University of Montana
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Theses, Dissertations, Professional Papers
Graduate School
1972
Effect of protein-calorie malnutrition on food
consumption weight gain serum proteins and
activity in the developing rhesus monkey (Macaca
mulatta)
Charles Ruh Geist
The University of Montana
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Geist, Charles Ruh, "Effect of protein-calorie malnutrition on food consumption weight gain serum proteins and activity in the
developing rhesus monkey (Macaca mulatta)" (1972). Theses, Dissertations, Professional Papers. Paper 6216.
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EFFECT O F PROTEIN-CALORIE MALNUTRITION O N FO O D C O N SU M PT IO N ,
WEIGHT G A IN , SERUM PROTEINS, A N D ACTIVITY IN THE DEVELOPING
RHESUS M O N K EY (MACACA MULATTA)
Chorles R. G eisf
B . S ., U niversify o f San D iego, 1968
V
Presented In p a rtia l fu lfillm en t o f th e requirem ents for the d e g re e o f
M aster o f Arts
UNIVERSITY O F M O N T A N A
1972
A pproved by:
Chairm an, JEkaord of
.
m ers
_____
roduartf'5 cl
b o te
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L a b o ra to ry
V ol. 22, N o . 3
P rin te d in U .S .A .
A n im a l S c ie n c e
C o p y rig h t © 1972
by th e A m erican A ssociation fo r L a b o ra to ry A n im al Science
EFFECT OF FROTEIN-CALORIE MALNUTRITION ON FOOD
CONSUMPTION, WEIGHT GAIN, SERUM PROTEINS, AND
ACTIVITY IN THE DEVELOPING RHESUS MONKEY
{M A C A C A M V L A T T A y ^ ^
CHARLES R. GEIST, ROBERT R. ZIMMERMANN, AND DAVID A. STROBEL
SUMMARY • Five groups o f infant rhesus m acaques were separated from their mothers
a t 90 days o f a g e, housed in individual cages, and placed on purified diets that were
isocaloric but contained either 2 5 % (high), or 2 % or 3.5% (low) protein b y weight
at 380, 2 JO, or 120 days o f age. The subjects sustained on the low protein diets
showed a m arked reduction in weight gain when com pared to high protein controls.
On the whole, monkeys on diets deficient in protein consumed less than animals fe d
normal quantities of protein. However, all groups, regardless o f diet regime, consumed
food in quantities that were proportional to their body weights. Analysis o f blood
serum components revealed values o f albumin and total protein which consistently
reflected the level o f dietary protein fed. Globulin serum levels, however, consistently
failed to relate to the dietary level o f protein. Activity, as measured in a living cage
situation, show ed no effects o f diet and suggested that the low protein animal had
a general level of activity that was equal to that o f the high protein control.
In recent years, interest arose concerning the
effects of protein-calorie m alnutrition on the
behavior an d developm ent of m an ( 1-3 ) and
animals (4—6 ). T h e term protein-calorie m al­
nutrition was first introduced by Jelliffe (7)
and later was proposed by the Joint Food
and A griculture O rganization and the W orld
H ealth O rganization E xpert Commission on
N utrition (8) in reference to a diversity of
clinical deficiency diseases. A ttention, how­
ever, was focused prim arily on kwashiorkor
(9, 10) o r on the kwashiorkor-like syndromes
( 11, 12).
A num ber of biochemical, clinical, and
behavioral factors are m anifest in calorie
and protein déficiences an d have been under
1 F ro m th e D e p a rtm e n t o f Psychology, T h e U n iv ersity of
M o n ta n a , M issoula, M o n ta n a 59801.
* T h is in v estig atio n w as s u p p o rte d in p a r t b y th e N u tritio n
F o u n d a tio n , In c ., g r a n t 401 a n d th e N a tio n a l In s titu te o f
C hild H e a lth a n d H u m a n D ev elo p m e n t, g ra n t R O I-H D 04863.
“ A ccep ted fo r p u b lic a tio n J a n u a ry 17, 1972.
investigation by a variety of researchers (IS ­
IS) . Barnes et al ( 19, 20) an d Levitsky an d
Barnes (5) found th a t food intake w hen
equated on the basis of body weight was
greater in previously m alnourished m ale rats,
bu t not female rats. W eight gain in in fan t
rhesus monkeys was shown to increase rap id ­
ly on diets containing high or standard pro­
tein concentrations while low protein anim als
m aintained their weight (2 1 ). Blood serum
protein changes included a decrease in total
serum protein, album in, and album in/ globu­
lin ratio for protein deficient hum an infants
(3) an d rhesus monkeys (2 1 ). Activity, as
a function of low protein diets, increased in
rats as m easured in an activity wheel (22,
23) and has been corroborated on o th er
activity m easures with previously m alnour­
ished rats and pigs (5 ).
This investigation was designed to delineate
4 param eters arising from diets deficient in
Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.
370
V oi. 22, N o. 3
L A B O R A T O R Y A N IM A L S C IE N C E
p ro tein w hich w ere fed to developing rhesus
m onkeys {M acaca m u la tta ). T hese factors
in clu d ed food consum ption, w eight gain,
serum p rotein, a n d activity. All of these
m easures have previously been show n to be
valuable indicators of th e biochem ical, clini­
cal, a n d behavioral concom itants o f proteincalorie m aln u tritio n . T h e diets w ere isoca­
loric, b u t th e protein concentration was
m an ip u lated to yield diets con tain in g eith er
2 5 % , 3 .5% , o r 2 % casein by w eight. O u r
p rim ary concerns, therefore, w ere to : 1) d e ­
term ine the ad libitum food consum ption
value as a function of dietary pro tein defi­
ciency in developing rhesus m onkeys eq u ated
w ith respect to age a n d size, 2) relate the
food consum ption figures w ith w eight gain
in p ro tein m alnourished anim als, 3) ev alu ­
a te th e effects of these diets on serum p ro ­
tein, album in, a n d globulin, 4) ascertain
w h eth er activity as a behavioral m easure
varies w ith increasing dietary p rotein restric­
tion.
M a t e r ia l s a n d M e t h o d s
E xperim ental groups: Five groups of in ­
fa n t rhesus m acaques w ere separated from
th eir m others a t 90 days of age a n d m a in ­
tained on th e m ilk form ula d iet described by
Blom quist a n d H arlow (2 4 ). Procedures
identical to those set fo rth by Z im m erm ann
(25) for th e introduction a n d w eaning to
solid food w ere em ployed, a n d a t specified
intervals the groups w ere placed o n th e ex­
perim en tal diets (T able 1). T hese diets w ere
isocaloric b u t contained eith er 25% (high)
p rotein, o r 2% o r 3.5% (low ) p ro tein by
w eight. G roups 1 ( N = 4 ) , 2 ( N = 6 ) , a n d 4
( N = 5 ) w ere introduced to th e 3.5% low
p ro tein d iet a t approxim ately 380, 210, a n d
120 days of age, respectively. A t 1,036, 728,
a n d 500 days, groups 1, 2, a n d 4 w ere shifted
to a 2 % low protein d iet in o rd er to m ain ­
tain a stable body w eight. C ontrol groups 3
( N = 4 ) a n d 5 ( N = 4 ) fo r anim als in groups
2 a n d 4 con tin ued on the 2 5 % high p ro tein
a t 210 a n d 120 days of age, respectively.
TABLE 1
C o m p o s itio n o f e x p e r im e n ta l d iets
C o m p o n e n ts
L o w p ro L o w p ro - H igh p ro ­
te in 2% te in 3 .5 % te in 25%
P rm iex M
9 .0
F a*-soluble v ita m in
1.0
C ru d e c a se in
2 .0
C ere lose 2 /
3 9 .7
D e x trin 3 /
3 9 .9
S a lts (HMVV) 4 /
4 .0
B-vitarrrin prem »x
2 .0
C h o lin e d ih y d r o g e n c itr a te 0 .3
A sco rb ic a c id
0 .0 3
A lp h acel 5 /
2 .0
9 .0
1.0
3 .5
3 9 .0
3 9 .2
4 .0
2 .0
0 .3
0 .0 3
2 .0
9 .0
1 .0
2 5 .0
2 9 .0
2 7 .7
4 .0
2 .0
0 .3
0 .0 3
2 .0
9 9 .9 3
1 0 0 .0 3
1 0 0 .0 3
^P rlm ex, P ro c te r a n d G a m b le C o, C in n c in n a ti, O h io
^C erelose, C oin P ro d u c ts C o, A rg o , III.
^ D e x trin (w h ite te c h ). N u tritio n a l B io c h e m ic a ls C o rp .
C leveland, O h io
^ H u b b e ll R B , M endel LB, W a k em an A J, S a lt M ix tu re,
N u tritio n a l B io ch em icals C o rp . C lev elan d , O h io
^A lp h ac el (n o n -n u tritiv e b u lk ). N u tritio n a l B io c h e m ­
icals C orp. C leveland, O h io
B v ita m in s in 2 g ram s cerelo se
T h ia m in e HCI
R iboflavin
P y rid o x in e HCI
Ca p a n to th e n a te
N iacin
In o sito l
B iotin
F o lic acid
V itam in B-12
M en ad io n e
mg
0 .4 0
0 .8 0
0 .4 0
4 .0 0
4 .0 0
2 0 .0 0
0 .0 2
0 .2 0
0 .0 0 3
1 .0 0
F a t so lu b le v itam in s in c o rn oil
mg
V itam in A a c e ta te
V itam in D (calciferol)
A lp h a -to c o p h e ro l
0 .3 1
0 .0 0 4 5
5 .0 0
Subjects in g ro u p 1 served as p ilo t an im als
w hich w ere placed o n restricted d iets in o r­
d e r to establish th a t rhesus m onkeys could
be satisfactorily m a in ta in e d a t low levels of
p ro tein deficiency w ith o u t m o rta lity . F o r
convenience, each g ro u p is re fe rre d to by
th e m ean age of th e g ro u p a t th e o n set of
eith er th e 25% o r 3.5% p ro te in diets.
F ood preparation : T h e diets w ere p re ­
p a re d by a d d in g e ac h of th e in g red ien ts to
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June, 1972
P R O T E IN -C A L O R IE M A L N U T R IT IO N IN R H E S U S M O N K E Y S
an 80 q u a rt H o b art m ixer (H o b art Co,
H elena, M ont) an d blended until a dry
homogeneous pow der was obtained. T o dif­
ferentiate each of the diets w ith respect to
protein concentration, a sufficient quantity
of either red o r blue food coloring was sus­
pended in the fat-soluble vitam in m ixture
prior to blending, coloring the diets as fol­
lows: 25% (high) protein— blue, 3.5%
(low) protein— yellow, a n d 2% (low) pro­
tein— red. T h e diets w ere then refrigerated
until needed. From the dry dietary p rep ara­
tions biscuits were form ed weighing from 150200 g each p rior to feeding the animals. T o
accomplish this, w ater ju st sufficient to m ake
a dough was added to the diets. T h e dough
was then rolled ou t on a cutting board and
individual biscuits were fashioned by the use
of a circular cookie-cutter approxim ately 2"
in diam eter. E ach of the anim als was fed
ad libitum quantities of their respective diets.
Food consumption'. F o r 30 consecutive
days the quantity of food consum ed was de­
term ined for the 380, 210, and 120 day low
protein groups a t 969, 786, an d 1,018 days
of age, respectively, and for the 210 day high
protein group a t 745 days of age. Subjects
were housed in 24" (I) x 24" (h) x 24"
(w) individual cages of a design th a t pro­
vided m oderate protection against food spill­
age b u t did not sacrifice visibility or cleanli­
ness. T h e anim als were fed a m easured 150—
200 g of diet in biscuit form every evening
a t 5 :0 0 pm . T his am ount had previously
been found to be greater than the m axim um
dietary intake th a t each anim al w ould con­
sume in 24 hr. T he following m orning the
drop-pans from each of the cages were re»
moved a n d the food residue separated from
the fecal m atter. T he collected food was air
dried and weighed. T h e w eight of the food
fed the anim als m inus the residue was taken
as the estim ate of food consum ption. T he
anim als could reach through the cage floor
to the p an in order to retrieve solid food th at
spilled through the wire mesh, thereby in­
creasing th e accuracy of this measure.
W eight gain : T he weighing procedure in­
371
volved training all anim als to enter a n alum i­
num transport cage containing a sliding door
th at was placed directly in front of the p er­
m anent cage door. A fter several training ses­
sions in which anim als were forced into the
transport cage, all subjects entered the cage
voluntarily. T hus, no m anual handling was
required in this procedure. Once trained in
this m anner, a tared transport cage, desig­
nated solely for weighing, was utilized to
determ ine the weights on every anim al each
m orning prior to feeding and daily testing
activities. T h e transport cage was cleaned
when necessary between weighings. W eights
were determ ined on a n O haus H eavy-D uty
Solution Balance (O haus Co, U nion, N J ) .
Serum protein^ albumin, globulin, and
album in/globulin ratio: A t least 2 cc of
whole blood was draw n from the fem oral or
saphenous vein of restrained monkeys w ith
a 23 ga, 1" needle, on a 2% cc heparinized
syringe. T h e serum was isolated by centrifu­
gation at 1500—2000 rpm for 10 m in in a
Sorvall, M odel SS-4 centrifuge (Sorvall, Inc,
Norwalk, C o n n ). An aliquot was then sub­
jected to electrophoretic analysis at a clinical
laboratory (Saint Patrick’s H ospital, Missou­
la, M ont) employing cellulose acetate strips
in phosphate buffer a t pH 8.6 in a Gelm an
M igration C ham ber (G elm an Instrum ent
Co, A nn Arbor, M ich) and a Photovolt D ensicord Scanner and Integrator, M odel 9
(Photovolt C orp, New York, N Y ). Electro­
phoretic values for album in, globulin, an d
total protein were determ ined annually for
2 yr. Periodic total protein determ inations
were conducted in our laboratory on all
groups at 6-m onth intervals by the colori­
m etric biuret m ethod of W eichelbaum (2 6 ),
as described by H iller (2 7 ), in a Leitz Photrom eter (E. Leitz, Inc, New York, N Y ).
S tandard control serum was used as a ref­
erence for comparison of values (H yland
Laboratories, Los Angeles, C a lif).
A ctivity: Activity was m easured as a gen­
eral m ovem ent w ithin a cage for all subjects
throughout the dietary regime. M ovem ent
was detected by 2 photocells, each m ounted
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372
L A B O R A T O R Y A N IM A L
15" from th e floor o f a cage approxim ately
3 0 " (1) X 30" (w) X 3 0 " ( h ) . T h e subjects
w ere placed singly in th e cage fo r 1 h r p e r
day, approxim ately every th ird day, allow ing
tim e to sim ilarly test o th er anim als in the
colony. I n o rd er to balance o u t daily cyclic
factors, th e tim e of day th e anim als w ere
placed in the ap p aratu s varied betw een th e
hours of 6 :0 0 am a n d 5 :0 0 pm . T h e cage
was located in a 6' (1) x 8 ' (w ) x 8 ' (h )
room th a t was em pty except fo r a 3 8 " ( 1 ) x
17" (w ) X 31" (h) box th a t contained re ­
co rd in g equipm ent. T h e box was lined w ith
insulation m aterial to a tten u a te electrom e­
chanical noise from relays a n d counters. T h e
room was lighted by a 30 w a tt overhead
light an d a 15 w a tt signal lam p located on
th e side of the recording ap p aratu s. Inside
th e cage a series of bars were m ou n ted across
th e floor to a h eight of 10" to insure th a t
th e anim als pacing ab o u t the cage w ould
break eith er of th e photobeam s. T h e a p p a ra ­
tus was designed to approxim ate the living
cage in size a n d shape. Subjects w ere not
tested in the same rooms as th eir living q u a r­
ters in o rd er to reduce variability in activity
records resulting from disturbances produced
e ith er by laboratory personnel d u rin g the
n orm al execution of their duties, o r d istrac­
tions produced by the presence of o th e r m o n ­
keys. T hese d a ta report activity m easured in
this device for a period of 2 yr.
R esu lts
D eveloping rhesus m acaques, e q u ated w ith
respect to age an d size, show little difference
in food consum ption across the dietary re­
gimes. As a whole, the m onkeys o n diets defi­
cient in p rotein consum ed less food th a n
e ith er those fed sta n d ard o r elevated protein
concentrations. F urtherm ore, the absolute
q u an tities o f th e diets consum ed w ithin the
p ro tein deficient groups a p p eared to be o r­
d ered by age, w ith the older anim als eatin g
a larg er am o u n t of food. T h e ratio of food
consum ed / g body w eight was used to d eter­
m ine if any in tergroup variations existed
V ol. 22, N o. 3
S C IE N C E
FOOD C O N S U M P T IO N
7 .0 - n
5 .0
i/>
S
»
4 .0
S
3 .0
S 2.0 —
<►......«
380
210
■ 210
o — —o 1 2 0
1
lo w
L ow
H ig h
L ow
P r o te in
P r o te in
P r o te in
P r o te in
2
3
1 0 DAY B L O C K S
Fig 1. Food consum ption ratio: m ea n gram s
fo o d consum ed p e r gram s b o d y w eig h t for
the 380, 2 JO, a n d 120-day low protein groups
a n d the 2 1 0 -d a y high protein group.
w hen th e absolute co n sum ption o f food w as
related to body w eight. N o sign ifican t d iffer­
ences w ere found. T h e re w as a considerable
overlap am o n g groups, in d ic a tin g th a t the
m onkeys, in d e p e n d e n t of th e p ro tein co n cen ­
tra tio n co n ta in e d in th e d iet, co n su m ed a
q u a n tity of food th a t w as p ro p o rtio n a l to
th eir body w eights (F ig 1 ) .
T h e diets deficient in p ro te in p ro d u c e d a
m ark ed effect on body w eig h t g ain . T h e
m ean body w eights over 800 days in 50-day
blocks for th e 380- a n d 210-day low p ro tein
groups, a n d th e age e q u iv alen t 210-day co n ­
trol g ro u p a re illu strated in F ig 2. T h e 380day low p ro tein anim als show ed less th a n a
15% w eight g ain o ver a 3-yr perio d . S im ilar­
ly, th e 210-day low p ro tein g ro u p h a d only
a 2 5 % g a in over a 2 % -y r p e rio d , w hile th e
210-day h ig h p ro te in co n tro l g ro u p m ad e
nearly a three-fold increase in body w eig h t
Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.
Ju n e, 1972
PR O T E IN -C A L O R IE M A L N U T R IT IO N IN R H E S U S M O N K E Y S
diverging values beginning only after the
introduction of the experim ental diets.
Protein electrophoretic values were deter­
m ined at 12-mo intervals over a period of
2 yr. T hirty days prior to the second analysis,
the 380, 210, an d 120 day low protein
groups were shifted from 3.5% to 2% pro­
tein by weight. T h e m ean electrophoretic
values an d standard errors for each group
obtained in both years are presented in
T able 2.
T h e first year analysis was conducted on
the 380- and 210-day low protein groups at
696 an d 358 days of age, respectively, an d
on the 210-day high protein group a t 424
days of age. T he total protein values were
m arkedly an d significantly different (analy­
sis of variance) between the low protein
groups and the high protein group. No sig­
nificant differences were detected between
the low protein groups. Similarly, the albu­
m in values were significantly different (analy-
WEIGHTS
3 .8
3 .4 —
5
3 .0 <
<
cc
O
5
2.6 —
3
z
*X
2 .2 — I
O
Ûàà
-—-o 3 8 0 Low P r o te in
* 210 Low P r o te in
• — • 210 High P r o te in
0
1.4 —
373
1.0 —
* I * I ' I ■ I ' I * I * I ■
2
4
6
50
8
10
12
14
I
16
DAY BLOCKS
2 ® /o P r o t * l n
Fig 3. M eon b o d y weights over 200 days in
10-day blocks for the 120-day high and
low protein groups before and after onset of
diets.
f ig 2. M ean b o d y weights over 800 d ays in
JO -day btoeks for the 380- and 210-day low
protein groups and the 210-day high protein
group from the onset o f diets.
WEIGHTS
1 .7 5 1
1 .5 0 -
1 .2 5 -
over the same period. D epicted in Fig 3 are
th e m ean body weights for the 120-day low
protein group an d its age equivalent 120-day
h igh protein control over a period of 200
riays in 10-day blocks. T h e 210-day high pro­
tein group gained 4 times the weight which
w as gained by the 120-day low protein group
■during the initial 120-day diet period. E ach
of the 120-day groups were fed a standard
h u m an m ilk form ula, Prosobee® (M ead
Johnson, Evansville, I n d ) , a n d the high p ro ­
tein diet following separation from their
m others. D u rin g this initial period the weight
g a in was sim ilar w ithin these groups, the
O
O'
q
1.00 -
»-
0 .7 5 -
-—-o 1 2 0 L ow P r o to ln
» * 1 2 0 H ig h P r o te in
0
X
o
lu
0 .5 0 -
0.00
IIQ U IO
DIET
PROTEIN
DIETS
1 0 DAY BLOCKS
Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.
374
L A B O R A T O R Y A N IM A L
V o l. 22, N o. 3
S C IE N C E
TABLE 2
M ea n e le c tro p h o re tic values o f b lo o d seru m c o m p o n e n ts
D iet
D ays o f
age a t
o n s e t o f d ie t
D ays o f
age a t
c o lle c tio n
N um ber
of
su b je c ts
T o ta l p ro te in
g/1 00 ml
L sE
A lb u m in
g /100 m l
iS E
G lo b u lin
g /1 0 0 ml
±SE
A n a ly sis 1
3.5% p ro te in
3.5% p ro te in
25% p ro te in
380
210
210
696
358
424
4
6
4
6 .5 ± 0.53
6.6 - 0.33
7.4 - 0 1 '^
4 .0 ±0.4*=
3 .9 ± O.3 C
4 .8 ± 0.2*3
2 .4 ± 0 . 5
2 .6 ± 0 . 3
2 .6 ± 0 . 2
3 .4
3 .7
3 .9
5 .0
2 .8
2 .5
2 .3
2 .0
a .b .c .d j\/je3ns w ith th e sam e le tte r d id n o t d iffe r sig n ific a n tly , P < 0 .0 1
A n aly sis 2
2% p ro te in
2% p ro te in
2% p ro te in
25% p ro te in
1 20
380
210
21 0
556
1106
768
834
4
4
6
4
6.2
6 .2
6 .2
7.1
- 0.43
± 0.33
L 0.33
± 0 .4 * ^
±0.3^=
±0.4*=
±0.4*=
± 0.2^*
± 0 .5
± 0 .4
± 0 .5
± 0 .4
a .b .c .d (\/feans w ith th e sam e le tte r d id n o t d iffe r sig n ifican tly , P < 0.01
sis of variance) betw een the low protein
groups a n d the high protein group, w hile
th ere w ere no significant differences be­
tween th e low protein group».
T h e second yr blood serum assay was con­
d u cted on the 380, 210, an d 120 day low
p ro tein groups a t 1106, 768, a n d 556 days
of age, respectively, a n d on th e 210-day high
protein group a t 834 days of age. T o ta l p ro ­
tein values w ere significantly different b e­
tw een th e h ig h protein group a n d all low
p ro tein group» (analysis of v a ria n c e ). T h e
low protein group» did not differ significant­
ly from one another. Significant differences in
alb u m in values w ere also found betw een th e
high p ro tein subjects a n d all low p rotein
groups. Again, the low pro tein groups did n o t
d iffer significantly from one another. T h u s,
on b o th o f these m easures, the high p ro tein
group h a d significantly hig h er values th a n
any of the low protein groups. N o significant
differences w ere found in globulin values.
Periodic to tal protein determ inations using
the b iu ret m ethod w ere conducted on all
groups. T h e results w ere sim ilar to those
found in the electrophoretic analysis. Abso­
lute values of total protein w ere consistently
lower, b u t the intergroup relations still ex­
isted, lead in g to th e sam e relativ e significant
differences betw een th e groups. A special
investigation a im ed a t discovering th e m o n th ­
ly flu ctu atio n s in to ta l seru m p ro te in was
perfo rm ed on th e 380-day low p ro tein
group. T h e m o n th ly m ea n to ta l seru m p ro ­
tein values ra n g e d from a m in im u m o f 6.10
m g / 100 m l to a m ax im u m of 6.64 m g / 100
m l over a 9-m o perio d (F ig 4 ) . F ro m these
d a ta a sta n d a rd d ev iatio n o f 0.18, a m ean
of 6.43, a n d a v arian ce of 0.03 w ere calcu­
lated , illu stra tin g a flu c tu a tio n w ith in very
n a rro w limits.
A ctivity records from 125 1-hr sessions
w ere tak en of low p ro tein m onkeys in the
380, 210, a n d 120 day group s a n d o n th e
210-day high p ro tein group. T h e fa c t th a t
th ere w ere no significant differences betw een
th e groups indicates th a t fo r this p a rtic u la r
m easure low p ro tein m onkeys d o n o t a p p e a r
in ferio r to high p ro tein m onkeys in general
activity.
D
is c u s s io n
T h e im p o rtan ce of d ie ta ry p ro te in fo r th e
norm al gro w th a n d d e v elo p m en t o f m a n an d
low er m am m als h as been stressed by sim ilar
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June, 1972
PR O T E IN -C A L O R IE M A L N U T R IT IO N I N R H E S U S M O N K E Y S
BIURET
TOTAL SERUM PROTEIN
GROUP I
7 .5 - 1
I
N.
7 .0 '
I—j
»
m
E
<
#-
o
6.0 —
I
I I
1
2
h ig h
p r o t e in
3
I
4
I I
I
1
5
7
8
6
lo w
I I
9
10
p r o te in
M O N T H S O N DIET
Fig 4. M onthly m ean total serum protein con­
centration ( m g / 100 cc) for the 380-day low
protein group.
observations in clinical and experim ental
studies (28). Protein-calorie m alnutrition has
induced a condition of experim ental prim ate
kwashiorkor (2 9 ). In response to decreased
protein intake, retardation of grow th and
physical developm ent represent the m ost con­
sistent clinical features (1 0 ). In experim en­
tal anim als the clinical features m ay include:
edem a (30) ; the h a ir becomes brittle, loses
natural lustre, appears thinner, a n d is easily
pulled out (4) ; w eight gain is significantly
decreased from norm al w ith the result th a t
protein-deficient anim als simply m aintain
their weight (2 1 ); anem ia of m oderate se­
verity is generally present (29) ; low body
tem perature a n d m etabolic rate are m arked
(31) ; and decreased levels of serum album in
and cholesterol are observed (3 2 ). T h e re­
sults of this investigation indicate th a t sim ilar
effects of protein-calorie m alnutrition on the
weight gain an d serum proteins of developing
rhesus m acaques can also be produced.
375
I t m ight be expected th a t because of their
reduced size the m alnourished monkeys would
consume a quantity of food far less than
those anim als fed a diet sufficient in protein.
In one respect this contention has been con­
firm ed in this investigation. Diets deficient in
protein are consumed to a lesser degree th an
those w ith adequate protein. T his reduced
caloric intake could be interpreted as one of
the prim ary sources of the phyical retard a­
tion of protein-restricted anim als; however,
this is not necessarily the case. Regardless of
the protein concentration of the diet, rhesus
m acaques were shown to consume an am ount
of food proportionate to their body weights.
T he im portant variable appears to be w heth­
er or not the anim al can ad ap t to a diet low
in protein a n d utilize the calories th a t are
available. W aterlow (33) suggested th a t this
adaptation to the diets m ay take 2 m ajor
forms: a decrease in the output of urinary
nitrogen and a change in the distribution of
protein in the body. His findings indicate
alterations in protein synthesis occurring to
a reduced degree in muscle and probably the
skin, whereas in the liver and perhaps other
essential organs it is not. It also appears
th at the am ino acids liberated by the cata­
bolism are m ore efficiently reutilized for syn­
thesis. Changes in endocrine activity m ay
help to explain the pattern of protein tu rn ­
over which occurs in adaptation. W hile it
has not been assumed th a t these represent
the only underlying factors peculiar to p ro ­
tein-calorie m alnutrition, they lend credence
to the need for future research in this area.
T h e finding th a t protein-calorie m alnutri­
tion results in significantly lower rates of
weight gain (2, 10, 19, 21, 29, 31) and de­
creased levels of total protein and album in
(3, 10, 17, 18, 31) has been confirm ed in
this investigation. W hen protein-restricted
anim als are com pared w ith either high or
standard protein anim als, there is a m arked
an d significant difference in m axim um weight
attained, rate of weight gain, and the level
a t w hich an asym ptote is reached. Blood
serum analysis showed significantly lower
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376
V ol. 22, N o. 3
L A B O R A T O R Y A N I M A L S C IE N C E
levels of to tal serum p ro tein a n d album in for
all groups of low p rotein anim als. A n analy:sis of variance revealed th a t each low p ro ­
tein group w hen com pared w ith th e h igh
p ro tein
g ro up
differed
significantly
( P < 0 .0 1 ) . N o significant differences w ere
n o ted betw een any of th e low p ro tein groups.
"These d a ta indicate th a t the effects of p ro ­
tein-calorie m aln u tritio n o n w eight gain,
-total serum protein, a n d alb u m in can be re­
liably reproduced in th e developing rhesus
anonkey.
T h e effects of protein-calorie m aln u tritio n
o n th e general level of activity in m a n a n d
•experim ental anim als is little understood a n d
h a s been seldom investigated. G u th rie (16)
investigated activity level in rats in o rd er to
•determ ine th e extent to w hich differences
i n learning m ight be explained on th e basis
o f m otivational o r m o to r factors. I t was
fo u n d th a t undernourished ra ts w ere m ore
a ctiv e th a n norm al rats. Sim ilarly, Collier,
Squibb, a n d Jackson (22, 23) found th a t
diets deficient in protein p roduced hig h er
levels of activity in a n activity w heel th a n
d iets providing adequate protein. T h e results
o f the present investigation have show n th a t
a ctiv ity in rhesus monkeys w hen m easured
a s general m ovem ent a ro u n d a cage p ro ­
d uces no significant differences betw een any
o f the low p ro tein groups w hen com pared
to the high p ro tein anim als. F ailu re to find
activity differences over an extended period
a n d degrees of deprivation despite th e clini­
c a l m anifestations of protein-calorie m aln u ­
tritio n w ould suggest th a t m aln u tritio n a f­
fects activity selectivity. T h a t is, activity lev­
els m ay be d ependent not only upon the
m easures used, b u t also show considerable
v a ria tio n across species.
Studies of m aln u tritio n involving h u m a n
in fan ts a n d young children a re generally no t
feasible a n d often result in confusion due to
the interaction of social, econom ic, a n d cu l­
tu ra l factors. Investigations concerning the
effects of protein-calorie m aln u tritio n are
m ore am enable to investigation w ith th e aid
o f experim ental anim als u n d e r controlled
lab o rato ry conditions. T h ere fo re , th e effects
of dietary p ro tein restrictions o n m e n ta l a n d
physical d evelopm ent as w ell as th e condi­
tions necessary for reh a b ilita tio n w o u ld app>ear to be m o re easily in v estig ated in th e
developing rhesus m onkey.
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