me. Told me it was toxic levels. I tried to explain she was wrong and about bowel tolerance. Said she didn’t know about scurvy though and would research it. Came back later with a script for 1000 mg twice daily. Told me not to exceed that because it causes iron levels to become toxic. So that’s where I’m at. The only thing they did for me that gave me any relief was a round of steroids that relieved the pleurisy pain. My legs are still killing me though. Still have the shortness of breath but only with exertion, like walking a few feet. I’m on day 15 of C. Hoping something gives soon. This 4 day hospital visit last week cost $36,000 and I’m uninsured. Can’t go back.

  7. I think the point missing here is that of oxidation. High fat diets, especially those high in PUFA and fish oils tend to easily oxidize and the body use up a lot of vitamin C to prevent this from happening. If the diet is high in coconut oil (and to a lesser extent dairy fats), this may however not happen. Excess carbohydrates will turn into saturated fats in the body. Hence carbs are better in this sense.

    Human milk is a food high in fat, but it is mostly saturated and monounsaturated, and human milk is also high in vitamin C, typically 150 mg/2000 kcal. I think this is not optimal amount, because if the mother ingest more vitamin C it can get up to 300 mg/2000 kcal, but not higher even if she ingests enormous quantities of vitamin C. Same seems to be the case for other primate milk and that of the guinea pig (unable to synthesize vitamin C).

    Compared to fish, red meat is a major problem because it is vastly higher in iron. A person that eat a lot of red meat, fried in vegetable oils, and then take rancid high EPA/DHA fish oil capsules and eat little vegetables, it´s going to be a disaster. Fish is also vasly richer in selenium than red meat. One can witness how fresh red meat turns brown in just a few days, indicating how quickly it oxidizes, like an opened apple, but not if vitamin C or lemon juice is added. The same will be the case in the human body.

    Fish from cold waters far north with temperatures inside of them close to zero degrees Celcius may be troublesome from an oxidation point of view. This fat is not designed to be put into the warm human body. However, the seal oil which is equally high in omega-3, seems to be much better protected against the oxidation. The seal is warm blooded and the structure of the fat and the antioxidants is provided to prevent the dangerous oxidation at such warm temperatures. Inuits obtains most of their fats from such seal oil.

  8. Thank you for this fascinating conversation. I am a 55 year old male who eats 30 – 35 grams of protein three times daily. Eggs, Chicken, Ground Beef and canned Salmon. I only eat Salmon two meals per week so the other 19 – meals per week is Ground Beef, Chicken and Eggs. Am I overdoing it on the Ground Beef? If so should are there other healthy protein alternatives?
    Best Wishes To All.
    Jim

    • You should try to eat non-muscle meat including liver.

      • Thank you PeterC

        Paul Jaminet recommends liver only once per week. Are his recommendations for the other nonmuscle meats the same as for liver? Just one nonmuscle meet per week?

        Thanks,

        • I’m not sure Paul ever made a precise recommendation for other organ meats… But I’ve been eating liver once per week every week, plus kidney once per week on most weeks.

    • Hi Aristotle,

      What about shellfish and non-oily fish? (Or a small amount of dairy if you enjoy it?)

      But first of all, PHD recommends intermittent fasting, so you only have 2 meals per day = 14 meals per week (each of which would contain 30–35 grams of animal protein).

      Then there are the supplemental foods. If you discard the whites, all 21 egg yolks for the week would add up to around 50g of protein, i.e. 1.5 meals worth. Two liters of bone broth for the week would also add up to 1.5 meals worth of protein. (To be clear: I’m not saying you should eat all those egg yolks, or all that bone broth, at once! I’d mix them with other protein sources for meals.) At a minimum, liver (4 ounces) plus a bit (2 ounces) of other organ meats would provide another meal worth of protein. Then salmon (or other oily fish) provides 2 meals.

      That leaves 8 more meals worth of protein for shellfish, non-oily fish, beef, additional organ meats, chicken, or dairy, as you desire. (If your additional organ meats includes additional liver: make sure the additional liver is poultry liver, not beef liver, so you don’t overdose on copper. And if you didn’t discard the egg whites, that would eat up another 2 meals worth of protein, leaving you with only 6 meals worth of protein to fill with these foods.)

      Best,
      -Eric

  9. Hi Eric,

    Thank you for the helpful advice. I truly appreciate you.
    I should probably clarify that I am not ketogenic but pretty low carb…
    I am extremely active with work in construction plus I run when I have time. Therefore I have gotten it into my head that I need 100-grams of protein daily to retain strength. I tried the two meals per day and enjoyed it but with that amount of protein I believe it needs to be divvied up a bit. I try to keep the amount per meal at about 33-grams.
    I like your source recommendations. The shellfish is too expensive and I don’t do too well on dairy but your other suggestions are nice. Broth, chicken liver, other organ meats and other non-oily fish sound scrumptious.
    May I ask why you would first suggest discarding the egg whites?

    Best Regards,

    Jim

    • Hi Jim,

      Yes, on a low-carb diet you will need more protein in order to retain strength — enough for maintaining your tissues, plus enough for your liver to synthesize all the glucose you aren’t eating. But why do you think you need to be low carb?

      For egg whites, see for example: http://perfecthealthdiet.com/recipe/phd-baby-food/#comment-1709534.

      Best,
      -Eric

      • Good question Eric. I guess my best answer is that I believe that I need to be low carb because….
        I am 55 years old, grew up on junk food (insane amounts of sugar growing up in New Orleans), find that too many carbs dampens my mood, find that when I eat carbs I cannot stop eating, find that I think better while not eating carbs, believe that by eating low carb I keep my cortisol level down, am swayed by all of the convincing rhetoric from the low carb community….
        All that said I eat a ton of non-starchy veggies per day but still keep the total carbs under 100.
        I hope these are considered legit reasons 🙂
        Thanks,

        • re cortisol,
          i always thought it was more likely to be the other way round…
          ie. low carb (or perhaps more vlc, zc, keto?) is more likely to raise cortisol…especially when/if you exercise

        • Hi Jim,

          Did you experience these negative effects on your mood and clarity of thought when eating safe starches (such as rice, potato, or taro)?

          Unsafe starches (such as wheat) contain a variety of toxins (unrelated to their starch content) which could cause symptoms. And sugar could be problematic even if starch is not (c.f. my comment below).

          So I wouldn’t conclude you need low carb on basis of symptoms unless you have symptoms when safe starches are your carb source.

          Best,
          -Eric

  10. In 2007 I was diagnosed with CSR central serous retinopathy and after doing research on the web concluded that I needed to lower my cortisol levels through less sugar consumption.

    • Hi Jim,

      It’s important to distinguish between sugar and starch.

      Sugar consumption generally triggers release of stress hormones such as adrenaline. However, starch consumption does not. See http://www.nature.com/ijo/journal/v21/n10/pdf/0800494a.pdf, c.f. Figure 6.

      Cortisol is generally released in response to either stress or low blood-glucose concentration (see for example https://en.wikipedia.org/wiki/Cortisol). Since starch consumption does not cause release of other stress hormones like adrenaline, and also raises blood glucose concentration, I would be very surprised if starch raised cortisol levels.

      Best,
      -Eric

      • Hi Eric,

        Thank you so much for the help.

        Looking at the label on sweet potatoes I discovered that one small sweet potato contains 7 – grams of sugar. Does the sugar in this sweet potato trigger the release of stress hormones? Will The sugar in this sweet potato raise blood glucose concentration?

        In health,

        Jim

        • Hi Jim,

          Sweet potato sugar triggers the release of stress hormones about half as much as regular sugar. So you should think of it as 3.5 grams of sugar, not 7 grams.

          All carbohydrates (including the sugar and the starch in sweet potato) will raise blood glucose concentration. You should eat them as part of meal (with vegetables, meat, etc.), so they cause a sustained increase in blood glucose as opposed to a sudden spike.

          Probably a modest amount of sugar from natural sources like sweet potatoes, beets, carrots, fruit, etc., would not hurt you and in fact be good for you. (I would stay away from sweeteners.)

          However, because you are concerned specifically with cortisol, I’d first experiment with the pure starches (rice, potato, or taro). Try a pound (cooked weight) per day, divided between your meals. If that causes no symptoms, then try adding sugary foods too. That way if you do get symptoms, you’ll know what was responsible.

          Best,
          -Eric

          • Good to know about the ‘half as much’ rule.
            My fruit intake is 0.5 cup of berries before bed. My starchy intake is maybe some butternut starch or a sweet potato a couple of evenings per week. My non-starchy intake is probably 9 – cups a day (including 0.5 cup raw fermented sauerkraut).
            In addition to that I have protein, coffee, cocoa powder, nuts and fat.
            I feel pretty good with this setup because I get to eat a lot of food and still keep my carbs with in a reasonable range.

            My greatest concern is not cortisol because I stopped the progression of CSR in 2007 by giving up sugar, alcohol and white processed flour. I also learned to control my stress better.

            My concern now is craving carbs. I will consider increasing my starchy vegetables if they may improve my health though.

            Thank you for the wonderful advice.

            Jim

          • talking of the post meal blood glucose response…
            i thought these couple of posts on the individuality of glucose responses were interesting;
            http://caloriesproper.com/personalized-nutrition-by-prediction-of-glycemic-responses/

            http://caloriesproper.com/personalized-nutrition-ii/

  11. I have to admit that I do eat a sweet potato once or twice a week. I will try to do a n = 1 experiment with rice and potatoes.
    Thank you,

Leave a Comment


NOTE - You can use these HTML tags and attributes:
<a href="" title=""> <abbr title=""> <acronym title=""> <b> <blockquote cite=""> <cite> <code> <del datetime=""> <em> <i> <q cite=""> <s> <strike> <strong>