Epidemiology

The most common reason for PEM is poor quality forages coupled with the animal’s inability to consume sufficient amounts relative to requirements.⁵ Growing animals, females in late pregnancy, and lactating females have the greatest energy and protein requirement and hence are most susceptible to PEM. Under South American conditions, animal body weight (BW) and body condition score (BCS) changes will mimic seasonal forage growth patterns. Camelids gain significant body weight and condition and give birth during the rainy season in concert with high-quality forage availability. During the dry season, animals lose considerable weight and condition and are in various stages of malnutrition (see discussion in Chapter 11). Animals giving birth during the dry season are much more prone to PEM, secondary infections, and parasitic disease problems, which often lead to death.

Llamas and alpacas raised outside of South America are exposed to a greater diversity of environmental conditions ranging from extreme hot and humid environments (Southern United States and Europe) to extremely cold winter conditions (Northern United States and Europe, Canada, and Alaska). Average winter daily temperature in northern North America falls below -5 °F (15°C) and may go down to –31 °F (–35°C).⁵ These are environmental extremes that llamas and alpacas never experience in their native environment. Hot and humid environments bring challenges such as prevention of heat stress, which is a significant health risk for llamas and alpacas. Cold, wet conditions also have challenges associated with providing effective protective shelter and increased energy intake to compensate for additional maintenance requirements. If animals are wet, mud covered, or exposed to wind chill, then maintenance energy may be increased by as much as 75%. Either environmental extreme may result in a situation of potential PEM with poor-quality forage.

In these cold conditions, camelids will expend additional energy to maintain body temperature. Data from other ruminant species suggest that maintenance energy is increased by 1% for every 33.8°F (1°C) below an animal’s lower critical temperature.⁶ On the basis of data from sheep and assuming a full fleece, the lower critical temperature (LCT) for llamas and alpacas would be approximately 32°F to 50°F (0°C to 10°C).⁶ Younger animals have greater surface area relative to body size and thus have greater heat loss and a higher LCT compared with adults.

Clinical Findings

Body weight loss and a decline in BCS are the most common presenting signs.5,7 Growing animals also show a slowing or near-total cessation in gain. Depending on the reproductive status of the animal, delayed puberty, anestrus, irregular estrus, decreased birth weights, and embryonic death may be observed. Lactating females show a marked decline to cessation of milk production. Pregnant and lactating females experiencing PEM may be prone to hepatic lipidosis as a secondary complication.^8,9 Time frame and severity of clinical manifestations will be dependent on the degree of dietary energy and protein deficiencies. Animals experiencing PEM maintain a healthy appetite until near terminal stages in contrast to animals afflicted by an infectious or parasitic disease, which have reduced appetites despite their energy deficit.

Diagnosis and Treatment

Routine BCS (refer to Chapter 12 for method) or BW determinations may be used to diagnose potential problems. A thick fleece may easily hide BW and condition changes from view, requiring direct palpation to determine the BCS. Once unexplained BW loss or BCS loss has been identified, a cause needs to be determined. Chronic infectious, parasitic, and dental diseases may induce BW loss and condition loss as in PEM.⁵ Protein-energy malnutrition is often a secondary process to chronic disease conditions.

Starvation or dietary insufficiency result in mobilization of adipose stores, characterized by an increase in blood nonesterified fatty acid (NEFA) up to about 0.6 to 1.0 milliequals per liter (mEq/L), a mild increase in blood β-hydroxybutyrate up to about 1 to 2 milligrams per deciliter (mg/dL), and little to no change in blood triglycerides.9,10 Hypoalbuminemia and hypoproteinemia are often observed, but total protein concentration as well as other serum chemistry parameters may be variable, depending on underlying or secondary conditions. Anemia, neutropenia, and lymphopenia often are associated with PEM, although altered white blood cell (WBC) number and differential count may reflect underlying chronic infectious or parasitic disease.

Elevation in blood NEFA concentration is often not associated with any clinical signs but may indicate risk. Experimentally, pregnant camelids and lactating camelids on restricted diets may develop more rapid and more severe fat mobilization, possibly resulting in hepatic lipidosis.⁹ Nonpregnant, nonlactating camelids develop a lower degree of fat mobilization and do not accumulate lipid in their liver from negative energy balance alone. Thus, camelids that do not develop exuberant fat metabolism with dietary caloric insufficiency rarely require any treatment beyond restoration of an appropriate diet. Animals identified early in the disease process can be recovered with appropriate feeding therapy and supportive care (see Chapter 33), although those becoming weak and recumbent have a very poor prognosis even with aggressive therapy.

Prevention

Appropriate feeding regimes where forage quality is matched to nutrient needs of the animal are the cornerstone of PEM prevention. Where forage quality is insufficient, feeding of supplemental feeds is necessary, especially in cold climatic conditions (Table 13-1). In cold environmental conditions, dry matter (DM) intake increases moderately to account for greater energy needs, although this response may not be sufficient under more severe conditions. To achieve such feeding programs, forage quality will need to be evaluated by chemical analysis (refer to Chapter 9, Nutritional Requirements). Routine assessment of animals’ energy status by body weight or condition scoring is a recommended practice, especially for those individuals with higher energy requirements and prior to and during the cold season. Important times to assess BCS would be during early to mid-pregnancy, early to mid-lactation, and periodically (4–6 times per year) to other animals of the herd to assess energy status.¹¹

Epidemiology

Obesity is considered one of the more prevalent nutritional problems in llamas and alpacas outside of South America.12,13 Consumption of energy in excess of requirement results in fat deposition leading to obesity. Recent work suggests excess protein intake in alpacas may also lead to obesity.¹⁴ Ad libitum feeding of high-quality forage or overfeeding additional supplements are primary contributors to obesity. Many commercially available nutritional supplements contain substantial amounts of cereal grains or readily fermentable fiber, which are good energy sources. Even “low energy” supplements may contain unwanted caloric intake given the efficient fiber fermentation process in SACs. The noted discrepancy in feed intake expectations between North and South American data explains the greater obesity issues in camelids in North America. Deleterious effects of obesity include greater susceptibility to heat stress (refer to Chapter 41), metabolic derangements, infertility, and associated locomotion problems.

Diagnosis

Increasing BW beyond what would be expected for pregnancy or growth coupled with BCS assessment exceeding 4 (5-point scale) or 7 (9-point scale) would be indicative of excess fat accumulation. Obesity is defined as the highest score in any BCS scale. An animal’s ideal BW would be based on a BCS of 3 (5-point scale) or 5 (9-point scale) at the time when the animal has stopped growing. BW will vary with frame size and BCS. The weight of accumulated or lost fat and body tissue relative to 1 BCS change has not been quantified for camelids.

Treatment and Prevention

Reducing energy intake, increasing energy expenditure, or some combination are methods for obesity treatment and prevention. An animal’s energy requirement is primarily a function of lean BW (3 or 5 BCS, depending on scale) and their physiologic state (maintenance, growth, pregnancy, lactation). Much individual animal variation exists in the propensity for obesity. Identified fat or obese animals should have their caloric intake reduced by limiting supplements, forage availability and quality, or some combination. Lower-quality forages should be provided exclusively or prior to grazing to minimize pasture intake. Obese animals should be segregated so that they cannot “steal” food from others. Increase stocking density or grazing intensity to reduce intake. Obese animals should be grazed only on mature pastures of lower quality. Larger paddock size with limited forage increases distance traveled during grazing, which, in turn, increases energy expenditure. Packing and other activities increase energy expenditure, but this may not be a viable option.

For weight reduction to be successful, a methodical approach to limiting energy intake and monitoring response should be instituted. In companion animal species, required energy intake is calculated based on ideal BW, then fractionally reduced to 60% to 65% or 70% to 75% of total in dogs and cats, respectively. In a feed restriction study, llamas that lost 15% to 20% of BW within a 10-to-14 day period were at high risk (50%) for some degree of hepatic lipidosis.⁹ The unique metabolic adaptations of camelids are similar to those of cats. Cats, unlike dogs, are susceptible to hepatic lipidosis with moderate to severe calorie restriction and rapid weight loss. Thus, the approach for weight reduction in cats might be an appropriate recommendation for weight loss in camelids. Caloric intake is restricted to 70% to 75% of ideal BW requirement to target 0.5% to 1% of weight loss per week in obese animals.

BW or BCS must be routinely assessed to achieve the appropriate nutritional balance to maintain optimum condition for a given animal. Ongoing monitoring is critical to the success of a weight loss program. Goals and progress should be assessed at regular intervals until the final desired weight and condition are achieved.

Epidemiology

Forestomach microbial populations are capable of utilizing NPN sources to synthesize microbial protein, which is ultimately digested and absorbed by the host animal. Dietary NPN sources are eventually reduced to ammonia, which supports forestomach microbial fiber fermentation. This is a unique feature of the ruminant animal and is a primary reason for their ability to utilize poor quality feeds. NPN toxicosis is a disease unique to ruminant animals as a direct result of microbial production of toxic compounds from excessive NPN consumed. Compounds of concern to ruminants are urea, nitrates, and nitrites, and a risk to camelids is presumed. Urea is a common nitrogen fertilizer and ruminant feed supplement. Urea is rapidly cleaved into carbon dioxide and two ammonia molecules. To assimilate ammonia into microbial protein, energy derived from microbial fermentation of dietary carbohydrate is required. Poor-quality forages do not provide sufficient amounts of energy in synchrony to support NPN utilization by forestomach microbes. If ammonia is not utilized by microbes, it will diffuse across the forestomach wall into portal blood circulation. The liver normally converts excess ammonia back into urea for recycling or excretion, but its capacity to shunt ammonia through the urea cycle may be exceeded. Free ammonia is a potent cellular toxin disrupting energy metabolism and potassium homeostasis.

Clinical Presentation

NPN toxicosis overwhelms the liver, with excess ammonia resulting in dramatically increased blood ammonia concentration and subsequent clinical signs. Urea toxicosis occurs rapidly as early as 10 minutes and typically within 0.5 to 2 hours of excess consumption. Clinical signs include frothy salivation, bruxism, colic, muscle tremors, incoordination, and recumbency followed by death in rapid progression.

Diagnosis and Treatment

Diagnosis is based on history, smell of ammonia to the animal, and quantification of ammonia in either blood (1–4 mg/dL) or forestomach (>80 mg/dL) contents. Forestomach pH is elevated (>7.5). Treatment is unrewarding for the most part unless identified very early in toxicity. Treatment objectives are to reduce ammonia production and absorption. Drenching with weak acids (vinegar, 5% acetic acid) and cold water are suggested. The most effective treatment is prompt emptying of the forestomach.

Prevention

Minimizing the risk of inappropriate exposure to NPN sources is the best method of control. Forestomach microbes may be adapted to NPN sources by slowly increasing their incorporation rate in the diet and ensuring adequate fermentable carbohydrate sources, although the use of NPN in camelid diets is not common. The toxic dose of urea for ruminants is 0.3 to 0.5 grams per kilogram (g/kg) of BW. A general recommendation is to have urea constitute no more than 3% of the concentrate, although many commercial supplements containing NPN sources targeted for sheep and cattle have greater amounts. The amount of urea in a supplement is determined by dividing the percent protein from NPN provided on the product label by 281 (25% protein equivalent from NPN = 8.8% urea [25/2.81]). An NPN source should not contribute more than 30% of the total dietary crude protein (CP) content.

Epidemiology

Inadequate intake of salt, more specifically sodium, and potassium may lead to pica, which is an aberrant feeding behavior in which animals chew on sticks, pipes, or other objects or eat dirt. Forages generally are low in sodium content, whereas potassium intake is more than adequate. Providing free-choice loose salt, either white or trace mineralized, minimizes the risk for salt or sodium deficiency.

In contrast to domestic ruminants and horses, clinical hypocalcemia and hypomagnesemia appear to be rare in camelids, except in New Zealand, where grass tetany and Ryegrass staggers are major differential diagnoses for camelids with staggering gaits (see under Neurologic Diseases, Chapter 38). Both blood abnormalities may occur secondary to hypoproteinemia, which is common in camelids, and more specifically secondary to hypoalbuminemia. However, lack of albumin does not affect the functional, ionized fractions of blood calcium and magnesium, and hence does not induce clinical abnormalities. Phosphorus deficiency is most often associated with vitamin D deficiency (see Vitamin Deficiency discussion below).

Diagnosis and Treatment

As indicated by clinician experiences, hypocalcemia and hypomagnesemia in camelids present with similar clinical signs, diagnostic criteria, and therapeutic response compared with other ruminants.1,2 As with ruminants, diagnosis is based on history, signalment, and response to therapy, with blood analysis used for confirmation of the diagnosis.

Hypocalcemia as a single abnormality appears to occur mainly as a complication of anorexia secondary to an illness during pregnancy or lactation and rarely progresses to the point of physical weakness. Before that occurs, it may affect smooth muscle function, principally resulting in ileus. Identifying hypocalcemia (total calcium <1.2 millimoles per liter [mmol/L], or <5 mg/dL) disproportionate to hypoalbuminemia on blood analysis, or identifying a decrease in ionized calcium (<0.5 mmol/L [<2 mg/dL]) may be used to justify treatment with intravenous calcium gluconate. Similar to other ruminant species, intravenous calcium therapy should be administered slowly, closely monitored, and given to effect. A suggested targeted dose is 1 g calcium per 100 lb (45 kg) body weight. Cardiac auscultation should be performed to identify changes in heart rhythm and rate.

Simultaneous hypoalbuminemia and hypomagnesemia may occur under some of the same circumstances as in ruminants. It is most common in camelids grazing lush spring pasture. Ataxia, weakness, tetany, and recumbency may be seen. Blood evaluation (<0.49 mmol/L [<1.2 mg/dL]) should provide confirmatory evidence, and concurrent hypocalcemia is common. Intravenous treatment with a product containing both calcium gluconate and magnesium usually leads to rapid resolution of clinical signs. Subcutaneous injection of 50% magnesium sulfate solutions (10–50 mL) minimizes relapses.

Prevention

Hypocalcemia and hypomagnesemia prevention is based on appropriate mineral supplementation and accounting for interfering mineral interrelationships (see Chapter 9). It is assumed that the same mineral interrelationships influencing calcium and magnesium homeostasis in ruminants are applicable to camelids. Excess dietary phosphorus and potassium and inadequate dietary magnesium adversely affects calcium homeostasis. Excess potassium is the primary dietary factor adversely influencing dietary magnesium availability. Although these mineral interrelationships are of concern, the most important factor is ensuring adequate dietary content of calcium and magnesium to meet requirements (refer to Table 9-6, Chapter 9). Once dietary calcium is deemed adequate, phosphorus intake should be evaluated to ensure a dietary calcium-to-phosphorus ratio between 2 : 1 and 1.5 : 1. For magnesium, the primary concern beyond adequate dietary amount is interference from potassium. If dietary potassium content is high, typical of high quality pasture or forages, dietary magnesium content needs to be increased. A suggested dietary potassium-to-magnesium ratio of 4 : 1 is suggested.

Epidemiology

Copper (Cu) deficiency is a concern in ruminant animals because of the unique interaction between molybdenum (Mo), sulfur, and dietary copper that results in reduced availability. Forestomach microbes metabolize dietary molybdenum and sulfates to generate a range of chelating thiomolybdate compounds. Thiomolybdates bind to dietary copper making it unavailable for incorporation into copper-dependent metalloenzymes. Some thiomolybdates are absorbed and bind to copper-containing enzymes reducing their biologic activity. Additionally, excessive dietary zinc and iron may impede dietary copper availability. Copper is usually provided in the forage or mineral supplements of camelids. In many geographic regions, forage copper is low (<4 parts per million [ppm]) or contains high concentrations of substances that interfere with copper absorption. Mineral supplements tend to contain enough or potentially too much copper, but this is also variable.

Clinical Presentation

Clinical signs in domestic ruminants include ill thrift, immunodeficiency, poor fiber quality, anemia, chronic diarrhea, dilute hair color (achromotrichia), and leukoencephalomalacia. Whereas all these signs have been identified in sick camelids, their connection to copper deficiency is difficult to confirm. Two llamas (10 and 23 months of age) with low serum copper concentrations (<0.14 microgram per milliliter [mcg/mL]; deficiency <0.29 mcg/mL) and responding to copper supplementation had presented with anemia and poor condition.¹⁵ Other reports had linked copper deficiency to neurologic deficits (hindlimb ataxia, posterior paresis) similar to the disease “swayback” observed in neonatal sheep.^1,16,17 Reported serum copper concentrations were not considered deficient and the affected animals did not respond to copper therapy, thus questioning the role of copper in the observed disease process. In one case of a 6-month old llama with ascending paralysis, very low liver ([5 microgram per gram [mcg/g]) and kidney (0 mcg/g) copper concentrations were determined, suggestive of copper deficiency.¹

Diagnosis

History and signalment can be suggestive of a copper deficiency disease process, but more supportive evidence must come from determinations of feed and animal copper status. Feed copper concentrations below 4 ppm dry weight are strongly suggestive of deficiency. Values between 4 and 7 ppm dry weight are marginal and may lead to deficiency. Animal copper status is best determined by liver copper concentration, although serum copper concentration may be supportive of a diagnosis. Hepatic copper concentration less than 10 mcg/g dry weight is strongly supportive of a deficiency diagnosis, whereas values between 10 and 90 mcg/g dry weight are marginal and may induce some deficiency disease signs (refer to Chapter 12). Serum copper concentration less than 0.3 microgram per milliliter (mcg/mL) is supportive of a deficient status. Higher serum copper concentrations do not rule out potential deficiency status as serum copper values are not as diagnostic for copper status.

Treatment and Prevention

Potential treatments include oral administration of copper oxide needles, copper calcium ethylenediaminetetraacetic acid (EDTA) injections (up to 2 mg/kg of copper), mineral supplements containing copper, and reduction of the dietary copper inhibitors. In particular, the need for dietary supplements containing high concentrations of zinc should be reassessed. Improvement may be noted within 2 to 4 weeks. Recommended dietary copper content to meet daily requirements ranges from 9 to 12 ppm (DM basis). However, higher dietary concentration may be necessary in the presence of dietary inhibitors. The recommended dietary Cu : Mo ratio for ruminants is between 6 : 1 and 10 : 1, whereas for sheep is recommended to be between 6 : 1 and 8 : 1. Ratios below 4 : 1 may lead to dietary copper deficiency. The sheep Cu : Mo ratio would be recommended in formulating camelid diets. Not all mineral sources of copper are equally available. Copper oxide is considered essentially unavailable for absorption in ruminant animals. Preferred copper mineral sources would be cupric sulfate or chloride, and these sources are highly concentrated and should be incorporated into a mineral supplement to prevent potential for toxicity.

Epidemiology

Iron (Fe) deficiency potentially results either from inadequate intake, which is typical of growing animals on milk-based diets, or from chronic blood loss most typically from parasite infestation.¹⁸ Younger animals are more susceptible to iron deficiency disease as a result of their higher requirement, lower intake, and high risk for parasitic disease. Adult herbivores consume a diet that is more than adequate in iron, even accounting for the low availability of dietary iron sources.

Clinical Presentation

Across a range of species, anemia of some form is the clinical manifestation. Three llamas (14–29 months of age) presenting with characteristic microcytic, hypochromic anemia and poor growth were considered to have iron deficiency.¹⁹ Serum iron concentrations in these cases were between 20.1 and 59.7 mcg/dL, below established reference range for adult llamas (see Table 12-11, Chapter 12) and the animals responded to iron supplementation.

Diagnosis

Hematologic indices measuring red blood cell (RBC) number, volume, and hemoglobin content and concentration characterize the state of anemia. The role of iron in inducing the anemic state is assessed by measuring serum iron concentration, transferritin saturation (total iron-binding capacity), serum ferritin concentration, or some combination of these measures. Serum iron and ferritin concentrations are influenced by a disease state in which iron is reduced and ferritin increases (acute phase protein). Hypoproteinemia may also cause a reduction in serum iron and ferritin concentrations without concurrent iron deficiency.

Treatment and Prevention

Depending on the severity of deficiency, iron supplementation may be implemented with whole blood transfusion or parenteral iron dextran. A safe dosing scheme for camelids using iron dextran has not been established. A conservative approach (150 mg per cria at a 2- to 3-week interval) is recommended, as anaphylactic or more severe toxic reactions may occur. In most cases of iron deficiency, dietary supplementation is all that is necessary. Ferrous sulfate and many calcium-phosphate minerals are readily available iron sources. Most trace mineralized salt products will have sufficient iron if consumed in adequate amounts. In mineral salt products, it must be ensured that the source of iron is not ferric oxide only, which is not available. Most forages and commercial supplements will have sufficient iron content to meet or exceed dietary requirements.

Epidemiology

Selenium (Se) is well recognized for its intracellular antioxidant role in the form of selenium-dependent glutathione peroxidase and its complementary actions with the membrane-bound antioxidant vitamin E. Both nutrients decrease tissue damage related to the superoxide burst or other mechanisms of free radical generation. Abundance of one of these antioxidants may partially or completely compensate for a deficiency of the other. Camelids have a number of unexplained ill-thrift, infertility, neuropathy, recumbency, and immunodeficiency syndromes, similar to disorders associated with antioxidant deficiency in other livestock species, and it may be possible that some of them relate to vitamin E or selenium deficiency. This association has been made and reported anecdotally, especially in herds without a regular plan for supplementation.

Nutritional myodegeneration (i.e., white muscle disease) resulting from clinical selenium deficiency has been reported in dromedary camels.²⁰ Although no published reports of selenium deficiency disease in llamas and alpacas exist, it has been empirically diagnosed and is a disease of concern in many regions of North America, Europe, Australia, and New Zealand.^1,2,13,21 Animals of any age may be affected, although younger animals most commonly experience clinical disease. More recently selenium has been associated with iodine function through the actions of selenium-dependent 5′-deiodinase enzymes that convert thyroxine (T₄) to the metabolically active triiodothyronine (T₃).²² This biologic action might account for selenium’s association with clinical disease manifestations other than myodegeneration.

Selenium deficiency results from inadequate dietary intake of biologically available selenium. Regional differences in selenium-associated disease prevalence may be attributed to soil selenium content, soil pH, and the presence of iron or aluminum complexes and their impact on plant selenium content. Plants incorporate available soil selenium into proteins as selenomethionine or selenocysteine, although some unique plants may accumulate selenium to toxic concentrations. Most continents have large geographic regions where plant selenium content is marginal or deficient.

Dietary inorganic selenium forms (selenite, selenate) are reduced to elemental or selenide states during passage through the rumen. These latter forms are biologically inert and excreted in feces. Thus, ruminant animals are more sensitive to dietary selenium status. Selenium is efficiently transferred across the placenta and concentrated in the fetal liver. Placental and colostral transfer of selenium is dependent on maternal selenium status. Milk generally is low in selenium content; thus neonatal animals are critically dependent on hepatic selenium reserves to support biologic and metabolic activities.

Clinical Presentation

Severe selenium deficiency results in pathologic degeneration of skeletal muscle fibers with secondary fibrosis.21,22 Affected animals show clinical signs reflective of specific muscles affected and severity of degenerative changes to muscle fibers. Typically, both hind legs are symmetrically affected; however, tongue and heart muscles are commonly involved in newborn or young growing animals. With skeletal muscle damage, affected young or older animals show various degrees of lameness, weakness, or difficulty moving. Sudden death may occur in younger animals with damaged heart muscle. Newborn animals with tongue lesions will have difficulty nursing and may be diagnosed as “dummy” animals. Severe selenium deficiency in pregnant females has been associated with abortion and stillbirth. All of these clinical presentations have been documented in most domesticated species, although overt myopathy is rare in camelids.

Diagnosis

Diagnosis of selenium deficiency may be achieved through assessment of selenium status using serum, whole blood, or hepatic selenium concentrations or of whole blood glutathione peroxidase activity. With respect to blood selenium distribution, llamas and alpacas are different from cattle, sheep, and goats. Llamas and alpacas have a greater amount of selenium-dependent glutathione peroxidase activity in serum, which results in less difference between serum and whole blood selenium concentrations. Deficient whole blood selenium concentrations are defined as <120 nanograms per milliliter (ng/mL) with adequate between 150 and 220 ng/mL for either llamas or alpacas (refer to Chapter 12). Serum selenium concentrations <80 or <110 ng/mL are considered deficient for adult alpacas and llamas, respectively. Criteria defining adequacy and deficiency are variable with age. Expected hepatic selenium concentrations range from 1.0 to 2.5 mcg/g dry weight, similar to expected values for other species. Fetal hepatic selenium concentrations are higher (5.25 mcg/g dry weight) because of the concentrating ability. Hepatic selenium concentrations below 0.4 mcg/g dry weight are considered deficient.