Diet associated canine dilated cardiomyopathy

This article aims to explain the recent rise in cases of dilated cardiomyopathy (DCM), primarily in dogs, in the United States. Anecdotally, cases are also rising in the UK, which would match the seeming popularity of grain-free diets here. DCM is a common cause of congestive heart failure in large and giant breed dogs. It is characterised by heart chamber dilation, frequently starting in the left ventricle, and affects the heart's ability to pump blood around the body. The exact underlying cause of DCM is often unknown, but there does appear to be an inherited breed predisposition in Dobermans, Great Danes, Irish Wolfhounds and Boxers. Secondary causes of DCM can include toxins, systemic and infectious disease, and nutritional deficiencies. Recently, there has been a growth in the number of dogs being diagnosed with DCM, and in particular, in atypical breeds. In the last couple of years, studies have shown that the rise in cases has been associated with grain-free, legume-rich and novel protein diets. In the United States, the Food and Drug Administration (FDA) issued a warning to pet owners about the risks of feeding grain-free diets in July 2018. The exact link, however, is still unknown. The good news is that studies show that unlike primary causes of DCM, nutritional DCM may be reversed with diet change and/or supplementation.

What is DCM?

DCM is a common cause of congestive heart failure in dogs, and historically, was linked to large and giant breed dogs (Adin et al, 2019). DCM is characterised by poor systolic function and ventricular dilatation. Genetic mutations have been found in Dobermans, Great Danes and Irish Wolfhounds (Oyama et al, 2009; Meurs et al, 2012; Simpson et al, 2016). Patients can present with vague clinical signs, such as cough, exercise intolerance or weight loss, or with acute life-threatening congestive heart failure. Clinical signs of acute congestive heart failure include respiratory distress, cough (sometimes producing pink froth), and collapse. Tachyarrhythmias are commonly associated with DCM and sudden death may also occur (Ware, 2007). Prognosis for dogs in congestive heart failure as a result of DCM is guarded to poor. Martin et al (2009) reported that 50% of dogs with congestive heart failure resulting from DCM died within 4 months. Secondary causes of DCM include toxins, systemic and infectious disease (such as Bartonella spp.), and nutritional deficiencies.

Link between diet and DCM

DCM used to be a common cardiac disease in cats until taurine supplementation was linked with significant clinical improvement (Pion et al, 1987). Nutritional DCM is thankfully now rare in cats, but still seen in cats that are fed home-prepared diets (Freeman et al, 2018). A few cases of grain-free diet and feline DCM have been reported to the FDA (FDA, 2019). Reports of nutrition-linked DCM in dogs started to appear in 1995 and included breeds such as American Cocker Spaniels (Kittleson et al, 1997), New-foundlands (Backus et al, 2003), Golden Retrievers (Belanger et al, 2005), and other breeds (Kramer et al, 1995; Fascetti et al, 2003). These nutritional forms of DCM were linked to dietary taurine deficiency, and to varying degrees improved with taurine and L-carnitine supplementation. However, some of these dogs received dietary changes at the same time, so the role of taurine deficiency was not proven (Freid et al, 2020). Subsequently, other diets such as lamb and rice, low protein and high fibre diets have also been linked with taurine deficiency (Freeman et al, 2001; Fascetti, 2003; Sanderson, 2006).

The numbers of DCM cases linked to nutrition have continued to rise; Tufts University diagnosed nine cases of DCM in 2014. In 2018, that number had increased to 21 in the first 9 months of the year (Freid et al, 2021). Adin et al's (2019) retrospective study (2015–2018) showed that 75% of dogs diagnosed with DCM were eating a grain-free diet. Freid et al's (2021) retrospective study (2014–2018) found that 79% were eating non-traditional diets. Non-traditional diets have been labelled as boutique, exotic and grain-free (BEGF) and include ingredients such as duck, lamb, salmon, kangaroo, bison, venison, and several types of legumes (see Box 1; note this list is not exhaustive). Obviously, these numbers can be interpreted in a variety of ways, such as increased client awareness, caseload, and/or referral bias, but the number of cases is increasing, so much so that in 2018, the FDA issued a report linking grain-free dog foods and DCM. The FDA have issued two more statements, the latest of which can be found here: https://www.fda.gov/animal-veterinary/outbreaks-and-advisories/fda-investigation-potential-link-between-certain-diets-and-canine-dilated-cardiomyopathy. In America in 2018, the Pet Food Industry reported that grain-free diets constituted 46% of the pet food market (Petfood Industry, 2019). See Figure 1 for an example of a range of grain-free and BEGF products for sale.

Box 1.Boutique, exotic and grain-free ingredients

• Novel animal-based protein:
• Kangaroo
• Duck
• Venison
• Lamb
• Salmon
• Bison
• Buffalo
• Alligator
• Legumes used as alternatives to grains:
• Lentils
• Peas
• Fava beans
• Tapioca
• Barley
• Chickpeas
• Potato
• Sweet potato

Diagnosis of nutritional DCM

The gold standard method of diagnosing DCM is echocardiography. It can be used to measure chamber size and systolic function, and as a serial assessment to evaluate clinical improvement. Arrhythmias are commonly reported with DCM, so electrocardiography can be useful. Radiographs can be used for vertebral heart scoring and for evidence of heart failure. Blood tests are also useful to rule out other causes of DCM (such as systemic or infectious disease), but can also be used to assess taurine or troponin levels. Troponins are released into the circulation as a result of myocardial damage.

Importance of taurine

Taurine is an essential amino acid in the cat, but is not classed as such in the dog. This is because dogs can endogenously synthesise taurine from its precursors, methionine and cystine, primarily in the liver. Taurine is used in various biological processes and is the most abundant amino acid intracellularly. It is needed to conjugate bile acids, therefore a dog could become taurine deficient in periods of high metabolic demand, or if it cannot be resorbed by the intestinal tract. Furthermore, taurine is the most abundant amino acid found in the heart. It is thought to play an important role in myocardial health, because it is involved in cardiac contractility, modulation of calcium flux and cell membrane stabilisation. It is the link with calcium that has led some to suggest that low dietary taurine, and/or reduced synthesis of methionine and cystine, can reduce calcium storage and hamper contraction of cardiac muscle, potentially leading to DCM (Bakker and Berg, 2002; Mansilla et al, 2019).

Measurement of taurine is problematic. It is an expensive test, and there are no breed or size specific ranges. This could be important because, as already discussed, Golden Retrievers seem to be predisposed to taurine deficient DCM. It is currently recommended to sample both whole blood and plasma taurine levels (Kaplan et al, 2018). Improper sample handling can give false results in both plasma (high) and whole blood (low) concentrations of taurine (Kaplan et al, 2018). It is also not known how different blood taurine concentrations are to cardiac muscle taurine concentrations. The only way to determine this, would be myocardial biopsy, which is not recommended. Taurine concentrations can also be affected by platelets, therefore the immune status of the animal could affect taurine concentrations. Mansilla et al (2019) hypothesised this might be why some dogs diagnosed with DCM have normal taurine levels, yet improved with taurine supplementation.

Carnitine deficiency and DCM

L-carnitine is often supplemented in dogs diagnosed with DCM. Carnitine is endogenously produced in the liver and kidneys from lysine and methionine, or exogenously from animal-based products. It is found largely in skeletal and cardiac muscle. It is essential for the metabolism of fatty acids used in energy production, and is particularly integral in the production of adenosine triphosphate (ATP), which drives muscle contraction (Mansilla et al, 2019). It is therefore not surprising that carnitine deficiency has been associated with DCM, a disease of poor muscle contractility. Blood sampling is not sensitive to dietary carnitine levels, and so the only way to accurately test for carnitine deficiency is by muscle biopsies, which again, is not recommended (Mansilla et al, 2019). This would explain the paucity of literature exploring the role of carnitine. However, carnitine and taurine are often supplemented together in dogs diagnosed with dietary DCM.

Problems associating dietary causes to DCM

Current literature suggests that there are insufficient data to prove exactly what is causing dietary-related DCM, just that there seems to be an increased risk of DCM with BEGF diets. Some dogs are taurine deficient, but some are not. Some of the dogs diagnosed with DCM were not taurine deficient, yet improved with diet change (to non-BEGF food) and taurine supplementation, so their DCM must relate to separate, but as yet unknown, dietary factors (Freeman et al, 2018). Furthermore, it has been reported that Golden Retrievers are susceptible to taurine deficiency, so this would suggest there are breed variations (Belanger et al, 2005). Also, some dogs not eating grain-free diets still had clinical improvement when taurine was supplemented (Freeman et al, 2018). This uncertainty has ultimately proved challenging for the pet food industry and has confused pet owners. The FDA advice has had a substantial impact on food sales, but as there is still no exact link between specific diets and DCM, and even if manufacturers wanted to adapt their food, it is not known exactly what they should change (Pet Food Industry, 2019).

The processing of food, or the lack of processing in some cases, can impact nutritional value. The bioavailability of nutrients can be changed during processing, or when combined with other ingredients. It has been reported that cooking and processing of food can result in taurine loss (Kaplan et al, 2018). The newer BEGF ingredients now being used (as shown in Box 1), add complexity to an already complex issue. BEGF ingredients have different nutrient profiles, are digested differently, and may be metabolised differently. Practically this means that at this moment, it is not known what exact role these new ingredients have metabolically, and what effects they may have. Some of these factors can affect the bioavailability of taurine or of its precursors, methionine and cysteine. For example, it is known that lamb has a different bioavailability than chicken (Freeman et al, 2018), and that rabbit is low in taurine (Kaplan et al, 2018). Animal muscle tissue contains the highest amount of taurine, but the bioavailability of taurine or its precursors is not known in BEGF diets. It is not clear what affect the novel animal muscle may have on digestion. If, for example, these exotic meats are undigested in the gut, bacterial overgrowth could interfere with enterohepatic taurine recycling. Some of the ingredients could cause nutritional imbalances, or even the inadvertent addition of toxic components, such is the lack of knowledge of these novel protein sources (Freeman et al, 2018a).

The increased use of legumes in novel diets has been shown to have a negative impact on the digestibility and availability of taurine and its precursors (Kaplan et al, 2018). Legumes are a source of carbohydrate, protein and fibre, but are low in sulphur amino acids. Legumes are used to replace grains in BEGF diets, and include peas, lentils, chickpeas and dry beans. Potato and sweet potato are also used to replace grains. Mansilla et al (2019) speculated that legume seeds constitute 40% of some diets. This is important because, as an example, soybeans are low in methionine. Another significant point is that dietary fibre can affect taurine status in dogs. Mansilla et al (2019) and Kaplan et al (2018) reported that diets containing high fibre, such as those containing a large proportion of legumes, may increase faecal excretion of dietary amino acids, including taurine in cats and dogs.

Walker's recent study (2021) showed that dogs diagnosed with DCM and fed a grain-free diet had better clinical outcomes (significantly increased survival times) compared with those not fed grain-free diets (Walker et al, 2021). They also found that dogs fed a grain-free diet longer and from a younger age, were at increased risk of DCM and congestive heart failure. One further complication, is that the Kaplan et al (2018) study, showed that many of the Golden Retrievers were not receiving their daily metabolic energy requirements (MER). Furthermore, while all the diets named in Kaplan's study (2018) said they met the Association of American Feed Control Official (AAFCO) protocols, none of them had been tested for nutritional adequacy. None of the diets met the recommendations of the World Small Animal Veterinary Association (WSAVA) guidelines. One obvious limitation with these data is the small numbers involved, and firm conclusions should not be drawn from such a small sample size. A summary of study results can be found in Table 1.

One aspect of veterinary nursing is to provide owners with practical, clear, and accurate dietary advice. As there is no clear guidance in the UK on grain-free or BEGF diets, it is suggested to continue advising owners to feed a nutritionally complete diet, unless different advice has been given by the veterinary surgeon. The WSAVA has produced Global Nutrition Guidelines and have a wide range of information for veterinary surgeons and nurses, and also for pet owners. For their ‘Nutrition Toolkit’ and further information see: https://wsava.org/global-guidelines/global-nutrition-guidelines/

Conclusion

The increase in the number of dogs diagnosed with DCM, particularly in atypical breeds, has been linked to nutritional deficiencies, but the exact causes remain unknown. The FDA in America are investigating the role of grainfree diets and protein sources, and it would appear that prolonged exposure to grain-free diets result in a poorer outcome. There is uncertainty about the role of taurine, just evidence to show that dogs can improve when it is supplemented, even if they do not have low taurine levels. The bioavailability of exotic meats, how they are metabolised in the body, and whether this has an impact on metabolism of taurine or its precursors are not understood. All studies are limited by the requirement of owners supplying dietary information, which can complicate food trials and may not include all food ingested by their dog. When providing advice to owners, it is as important now as it ever was, to ensure that all pets are fed a complete diet, which meets their daily requirements and is nutritionally balanced, unless advised differently by their veterinary surgeon.

KEY POINTS

• There has been an increase in the number of canine dilated cardiomyopathy (DCM) cases in the United States, and anecdotally in the UK.
• All evidence is currently based in the United States, but it is suspected that the problem exists in the UK because of the popularity of boutique, exotic and grain-free (BEGF) diets and anecdotal evidence.
• The rise in cases has been linked to BEGF diets.
• The exact relationship between diets and DCM is yet unknown.
• DCM can be reversed in some cases with diet change and supplementation.