Puppy nutrition

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6 healthy puppies getting nutrition at feeding time Puppynutrition.jpg
6 healthy puppies getting nutrition at feeding time

The developmental life stage of dogs requires a specific intake of nutrients to ensure proper growth and development and to meet energy requirements. Despite the fact that puppies have different nutritional requirements compared to their adult counterparts, of the 652 breeders surveyed in the United States and Canada in 2012, 8.7% report feeding puppies commercial diets not intended for the developmental life stage of canines. [1] Large and small dog breeds have even more specific nutrient requirements during growth, such as adjusted calcium to phosphorus ratio, and as such should receive a breed specific growth formula. [2] Feeding diets formulated by a nutritionist for specific breeds and life stage differences in nutrient requirements ensures a growing puppy will receive the proper nutrition associated with appropriate skeletal, neurological and immune development. This includes nutrients such as protein, fibre, essential fatty acids, calcium and vitamin E. [3] [4] [5] It is therefore important to feed puppies a diet that meets the minimum and/or maximum requirements established by the National Research Council. [6]

Contents

The nutritional requirements determined by the NRC are based on scientific evidence and used as the basis for nutritional adequacy in cats and dogs. However, these values are based on the assumption that the availability and digestibility of the nutrients are not variable, although in reality, this is not the case. The Association of American Feed Control Officials (AAFCO) also has recommended nutrient levels, but their values serve primarily as regulatory guidance. AAFCO bases their recommendations on feeding trials and are not necessarily supported by scientific evidence; however their nutritional adequacy statement on pet food bags is considered an important part of the label because their recommendations account for ingredient variability. Other agencies involved in pet food regulations include the FDA in the United States who directly regulates the sales of pet food, the FEDIAF in Europe and PFIAA in Australia who recommend regulatory requirements for the pet food industry, as well as others. When selecting puppy food, it is important to consult the labels and ensure products meet the standards of regulatory agencies of your respective country.

Energy

Young growing dogs require greater amounts of energy per unit body mass than fully grown adult dogs. [7] From time of weaning until the puppy reaches 40% of the adult body weight, the optimal energy intake per unit body weight is twice that of an adult dog of the same breed. [7] From 40% to 80% of adult body weight, energy requirements decrease to 1.6 times the adult requirement, and from 80% to the end of growth, this decreases further to 1.2 times the adult energy requirement. [7] Because of this, it is important to ensure that puppy diets contain higher amounts of energy than adult dog foods. However, over nutrition associated with feeding ad libitum results in accelerated skeletal growth and weight gain leading to osteopenia, especially in large breed dogs. [8] Therefore, appropriate energy requirements should be met, but not exceeded in the growing dog.

Owners and puppy raisers should monitor their puppy’s weight gain by referencing a 9-point body condition score scale which is easily accessible on the internet, regularly weighing the puppy, and consulting with their veterinarian. Owners should also be mindful as to the energy level of their puppy; high energy level puppies will require more energy and may need to be fed extra amounts of food, just as lower energy puppies may require less food. The 9 point body condition score has been shown to be an effective method for estimating percent body fat in dogs. [9] Therefore, by adhering to the 9 point body condition scale, and adjusting food intake accordingly, owners will be able to maintain their puppy at an appropriate weight throughout its growth. In addition to visual estimates of body condition, physical palpation of the pet can provide insight on general health and weight. Speaking to a licensed veterinarian can be very beneficial, as they can help develop these dietary and weight monitoring skills.

Calcium and Phosphorus

An important aspect of the composition of puppy food is the calcium and phosphorus content. Bone mineral is composed mainly of calcium, which functions in skeletal mineralization during growth. [4] Puppies younger than 5 months are not able to adjust the absorption of calcium in response to intake, therefore an oversupply or undersupply can be harmful. [10] When raised on diets deficient in calcium, pathological bone fractures can result. [11] These fractures have been shown to occur in smaller breed puppies when their diet contained less than 0.33% calcium on a dry matter (DM) basis. [11] Larger breeds present with fractures at a calcium level of less than 0.55%, thus requiring these breeds to have greater calcium requirements. [12]

The ratio of calcium to phosphorus greatly impacts the retention of phosphorus. A ratio of 1.3:1 will allow for good phosphorus retention, but levels above a ratio of 2:1 will decrease phosphorus retention. [13] Raising puppies on diets containing excess calcium and phosphorus will result in osteochondrosis which disturbs bone remodeling and cartilage and bone maturation. [11] [14] These changes are noticed in larger breed puppies at lower levels of excess than in smaller breeds. [2] Because large breed puppies are more sensitive to deficient and excess calcium and phosphorus levels, it is important to ensure that their diets contain sufficient amounts of both. [11] The minimum requirement laid out by the NRC is 8.0g/kg DM calcium (0.8%), with a 12g/kg DM (1.2%) recommended allowance. [6] However, recommendations laid out by AAFCO consist of slightly higher calcium values; 1.2% to 1.8% on a DM basis, whereas phosphorus levels should be between 1.0% and 1.6%, with a ratio of calcium to phosphorus between 1:1 and 2:1. [15] Many commonly used ingredients, such as corn, which are added in high amounts to commercial dog foods do not contain adequate amounts of calcium, and as such, calcium supplements are often added to the formulation to ensure proper amounts for development. [16] In addition, a descriptive study of over-the-counter maintenance dog foods determined that 4/45 of the foods studied contained calcium concentrations that exceeded the AAFCO recommendation, but were labeled for all life stages. [17] Therefore, it is important to feed a diet specifically recommended for the developmental life stage and consult the calcium and phosphorus levels in puppy foods.

Fats and Fatty Acids

Fat is a nutrient that provides more energy per gram than all other nutrients. [18] Fat provides 9.4kcal/g of gross energy (GE) compared to protein and carbohydrate which only provide 5.56 and 4.15 kcal/g respectively. [18] Due to this greater energy concentration and the higher energy demand of puppies, the higher fat content of canine development diets helps reach these increased energy requirements while also providing the essential fatty acids necessary for the growing dog. Omega-3 (n-3) fatty acids are an important component of puppy diets. Multiple studies suggest brain and retinal function are dependent on the level of n-3 polyunsaturated fatty acids acquired during in utero development and postnatal life. [3] [19] [20] DHA is the main n-3 fatty acid and can be obtained as DHA itself from dietary sources such as fish and fish oils, or as the DHA precursor linolenic acid. [3] With a high DHA intake, plasma lipid DHA content increases, aiding neurological development, as demonstrated by increases in memory and learning ability. [3] [20] Other benefits of n-3 and DHA include promotion of neurogenesis, increased neuron size and phospholipid synthesis, as well as protection against cell death and peroxidative brain damage by damaging free radicals [21] in the rodent model and presumably across the mammalian kingdom. A deficit of dietary n-3 fatty acids leads to a reduction in brain DHA content by 50-80%, leading to cognitive deficits and increased n-6 fatty acid level which increases inflammation. [20] Adequate intake and recommended allowance levels of 85g/kg (DM) of total fat (8.5%), and 0.5g/kg (DM) of omega 3 fatty acids (EPA+DHA) are laid out by the NRC. [6] Both of these values are also laid out as recommendations by AAFCO. However, according to a study on the effects of supplementing DHA in puppy diets, diets containing 1.4% n-3 fatty acids, or 0.19% DHA resulted in optimal neurological function. [3] [15]

Vitamin E

Along with DHA, vitamin E also supports the proper development of eyesight, reduces oxidative damage, and provides additional immune function support. [4] During instances of immune system stimulation, such as vaccinations and infection, immune cells generate more tissue damaging free radicals. [4] These free radicals are reduced by the action of antioxidants such as vitamin E, which promote the formation and maintenance of healthy immune cells. [4] The adequate intake level laid out by the NRC consists of 24 mg/kg (36 IU/kg) of vitamin E, with a recommended allowance of 30 mg/kg (45 IU/kg). [6] However, the regulatory guidance laid out by AAFCO states a vitamin E minimum recommendation of 50 IU/kg DM. Nonetheless, these values have been shown to be insufficient for immune protection; immune function is best optimized at a level of 500 IU/kg. [4] In addition to prevention of free radical damage, this higher level of vitamin E greatly increases the number of memory CD4+ immune cells, aiding in a greater and a longer response to infection. [4] Due to their still-developing immune system, puppies are more susceptible to infection than adult dogs, and proper levels of vitamin E, as indicated above, are needed in their diet.

Fibre

Although young growing dogs have immature gastrointestinal tracts, they do contain microflora which can ferment fibre and generate short chain fatty acids beneficial to gut health. [22] [23] Colonization and establishment of these bacterial populations happens over time, beginning immediately after birth. [24] Even with the ability for fermentation, addition of fibre to the diet should be done carefully, as fibre will dilute other nutrients in the feed. [6] [25] There are different types of fibre, all are made of carbohydrates, and NRC classifies them into fermentable and non-fermentable carbohydrates. [6] Fermentable carbohydrates are generally 3-10 monosaccharide units joined by glycosidic bonds which cannot be degraded by endogenous enzymes and require the fermentation processes of intestinal microflora for proper degradation. [6] Non-fermentable fibres are carbohydrate structures which are not fully fermented even by intestinal microflora. Little research has been done on non-fermentable fibre, however it is known that it causes fecal bulking and reduced intestinal transit time. [11] It has been shown that addition of non-fermentable fibre in concentrations of 22% or greater of the total diet will reduce growth, feed intake and feed efficiency. [25]

Fermentable fibre is more beneficial for growing puppies, and it is often considered a prebiotic, meaning it supports the growth of beneficial microflora species in the intestinal tract. [26] Fermentable fibre often contains fructo-oligosaccharides (FOS) and mannanoligosaccharides (MOS), both of which greatly stimulate gut health. [27] FOS are fermented by beneficial bacteria such as bifidobacteria promoting their growth, while most pathogenic bacterial strains such as E. coli, C. perfringens and Salmonella are unable to ferment it. [27] MOS has been shown to stimulate the immune system and increase resistance to pathogenic bacteria. [27] Beet pulp is generally the standard fermentable fibre used in canine diets, however blends of fermentable fibre sources have been shown to be as effective at promoting gut health. [28] Although fermentable fibre is extremely beneficial, it should still be added in moderate amounts as addition of fermentable fibre to a concentration of 14.1% or greater will result in lower digestibility of the feed. [6] [22]

Protein

Growing puppies require higher levels of protein than adult dogs of the same breed to promote proper growth and development. [29] Protein should account for at least 25% of energy; however protein requirements also depend on the digestibility of the protein and age of the puppy. [29] Amino acid and nitrogen requirements decrease between 10–14 weeks, indicating that different protein levels are often beneficial before and after 14 weeks of age. [6] Before 14 weeks of age, a protein level of 250 g/kg of diet (25% of the diet) containing 4.0 kcal ME/g will result in optimal growth. [25] [29] [30] After 14 weeks of age, protein requirements decrease to 200 g/kg of diet (20% of the diet) for optimal growth. [6] [31] [32] [33]

Protein in excess of these levels is metabolized and leads to an increase of the glomerular filtration rate, and increased urea excretion in the urine, with no evidence of damage to the kidneys. [34] However, addition of protein past these requirements is not recommended, although the NRC has not quantified a safe upper limit. [6] Considering that the energy density of protein is similar to that of carbohydrates, an excess of protein in the diet may lead to fat deposition and weight gain. [18] This excess weight can lead to abnormal joint development, potentially giving rise to joint issues in the future. Additionally, excess of some amino acids may also have detrimental impacts; for example, excess lysine will negatively antagonise arginine. [35] The minimal requirement laid out by the NRC is 180g/kg (18%) DM of crude protein, with a recommended allowance of 225g/kg (22.5%) DM. [6] With this in mind, it is also important to consider the quality and digestibility of the protein used.

Iodine

To date, there is little information available about minimum requirements of dietary iodine for developing puppies. However, literature suggests that overdosage of iodine in puppies has deleterious effects on the thyroid gland. [36] [37] High dietary iodine may cause both hypothyroidism and changes in bone metabolism, considering that thyroid hormones are key factors in osteogenesis, as they stimulate osteoblasts, and promote collagen synthesis and mineralization of the osteoid. [36] [37] This is particularly important during juvenile development, as these hormones favor the action of growth hormone (GH) and its facilitator, insulin growth factor-1 (IGF-1) at the osteoplastic level. [36] [37] Hypothyroidism acquired at an early age presents a delay in the maturation and development of the ossification sites of newly-developing bone. [36] It is therefore important to closely monitor the amount of iodine in puppy diets in order to prevent overdosage. The NRC states an adequate intake and recommended allowance of 900 μg/kg (DM) which translates into 220μg/1000 kcal. [6] These values have been shown in multiple studies to be the recommended maximum allowance of iodine that would result in no abnormalities. [6] [38] [39]

Synopsis

Canine development diets are designed specifically to meet the energy demands and nutritional requirements for healthy growth. Proper nutrition is imperative to support development of bones, joints, muscles, and the immune system, and includes the addition of nutrients such as protein, essential fatty acids, calcium, fibre, vitamin E, and others. Ensuring optimal energy intake allows the diet to meet the high energy demands of puppies while avoiding over nutrition, over-accelerated growth, and unhealthy weight gain. Dietary fats also help to meet these high energy demands and provide the essential fatty acids necessary for brain, neuron, and retinal development and function. Since growing puppies require greater amounts of protein than their adult counterparts, it is important to include the appropriate amounts to support healthy development. Correct levels of both fermentable and non-fermentable fibre help to support GI and immune health. During growth, young dogs are more susceptible to infection, but the addition of proper levels of vitamin E to the diet reduces free radical oxidative damage and leads to an increase in immunity. Calcium and phosphorus, in the appropriate amounts and ratio, aid in proper bone and cartilage growth and maturation. It is imperative to be aware of the levels of other minerals as well, as the over-dosage of iodine can lead to hypothyroidism, and the delay in maturation and development of bones. It is therefore important to feed a diet that meets the nutrient minimum and/or maximum requirements established by the National Research Council in order to ensure optimal growth and development of young dogs of all breeds.

Related Research Articles

Omega−3 fatty acids, also called Omega−3 oils, ω−3 fatty acids, Ω-3 Fatty acids or n−3 fatty acids, are polyunsaturated fatty acids (PUFAs) characterized by the presence of a double bond three atoms away from the terminal methyl group in their chemical structure. They are widely distributed in nature, being important constituents of animal lipid metabolism, and they play an important role in the human diet and in human physiology. The three types of omega−3 fatty acids involved in human physiology are α-linolenic acid (ALA), eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). ALA can be found in plants, while DHA and EPA are found in algae and fish. Marine algae and phytoplankton are primary sources of omega−3 fatty acids. DHA and EPA accumulate in fish that eat these algae. Common sources of plant oils containing ALA include walnuts, edible seeds, and flaxseeds as well as hempseed oil, while sources of EPA and DHA include fish and fish oils, and algae oil.

<span class="mw-page-title-main">Kitten</span> Juvenile cat

A kitten is a juvenile cat. After being born, kittens display primary altriciality and are fully dependent on their mothers for survival. They normally do not open their eyes for seven to ten days. After about two weeks, kittens develop quickly and begin to explore the world outside their nest. After a further three to four weeks, they begin to eat solid food and grow baby teeth. Domestic kittens are highly social animals and usually enjoy human companionship.

<span class="mw-page-title-main">Dietary fiber</span> Portion of plant-derived food that cannot be completely digested

Dietary fiber or roughage is the portion of plant-derived food that cannot be completely broken down by human digestive enzymes. Dietary fibers are diverse in chemical composition, and can be grouped generally by their solubility, viscosity, and fermentability, which affect how fibers are processed in the body. Dietary fiber has two main components: soluble fiber and insoluble fiber, which are components of plant-based foods, such as legumes, whole grains and cereals, vegetables, fruits, and nuts or seeds. A diet high in regular fiber consumption is generally associated with supporting health and lowering the risk of several diseases. Dietary fiber consists of non-starch polysaccharides and other plant components such as cellulose, resistant starch, resistant dextrins, inulin, lignins, chitins, pectins, beta-glucans, and oligosaccharides.

A nutrient is a substance used by an organism to survive, grow, and reproduce. The requirement for dietary nutrient intake applies to animals, plants, fungi, and protists. Nutrients can be incorporated into cells for metabolic purposes or excreted by cells to create non-cellular structures, such as hair, scales, feathers, or exoskeletons. Some nutrients can be metabolically converted to smaller molecules in the process of releasing energy, such as for carbohydrates, lipids, proteins, and fermentation products, leading to end-products of water and carbon dioxide. All organisms require water. Essential nutrients for animals are the energy sources, some of the amino acids that are combined to create proteins, a subset of fatty acids, vitamins and certain minerals. Plants require more diverse minerals absorbed through roots, plus carbon dioxide and oxygen absorbed through leaves. Fungi live on dead or living organic matter and meet nutrient needs from their host.

<span class="mw-page-title-main">Human nutrition</span> Provision of essential nutrients necessary to support human life and health

Human nutrition deals with the provision of essential nutrients in food that are necessary to support human life and good health. Poor nutrition is a chronic problem often linked to poverty, food security, or a poor understanding of nutritional requirements. Malnutrition and its consequences are large contributors to deaths, physical deformities, and disabilities worldwide. Good nutrition is necessary for children to grow physically and mentally, and for normal human biological development.

<span class="mw-page-title-main">Dietary supplement</span> Product providing additional nutrients

A dietary supplement is a manufactured product intended to supplement a person's diet by taking a pill, capsule, tablet, powder, or liquid. A supplement can provide nutrients either extracted from food sources, or that are synthetic. The classes of nutrient compounds in supplements include vitamins, minerals, fiber, fatty acids, and amino acids. Dietary supplements can also contain substances that have not been confirmed as being essential to life, and so are not nutrients per se, but are marketed as having a beneficial biological effect, such as plant pigments or polyphenols. Animals can also be a source of supplement ingredients, such as collagen from chickens or fish for example. These are also sold individually and in combination, and may be combined with nutrient ingredients. The European Commission has also established harmonized rules to help insure that food supplements are safe and appropriately labeled.

<span class="mw-page-title-main">Dog food</span> Food intended for consumption by dogs usually made from meat

Dog food is specifically formulated and intended for consumption by dogs and other related canines. Dogs are considered to be omnivores with a carnivorous bias. They have the sharp, pointed teeth and shorter gastrointestinal tracts of carnivores, better suited for the consumption of meat than of vegetable substances, yet also have ten genes that are responsible for starch and glucose digestion, as well as the ability to produce amylase, an enzyme that functions to break down carbohydrates into simple sugars – something that obligate carnivores like cats lack. Dogs evolved the ability living alongside humans in agricultural societies, as they managed on scrap leftovers and excrement from humans.

<span class="mw-page-title-main">Vegetarian nutrition</span> Nutritional and human health aspects of vegetarian diets

Vegetarian nutrition is the set of health-related challenges and advantages of vegetarian diets.

<span class="mw-page-title-main">Cat food</span> Food for consumption by cats

Cat food is food specifically formulated and designed for consumption by cats. As obligate carnivores, cats have specific requirements for their dietary nutrients, namely nutrients found only in meat or synthesised, such as taurine and Vitamin A. Certain nutrients, including many vitamins and amino acids, are degraded by the temperatures, pressures and chemical treatments used during manufacture, and hence must be added after manufacture to avoid nutritional deficiency. Cat food is typically sold as dry kibble, or as wet food in cans and pouches.

Raw feeding is the practice of feeding domestic dogs, cats, and other animals a diet consisting primarily of uncooked meat, edible bones, and organs. The ingredients used to formulate raw diets vary. Some pet owners choose to make home-made raw diets to feed their animals but commercial raw diets are also available.

<span class="mw-page-title-main">Dog coat</span> Hair that covers its body

The coat of the domestic dog refers to the hair that covers its body. Dogs demonstrate a wide range of coat colors, patterns, textures, and lengths.

<span class="mw-page-title-main">Nutrition and pregnancy</span> Nutrient intake and dietary planning undertaken before, during and after pregnancy

Nutrition and pregnancy refers to the nutrient intake, and dietary planning that is undertaken before, during and after pregnancy. Nutrition of the fetus begins at conception. For this reason, the nutrition of the mother is important from before conception as well as throughout pregnancy and breastfeeding. An ever-increasing number of studies have shown that the nutrition of the mother will have an effect on the child, up to and including the risk for cancer, cardiovascular disease, hypertension and diabetes throughout life.

<span class="mw-page-title-main">Protein (nutrient)</span> Nutrient for the human body

Proteins are essential nutrients for the human body. They are one of the building blocks of body tissue and can also serve as a fuel source. As a fuel, proteins provide as much energy density as carbohydrates: 4 kcal per gram; in contrast, lipids provide 9 kcal per gram. The most important aspect and defining characteristic of protein from a nutritional standpoint is its amino acid composition.

Animal nutrition focuses on the dietary nutrients needs of animals, primarily those in agriculture and food production, but also in zoos, aquariums, and wildlife management.

Canadian health claims by Health Canada, the department of the Government of Canada responsible for national health, has allowed five scientifically verified disease risk reduction claims to be used on food labels and on food advertising. Other countries, including the United States and Great Britain, have approved similar health claims on food labels.

<span class="mw-page-title-main">Vegan nutrition</span> Nutritional and human health aspects of vegan diets

Vegan nutrition refers to the nutritional and human health aspects of vegan diets. A well-planned vegan diet is suitable to meet all recommendations for nutrients in every stage of human life. Vegan diets tend to be higher in dietary fiber, magnesium, folic acid, vitamin C, vitamin E, and phytochemicals; and lower in calories, saturated fat, iron, cholesterol, long-chain omega-3 fatty acids, vitamin D, calcium, zinc, and vitamin B12.

High performance sport dogs are those bred and trained to compete in various athletic events. Events include but are not limited to, agility trials, hunting and racing. These events are physically and metabolically demanding. As a result, canine athletes require specialized nutrition in order to perform at high levels during events and for maintenance and recovery. The main nutritional concern for sport dogs is adequate energy. A well-balanced diet, containing the appropriate amounts of protein, fat, carbohydrate, fiber and micronutrients is essential to meet these energy requirements.

<span class="mw-page-title-main">Senior dog diet</span>

Senior dog food diets are pet foods that are catered toward the senior or mature pet population. The senior dog population consists of dogs that are over the age of seven for most dog breeds, though in general large and giant breed dogs tend to reach this life stage earlier when compared to smaller breed dogs. Senior dog foods contain nutrients and characteristics that are used to improve the health of the aging dog. Aging in dogs causes many changes to occur physiologically that will require a change in nutrient composition of their diet.

In general, cognitive support diets are formulated to include nutrients that have a known role in brain development, function and/or maintenance, with the goal of improving and preserving mental processes such as attentiveness, short-term and long-term memory, learning, and problem solving. Currently, there is very little conclusive research available regarding cat cognition as standardized tests for evaluating cognitive ability are less established and less reliable than cognitive testing apparatus used in other mammalian species, like dogs. Much of what is known about feline cognition has been inferred from a combination of owner-reported behaviour, brain necropsies, and comparative cognitive neurology of related animal models. Cognition claims appear primarily on kitten diets which include elevated levels of nutrients associated with optimal brain development, although there are now diets available for senior cats that include nutrients to help slow the progression of age-related changes and prevent cognitive decline. Cognition diets for cats contain a greater portion of omega-3 fatty acids, especially docosahexaenoic acid (DHA) as well as eicosapentaenoic acid (EPA), and usually feature a variety of antioxidants and other supporting nutrients thought to have positive effects on cognition.

<span class="mw-page-title-main">Vegetarian and vegan dog diet</span> Adequate meat-free or animal-free nutrition

As in the human practice of veganism, vegan dog foods are those formulated with the exclusion of ingredients that contain or were processed with any part of an animal, or any animal byproduct. Vegan dog food may incorporate the use of fruits, vegetables, cereals, legumes including soya, nuts, vegetable oils, as well as any other non-animal based foods.

References

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  30. ↑ Ontko, J.A.; Wuthier, R.E.; Phillips, P.H. (1957). "The effect of increased dietary fat upon the protein requirement of the growing dog". Journal of Nutrition. 62: 163–169. doi:10.1093/jn/62.2.163.
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  33. ↑ Delaney, S.J.; Hill, A.S.; Backus, R.C.; Czarnecki-Maulden, G.L.; Rogers, Q.R. (2001). "Dietary crude protein concentration does not affect the leucine requirements of growing dogs". Journal of Animal Physiology and Animal Nutrition. 85: 88–100. doi:10.1046/j.1439-0396.2001.00306.x.
  34. ↑ Nap, R.C.; Hazewinkel, H.A.; Voorhout, G.; Van den Brom, W.E.; Goedegebuure, S.A.; Van'T Klooster, A.T. (1991). "Growth and skeletal development in Great Dane pups fed different levels of protein intake". Journal of Nutrition. 121: 107–113.
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  39. ↑ Belshaw, B.; Cooper, T.; Becker, D. (1975). "The iodine requirement and influence of iodine intake on iodine metabolism and thyroid function in the adult beagle". Endocrinology. 96: 1280–1291. doi:10.1210/endo-96-5-1280.
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