June 20, 2005
x
In response to the letter from Hill’s Pet Nutrition,
dated June 6, 2005, regarding “Inaccurate information published in article:
When to Say No to Low-Protein, Only Dogs Whose Kidney Failure is Advanced
Need Very Low-Protein Foods by C.J. Puotinen.
I would like to respond to the allegations in this letter regarding
supposed inaccuracies in the above article, and that some of the recommendations
in the article “could cause significant harm to dogs suffering from CKD,”
which I believe are wholly without foundation.
The letter says that “current recommendations made by veterinary
nephrologists contradict those made by the author of this article,” then
goes on to give the results of a study that compared the use of Prescription
Diet® Canine k/d® with maintenance kibble.
I do not believe that dogs with CKD should be fed maintenance kibble,
nor does the article we wrote advocate this. We made it clear that dogs
with CKD need a reduced phosphorus diet, and advocated feeding a home made
diet that reduces phosphorus, without overly restricting protein. Studies
such as the one cited by Hill’s have provided some information to veterinarians
on clinical responses to various commercially available foods, but they
have not provided information to define the role of dietary protein intake
on progressive renal injury.
“In addition, therapeutic foods such as Prescription Diet® Canine
k/d® are indicated before kidney disease becomes severe; they should
be fed when serum creatinine concentration is > or = 2 mg/dl.”
I agree that diet should be modified before kidney disease becomes
severe, and the article we wrote specifically suggests reducing phosphorus
“even with early stage CRF.” I do not agree that protein should be restricted
at this stage, or that the level of phosphorus restriction in Prescription
Diet® Canine k/d® is required for early stage renal disease. According
to the Nutrition Support Service at Ohio State University Veterinary Hospital
[
1], “Results of recent research are changing our recommendations
for nutrient modification in dogs with early signs of CRF. Restricting
phosphorus intake to about 30 mg/pound/day [about half the amount found
in normal diets] as soon as polyuria is recognized, and supplementing potassium
intake (with alkalinizing salts if acidosis is a concern) to maintain serum
potassium within the normal range may be all that is necessary until patients
develop severe disease.” This compares to recommended levels of phosphorus
intake as low as 10 mg/pound/day for late stage CRF.
“Prescription Diet® Canine k/d® contains a reduced amount
of protein; however, it provides complete and balanced nutrition for maintenance
of adult dogs as determined by animal feeding trails using Association
of American Feed Control Official (AAFCO) procedures.”
Again according to the Nutrition Support Service at Ohio State University
Veterinary Hospital [
2], the minimum protein requirement
for dogs with mild to severe CKD is 1 gram/pound/day. They recommend this
amount be reduced only when the dog is uremic: “Protein restriction may
be instituted when the BUN is greater than 80 mg/dl.”[
1]
Prescription Diet® Canine k/d® (dry) [
3] contains
only 12-13.4% protein as fed, or 3.3 grams/100 kcals. Hill’s recommends
feeding 4 ¼ to 5 ¾ cups to a 100 lb dog (420-570 grams).
At 13% protein, 420-570 grams of food would have 55 to 74 grams of protein,
which is below the minimum requirements for an adult dog of 1 gram per
pound of bodyweight (100 grams of protein for a 100 lb dog). The Merck
Veterinary Manual [
4] and other sources [
5]
recommend 2.0 to 2.2 grams of protein per kg of bodyweight for dogs with
CKD, which is equivalent to 1 gram/lb.
“As the quality and digestibility of the protein source increases,
the amount of protein required in pet foods decreases. Prescription Diet®
Canine k/d® contains proteins that are of high quality and digestibility,
therefore, a lesser amount of protein can be used to meet maintenance requirements
of dogs.”
There have been no studies done that I’m aware of showing that lower
amounts of high quality protein do not cause problems due to protein deficiency
in dogs with CKD. Suggestions I saw regarding the use of high quality proteins
for dogs with kidney disease specifically suggested not reducing the quantity
of protein below levels referenced above, but instead increasing the quality
of protein fed [
4].
I would also dispute Hill’s claim that it contains “proteins that are
of high quality and digestibility.” The ingredients in Canine k/d®
are “Brewers rice, pork fat (preserved with mixed tocopherols and citric
acid), dried egg product, flaxseed, corn gluten meal, chicken liver flavor,
soy fiber” plus supplements and artificial preservatives [
3].
Of these, only eggs would be considered high quality protein (and “dried
egg product” is almost certain lower quality than fresh eggs). Corn gluten
meal and brewers rice are poor quality and incomplete proteins. None of
the other ingredients provide protein at all. As a side note, the ethoxyquin
used in k/d® has been shown to cause kidney damage [
6].
“To date, studies have not shown a conclusive effect on delaying
progression of experimentally-induced CKD in dogs; however, there have
been beneficial effects observed in dogs with naturally occurring kidney
disease. It is generally accepted that reducing protein intake decreases
blood urea nitrogen (BUN) concentrations and ameliorates clinical signs
of uremia in patients with CKD.”
It is true that reducing protein decreases BUN, but this is only significant
when BUN is high enough to cause signs of uremia (in general, over 80 mg/dl).
Our article did advise reducing protein when a dog is uremic: “The only
time dietary protein restriction is appropriate in renal failure is when
the disease has become severe.” No studies have shown that reducing protein
improves quality of life, extends life, or slows the progression of kidney
disease when instituted before a dog is uremic. The studies cited by Hill’s
that purportedly show otherwise apply only to dogs with canine X-linked
hereditary nephritis (a rare, breed-specific form of juvenile renal disease),
and the first study only indicates that a protein restricted diet reduces
proteinuria, which is a symptom (comparable to BUN) that is related to
the amount of protein in the diet and does not mean that there is any actual
benefit from the reduction. The first study [
7] also indicates
that the dogs fed the low protein diet “did not maintain starting BW or
plasma albumin concentration within the normal reference range,” dangerous
side effects of low protein diets, and that “unintended differences in
digestibility of protein and energy (P < or = .01) prevented assignment
of the diet effect exclusively to protein.” I would argue that this study
actually supports our contention that low protein diets can be harmful.
The modified diet in the second study [
8] also included
reduced phosphorus, which has been shown to be beneficial to dogs with
renal disease, so any positive effects cannot be attributed to reduced
protein.
x
“In addition, restricting dietary protein may
help ameliorate effects of metabolic acidosis, which is common in CKD.
Although further evaluation is needed, dietary protein restriction is associated
with reduced magnitude of urine protein loss (i.e., proteinuria) in dogs
with glomerular diseases (i.e., kidney diseases characterized by increased
permeability of glomerular blood vessels that allow protein leakage into
the urine). Protein supplementation (e.g., meat, eggs, tripe) is contraindicated
in these patients because it may worsen severity of proteinuria and subsequent
hypoalbuminemia (decreased protein concentration in the blood).
I looked up the references cited in the quote from above. The first
one cited is the study noted above [
7], which indicates
that low protein diets led to loss of body weight and hypoalbuminemia.
Proteinuria may lead to hypoalbuminemia as well, but not because there
is too much protein in the diet, but rather because protein is being lost
faster than it is being restored. Proteinuria is a symptom, not a cause,
of renal disease. In reality, higher protein diets may be required when
dealing with proteinuria and hypoalbuminemia, due to the excessive loss
of protein through the kidneys. A paper on Strategies for Protein Losing
Nephopathy presented at the Atlantic Coast Veterinary Conference in 2001
specifically recommends adding protein in the form of egg whites to treat
hypoalbuminemia [
9].
The second citation is to information on Glomerular Diseases written
by S.L. Vaden. I do not have access to the book cited, but did find articles
by and about the same author on this topic on the web. One of them, Glomerulonephritis
remains an important cause of renal disease in dogs[10],
has specific suggestions for controlling proteinuria in dogs with glomerulopathy.
These suggestions include controlling inflammation, controlling systemic
infections, and using angiotensin-converting enzyme (ACE) inhibitors. There
is no mention of restricting protein in the diet. Another article by Dr.
Vaden [11] concerning the treatment of SCWT with PLE/PLN
advises moderate (not severe, as with Canine k/d®) protein restriction,
coupled with ACE inhibitors and aspirin therapy to control proteinuria
and hypoalbuminemia: “Dogs with PLN should be fed a diet that is moderately
reduced in protein. Angiotensin converting enzyme inhibitors (usually enalapril)
are frequently used to decrease the degree of proteinuria. Dogs that have
serum albumin of < 2.0 g/dl should be given a low-dose of aspirin to
help prevent thromboembolic disease. Systemic hypertension must be controlled.”
An article by Gregory F. Grauer, DVM [12] specifically
on Proteinuria in dogs states that a direct link between proteinuria and
renal damage has not been established in dogs, and again finds that the
use of ACE inhibitors, and in this case omega-3 fatty acid supplementation,
do more to reduce proteinuria than dietary changes. Protein malnutrition
can be as harmful as protein excess and can even lead to death in dogs
with kidney disease [13]. Lastly, although moderate protein
restriction may help with metabolic acidosis, this is not a common occurrence
in dogs with kidney disease, particularly in the early and moderate stages,
and is usually treated using alkalinizing agents such as sodium bicarbonate
and potassium citrate, not by further protein reduction [14].
x
“The reader should also be aware that feeding
a food with reduced protein is only part of the picture when talking about
therapeutic foods such as Prescription Diet® Canine k/d®. Other
beneficial components of these foods include moderate phosphate restriction,
moderate sodium restriction, increased supplementation with polyunsaturated
fatty acids (PUFA), increased B vitamins, and increased buffering capacity
(to counteract the tendency toward decreased acid excretion by the kidneys).
Our article recommended phosphorus restriction and supplemention with
B vitamins. Supplementation with omega-3 fatty acids was also highly recommended.
Supplementation with omega-6 polyunsaturated fatty acids, which are found
in flaxseed (an ingredient in Canine k/d®) along with omega-3 fatty
acids, is not recommended and may be harmful to dogs with kidney disease.
The Washington State University College of Veterinary Medicine [
15],
for example, says, “The omega 3 and omega 6 fatty acids are degraded to
different eicosanoids. Preliminary studies suggest that diets high in omega
3 polyunsaturated fatty acids preserve renal function in dogs with induced
renal failure whereas diets high in omega 6 fatty acids hasten decline.“
In addition, omega-3 fatty acids are quite fragile and oxidize quickly
when exposed to light, heat or air. Adding them to a dry food is not likely
to be helpful. Sodium restriction is only necessary when blood pressure
levels are elevated; our article noted that a reduction in sodium might
be necessary when this occurs. Regarding increased buffering capacity,
calcium carbonate is one of the agents recommended to do this [
13],
and is the primary ingredient in the ground eggshells that our article
recommended for use with home made diets for dogs with kidney disease.
In summary, our diet recommendations had the same or better beneficial
components as those in Prescription Diet® Canine k/d®.
x
“The author notes that feeding low amounts of
phosphorus is a dietary goal for CKD patients, yet does not define what
constitutes low phosphorus. A food that contains 0.15 to 0.3% phosphorus
(dry matter basis) is recommended for most dogs with chronic kidney failure;
Prescription Diet® Canine k/d® contains 0.22% phosphorus (dry matter
basis). Because protein is a major source for phosphorus, it is usually
necessary to limit dietary protein intake in order to limit dietary phosphorus
intake. Following your recommendations to feed a food whose calories come
1/3 from fat, 1/3 from protein, and 1/3 from carbohydrates would result
in excessive phosphorus intake, which could be detrimental to patients
with CKD. In addition, your recommendation to supplement with fresh protein
foods such as raw or cooked meat, eggs, or tripe will contribute further
to consumption of excessive dietary phosphorus and worsening of kidney
disease.”
Such extreme levels of phosphorus restriction are
not indicated for early and moderate stage kidney disease, particularly
when serum phosphorus levels are normal. The Virginia-Maryland Regional
College of Veterinary Medicine [
16] recommends 0.4% phosphorus
for moderate stage kidney disease, dropping to 0.2% for advanced stage.
The Nutrition Support Service at Ohio State University Veterinary Hospital
[
1] advises no phosphorus restriction for mild CKD, then
restricting to about half the normal amount as the disease progresses to
the moderate stage. Treating dogs with mild kidney problems the same way
as dogs with severe kidney disease has not been shown to be beneficial
and may in fact be harmful, due to excessive protein restriction. When
attention is paid to the actual amount of phosphorus in various high protein
foods, it is quite possible to restrict phosphorus substantially without
having to reduce protein to dangerously low levels. For example, egg whites
have a great deal of protein with very little phosphorus. Fatty meats can
provide substantial amounts of protein with only moderate amounts of phosphorus.
To say that one must restrict protein amounts to very low levels in order
to achieve reductions in phosphorus is overly simplistic. By adding proper
fresh food sources to Canine k/d®, as suggested in our article, protein
levels can be raised to a healthier level with only nominal increases in
the amount of phosphorus. For example, Canine k/d® [
3]
provides 57 mg phosphorus per 100 kcals, while ground lamb provides 56
mg phosphorus per 100 kcals, egg whites 29 mg, green tripe 84 mg, and 20%
fat ground beef 62 mg [
17]. Feeding a diet whose calories
come 1/3 from protein is considered a moderate level, and has been shown
to be beneficial in dogs with renal disease [
18]: “Only
beneficial responses, such as less proteinuria, less renal impairment and
lower mortality, have been reported for diets containing low phosphorus
[0.4% DM] and moderate protein (20-31% ME).” Note that with 3.3 grams of
protein per 100 kcals, Canine k/d® derives only 13% of its calories
from protein [
2,
3].
Also, although the article itself did not delve
into the exact amounts that define “low phosphorus”, the additional resources
to which the article referred do include that information. The specific
home made diet suggestions found there, on which the article was based,
produce a diet that is 0.37% phosphorus.
x
“In the past, owners of dogs with CKD often found
that therapeutic kidney foods were not very palatable. Prescription Diet®
Canine k/d® dry and wet formulas have undergone several improvements
in palatability during the past several years and most dogs with CKD readily
accept these foods.”
x
Hill’s admits that their diets have not been palatable
in the past, but claims they are improved now. I would suggest that they
would have made the same claims in the past, and will at some point in
the future likely make further changes that they will then claim make their
food more palatable than it is now. The fact is that low protein foods
are inherently less palatable, and that commercial diets will never appeal
as much to a dog as fresh food diets. Anecdotally, many people still report
their dogs refusing to eat Prescription Diet® Canine k/d®. Even
if some dogs are willing to eat this food, it is not unreasonable to suggest
alternatives for those that will not, or additives that will make it more
appealing, as well as healthier, for dogs with early to moderate stage
CKD.
x
“The author incorrectly states that flax seed
oil (a source of omega-3 polyunsaturated fatty acids) is not recommended
for CKD patients. Dogs with CKD that consumed a food supplemented with
omega-3 polyunsaturated fatty acids (PUFA) had lower mortality, better
kidney function, fewer kidney lesions, and less proteinuria than dogs fed
saturated fats or omega-6 PUFA. Based on these findings, supplementation
with omega-3 PUFA are recommended for dogs with CKD.”
x
I couldn’t agree more that supplementation with
omega-3 fatty acids is highly recommended for dogs with CKD, and our article
made this recommendation several times. The critical difference is the
source of the omega-3 fatty acids. Fish body oil supplies omega-3 fatty
acids in the form of EPA and DHA, which are directly utilizable by the
dog’s body, and fish oil does not contain any omega-6 fatty acids. Flax
seed oil provides omega-3 fatty acids in the form of ALA (alpha-linolenic
acid), which must be converted to EPA and DHA in the body. Even in humans,
this conversion is inefficient, ranging from 0-15% [
19,
20],
and is almost certainly lower in dogs [
21]. In addition,
flax seed oil is only about 55% ALA, containing omega-6 as well as omega-3
fatty acids, and omega-6 fatty acids have been shown to be harmful to dogs
with CKD [
15].
“There are no nutritional reasons that support
providing excessive amounts of dietary protein; older dogs (>7 years) do
not require more protein than young adults. In fact, subclinical kidney
disease may exist in apparently healthy older or geriatric dogs and kidney
function can be worsened by feeding excessive protein (and phosphorus)
to these patients.”
x
There are many recent studies that indicate older dogs, even those
with kidney disease, may need more protein than younger dogs.
“There are, however, potential problems with excessive
protein restriction, which can result in protein malnutrition. The protein
requirements of dogs and cats with CRF have not been established but it
is likely that they may be quite similar or even higher than those of the
healthy animal.”[
22]
“However it is highly questionable whether protein
restriction is appropriate in the azotaemic, but non-uraemic patient. The
main risk of protein restriction is protein deficiency. The protein and
amino acid requirements of dogs and cats with chronic renal failure have
not been established, but may well be increased. Uraemia is a catabolic
state causing a range of abnormalities in protein metabolism. In addition,
gastrointestinal blood loss and urinary loss of some amino acids may increase
protein requirements.”[
23]
“A diet rich in protein is especially important
for older dogs. Senior dogs appear less efficient at metabolizing protein,
so they require additional protein in their diets to help compensate. In
fact, research has shown that healthy older dogs may need as much as 50
percent more protein than normal young healthy adult dogs.”[
24]
“The importance of providing adequate dietary protein
to senior dogs was brought out in research conducted at the Purina Pet
Care Center. In this study, 26 English pointers, ranging from 7 to 9 years
old, were fed diets that were either 15 percent or 45 percent protein over
several years. Dogs fed the high-protein diet maintained a directionally
higher percent of lean body mass and lower percent of body fat.”[
24]
“There is significant evidence, however, that the
daily protein requirements actually increase slightly for dogs in chronic
renal failure. Therefore, severely restricting the protein for such a dog
is likely to result in protein malnutrition, in spite of the fact that
the levels of blood urea nitrogen, or BUN (the primary by-product of protein
metabolism) would be correspondingly lower.”[
25]
As to older dogs that “may” have subclinical kidney
disease, low protein diets have not been shown to benefit dogs that do
have kidney disease, nor have they been shown to reduce the risk of kidney
disease or slow its progression. There are no studies indicating that feeding
excessive protein to older dogs is harmful. “In contrast, research over
the past 10 years or so has shown that protein does not harm the kidney
of dogs. In studies conducted at the University of Georgia in the early
1990s, both in dogs with chronic kidney failure and in older dogs with
only one kidney, protein levels as high as 34 percent caused no ill effects.
. . . 'Our work was directed at learning whether a high-protein diet damages
the kidney. After four years' studying geriatric dogs and two years' studying
dogs with chronic renal failure, we found no indication that a high-protein
diet was injurious to the kidney. However, the data did raise the question
whether low-protein diets in geriatric dogs could be considered injurious.'”[
26]
“Julie Churchill, D.V.M., assistant clinical specialist in companion animal
nutrition at the University of Minnesota, was an investigator in studies
to learn whether altering the amounts of dietary protein and fat could
protect the kidney in aging dogs. "We found there is no benefit in restricting
protein in geriatric dogs," Churchill says. "We observed no changes in
morbidity or mortality. So, the question is, 'Why restrict protein if there
is no benefit?'"”[
27]
In a study designed to test the hypothesis that
restricting protein intake in older dogs may be renoprotective, experimental
dogs seven to eight years of age were divided into two groups. Dogs in
both groups had uninephrectomy performed to increase vulnerability of the
remaining kidney to any protein effects. One group was fed a low protein
diet (18% protein), and the other group received a high protein diet (34%
protein) for the subsequent four years. Results of this study indicated
that there were no adverse effects from the high protein diet, and mortality
was actually higher in the low protein group [
28].
A summary of eight studies done on dogs with reduced
renal mass found that levels of protein up to 44% in the diet had no harmful
effect on the kidneys [
14].
x
“Dogs are omnivores and are capable of meeting
their nutrient requirements by eating a variety of animal and vegetable
substances including grains and starch (e.g., rice, corn starch). The carbohydrates
in Prescription Diet® Canine k/d® are highly digestible (i.e.,
97%).”
x
The question of whether dogs are carnivores are omnivores is beyond
the scope of this letter. Suffice it to say that, while dogs are not obligate
carnivores as cats are, their digestive systems, dentition, and classification
as a subspecies of the grey wolf (canis lupus familiaris) would argue that
dogs are, in fact, far more closely related to carnivores than to omnivores,
such as humans. Although dogs may be capable of deriving nutrition from
grains and starches, that does not mean these foods are an optimal diet
for them, nor can dogs survive without any animal protein in their diet
at all. Those of us interested in giving our dogs the best nutrition, and
not just the cheapest, use primarily animal products, not low quality waste
products from the human food industry such as Brewers Rice [
29]
and Corn Gluten Meal [
30].
In summary, I stand by the recommendations in our
article, and will continue to recommend that dogs with kidney problems
receive adequate amounts of protein that Prescription Diet® Canine
k/d® does not provide, along with fish oil (not the flaxseed found
in Canine k/d®) and high quality fresh foods that they enjoy, and that
moderate, rather than severe, restriction of phosphorus is all that is
needed for early stage renal disease. I also stand by the assertion that
older dogs, including those with CKD, do not benefit, and may be harmed,
by excessive protein restriction.
I would also suggest that Hill’s, rather than defending
their outdated formulas, might better direct that effort toward revising
those formulas in light of recent research that even they admit “has radically
changed and fine-tuned the dietary recommendations for canine CKD patients”,
so that it would not be necessary to warn people about using them.
Sincerely,
Mary Straus
Researcher for the article in the Whole Dog Journal
References
1. Nutrition and Chronic Renal Failure from the Nutrition
support service at The Ohio State University Veterinary Hospital.
2. Veterinary Diet Manual Home Page, Nutrition support
service at The Ohio State University Veterinary Hospital.
5. Allen et al Compendium of Continuing Education,
July 1990
6. Manson MM, Green JA, Driver HE. Ethoxyquin alone
induces preneoplastic changes in rat kidney whilst preventing induction
of such lesions in liver by aflatoxin B1. Carcinogenesis. 1987 May;8(5):723-8.
7. Burkholder WJ, Lees GE, LeBlanc AK, et al. Diet
modulates proteinuria in heterozygous female dogs with X-linked hereditary
nephropathy. J Vet Intern Med. 2004 Mar-Apr;18(2):165-75.
8. Valli VE, Baumal R, Thorner P, et al. Dietary modification
reduces splitting of glomerular basement membranes and delays death due
to renal failure in canine X-linked hereditary nephritis. Lab Invest. 1991
Jul;65(1):67-73.
9. Melissa S. Wallace, DVM, Dipl. ACVIM Strategies
for Protein Losing Nephropathy. Atlantic Coast Veterinary Conference 2001
10. Hoskins, J. Glomerulonephritis remains an important
cause of renal disease in dogs. DVM Newsmagazine Mar 1, 2004.
11. Vaden, S. Description of PLE/PLN: Protein Losing
Enteropathy/Nephropathy in Soft Coated Wheaten Terriers. NC State University
College of Veterinary Medicine.
12. Gregory F. Grauer, DVM, MS, Diplomate, ACVIM (Internal
Medicine) Proteinuria and the Progression of Chronic Renal Disease in the
Dog. 27th WSAVA Conference
13. Andrea J. Fascetti and Sean J. Delaney Nutritional
Management of Chronic Renal Disease
14. Summary of Experiments on Dogs With Reduced Renal
Mass That Examined Renal Effects of Diet.
15. Chronic Renal Disease and Failure (CRD, CRF).
Washington State University College of Veterinary Medicine
16. Dietary Management of Renal and Cardiac Disease.
Virginia-Maryland Regional College of Veterinary Medicine
17. USDA National Nutrient Database and GreenTripe.com
18. Kronfeld DS. Dietary management of renal senescence
and failure in dogs. Aust Vet J. 1994 Oct;71(10):328-31.
19. Davis, B. C. and P. M. Kris-Etherton (2003). Achieving
optimal essential fatty acid status in vegetarians: current knowledge and
practical implications. Am J Clin Nutr 78(3 Suppl): 640S-646S.
20. Gerster H. Can adults adequately convert alpha-linolenic
acid (18:3n-3) to eicosapentaenoic acid (20:5n-3) and docosahexaenoic acid
(22:6n-3)? Int J Vitam Nutr Res. 1998;68(3):159-73.
21. “In dogs, a recent study published in the Journal
of Nutrition showed that supplementation with ALA did not raise blood DHA
levels.” Quoted by Susan G. Wynn, DVM
22. Dietary Management of Chronic Renal Failure.
23. Dietary Management of Chronic Polyuric Renal Failure.
24. D.P. Laflamme, DVM, PhD, DACVN, S.S. Hannah, PhD
and R.D. Kealy, PhD, Geriatric Nutrition: Protein
26. Delmar R. Finco, D.V.M., Ph.D., professor of veterinary
medicine at the University of Georgia. Proc the Waltham/OSU Symposium on
Nephrology and Urology, Columbus, OH. Oct. 1992, p. 39.
http://www.purina.ca/dogs/puppies.asp?article=471
28. Finco DR, Brown SA, Crowell WA, Brown CA, Barsanti
JA, Carey DP, Hirakawa DA. Effects of aging and dietary protein intake
on uninephrectomized geriatric dogs. Am J Vet Res. 1994 Sep;55(9):1282-90.
29. The Composition of Rice and Various Processed
Types
30. Dr. Nick Christians, Corn Gluten Meal Research
Site