Gene
A. Spiller,
Sidney
Saperstein,
Myron
A. Beigler
and Ronald
J. Amen
ABSTRACF Fiber-free liquid diets containing isonitrogenous amounts of various dietary nitrogen sources were fed to five adult male pig-tailed monkeys (Macace nemestrina) with a mean weight of approximately 10 kg. All liquid diets supplied 3.0 g N/day per monkey and maintained the animals in a positive nitrogen balance. Initial baseline fecal output data were obtained by feeding the animals a commercial solid monkey chow. The dietary nitrogen sources fed were a) egg white protein, b) an enzymatic hydrolysate of fish protein supplemented with L-amino acids to simulate the egg albumin pattern, c) a mixture of pure L-amino acids simulating the egg pattern, d) a casein hydrolysate supplemented with amino acids, and e) an amino acid mixture with Rose’s pattern. Total fecal matter, dry fecal matter, percent of moisture, fecal nitrogen, lipids and ash were determined for a 1 0-day period for each experimental diet. A very significant difference (P < 0.001) was noted between each liquid diet and the solid chow, but no significant differences were found between the various fiber-free liquid diets, pointing to the effect of fiber as a major factor affecting fecal output. Monkeys fed liquid diets excreted fecal matter with a mean of 12.9 g/day, of which 4.7 g/day was dry feces (fecal dry matter 28.5%). Fecal nitrogen was found to be 0.25 g, fecal lipids were 0.19 g, and fecal ash was 0.59 g/day per monkey, respectively. Am. J. Clin.Nutr. 28: 502-506, 1975.
The amount of fecal output is of interest in pre- and postsurgical nutrition and in other clinical situations where the intestine should contain little or no food residue and as little as possible endogenous output (1, 2). In recent years there has been increasing interest in the use of well-defined soluble diets for this purpose (3-6), often called “elemental” or “chemically defined” diets. These diets have often been used to replace the regimen of low-residue foods (7-11). Macronutrients, as well as fiber, change fecal output and composition either because some undigested nutrients reach the colon, or, because of their effect on various gastrointestinal endogenous secretions, cell loss or bacterial growth. This study was designed to examine the effect on fecal output in nonhuman primates of an intact protein, an enzymatic protein hydrolysate, an L-amino acid mixture with a similar essential amino acid pattern, and two commercially available low-residue diets. Pigtailed monkeys (Macaca nemestrina) were used as models. The gastrointestinal tract of this 502
TheAmerican
Journal
of Clinical
animal is extremely similar is free from the large cecum
Materials Animals
to that present
of man in rats.
and
and Methods and housing
Male, adult pig-tailed
monkeys (Macace nemestrina) weighing 8 to 15 kg were quarantined according to standard procedures. After termination of quarantine, they were preconditioned by placing them on a regimen of liquid diets for 30 days prior to the start of the experiment. The animals were housed individually in metabolic cages that had been designed so that the lower half was covered with a solid vertical sheet of metal to prevent loss of feces or urine to the outside of the cage. There were two internally stacked floors which were removable and allowed for complete collection of feces. Water was supplied ad libitum and the diet ‘From the Institute of Agriscience and Nutrition, Syntex Research, 3401 Hillview Ave., Palo Alto, California 94304. ‘ data presented at the 58th Annual Meeting of the Federation of American Societies for Experimental Biology, April 10, 1974. Atlantic City, New Jersey.
Nutrition
28: MAY
1975,
pp 502-506.
Printed
in U.S.A.
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Effect on fecal output of various dietary nitrogen sources in pig-tailed monkeys (Macaca nemes trina) fed fiber-free, semisynthetic diets1’ 2
DIETARY TABLE
Protein, pig-tailed
1 fat and carbohydrate monkeys (Mactwa
composition of fiber-free nemestrina), g/100 ml diet Hydrol
Diets
AND
FECAL
liquid
1
diets
Serine Glutamic Glutamine
acid
Proline
Cystine Alanine Valine Methionine Isoleucine Leucine Tyrosine Phenyalanine Tryptophan Fat Corn oil Safflower oil Soy oil and medium triglycerides Carbohydrate Corn syrup
2
A.A.
220b
1
A.A.
2
2.so
2.04”
0.262 0.075 0.159 0.267 0.124 0.107 0.394
0.262 0.075 0.159 0.267 0.124 0.107 0.394
0.10 0.04 0.17 0.20
0.093 0.013 0.116 0.162 0.124 0.163 0.214 0.068 0.144 0.026
0.093 0.013 0.116 0.162 0.124 0.163 0.214 0.068 0.144 0.026
2.6
2.6
Egg white 250d
0.09 0.06 0.33 0.13 0.10 0.10 0.09 0.09 0.14 0.11 0.10 0.03
2.6 0.13
3.4
chain
17.0
solids
and glucose
fed to
Hydrol
2.50#{176}
Amino acid pattern of the protein Lysine Histidine Arginine Aspartic acid Threonine
503
OUTPUT
15.4
17.0
17.0 22.6
oligo-
saccharides a
Enzymatic
hydrolysate
of fish
protein
supplemented
supplemented with L-methionine, L-tryptophan manufacturer. C Made up entirely of pure L-amino acids. casein,
was fed by means of a watering bottle fitted with a ball point feeding tube to prevent dripping. The feces and urine were collected once a day between 8:00 and 9:00 AM, before the morning feeding. After weight or volume was determined, the specimens were immediately frozen for future analyses. Diets
A commercial monkey chow (Purina Monkey Chow),3 supplemented with vitamin C, was used for comparison with the fecal output on the other diets. All determinations on the solid chow were performed first. The monkeys were then adapted to a liquid diet regimen by feeding an egg white diet (Table 1) plus 10% apple juice and 2% cellulose4 for 1 week. This was followed by 3 weeks on a liquid egg white diet in which the fiber and apple juice had been omitted. No physiological measurements were performed during this period. After adaptation, each experimental liquid diet was
with
L-amino
acids.
b Enzymatic
and
L-tyrosine; amino acid d Intact egg white protein.
fed twice daily morning after afternoon.
pattern
hydrolysate not
given
of by
for a period of 2 weeks; once in the fecal collection and once in the
The diet composition is presented in Tables 1 and 2. All diets were mixed to supply a caloric density of 1 kcal/ml and a total of 3.0 g of nitrogen/day per monkey. These values had been previously established as the amount necessary to maintain adult male pig-tailed monkeys weighing approximately 1 0 kg in a positive nitrogen balance. Hydrol 1 contained a fish protein hydrolysate suppleffiented with L-amino acids to yield the pattern given in Table I , column 1 : A.A.1 contained a mixture of L-amino acids with the same pattern as Hydrol 1 . The latter two diets simulated the pattern of the egg white diets. All other ingredients 3 Approximate analysis per 100 g: protein 15.0%, fat 5.0%, carbohydrate (by difference) 65.0%, crude fiber 3.0%, ash 5.0%, moisture 7.0%. Fed ad libitum. 4
Solka
Hampshire.
Floc, 90% cellulose,
Brown
Co., Berlin,
New
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Protein
Glucose
NITROGEN
SPILLER
504 TABLE
2
Vitamin
and mineral
pig-tailed
monkeys
Hydrol
ml
Riboflavin,mg/lOOml
Pyridoxine,mg/lOOml Biotin, g/100 ml Folic acid, mg/100 ml VitaminB,2 ig/100ml
Choline,mg/lOOml VitaminA,IU/lOOml VitaminD3,IU/lOOml Vitamin E, IU/100
ml
Minerals Potassium,mg/looml Sodium, mg/l00 ml Calcium, mg/100 ml Magnesium, mg/100 ml Phosphate(P04),mg/lOOml Chloride, mg/100 ml Iron, mg/100 ml Zinc, mg/100 ml Manganese, mg/100 ml Copper,mg/lOOml Iodine, ig/l00 ml
1
Hydrol
pasteurized
after
each
experimental
at
71
rapidly
cooled
did not
begin
diet
was
C
for
was
determined
by
drying
the
Egg white
14.30 0.14 14.30 0.71 0.14 0.14 2.86 0.06 0.71 14.30 286 57 1.5
90.1 39.8 78.8 1 8.9 99.3 121.5 0.9 0.3 0.1 0.02 7.5
152.0 36.0 52.0 1 7.5 120.4 120.0 0.5 0.5 0.2 0.1 7.0
90.1 39.8 78.8 1 8.9 99.3 121.5 0.9 0.3 0.1 0.02 7.5
116.8 85.9 44.4 19.4 121.0 180.1 0.5 0.7 0.2 0.1 7.9
90.1 39.8 78.8 18.9 99.3 121.5 0.9 0.3 0.1 0.02 7.5
and
at 5 C
insured
day that
the previous diet had cleared the intestinal tract. All values reported are daily means for a 10-day period. Five-day fecal composites for each monkey were acidified with acetic acid, defoamed with octanol and homogenized in a Waring Blendor. Aliquots of the homogenate were used for subsequent analyses. Dry matter
2
3.80 0.07 0.73 0.55 0.07 0.11 1 .10 0.006 0.27 8.47 275 3 0.08
the fourth
This
A.A.
14.30 0.14 14.30 0.71 0.14 0.14 2.86 0.06 0.71 14.30 286 57 1.5
stored
until fed.
1
5.00 0.07 0.90 0.50 0.08 0.10 7.52 5.00 0.25 5.00 250 20 1.5
1 5 min
and
A.A.
14.30 0.14 14.30 0.71 0.14 0.14 2.86 0.06 0.71 14.30 286 57 1.5
were similar in these three diets. Hydrol 2 was a commercial low-residue diet made from casein hydrolysate and supplemented with amino acids Lmethionine, L-tyrosine and L-tryptophan. A.A.2 was also a commercial low-residue diet containing L-amino acids with the pattern recommended by Rose (12) for man, shown in Table 1 , column 4. A total of 800 ml of Hydrol 2 and 850 ml of A.A.2 were fed daily to supply isonitrogenous levels per day in all diets. The caloric density of 1 kcal/ml was maintained. All ingredients were dispersed in water. The was
2
homogenate
to
constant weight in a vacuum oven at 70 C. The dried feces were then ashed in a muffle furnace at 600 C. Nitrogen content was determined by the A.O.A.C. macro-Kjeldahl method (1 3). Lipid content was determined by the method of Van de Kamer et al. (14).
Monkey body weights were after the liquid diet conditioning of the experiment.
Results
determined before and period and at the end
and discussion
The weights of dry and wet feces are presented in Table 3. The weights are calculated as the mean per day per monkey on each diet for the 10-day period. In addition, this table shows the percentage of dry matter in the feces as well as the wet and dry fecal induction ratios (FIR). The FIR are expressed as follows: Wet FIR
-
daily fecal output daily
food intake
(g) (kcal) x
D ry FIR
--
100 (g/100
kcal)
100 (g/100
kcal)
daily daily fecal food dry intakematter (kcal) (g) x
The possible effects of variation due to caloric intake on fecal output are taken into account by means of these calculations. Table 3 compares the values for wet and dry
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Vitamins Ascorbic acid, mg/100 ml Thiamin,mg/lOOml Niacinamide,mg/lOOml D-Pantothenic acid, mg/100
homogenized, then until feeding time. Fecal collections
AL.
composition of fiber-free liquid diets fed to (Macace nemestrina), analysis/100 ml diet
Diets
mixture
ET
DIETARY
NITROGEN
AND
FECAL
OUTPUT
Liquid containing as those
diet A.A.1 the same produced
However,
feces
liquid
diets
content
produced
showed
the
72.4%; physiological
1,
not
statistically
further interest
colonic
values
show
no
the
The
values
mean
and
based
for
mens.
animals are It appears
and
between
on
ash
any
of
hydroysates
(Table
or
4).
nitrogen
given
levels
in Table
found
pig-tailed
(0.22
processes.
lipid
difference
per
4 are
(unpublished
monkeys
g/day
In the absence of feces are primarily
the
73.8%;
content
disease
nitrogen,
mixtures
diets
2,
of the recently low fiber diets,
several
fecal
for
tein-free
Hydrol
moisture
endogenous
observations)
four
moisture
significant
diets acid
other
70.3%). Perhaps of this higher, but
significant
L-amino
76.1%;
study in view in high and
for
liquid
the
higher
egg white, significance
function,
The
the
and
by
a slightly
(Hydrol
A.A.2,
deserves renewed
(Table 3) produced feces amount of fecal moisture by solid chow (64.7%).
10-kg
fed
pro-
monkey).
fiber, this suggests that the of endogenous origin when
placed on these dietary regithat the egg white protein is
TABLE3
Daily fecal output on liquid fiber-free compared to output on solid monkey
diets for adult, chow#{176}
male
pig-tailed
monkeys
(Macaca
nemestrina)
Mean
Hydrol Number
of monkeys
Wetfecaloutput,g Dry fecal output, g WetFIR,g/lOOkcal Dry FIR, g/100 kcal Fecal dry matter,%
1
5 12.0±1.9 2.9 ± 0.3 1.9±0.4 0.4 ± 0.1 23.9 ± 3.5
Hydrol
2
5 11.2±1.6 ± 0.2 1.8±0.2
2.7 0.4
±
0.0
26.2
±
1.8
A.A.1
A.A.2
5 11.6±2.2 3.6 ± 0.8 1.7±0.4 0.5 ± 0.1 35.3 ± 7.0
Values are daily means ± standard error of the mean fecal output, dry fecal output, wet FIR and dry FIR
for
#{176}
wet
Egg
5 13.4±3.3 2.8 ± 0.3 1.9±0.4 0.4 ± 0.1 27.6 ± 4.0 a 10-day
are significantly
white
5 16.4±1.4 4.7 ± 0.3 2.4±0.2 0.7 ± 0.0 29.7 ± 1.3
period. b Solid different from
liquid
Solid
diets
12.9±0.9 3.3 ± 0.3 1.9±0.1 0.5 ± 0.1 28.5 ± 1.9
monkey
chowb 5 93.1±7.3 33.3 ± 3.4 31.8±2.9 11.1 ± 0.8 35.3 ± 1.2
monkey chow values for values for liquid diets (P
the
0.5).
liquid
the
liquid
diet
1 1 .8 ± 1 .8 kg,
diet
1 1 .4 ± period,
conditioning
Hemoglobin,
electrolytes, show
of
was
± 1.6 kg at the end of the experiment. the changes are statistically significant
of
(P
beginning
period
hematocrit,
albumin
any
and
significant
did
throughout
not
from
the
difference
between
drolysates
or
lating fecal
present
a low output.
the
L-amino lack
egg white
respect
to
slight
increase
in
of
there
8.
9.
hy-
diet,
digestibility
which
relative
to with
resulted
obtain
a low
time,
dietary
factor Further
affecting studies
fecal
fiber
output. appears
fecal output are in progress
At to
be
the the
10.
in a
is probably
of
little clinical significance. It appears that the choice of diet for clinical use should be based on the patient’s need and ability to handle intact protein and not entirely on the presentation of amino acid diets in order to
7.
in formu-
clinical
residue
5.
is no
protein
mixtures
of total
protein fecal
that
use
acid
residue The
study,
Bela Szakacs
various
macronutrients
on
El
composition.
thank
William
for their
1 . AHRENS, E. H. The metabolic studies: vances in Metabolic Levine and R. Luft. 2. BUNTE, H. Preparing cally defmed diet. on Balanced Nutrition Lang, W. FekI and 1971. 3. WINITZ, M., D. A. Studies in metabolic cally defined diets. human males. Am. 4. BEIGLER, M. A.
the
liquid diet conditioning or the experimental diet period; therefore, no values are reported. If the intestinal physiology of the Macaca nemestrina is similar to that of man, it would appear
authors
of
and
Benken,
technical
Robert
Marks
assistance.
References
6.
plasma
globulins
change
and
ratios
in Table
ash for animals higher (P < 0.001) than those fed liquid fiber-free diets. The loss of nitrogen, lipids and ash in the feces induced by the solid chow diets appears fed
nitrogen,
the
nitrogen
present major
and composition. to determine the
11. 12. 13.
14.
use of liquid formula diets in 15 years experience. In: AdDisorders, edited by R. New York: Academic, 1970. for surgery with a chemiIn: International Symposium and Therapy, edited by K. G. Berg. Stuttgart: Thieme,
SEEDMAN AND J. GRAFF. nutrition employing chemiI. Extended feeding of normal J. Clin. Nutr. 23: 525, 1970. The elemental diet: a new concept in nutritional support of the debilitated patient. Surg. Digest. 6: 18, 1971. GLOTZER, D. J., P. L. BOYLE AND W. SILEN. Preoperative preparation of the colon with an elemental diet. 74: 703, 1973. KARK, R. M. Liquid formula and chemically defined diet. J. Am. Dietet. Assoc. 64: 476, 1974. HOSOL, K., W. C. ALVAREZ AND F. C. MANN. Intestinal absorption: a search for a low residue diet. Arch. Intern. Med. 41: 112, 1928. WILLIAMS, R. D., AND W. H. OLMSTED. The manner in which food controls the bulk of the feces. Ann. Intern. Med. 10: 717, 1936. AMERICAN DIETETIC ASSOCIATION, AMERICAN MEDiCAL ASSOCIATION, JOINT COMMITTEE ON DIET. Diet as related to gastrointestinal function. J. Am. Dietet. Assoc. 38: 426, 1961. CALLOWAY, D. H. End products of human metabolism as affected by diet and space conditions. Environ. BioL Med. 1: 197, 1971. KRAMER, P. The meaning of high- and low-residue diets. Gastroenterology 47: 649, 1964. ROSE, W. C. Amino acid requirements of man. Federation Proc. 8: 546, 1949. ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS. Official Methods of Analysis. Washington: Association of Official Analytical Chemists, 1970, p. 16. VAN DE KAMER, J. H., T. B. HUININK AND H. A. WEYERS. Rapid method for the determination of fat in feces. J. Biol. Chem. 177: 347, 1948.
Downloaded from https://academic.oup.com/ajcn/article-abstract/28/5/502/4732914 by East Carolina University user on 16 January 2019
levels
AL.