![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
Departments of Endocrinology and Chemical Endocrinology, St. Bartholomew's Hospital, London EC1A 7BE, UK;
*
WALTHAM Centre for Pet Nutrition, Waltham-on-the-Wolds, Leicestershire, LE14 4RT, UK; and
Department of Small Animal Medicine and Surgery, Royal Veterinary College, University of London, North Mymms AL9 7TA, UK
3To whom correspondence and reprint requests should be addressed at Department of Veterinary Basic Sciences, Royal Veterinary College, University of London, Royal College Street, London NW1 0TU, UK.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
KEY WORDS: • cats • insulin-like growth factor • nutritional restriction
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
) or zoometry e.g., body mass index
(Nelson et al. 1990
) and body condition scoring
(Donaghue and Kronfeld 1994
), have either not been
validated for use in cats or may be insensitive as a result of wide
interobserver variation. Assessment of whole-body metabolism, e.g.,
nitrogen balance, direct and indirect calorimetry (Long 1977
) or body composition, e.g., dual emission X-ray
absorptiometry scanning (Munday et al. 1994
) and
double-labeled water techniques (Ballevre et al. 1994
), although accurate, may not be practical in feline
patients. Biochemical markers such as serum albumin, prealbumin
(transthyretin), retinol binding protein and transferrin have shown
good correlations with nutritional status in humans, but their
relatively long half-lives and interference by factors other than
nutrition have reduced their usefulness in monitoring response to
nutritional support (Clemmons et al. 1985
). Recently,
serum creatinine kinase activities have been assessed for monitoring
response to refeeding in hospitalized cats, and good correlations
between cessation of anorexia and decreasing enzyme activity have been
demonstrated (Fascetti et al. 1997
). However this marker
may be influenced by muscle trauma such as surgery or venous catheter
insertion. Insulin-like growth factor
(IGF)4
-I, a single-chain polypeptide hormone with a structural similarity
to proinsulin, is regulated predominantly by growth hormone (GH), but
nutrition also plays a major role (Thissen et al. 1994
).
It has a half-life in humans of 14–18 h in circulation
(Guler et al. 1989
) and is not stored before release
from the liver. Serum IGF-I concentrations have been used in humans
to monitor response to nutritional support in which they reflected
improving nitrogen balance (Hawker et al. 1987
). Serum
IGF-I concentrations were significantly more sensitive to improving
nutritional status compared wih serum prealbumin, retinol binding
protein, transferrin and albumin (Clemmons et al. 1985
).
Nutritional modulation of IGF and their binding proteins (IGFBP) has
been established in many species (Thissen et al. 1994
)
but not in domestic cats. This study was undertaken to investigate
nutritional modulation of the feline IGF/IGFBP system in order to
assess the potential of serum IGF-I concentrations as a marker of
nutritional status in adult cats. |
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Animals used in these studies were healthy nonobese adult cats (domestic short-haired) that were bred on-site. Females were excluded if pregnant, lactating or in estrus. Cats were group-housed unless required otherwise for recording voluntary food intake. Body weight was recorded daily. Health of the cats was ensured throughout the study by regular veterinary examination and monitoring of blood biochemistry and hematology. Blood for analysis of IGF, IGFBP, insulin and albumin was taken from the cephalic vein after overnight food withdrawal, unless otherwise indicated. Serum samples were stored in aliquots at -20°C until assay. Care of animals and experimental use conformed to UK Home Office guidelines under the Animals (Scientific Procedures) Act 1986.
Diets.
All diets were fed at maintenance requirements unless indicated. Water was available at all times and was not restricted.
Study protocols.
Samples for validation studies were taken from 46 cats [11 male neuter
(mn), median age, 2.24 y, range 2.16–8.23 y; 35 female (f),
median age, 5 y, range 1.8–9.1 y]. All cats were receiving
adequate maintenance diets based on previously established nutritional
guidelines (Earle and Smith 1991
) in which daily
maintenance energy requirements are 293 kJ/kg body weight. A
modification for inactivity due to kenneling further reduced the daily
energy supplied in the rations by ~14%.
Nine cats (5 f, 4 mn, median age, 7.1 y, range 2.8–9.3 y; median weight, 4.6 kg, range 2.8–6 kg) were studied to investigate the effects of overnight food withdrawal followed by refeeding. Samples were taken after food had been withdrawn for 18 h and again 3 h after feeding. Direct observation confirmed that food had been eaten by each cat.
The effects of nutritional restriction for 14 d were studied in
nine nonobese healthy adult cats [6 f, 2 female neuter (fn) and 1 mn,
median weight, 4.8 kg, range 3.7–5.9 kg; median age, 5.4 y, range
3.1–6.9 y]. Short-term dietary restriction was followed by free
access to the diet. Cats were fed maintenance rations (M) for 5 d
before restriction to first 56% (56%M) and then 42.5% (42.5%M) of
calculated maintenance energy requirements for 14 d, with an
intervening 14 d of free access to the diet. Serum samples were
taken throughout the study, including the 5-d maintenance period at the
start. Weight was measured regularly and voluntary food intake was
recorded daily. The same diet [Whiskas Calorie Control Diet, WALTHAM,
containing (per kg) 818 kJ energy, 426 g protein and 98 g
fat] was fed throughout the study and formulated to exceed minimum
adult maintenance nutrient requirements except for energy where
indicated. These restriction levels were based on similar studies in
dogs (Maxwell et al. 1998
) and current recommendations
for weight reduction in cats (Butterwick and Markwell 1996
).
Assays.
Serum concentrations of IGF-I and -II, and IGFBP-2 were measured
using validated in-house heterologous RIA. Recombinant human (rh)
IGF-I and -II (a gift from Pharmacia and Upjohn, Stockholm, Sweden)
were radiolabeled with [125I] (Amersham International,
Bucks., UK) using the chloramine-T
(N-chloro-p-toluenesulfonamide sodium
salt) method. Before assay, serum samples underwent formic acid/acetone
extraction (FAE) to separate IGF from their endogenous IGFBP to prevent
interference in the assay. Monoclonal antibodies to human IGF-I
(Blood Products, Hertfordshire, UK) and rat IGF-II [Upstate
Biotechnology (UBI), Lake Placid, NY] were incubated overnight with
radiolabeled peptide and then separated (Sac-Cel, Immunodiagnostic
Systems, Tyne and Wear, UK) and compared with a standard curve of rhIGF
standards. For the IGF-I RIA, the intra- and interassay CV were 6.8
and 12%, respectively, for a pooled serum source of 25 nmol/L. For the
IGF-II RIA, the CV were 8.9 and 6.8%, respectively, for 62 nmol/L.
For comparison of extraction methods, acid gel chromatography was used
to separate serum IGF from IGFBP as previously described (Horner et al. 1978
). Fractions were then assayed for IGF without
further extraction.
Serum IGFBP were examined using western ligand blotting (WLB) methods
as described by Hossenlopp et al. (1986),
followed by
electroblotting onto a nitrocellulose membrane and subsequent probing
with [125I]-rhIGF-I. The resulting autoradiographs were
analyzed by scanning densitometry (image densitometer GS-670 and
Molecular Analyst software, Bio Rad, Herts., UK). Individual IGFBP were
identified by immunoblotting using Enhanced Chemiluminescence (Amersham
International). Bovine IGFBP-2 antiserum (kindly provided by Dr. D.
Clemmons, University of North Carolina, Chapel Hill, NC) at 1:4000 and
human IGFBP-3 antiserum (UBI) at 1:2000 were used as previously
described (Camacho-Hübner et al. 1992
).
IGFBP-2 concentrations were further analyzed through RIA using a
validated commercial kit (Diagnostic Systems Laboratories, Webster,
TX,). The intra-assay CV was 9.3% for 42 nmol/L and the interassay
CV was 8.5% for 40 nmol/L. Serum albumin (Roche Cobas Mira and BCG
kit, Roche Diagnostics, Lewes, E. Sussex, UK) and insulin
(Nelson et al. 1990
) were assayed at external
laboratories (WALTHAM Centre for Pet Nutrition) using established
methods previously validated for feline serum. A normal human serum
(NHS) pool, collected from volunteers (3 m, 7 f, 30.6 ± 3.2 y), was used as an internal quality control in the assays.
Statistical analysis.
Normality of data distribution was determined through the use of the
Shapiro-Wilks and Kolmogorov-Smirnov tests (Conover 1980
) and examination of the symmetry of box-and-whisker plots.
Data were not normally distributed, due in part to study population
size; therefore they were analyzed by nonparametric methods. These data
were expressed as the median plus range. Data from the study population
used for assay validation (n = 46) were analyzed
using Spearman's test for correlations, e.g., between serum IGF-I
concentration and weight, and comparisons, e.g., between males and
females, made using a nonpaired t test (Mann and
Whitney). Paired observations, e.g., samples taken at different time
points from the same individual during the nutritional restriction
studies, were compared using Wilcoxon's matched pairs signed-ranks
test, which is a distribution-free analysis. The Bonferroni
correction was applied in cases in which multiple analyses were made.
In all cases, significance was assumed when P < 0.05. SPSS 6.1.3, Network version for Windows (SPSS, Chicago, IL) and
Graph Pad Prizm 2.01 for Windows 3.1 (Graph Pad Software San Diego, CA)
were used to analyze the data.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Serial dilutions of feline serum were parallel to standard curves in
the IGF and IGFBP-2 RIA as shown in Figure 1
. Examination of extracted serum by WLB revealed residual IGFBP,
predominantly IGFBP-3 and -2 (data not shown). The potential
interference of these residual binding proteins in the RIA for IGF was
investigated by assessing recovery of unlabeled IGF from serum samples
pre- and post-FAE, and also by comparison with acid gel
chromatography.
|
Serum IGFBP concentrations were analyzed as described. IGFBP-3, a
doublet at 39- and 43-kDa molecular weight, was the predominant binding
protein (Fig. 2
) and was further identified by immunoblotting (data not shown). Serum
IGFBP-3 concentrations analyzed by WLB reflected body weight and
IGF-I concentrations (Fig. 2)
. Compared with NHS, feline serum
IGFBP-2 band intensity was increased by WLB analysis; this was
confirmed by immunoblotting (Fig. 3
) and RIA using sera from cats in the initial validation population
(n = 7 cats, range 13–31 nmol/L; NHS pool 9–11
nmol/L). This was a consistent finding throughout the study.
|
|
, although the normal ranges for this population were wide. Male cats
were heavier (m = 5.1 kg, 4.1–6.8; f = 3 kg, 2.2–4.9,
P < 0.0001) and this was reflected by higher serum
IGF-I (m = 50 nmol/L, 18–83; f = 17 nmol/L, 11–74;
P < 0.0001) and IGF-II concentrations (m = 56
nmol/L, 22–89; f = 37 nmol/L, 6–95; P < 0.02).
There were no significant correlations between age and IGF
concentration. Increased IGFBP-3 band intensity [m = 33.6 ± 5.1 (SD) densitometry units, f = 21.9 ± 8.6
densitometry units] was evident on WLB as shown in a representative
autoradiograph (Fig. 2)
.
|
There were no changes in serum IGF or IGFBP concentrations, including IGFBP-1, with overnight food withdrawal or 3 h after refeeding (data not shown).
Short-term dietary restriction.
Feeding records indicated incomplete ration uptake during the study
(Table 1
). Therefore, expressed as a percentage, energy restriction was shown to
be first 67% and then 45% of actual intakes during the maintenance
periods.
|
After 14 d of 56%M restriction, weight was reduced (-7.1%,
P < 0.01) from 4.7 kg (3.5–5.5) to 4.3 kg (3.2–5.4)
and after 14 d of 42.5%M restriction (-8.5%, P
< 0.01) from 4.5 kg (3.4–5.5) to 4.1 kg (3.1–5.2). Body weights
at the start of each restriction period did not differ significantly as
a result of weight gain during the intervening 14-d refeeding period.
Serum IGF-I concentrations fell by 37%, from 78 nmol/L (29–87) to
50 nmol/L (32–61) with 56%M restriction (Fig. 5
). However, concentrations normalized with refeeding; thus there was no
difference at the start of each restriction period. Serum IGF-I
concentrations fell significantly only after 14 d of 42.5%M
restriction (-51%, P < 0.01) from 71 nmol/L
(29–106) to 34 nmol/L (15–60).
|
Densitometric analysis of WLB showed no significant change in serum
IGFBP band intensities with dietary restriction or refeeding (Fig. 3
A). The slight decrease in serum IGFBP-3 band intensity on
WLB (P = 0.055) was further investigated and shown not
to be due to post-translational modification through protease
induction (data not shown). There were no changes in serum albumin
(Fig. 5)
or insulin during the study with 42.5%M restriction or
refeeding. Serum insulin concentrations fell from 39.5 pmol/L
(31.6–74) to 38 pmol/L (20.1–48.1) after 14 d of restriction to
42.5%M and fell further to 34.5 pmol/L (18.7–40.9) with subsequent
refeeding.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
); however, it appears to be less sensitive to modulation
by nutrition (Thissen et al. 1994
).
The absence of raised IGFBP-1 concentrations after overnight food
withdrawal in adult cats is also seen in adult dogs (Maxwell et al. 1998
), but these findings differ from similar studies in
humans (Busby et al. 1988
, Cotterill et al 1993
) and
rats (Rivero et al. 1995
). Similarly, feline serum
IGFBP-1 concentrations did not change during prolonged dietary
restriction or ad libitum consumption of the diet, but we have not
assessed the influence of prolonged food withdrawal. Although we have
not positively identified the 29-kDa band on WLB autoradiographs as
IGFBP-1, specific immunoblotting has shown that it is not IGFBP-2.
It is also unlikely to be a fragment of IGFBP-3 because under the
denaturing WLB conditions used, the lower-molecular-weight fragments of
IGFBP-3 do not bind radiolabeled IGF-I (Suikkari and Baxter 1991
). In humans (Busby et al. 1988
) and rats
(Rivero et al. 1995
), IGFBP-1 is inversely regulated by
serum insulin. During overnight or longer-term food withdrawal,
concentrations of insulin fall and IGFBP-1 increases, whereas rising
postprandial insulin concentrations down-regulate hepatic IGFBP-1
mRNA transcription. Feline serum IGFBP-1 concentrations may not rise
with overnight food withdrawal because of an insufficient decrease in
serum insulin concentrations, which could be compounded by increased
sensitivity to the suppressive effects of insulin. It also may not be
regulated by insulin.
A significant decrease in serum IGF-I concentrations was seen only
after 14 d of 42.5%M restriction. In other species, there is a
threshold energy intake below which serum IGF-I concentrations
decrease, and this was expected with 56%M restriction for 14 d in
the feline study population, as shown previously in dogs
(Maxwell et al. 1998
). The apparent discrepancy is
partially resolved by analyzing the feeding records and expressing
restriction concentrations as a percentage of intake during each
preceding maintenance period (Table 1)
. Cats did not eat their full
diet allowances during each maintenance feeding period. Therefore, if
the subsequent restriction period intakes are expressed as a percentage
of actual intake recorded during previous maintenance feeding, cats
were restricted only to 67% and 45%. Comparison with studies in other
species (Oster et al. 1995
, Smith et al. 1995
) shows that restriction below 67%M is required to
decrease serum IGF-I. Hirsch et al. (1978)
found
that 10 cats with free access to food for 10 d consumed a median
of 39.5 kcal/(kg·d) (range 25.9–68.4), which was considerably lower
than expected. It is possible that dietary energy requirements for our
study population were overestimated, perhaps because of the effect of
kenneling on activity. Alternatively, the significant decrease in serum
IGF-I concentrations during the second period (42.5%M) of
nutritional restriction was a result of priming by the first (56%M)
restriction. Although this explanation is unlikely due to normalization
of serum IGF-I concentrations with the intervening refeeding
period, a crossover study would address this question.
During 42.5%M restriction, in addition to energy, protein intake was
reduced to the recommended minimum dietary protein content for adult
cats (Table 1)
. Dietary protein restriction also modulates the
IGF/IGFBP system, resulting in lower serum IGF-I and higher IGFBP-1
and -2 concentrations in rats (Lemozy et al. 1994
). It
is possible therefore that feline serum IGF-I concentrations may be
more sensitive to dietary protein than caloric restriction. Dietary
protein requirements in adult cats have been extrapolated from growth
studies in kittens and may therefore overestimate maintenance levels.
Feline serum IGF-II concentrations were unaffected by
short-term dietary restriction, as also demonstrated in humans
(Davenport et al. 1988
), but rose overall throughout the
study. The reason for this is unclear but may be related to decreased
serum IGF-I concentrations.
Serum IGFBP concentrations by WLB analysis and RIA were also unchanged
with short-term dietary restriction, which differs from other
species (Oster et al. 1995
, Smith et al. 1995
). In common with adult dogs, adult cats have greater
concentrations of serum IGFBP-2 when nutritionally replete compared
with humans, rats and guinea pigs. The role of IGFBP-2 has not been
established but the protein may have a regulatory role. Increased
IGFBP-2 concentrations have been noted in porcine neonates
(McCusker et al. 1991
), anorexia (Counts et al. 1992
), endotoxemia (Rodriguéz Arnao et al. 1996
), hyperthyroidism (Frystyk et al. 1995
) and
nutritional restriction (Clemmons et al. 1991
), which in
rats is due to up-regulation of hepatic IGFBP-2 mRNA (Straus and Takemoto 1990
). Increased hepatic gluconeogenesis or
increased catabolism may be important in these physiologic and
pathologic states.
Cats are obligate carnivores, and it is possible that differences in
nutritional modulation of their IGF system may be due to their
carnivorous metabolism. The majority of energy is obtained by
carnivores from dietary protein and there is no requirement for
carbohydrate. Overall, an obligate carnivore's metabolism is directed
to using amino acids as energy with the elimination of nitrogen as a
by-product. The rate of hepatic gluconeogenesis varies according to
the dietary protein content and is up-regulated during nutritional
restriction. Compared with rats, this already proceeds at a greater
rate, even with optimal nutrition (Belo et al. 1976
,
Kettlehut et al. 1980
), and down-regulation due to
nutritional restriction in cats is less (Kettlehut et al. 1980
). In vitro studies have shown a lack of adaptation to
nutrient deprivation by feline hepatic cells compared with other
species (Silva and Mercer 1986
and 1991
). During
long-term voluntary fasting caused by provision of a highly
unpalatable diet, obese cats improved nitrogen conservation, but not as
efficiently as obese humans and rats (Biourge et al. 1994
). Therefore, relative to other species, nitrogen
conservation is either not practiced or is inefficient, resulting in
the demand for high protein diets. Additionally, certain feline
metabolic pathways, e.g., urea cycle and bile acid conjugation, are
entirely dependent on a dietary supply of a single amino acid, e.g.,
arginine, taurine (Knopf et al. 1978
, Morris 1985
). The low level of nutritional modulation of the feline
IGF/IGFBP system may be a protective response that conserves body
resources more efficiently than do omnivores or herbivores or as a
specific adaptation to an obligate carnivore lifestyle in which
metabolic pathways are less responsive to nutrient change or depletion.
However, our previous studies on short-term energy restriction of
adult dogs have demonstrated a greater sensitivity of canine serum
IGF-I to nutritional restriction (Maxwell et al. 1998
). Dogs are classed as carnivores but, unlike cats, do not
have a dietary requirement for animal protein and may more correctly be
described as omnivores. Differences between the two species in
nutritional modulation of serum IGF-I may be explained by this
observation or indeed may simply represent overestimation of feline
daily maintenance energy requirements.
In conclusion, serum IGF-I concentrations are modulated by nutrition in adult cats and reflect short-term change in nutrition more sensitively than serum albumin. However, the wide range of normal values in our study population precludes its use for the diagnosis of malnutrition in an individual. Furthermore, its apparent insensitivity to declining nutrition raises doubts over its suitability as a biochemical marker of nutritional status in this species, although evaluation of the maintenance energy requirements of adult cats is necessary. Investigation into the effect of dietary components, especially protein, on serum IGF and their binding proteins is also indicated. However, the rapid normalization of serum IGF-I during refeeding after nutritional restriction suggests that serial measurements may be of use in monitoring the response of an individual to nutritional therapy.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
2 Supported by a grant from the WALTHAM Centre for
Pet Nutrition, Leicestershire, UK.
4 Abbreviations used: f, female; FAE, formic
acid/acetone extraction; fn, female neuter; GH, growth hormone; IGF,
insulin-like growth factor; IGFBP, IGF-binding protein; M,
maintenance rations; m, male; mn, male neuter; NHS, normal human serum
pool; rh, recombinant human, WLB, western ligand blotting.
Manuscript received December 28, 1998. Initial review completed February 16, 1999. Revision accepted June 21, 1999.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
1. Ballevre O., Anantharam-Barr G., Gicquello P., Piguet-Welsh C., Thielin A.-L., Fern E. Use of the doubly-labeled water method to assess energy expenditure in free living cats and dogs. J. Nutr. 1994;124:2594S-2600S
2. Belo P. S., Romsos D. R., Leveille G. A. Influence of diet on glucose tolerance, on the rate of glucose utilization and on gluconeogenic enzyme activities in the dog. J. Nutr. 1976;106:1465-1467
3. Biourge V., Grof J. M., Morris J. G., Rogers Q. R. Long-term voluntary fasting in adult obese cats: nitrogen balance, plasma amino acid concentrations and urinary orotic acid excretion. J. Nutr. 1994;124:2680S-2682S
4.
Busby W. H., Snyder D. K., Clemmons D. R. Radioimmunoassay of a 26,000 dalton plasma insulin-like growth factor binding protein: control by nutritional variables. J. Clin. Endocrinol. Metab. 1988;67:1225-1230
5.
Butterwick R. F., Markwell P. J. Changes in the body composition of cats during weight restriction by controlled diet energy restriction. Vet. Rec. 1996;138:354-357
6.
Camacho-Hübner C., Busby W. H., McCusker R. H., Wright G., Clemmons D. R. Identification of the forms of insulin-like binding proteins produced by human fibroblasts and the mechanisms which regulate their secretion. J. Biol. Chem. 1992;267:11949-11956
7.
Clemmons D. R., Snyder D. K., Busby W. H. Variables controlling the secretion of insulin-like growth factor binding protein-2 in normal human subjects. J. Clin. Endocrinol. Metab. 1991;73:727-733
8.
Clemmons D. R., Underwood L. E., Dickerson R. N., Brown R. O., Hak L. J., MacPhee R. D., Heinzer W. D. Use of somatomedin C/insulin-like growth factor-I measurements to monitor the response to nutritional repletion in malnourished patients. Am. J. Clin. Nutr. 1985;41:191-198
9. Conover W.J. Practical Nonparametric Statistics 1980 Wiley New York, NY.
10. Cotterill A. M., Holly J.M.P, Wass J.A.H. The regulation of IGFBP-1 during prolonged fasting. Clin. Endocrinol. 1993;39:357-362[Medline]
11. Counts D. R., Gwirtsman H., Carlsson L., Lesem M., Cutler G. B., Jr The effect of anorexia nervosa and refeeding on growth hormone binding protein, the insulin-like growth factors (IGF) and the IGF-binding proteins. J. Clin. Endocrinol. Metab. 1992;75:762-767[Abstract]
12.
Davenport M. L., Svoboda M. E., Koerber K. L., Van Wyk J. J., Clemmons D. R., Underwood L. E. Serum concentrations of insulin-like growth factor-II are not changed by short term fasting and refeeding. J. Clin. Endocrinol. Metab. 1988;67:1231-1236
13. Donaghue S., Kronfeld D. S. Feeding hospitalised dogs and cats. Wills J. M. Simpson K. W. eds. The WALTHAM Book of Clinical Nutrition of the Dog and Cat 1994:25-37 Elsevier Science Ltd. Oxford, England
14. Earle K. E., Smith P.M. Digestible energy requirements of adult cats at maintenance. J. Nutr. 1991;121:S45-S46
15. Fascetti A. J., Mauldin G. E., Mauldin G. N. Correlation between serum creatinine kinase activities and anorexia in cats. J. Vet. Intern. Med. 1997;11:9-13[Medline]
16.
Frystyk J., Gronbaek H., Skjaerbaek N., Flyvberg A. Effect of hyperthyroidism on circulating free and total IGF-I and IGFBPs in rats. Am. J. Physiol. 1995;269:E840-E845
17. Guler H. P., Zapf J., Schmid C., Froesch E. R. Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinol. 1989;121:753-758
18. Hawker F. H., Stewart P. M., Baxter R. C., Borkmann M., Tan K., Caterson I. D., McWilliam D. B. Relationship of somatomedin-C/insulin-like growth factor I levels to conventional nutritional indices in critically ill patients. Crit. Care Med. 1987;15:732-736[Medline]
19. Hirsch E., Dubose C., Jacobs H. L. Dietary control of food intake in cats. Physiol. Behav. 1978;20:287-295[Medline]
20.
Horner J. M., Liu F., Hintz R. L. Comparison of [125I]-somatomedin A and [125I]-somatomedin C radioreceptor assays for somatomedin peptide content in whole and acid-chromatographed plasma. J. Clin. Endocrinol. Metab. 1978;47:1287-1295
21. Hossenlopp P., Seurin D., Segovia-Quinson B., Hardouin S., Binoux M. Analysis of serum IGFBPs using Western Ligand Blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal. Biochem. 1986;154:138-143[Medline]
22.
Jones I. J., Clemmons D. R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 1995;16:3-34
23. Kettlehut I. C., Foss M. C., Migliorini R. H. Glucose homeostasis in a carnivorous animal (cat) and in rats fed a high-protein diet. Am. J. Physiol. 1980;239:R437-R444
24. Knopf K., Sturman J. A., Armstrong M., Hayes K. C. Taurine: an essential amino acid for the cat. J. Nutr. 1978;108:773-778
25. Lemozy S., Pucilowska J., B & Underwood L. E. Reduction of IGF-I in protein restricted rats is associated with differential regulation of IGFBP mRNA in liver and kidney, and peptides in liver and serum. Endocrinology 1994;135:617-623[Abstract]
26.
Long C. L. Energy balance and carbohydrate metabolism in infection and sepsis. Am. J. Clin. Nutr. 1977;30:1301-1310
27.
Lukaski H. C. Methods for the assessment of human body composition: traditional and new. Am. J. Clin. Nutr. 1987;46:537-556
28. Maxwell A., Butterwick R., Yateman M., Batt R. M., Cotterill A., Camacho-Hübner C. Nutritional modulation of canine insulin-like growth factors and their binding proteins. J. Endocrinol. 1998;158:77-85[Abstract]
29.
McCusker R. H., Cohick W. S., Busby W. H., Clemmons D. R. Evaluation of the developmental and nutritional changes in porcine insulin-like growth factor binding proteins-1 and -2 by radioimmunoassay. Endocrinology 1991;129:2631-2638
30. Morris J. G. Nutritional and metabolic responses to arginine deficiency in carnivores. J. Nutr. 1985;115:524-531
31. Munday H. S., Booles D., Anderson P., Poore D. W., Earle K. E. The repeatability of body composition measurements in dogs and cats using dual energy X-ray absorptiometry. J. Nutr. 1994;124:2619S-2621S
32. Nelson R. W., Himsel C. A., Feldman E. C., Bottoms G. D. Glucose tolerance and insulin response in normal-weight and obese cats. Am. J. Vet. Res. 1990;51:1357-1362[Medline]
33. Oster M. H., Fielder P. J., Levin N., Cronin M. J. Adaptation of the growth hormone/insulin-like growth factor-I axis to chronic and severe caloric or protein malnutrition. J. Clin. Investig. 1995;95:2258-2265
34.
Rivero F., Goya L., Aláez C., Pascual-Leone A. M. Effects of undernutrition on serum and liver mRNA expression of IGFs and their binding proteins during rat development. J. Endocrinol. 1995;145:427-440
35.
Rodríguez-Arnao J., Yarwood G., Ferguson C., Miell J., Hinds C. J., Ross R.J.M. Reduction in circulating IGF-I and hepatic IGF-I mRNA levels after caecal ligation and puncture are associated with differential regulation of hepatic IGF-binding protein-1, -2 and -3 mRNA levels. J. Endocrinol. 1996;151:287-292
36. Silva S.V.P.S., Mercer J. R. Protein degradation in cat liver cells. Biochem. J. 1986;240:843-846[Medline]
37. Silva S.V.P.S., Mercer J. R. The effect of lysosomal inhibitors on protein degradation in cat hepatocyte monolayers. Int. J. Biochem. 1991;23:525-529[Medline]
38. Smith W. J., Underwood L. E., Clemmons D. R. Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J. Clin. Endocrinol. Metab. 1995;80:443-449[Abstract]
39.
Suikkari A.-M., Baxter R. C. Insulin-like growth factor (IGF) binding protein-3 in pregnancy serum binds native but not iodo-IGF-I. J. Clin. Endocrinol. Metab. 1991;73:1377-1379
40.
Straus D. S., Takemoto C. D. Effect of dietary protein deprivation on insulin-like growth factor-I (IGF-I) and -II, IGF-binding protein-2 and serum albumin gene expression in rats. Endocrinology 1990;127:1849-1860
41.
Thissen J. P., Ketelslegers J. M., Underwood L. E. Nutritional regulation of the insulin-like growth factors. Endocr. Rev. 1994;15:80-101
This article has been cited by other articles:
|
|
 |
|
  M. L. Chandler and D. A. Gunn-Moore Nutritional Status of Canine and Feline Patients Admitted to a Referral Veterinary Internal Medicine Service J. Nutr., August 1, 2004; 134(8): 2050S - 2052S. [Full Text] [PDF]
|
|
|
|
 |
|
 N. E. Allen, P. N. Appleby, G. K. Davey, R. Kaaks, S. Rinaldi, and T. J. Key The Associations of Diet with Serum Insulin-like Growth Factor I and Its Main Binding Proteins in 292 Women Meat-Eaters, Vegetarians, and Vegans Cancer Epidemiol. Biomarkers Prev., November 1, 2002; 11(11): 1441 - 1448. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
