Vol. 22, No.
12 December 2000
CE Refereed Peer Review
FOCAL POINT
★ Weight loss, a common
presenting sign in adult alpacas
with protein–energy malnutrition,
can be caused by many diseases;
definitive diagnosis is difficult
but can often be achieved by
thorough clinical examination,
laboratory tests, and feed
analysis.
KEY FACTS
■ Regular weighing and body
condition scoring by owners are
integral components of a history
of weight loss or failure to gain
weight in alpacas.
■ Failure to exhibit normal grazing
and browsing behavior are
common presenting signs of
alpacas with weight loss and
illthrift.
■ Feed analysis and accurate
knowledge of each ration
component enable veterinarians
to calculate protein and energy
intake in alpacas.
■ Maximum third-compartment
capacity of 2% body weight dry
matter is a significant limiting
factor in meeting protein–energy
requirements during times of
nutritional stress.
Protein–Energy
Malnutrition in
Alpacas
University of Saskatchewan
Saskatoon, Canada
James L. Carmalt, MA, VetMB
ABSTRACT: Alpacas commonly present with clinical signs of weight loss and illthrift but often
have no other abnormalities on physical examination, making diagnosis difficult and frustrat-
ing for veterinarians. Protein–energy malnutrition is a diagnosis of exclusion supported by ba-
sic protein–energy calculations, body condition scoring, and feed analysis. Although protein–
energy malnutrition has been described in domestic ruminants, this syndrome has not been
studied in camelids.
P
rotein–energy malnutrition (PEM) has been defined as insufficient provi-
sion of feed (quality and/or quantity) to ruminant livestock.1–3 This syn-
drome has not been described in camelids, in which clinical signs differ
from those seen in domestic ruminants. In camelidae weight loss, illthrift and
failure to exhibit normal grazing and/or browsing behavior are common present-
ing signs.
The number of camelids seen by veterinary practitioners has been steadily in-
creasing. Most commercial camelid owners weigh and determine the body con-
dition score (BCS) of their animals on a regular basis and are thus aware of
changes in their animals’ weight, BCS, and demeanor; however, this is often un-
true for noncommercial camelid owners.
The exact nutritional requirements of lamoids are unknown.4 The values pre-
sented in current literature are based on extrapolations from studies in sheep,4
goats,5,6 and cattle.7 The digestive system of lamoids—especially those on low-
quality diets—is considered to be superior to that of other ruminants8; therefore,
the extrapolation of nutrient values may not be wholly accurate. Because both
llamas and alpacas are lamoids, values presented for one are often assumed to be
applicable to the other.
In the alpaca’s natural habitat (i.e., the South American Andes), the tempera-
ture rarely falls below –10˚C.4 The average daily temperature in North America
and Canada during winter often falls below –15˚C and can be as low as –35˚C,
excluding wind chill. Published nutritional guidelines4,9 for camelids do not ac-
count for these extremes. Nutrition has a significant effect on fiber growth in al-
Compendium December 2000
pacas.10,11 Because fiber insulates these animals against
heat loss, poor nutrition compounds the thermoregula-
tory stress experienced in these extreme climates and
thus predisposes alpacas to PEM.
The need for high-quality, nutritious, palatable feed
along with regular body condition scoring and weigh-
ing in these climates cannot be overemphasized. In ani-
mals with suspected malnutrition, feed analysis is a
simple and cost-effective way for practitioners to calcu-
late the nutritional needs of each animal and compare
those needs with what is being provided by the current
diet.
ENERGY AND PROTEIN CALCULATIONS
Initially, daily maintenance metabolizable energy (ME)
should be calculated using the following equation9:
ME (Mcal) = (84.5 × Body weight0.75 [BW; kg]) ÷ 1000
[Equation 1]
Digestible energy (DE), a relatively constant propor-
tion of ME,12 is calculated as follows:
DE (Mcal) = ME × 1.22 [Equation 1a]
Additional factors4–7 important to the DE equation are
often overlooked during calculation (see Essential Fac-
tors in the Digestible Energy Equation). Omission of
these factors can lead to inadequate feeding of energy
and protein and the development of PEM.
Maintenance crude protein (CP) or total protein lev-
els are directly related to the DE value calculated in
Equation 1a; CP is calculated as13:
CP (g) = 31 g × DE (Mcal) [Equation 2]
Maximum dry matter (DM) intake or third-compart-
ment limitation is calculated as:
DM (kg) = BW (kg) × 0.02 [Equation 3]
During free-choice feeding, llamas will not eat more
than 2% BW (DM) over 24 hours, even during periods
of growth.14 Sheep, however, can increase DM intake to
3.0% BW DM.13 The camelid diet has to be sufficient-
ly energy- and protein-dense to satisfy their nutritional
requirements within the limitations of DM intake.
BODY CONDITION SCORING
Determining the BCS of alpacas is essential and re-
quires handling of the animal for accurate measure-
ment. It is simple, cost-effective, and can easily be per-
formed on a regular basis. This assessment is subjective,
FEED ANALYSIS ■ METABOLIZABLE ENERGY ■ CRUDE PROTEIN
Small Animal/Exotics
Essential Factors in the
Digestible Energy Equation
a. Pregnancy—During the last 4 months of gestation,
0.093 Mcal DE × BW0.75 should be added.4,6
b. Growth—An additional 0.00892 Mcal DE/gram
increase in BW should be added for juvenile
animals that are still gaining in height and weight.
The figure is often 1.78 Mcal DE/day.4
c. Lactation—1.533 Mcal DE should be added for
each kilogram of milk produced (crias should be
consuming 10% BW/day 4,6).
d. Pack Animals—An increase in energy as much
as 75% above normal adult maintenance
requirements may be needed.4
e. Temperature—0.04 Mcal DE should be added for
every degree below +15˚C. Although not specific to
camelids, this has been evaluated in Canadian
cattle.7
Note: Because literature on camelid nutrition is scarce, these
values have been extrapolated from studies in sheep, goats,4–6
and cattle.7
BW = body weight; DE = digestible energy.
however, and thus consistency of scoring is important.
Alpacas are assigned a numeric value ranging from 1
(emaciated) to 9 (very obese) based on their body con-
dition. Although 5 represents optimal condition, scores
from 4 to 6 are acceptable (Table I).
The chest, front legs, lumbar area, ribs, and dorsal
hindlimbs should be assessed. Contrary to the condi-
tion scoring of sheep and cattle, assessment of the pel-
vis is not performed in alpacas because the musculature
and adipose tissue distribution is such that even an
overconditioned animal will appear thin.
In thin alpacas, the lumbar musculature between the
dorsal and transverse spinous processes of the lumbar
vertebrae appears concave because of a lack of covering
adipose tissue. In obese animals, however, the tissue is
convex between the spinous processes and may pro-
trude above the vertical processes of the spine in the
lumbar area. In alpacas with optimal BCSs, the vertical
processes of the spine can be felt using gentle pressure
and the cross-sectional shape of the epaxial muscles
over the vertebra is flat.
Ribs should be palpated in the fiberless area directly
behind the elbow of the forelimb and over the middle
and widest part of the ribcage. The fiber must not in-
Small Animal/Exotics Compendium December 2000

TABLE I should come close together without

Body Condition Score and Interpretation in Alpacas
touching. The caudal abdomen is eas-
ily seen between the hindlimbs.
Body Score Description Nonlactating females and those in
1 Severely emaciated Ribs easily viewed and palpated
early to mid-pregnancy should be
V-shaped thorax as viewed from the front maintained at a BCS of 5+ because
Hindlimb musculature does not oppose dorsally maximum fetal growth and udder de-
Epaxial muscles appear concave between the dorsal velopment occur in the last trimester
and transverse spinous processes of gestation. To compound this nutri-
tional stress, voluntary intake will also
2 Emaciated Ribs are easily felt be reduced at this time because the
V-shaped thorax uterus commands more space in the
Hindlimb musculature does not oppose dorsally abdomen, thus reducing the effective
Overall loss of muscle forestomach size. Birthing should oc-
cur at a BCS of 6 because the stress of
3 Very thin Ribs can be easily felt
Slight V shape to thorax
lactation and early rebreeding will
Decreased space between hindlimb musculature cause a reduction in BCS. If BCS de-
creases excessively (i.e., below 4), ear-
4 Thin Ribs can be felt ly weaning of the cria may be pru-
U shape to thorax dent. Growing animals should be
Little loss of muscle maintained at a BCS of 4 to 6.15
Defined adductor musculature on hindlimbs
CASE SCENARIO
5 Optimal Ribs can be felt with gentle pressure Four female alpacas were presented
Slight space between hindlimbs as representatives of a herd of 150
Well-defined adductor musculature on hindlimbs mature alpacas in which 4 had died.
Epaxial muscles appear flat between the dorsal and
transverse spinous processes
Two of the animals were in mid- to
late-gestation, and two were in early
6 Slightly overweight Ribs can be felt with some pressure lactation. BCSs ranged from 2 to 2.5
Dorsal adductor musculature touches between (on a scale of 1 to 9), and the animals
hindlimbs weighed from 54 to 67 kg (119 to
Less-defined adductor muscle groups 147 lb). The males in the herd were
also thin but, according to the owner,
7 Somewhat overweight Ribs can be felt with moderate pressure had an average BCS of 3.0 to 4.0.
Less-defined adductor muscle groups The average daily temperature inside
the animals’ enclosure was –15˚C.
8 Obese Ribs can be felt with firm pressure Other than low BCSs, no abnor-
Thorax appears “barrel shaped”
Adductor musculature has little definition
malities were found on physical ex-
amination. Differential diagnosis in-
9 Very obese Ribs cannot be felt, even with firm pressure cluded gastrointestinal parasitism,
Significant contact between hindlimbs mineral deficiencies, PEM, and ep-
No definition of hindlimb musculature erythrozoonosis. Other causes of weight
Normal ambulation impeded loss (Table II) were excluded because
Epaxial muscles appear convex between the dorsal this was a herd problem.
and transverse spinous processes No significant abnormalities were
found on hematologic and biochemi-
terfere with the measurement in this area. When lightly cal examination or fecal flotation and culture. Based on
palpated, the brisket area should feel firm. the results of diagnostic testing and feed analysis, a di-
The chest of thin alpacas is V shaped; in obese ani- agnosis of PEM was made.
mals, the forelimbs appear to be closer together because The alpacas were being fed 0.14 kg (0.3 lb) per head
of the excess adipose tissue on the thorax. When an al- of oats/grain per day and allowed hay ad libitum. Anal-
paca is in optimal condition, the muscles of the inner ysis of the grain revealed 91.8% DM, 10.7% CP DM,
thigh in the hindlimbs have visible definition and and a DE of 3.3 Mcal/kg DM. The grass hay contained

ADIPOSE TISSUE ■ NUTRITIONAL STRESS ■ FORESTOMACH SIZE

Compendium December 2000 Small Animal/Exotics

TABLE II
Diagnostic Differentials, Clinical Signs, and Additional Tests for Weight Loss in Adult Alpacasa
Condition Possible Clinical Signs Additional Tests
Gastrointestinal Decreased milk production, poor growth Fecal flotation, fecal microscopy
parasitism16,17 and/or feed conversion, diarrhea, dehydration,
emaciation

Dental problems18,19 Abnormal chewing/pain, quidding, partially
chewed fibers in fecal pellets, mandibular
swellings or swellings over maxillary teeth roots,
odor or exudation from a nostril, apparent
sensitivity to cold water, visibly worn or
deformed teeth
Thorough buccal examination (sedation
may be needed), oblique radiographs of the
jaw,20 computed tomography and/or
magnetic resonance imaging

Hypothyroidism21 Depression, poor growth/haircoat, nonspecific CBC, resting triiodothyronine or thyroxine

(affected animals are dermatitis, anemia and/or leukocytosis levels22,23 or thyroid-stimulating hormone
typically <1 yr test24
of age)

Hypophosphatemia25 Poor growth, shifting lameness, angular limb Serum phosphate levels26,27
deformities/bony joint enlargement

Iron deficiency Poor growth, lethargy/diarrhea CBC, serum iron concentration,26–28 total
iron-binding capacity,28 bone marrow
aspirate

Copper deficiency29 Ataxia, anemia/immunosuppression, chronic
(primary or secondary) diarrhea (secondary), lameness, reduced growth
rate, infertility and reduced milk production,
excessive shedding/stringy hair fibers,
depigmentation of haircoat
Liver biopsy, hepatic copper concentration,
serum copper26,27 concentration (the
accuracy of this method is questionable)

Selenium deficiency Chronic diarrhea, immunosuppression, repeated Dietary analysis, whole blood selenium
infection, poor libido/fertility/abortion, concentration26,30
weak/stillborn/lethargic crias, white muscle
disease, hyperthermia

Zinc deficiency Zinc-responsive dermatitis, zinc-responsive CBC, serum alkaline phosphatase, serum
parakeratosis, weight loss/anorexia, reduced zinc concentration,26,27 dietary analysis
fertility

Third-compartment Depression/anorexia; colic/reduced gut sounds; Diagnosis based on eliminating other

ulcerations31 bruxism, reduced fecal production and/or pyrexia nonspecific gastrointestinal disease

Third-compartment Weight loss/anorexia, reduced fecal production, First-compartment fluid analysis (including
emptying defects32 abdominal distention chloride concentration), abdominal
radiography, exploratory laparotomy

Eosinophilic enteritis32 Weight loss, diarrhea Diagnosis based on eliminating infectious

causes of clinical signs, intestinal biopsy or
necropsy

Johne’s disease33,34 Poor growth/weight loss and/or diarrhea in Acid-fast stained fecal smear, fecal culture,
young animals >2 yr of age agar gel immunodiffusion test, necropsy
examination, impression smears of fresh
intestine, polymerase chain reaction testing
of mesenteric lymph nodes
Small Animal/Exotics Compendium December 2000

TABLE II (continued)
Condition Possible Clinical Signs Additional Tests
Juvenile Low-grade chronic problems, failure to respond CBC, blood smear, serum iron
immunodeficiency to treatments, repeated infections, depression, concentration, total iron-binding capacity,
syndrome35–37 (usually failure to gain weight, respiratory tract infection, transferrin saturation, bone marrow
detected in animals ocular infection, dermatitis/gingivitis, lameness, aspiration, serum biochemical analysis, fecal
6–18 mos of age) ataxia examination and urinalysis, bacterial culture
of infected focus, serum IgG concentration,
lymph node biopsy, paired sera (pre and 2
wk post), Clostridium perfringens C and D
vaccination

Wasting syndrome38 Anorexia/weight loss, death with no attendant Diagnosis of exclusion

identification of an infectious or parasitic disease
process

Protein–energy Weight loss; absence of anorexia, diarrhea, or Feed analysis and comparison of
malnutrition other significant clinical findings requirements with availability

Eperythrozoonosis39 Poor weight gain, chronic diarrhea and/or Complete physical examination, ELISA,
anemia stained blood smears, fecal examination
a Except for references 18, 25, and 33, these conditions have only been described in llamas but should be considered in all cases of
weight loss and illthrift in alpacas until further studies indicate otherwise.
CBC = complete blood count.

91.3% DM, 12.5% CP DM, and a DE of 2.74 Energy provided by grain = (0.13 kg DM ×
Mcal/kg DM. All calculations are performed on a DM 3.33 Mcal/kg DM) = 0.43 Mcal
basis. Therefore, 0.14 kg of oats is converted into 0.13 Protein provided by grain = (0.13 kg DM ×
kg DM (0.14 × 91.8% = 0.14 × 0.918). 10.7%) = 13.91 g

Requirements Assuming the animal consumes the entire oat ration:

An average 60-kg (BW) alpaca in this scenario, in the
last 4 months of gestation and in the middle of winter,
had the following energy (Equations 1 + 1a + Essential
factors a + e) and protein (Equation 2) requirements,
within the maximum third-compartment limitation
(Equation 3).
Energy (Mcal DE) = Equations 1 + 1a + Essential
factor a + Essential factor e; that is:
Energy (Mcal DE) = {[(84.5 × 600.75) ÷ 1000] ×
1.22} + (0.093 × 600.75) + (0.04 × 30) = 2.22 +
2.00 + 1.2 = 5.42 Mcal DE
Total protein (g) = 31 g × Mcal DE = 31 g × 5.42 =
168.02 g
Maximum intake = 60 × 0.02 = 1.2 kg DM
Feed Analysis
The grain being fed to the alpacas in the case sce-
nario was analyzed to determine the protein and energy
the animals were receiving.
Energy requirements remaining after grain =
(5.42 Mcal DE − 0.43 Mcal) = 4.99 Mcal DE
Protein requirements remaining after grain =
(168.02 g – 13.91 g) = 154.11 g
Having consumed the oat ration (0.13 kg DM),
the remaining maximum DM intake = (1.2 kg –
0.13 kg) = 1.07 kg DM.
Energy gained from maximum hay intake =
(1.07 kg DM × 2.74 Mcal/kg DM) = 2.93 Mcal
Protein gained from maximum hay intake =
(1.07 kg DM × 12.5%) = 133.75 g
The hypothetical amount of hay that the alpacas would
need to eat to meet their energy needs is 1.81 kg DM
(4.99 Mcal DE ÷ 2.74 Mcal/kg DM). This total ex-
ceeds the calculated remaining maximum DM intake.
Totals
Total energy in ration = 2.93 Mcal (hay) + 0.43
Mcal (grain) = 3.36 Mcal

PROTEIN–ENERGY MALNUTRITION ■ WEIGHT LOSS ■ OAT/GRAIN RATION

Compendium December 2000
Total protein in ration = 133.75 g (hay) + 13.91 g
(grain) = 147.66 g
Energy deficit = 5.42 Mcal – 3.36 Mcal = 2.06 Mcal
Protein deficit = 168.02 g – 147.66 g = 20.36 g
Maximum per-animal achievable DM intake of
hay – Intake needed to meet energy needs =
1.07 kg DM – 1.81 kg DM = – 0.74 kg DM.
This calculation indicates that the animals did not have
adequate forestomach capacity to allow sufficient inges-
tion of hay to meet energy or protein requirements un-
der the stresses of advanced gestation and winter weath-
er. Weight loss and illthrift are obvious sequelae.
The grain portion accounts for 10.8% of the diet,
leaving 89.2% as forage. Dietary crude fiber (CF) must
not be reduced below 25%14 because CF has a signifi-
cant effect on saliva production and, combined with
first-compartment bicarbonate-secreting glands, first-
compartment pH. Camelids differ from any other ru-
minant-type animals because of the bicarbonate-secret-
ing glands of their first compartment. The 25% CF
equates to approximately 40% forage in the total diet
but is heavily dependent on forage quality.
The diet of camelids may need to be supplemented
with corn,14 canola, flax, or cotton seed to increase the
energy density of the ration during nutritional stress.
An alternative method is to invest in more expensive
commercial pellet or textured feeds, such as mixtures of
grain, protein supplements, vitamins, and minerals
bound together to increase the protein–energy density
of the ration.
CONCLUSION
Literature published in the United States4,14 indicates
that camelids are prone to overcondition when re-
moved from their typical environment. Nutritional
guidelines for camelids are available in the scientific
and lay press as well as on the Internet; most of these
guidelines, however, are extrapolated from ruminant
data. Based on these guidelines, owners resist feeding
their camelids more than 0.14 kg (0.3 lb) of grain daily
because they believe that feeding more will induce
third-compartment ulceration. Although no evidence
supports this belief, the role of diet in the development
of third-compartment ulceration is indirectly supported
by the fact that llamas and alpacas in South America
have both low-grain consumption and a low incidence
of gastric ulceration.31
Protein and energy needs of alpacas vary according to
the specific conditions on the individual farms or
ranches. Calculating the correct dietary needs is integral
to the complete diagnostic workup of an individual or
herd problem. Despite the irrefutable evidence of BCS
FIRST COMPARTMENT ■ SUPPLEMENTED DIET ■ OVERCONDITION
Small Animal/Exotics
and feed analysis in the absence of other disease, some
owners are unwilling to accept a diagnosis of PEM, as-
suming that it indicates a degree of mistreatment on
their behalf. In my experience, however, the benefits of
dietary management can generally be appreciated with-
in 5 to 7 days and supports the diagnosis.
ACKNOWLEDGMENT
The author thanks Miss K. P. Rosel, Department of Tox-
icology, and Dr. M. Smart, Large Animal Clinical Sci-
ences, Western College of Veterinary Medicine, Universi-
ty of Saskatchewan, Saskatoon, Canada, and Dr. J.
Vaughn, Division of Veterinary and Biomedical Sciences,
Murdoch University, Murdoch, Western Australia, for
their help in the preparation of this manuscript.
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About the Author
Dr. Carmalt is affiliated with the Department of Large
Animal Clinical Sciences, Western College of Veteri-
nary Medicine, University of Saskatchewan, Saskatoon,
Canada.