22833

2014
NCPXXX10.1177/0884533614522833Nutrition in Clinical PracticeEdakkanambeth Asfaw et al

Clinical Observations
Nutrition in Clinical Practice
Volume 29 Number 2
How Hyperalimentation May Be Necessary to Reverse April 2014 229­–233
© 2014 American Society
Severe Malnutrition in Selected Patients Receiving Home for Parenteral and Enteral Nutrition

Parenteral Nutrition DOI: 10.1177/0884533614522833

ncp.sagepub.com
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Jithinraj Edakkanambeth Varayil, MD1,2; Ryan T. Hurt, MD, PhD1,3; and

Darlene G. Kelly, MD, PhD4,5

Abstract
Standard predictive equations may under- or overestimate caloric requirements in disease states such as obesity or in patients with a low
body mass index (BMI). Although this principle is common knowledge among nutrition specialists, it is often not prioritized with other
clinicians outside the intensive care unit (ICU). Indirect calorimetry (IC) is often used in the ICU to estimate caloric requirements. This
article outlines a very complicated case of a cachectic man with an enterocutaneous fistula who had lost more than 50% of body weight
over 2 years. In rehabilitating this patient, we found that the most common formulas of basal needs greatly underestimated the calories
required to prepare him for restorative surgery. Key learning points are that in malnourished ambulatory patients, predictive equations
may not adequately estimate caloric needs and IC may be required. (Nutr Clin Pract. 2014;29:229-233)

Keywords
home nutrition support; nutritional support; calorimetry; parenteral nutrition; enteral nutrition; nutrition assessment

Background [BMI], 13.2 kg/m2), blood pressure of 92/61 mm Hg (sitting),

Over the past year, we encountered an extremely malnourished
patient in whom the various equations for calculating caloric
needs and usual ways of evaluating laboratory findings were
very misleading. This case is described below.
A 62-year-old man presented to our clinic for evaluation of a
longstanding jejunocutaneous fistula and weight loss. He had a
history of gastric cancer that was resected with Billroth II gas-
trectomy in 2004 with subsequent chemotherapy and radiation
therapy. In 2010, he had proximal bowel ischemia and gangrene,
leading to several reconstructive surgeries of the gastrojejunos-
tomy anastomosis, resulting in conversion of his Billroth II into
a Roux-en Y gastrojejunostomy. These repetitive abdominal sur-
geries led to skin breakdown and a fistula. He stated that he had
lost 45.3 kg from a baseline of 81 kg, amounting to 56% weight
loss in the past 3 years. Since then, he has been hospitalized mul-
tiple times elsewhere with sepsis, aspiration pneumonia, and
other complications. These events as well as his decreased appe-
tite and extreme fluid losses from the fistula led to his poor nutri-
tion status. He had received enteral nutrition (EN) support at
times (details of the volume and calories unavailable), but he
continued to lose weight. The patient described some dysphagia
but denied nausea, vomiting, or abdominal pain. He reported an
anxious mood for the past 2 years. He had no history of liver or
kidney disease. He was a smoker with a 55-pack-year history but
denied heavy alcohol use. He received parenteral nutrition (PN)
elsewhere for 1 week prior to coming to our clinic.
On initial examination, he appeared weak and fatigued. He
weighed 35.7 kg with a height of 165.2 cm (body mass index
and pulse of 100 bpm. His abdomen was scaphoid with a large
enterocutaneous fistula that had associated skin breakdown, as
well as multiple healed surgical scars (Figure 1A). He had a
significantly decreased muscle mass and fat store as shown in
the computed tomography (CT) scan (Figure 2A).
Investigations
His laboratory studies at the time of admission showed a nor-
mal complete blood count, except that the mean corpuscular
volume (MCV) was borderline low with an elevated red blood
cell (RBC) distribution width (18.7%), suggestive of iron defi-
ciency (iron, 25 mcg/dL; normal, 50–150 mcg/dL). Hemoglobin
decreased from 13.3 g/dL to 8.6 g/dL in the first 3 days as a
From 1Department of Internal Medicine, Mayo Clinic, Rochester,
Minnesota; 2Second Department of Internal Medicine, Charles University
Faculty of Medicine, Hradec Kralove, Czech Republic; 3Department
of Internal Medicine, University of Louisville, Kentucky; 4Division of
Gastroenterology and Hepatology, Mayo Clinic, Rochester, Minnesota;
and 5Oley Foundation, Albany, New York.
Financial disclosure: None declared.
This article originally appeared online on February 25, 2014.
Corresponding Author:
Ryan T. Hurt, Division of General Internal Medicine, Mayo Clinic, 200
First Street SW, Rochester, MN 55905, USA.
Email: hurt.ryan@mayo.edu
230 Nutrition in Clinical Practice 29(2)

Figure 1.  (A) Abdomen at the start of home parenteral nutrition (HPN) shows extreme cachexia with absence of subcutaneous fat and
jejunocutaneous fistula with a feeding tube near the costal margin. (B) Abdomen after 6 months of HPN shows partial resolution of
cachexia with restoration of some subcutaneous fat but with persistence of the jejunocutaneous fistula and peristomal erythema.

Figure 2.  (A) Abdominal computed tomography (CT) at the beginning of home parenteral nutrition treatment showing a clear lack
of subcutaneous fat and muscle tissue (arrow). (B) Abdominal CT 6 months later clearly showing restoration of subcutaneous fat and
muscle tissue (arrow).

result of correction of dehydration. The abnormal electrolyte Treatment

levels included sodium, 131 mmol/L; potassium, 5.5 mmol/L;
creatinine, 1.1 mg/dL; and serum urea nitrogen, 61 mg/dL
(normal, 8–24 mg/dL). Other parameters of nutrition status
that were abnormal included serum albumin, 2.3 g/dL (normal,
3.5–5.0 g/dL); phosphate, 2.0 mcg/mL (normal, 2.5–4.5 mcg/
mL); zinc, 0.51 mcg/mL (normal, 0.66–1.10 mcg/mL); and
magnesium, 1.4 mg/dL (normal, 1.7–2.3 mg/dL).
Resting energy expenditure (REE) was measured to esti-
mate caloric expenditure for basal requirements given that his
BMI was well below the normal range. Using the Harris-
Benedict (HB) equation, we estimated his basal caloric require-
ments to be 939 kcal/d. Using indirect calorimetry, the REE
was measured to be 1270 kcal/d, with VCO2 of 167 mL/min,
VO2 of 177 mL/min, and respiratory quotient (RQ) of 0.95.
An upper endoscopy and placement of a Surgisis (Cook
Surgical, Bloomington, IN) fistula plug with both abdominal
wall suturing and intraluminal endoscopic suturing was per-
formed in an attempt to close the fistula. In addition, a nasoje-
junal feeding tube and a stent across his gastrojejunostomy was
placed. The patient tolerated nasojejunal feeding with a goal of
60 mL/h × 24 hours using Osmolite 1.0 (Abbott Nutrition,
Columbus, OH).
He also received nasogastric (NG) decompression, and the
patient was discharged home with a suction device. He reported
diarrhea (from 1–3 stools per day to 8–13 per day) with his
continuous nasojejunal enteral feedings and blocked NG
decompression tube. He was readmitted 3 days later with
Edakkanambeth Varayil et al 231

Table 1.  Various Validated Tools for Calculating BEE, Predictions in Our Patient, and Comparison of REE Determined With Indirect
Calorimetry.

Variation From Indirect

Equation Formula Calculated BEE/REE, kcal/d Calorimetry, %
Harris-Benedict equation8 66.5 + 13.8(wt-kg) + 5(ht-cm) – 6.8(age) 939 –26
Mifflin equation9 5 + (10 × Act BW) + (6.25 × Ht) − (5 × age) 1070.7 –16
Ireton-Jones equation10 629 – 11 × age (y) + 25 × W (kg) – 609 × 0 839.5 –34
ACCP guidelines11 (BMI <25): Act BW × 25 892.5 –30
Owen equation1 879 + (10.2 × Act BW) 1243 –2
WHO/FAO/UNU2 31–60 y: 11.6 × W (kg) + 879 1293 +2

ACCP, American College of Clinical Pharmacology; BEE, basal energy expenditure; BMI, body mass index; BW, body weight; REE, resting energy
expenditure; WHO/FAO/UNU, World Health Organization/Food and Agriculture Organization/United Nations University.

increased NG output. On readmission, nasogastric decompres-
sion was accomplished with a new pump and frequent saline
flushing to prevent obstruction. However, an extended upper
gastrointestinal (GI) study with water-soluble contrast showed
high-grade small bowel obstruction and most of the contrast
refluxing through the gastrojejunostomy into the stomach.
After this, PN was started, and he stayed nil per os. He was sent
home with an average daily intake of 1787 kcal (HB + 90%,
but measured REE + 40%) with fat emulsion 5 days per week
(50.1 kcal/kg/d). This level was chosen to provide about 500
kcal in excess of REE (1270 kcal), which would be expected to
increase the weight by about 1 pound per week.
Outcome and Follow-Up
During the following months, the patient’s nutrition status
improved remarkably. At the 1-month follow up, he had gained
4 kg with total calories of 1644 kcal/d (HB + 75%/REE +
29%), lipids 3 d/wk. His serum albumin level was 2.6 g/dL,
1.8 g/dL, and 2.9 g/dL after 1 month, 3 months, and 6 months
of home PN (HPN), respectively. Because of the improvement
in the subcutaneous fat as evidenced by his abdominal wall
improvement (Figure 1B and Figure 2B), the patient was able
to undergo placement of a tunneled single-lumen Hickman
catheter line at 6 months. Eight months after initial HPN evalu-
ation, the patient had gained almost 12.8 kg. The indirect calo-
rimetry was repeated after treating the infection during the
6-month visit. At that time, the results were the following:
measured REE was 1041 kcal/24 h, VCO2 was 146 mL/min,
VO2 was 132 mL/min, and RQ was 0.91. The estimated basal
energy expenditure (BEE), based on the Harris-Benedict equa-
tion at that time, was 1082 kcal, within 4% of the REE
measurement.
After 11 months, a surgical procedure was performed to
take down the complex jejunocutaneous fistulae and recon-
struct the complicated post–Roux-en-Y abdomen, with cre-
ation of a duodenojejunostomy, gastrojejunostomy, and
complex abdominal wall closure. Two months following the
procedure, the patient was still receiving HPN. Once
stabilized, further decisions could be made to wean off the
infusions.
Discussion and Clinical Lessons
His case posed a unique challenge, and a combined team
approach with experts from multiple fields has been required
for successful management. The use of typical guidelines
would have presented several potential opportunities for clini-
cal errors.
1. Equations for estimation of basal metabolic rate/REE may
fail in some patients.  This extremely malnourished patient’s
actual basal caloric expenditure was markedly underestimated
by 4 of the frequently applied formulas (Table 1). In fact, these
equations underestimated his REE by 16%–34%. This was
demonstrated by the fact that the tube feedings and even prior
PN formulas calculated using predictive equations were asso-
ciated with continued weight loss. Only 2 equations, the Owen
equation1 and the World Health Organization/Food and Agri-
culture Organization/United Nations University (WHO/FAO/
UNU),2 approximated the measured value (–2% and +2%,
respectively). While it is generally understood that such equa-
tions are typically designed to meet needs of most patients, the
cachectic and markedly obese patients are frequent exceptions
and may require indirect calorimetry to determine actual
caloric requirements.3 This is largely related to the fact that
cachectic patients are universally nearly devoid of fat mass,
making the muscle mass (albeit depleted) a higher percentage
of actual body weight. In such individuals, the ratio of muscle/
fat determines the basal metabolic rate (BMR). Since muscle is
a more metabolically active tissue than fat, the caloric expendi-
ture is higher than expected solely by height and weight. The
reverse is true in the markedly obese.
Several studies have reported increased caloric require-
ments in severely malnourished patients: 42.3 ± 4.4 kcal/kg/d
by Matarese et al4 and 50 kcal/kg/d by Hill et al.5 Our patient
received 50.1 kcal/kg/d at the beginning of HPN, after we had
been assured that refeeding syndrome was not occurring. After
232 Nutrition in Clinical Practice 29(2)

Table 2.  Weight, Calories in Tube Feeding, and HPN Formula and Laboratory Results During Treatment.

After 6 mo With Catheter Removal

Initial +2 Days of Staphylococcus + 5 Days of
Characteristic Evaluation Hydration Start of HPN After 1 mo After 3 mo aureus Antibiotics
Weight, kg 35.7 37.4 35.9 35.6 43.6 44.8 —
Serum albumin — 2.3 2.6 — 1.8 2.9 2.3
(3.5–5.0 g/dL)a
Amount of calories — 1440 1787 1644 1885 (at 4.5 mo) 1742 —
provided (= REE + 13%)
Alkaline phosphatase — — 77 480 146 406 155
(45–155 ULN)a (0.6 X ULN) (4.2 X ULN) (0.9 X ULN) (3.5 X ULN) (1.3 X ULN)
AST (8–48 U/L)a — — 21 — 31 55 17
ALT (7–55 U/L)a — — 9 — 17 59 8

AST, aspartate aminotransferase; ALT, alanine aminotransferase; HPN, home parenteral nutrition; REE, resting energy expenditure; ULN, upper limit of
normal.
a
Normal reference range in parentheses.

his weight loss had been reversed, the Harris-Benedict equa-
tion was a much better estimate of his requirements determined
by indirect calorimetry.
2. Initially obtained labs of the malnourished will be erroneous
in the dehydrated.  Most laboratory values are heavily affected
by dehydration, which results in hemoconcentration. In evalu-
ating the clinical status of patients, these may be misleadingly
reassuring. For example, in the first 2 days, this patient’s
hemoglobin dropped by 4.7 g/dL, with correction of
dehydration.
3. Laboratory studies may not be what they appear. This
patient had a major elevation in his liver enzymes on 2 differ-
ent occasions. Often, these can be associated with a decreased
serum albumin. The typical response from clinicians who are
not extensively trained in nutrition is that liver dysfunction and
malnutrition are the clinical problems. However, this can be a
warning sign that there is a bloodstream infection. In this
patient, the laboratory studies demonstrate this nicely. When
he returned after 6 months of HPN, his serum albumin had actu-
ally dropped to 2.3 g/dL, and he had gained only 0.34 kg/wk
(Table 2). Blood tests at the time of his 6-month return identi-
fied that the alkaline phosphatase and transaminases were both
markedly elevated. Blood cultures were positive for Staphylo-
coccus aureus. Over the next 5 days, his catheter was removed
and he was treated with antibiotics. The liver enzymes were
nearly completely corrected after effective antibiotic treat-
ment. This was demonstrated and presented in a prior study.6
4. Monitoring patients on nutrition support must include more
than laboratory studies.  Body temperature, urine output, and
weight trends are all critical parameters to be monitored, par-
ticularly in those receiving long-term support. In this patient,
his continued weight loss despite nutrition support could have
identified compromised caloric intake earlier in his course.7
5. In patients with an enterocutaneous fistula, care must be
used to determine whether tube feedings are a component of
effluent volume. This must be considered in trying to correct
nutrition status. This patient had fistula outputs that were
directly related to infusion of his tube feeding. The output
ranged from 1858 mL at one point during enteral feedings
down to as low as 25 mL when feedings were stopped. Subse-
quent radiological studies demonstrated that there was a tight
stricture in the small bowel distal to the tube and that contrast
(thus enteral feedings) refluxed from the gastrojejunostomy
back into the gastric remnant. This precluded enteral feedings
for this patient, which might have been suspected based on the
extremely large effluent volumes.
Conclusion
There are certain nutrition clinical scenarios in which standard
predictive equations may under- or overestimate caloric
requirements (eg, obesity or malnourished). Nutrition support
teams will often recommend indirect calorimetry for such
patients in the intensive care unit, but its use in the ambulatory
setting is often limited. This case demonstrates that what is
expected to be normal in the general population may not be
normal in those who are severely malnourished. Furthermore,
it often requires interaction between multiple disciplines to
successfully manage such patients.
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