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The growth hormone secretagogue ipamorelin counteracts

The ability of the growth hormone secretagogue (GHS) Ipamorelin to counteract the catabolic effects of glucocorticoid (GC) on skeletal muscles and bone was investigated in vivo in an adult rat model. Groups of 8-month-old female rats were injected subcutaneously for 3 months with GC (methylprednisolone) 9 mg/kg/day or GHS (Ipamorelin) 100 microg/kg three times daily, or both GC and GHS in combination. The maximum tetanic tension of the calf muscles was determined in vivo in a materials testing machine. The maximum tetanic tension was increased significantly, and the periosteal bone formation rate increased four-fold in animals injected with GC and GHS in combination, compared with the group injected with GC alone. In conclusion, the decrease in muscle strength and bone formation found in GC-injected rats was counteracted by simultaneous administration of the growth hormone secretagogue. Figures - uploaded by Peter B Johansen Author content All figure content in this area was uploaded b

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Study findings do not automatically establish clinical benefit, safety, dosing, or suitability for an individual.

The ability of the growth hormone secretagogue (GHS) Ipamorelin to counteract the catabolic effects of glucocorticoid (GC) on skeletal muscles and bone was investigated in vivo in an adult rat model. Groups of 8-month-old female rats were injected subcutaneously for 3 months with GC (methylprednisolone) 9 mg/kg/day or GHS (Ipamorelin) 100 microg/kg three times daily, or both GC and GHS in combination. The maximum tetanic tension of the calf muscles was determined in vivo in a materials testing machine. The maximum tetanic tension was increased significantly, and the periosteal bone formation rate increased four-fold in animals injected with GC and GHS in combination, compared with the group injected with GC alone. In conclusion, the decrease in muscle strength and bone formation found in GC-injected rats was counteracted by simultaneous administration of the growth hormone secretagogue.

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Growth Hormone & IGF Research 2001, 11, 266–272

doi:10.1054/ghir.2001.0239, available online at http://www.idealibrary.com on

The growth hormone secretagogue

ipamorelin counteracts

glucocorticoid-induced decrease

in bone formation of adult rats

N. B. Andersen1, K. Malml ̈of2, P. B. Johansen2, T. T. Andreassen1, G. Ørtoft1

and H. Oxlund1

1Department of Connective Tissue Biology, Institute of Anatomy, University of Aarhus, DK-8000 Aarhus C, Denmark and 2Novo Nordisk A/S,

DK-2760 Maaloev, Denmark

Summary The ability of the growth hormone secretagogue (GHS) Ipamorelin to counteract the catabolic effects

of glucocorticoid (GC) on skeletal muscles and bone was investigated in vivo in an adult rat model. Groups of

8-month-old female rats were injected subcutaneously for 3 months with GC (methylprednisolone) 9 mg/kg/day

or GHS (Ipamorelin) 100 μg/kg three times daily, or both GC and GHS in combination. The maximum tetanic

tension of the calf muscles was determined in vivo in a materials testing machine. The maximum tetanic tension

was increased significantly, and the periosteal bone formation rate increased four-fold in animals injected with

GC and GHS in combination, compared with the group injected with GC alone. In conclusion, the decrease in

muscle strength and bone formation found in GC-injected rats was counteracted by simultaneous administration

of the growth hormone secretagogue.

C°2001 Harcourt Publishers Ltd

Key words: growth hormone secretagogue, muscle tetanic tension, bone formation, bone bending strength,

muscle strength, glucocorticoid.

INTRODUCTION

Long-term glucocorticoid treatment may result in

weakening of both skeletal musculature1,2, 3 and bone

structures4,5 in man. The interaction between gluco-

Received 19 March 2001

Revised 12 July 2001

Accepted 16 July 2001

Correspondence to: Hans Oxlund, MD, DMSc, Department of Connective

Tissue Biology, Institute of Anatomy, University of Aarhus, DK-8000 Aarhus

C, Denmark, Tel: +45 89423017; E-mail: [email protected]

The data were presented at the 3rd International Conference of the Growth

Hormone Society, San Francisco, CA, 1998: Andersen NB, Oxlund H,

Malml ̈of K, Johansen PB, Ørtoft G, Andreassen TT. Effects of Ipamorelin—a

growth hormone secretagogue—on bone formation and skeletal muscle

contraction force. Growth Horm IGF Res 1998; 8: 313 (abstract).

corticoid-induced muscle weakness and osteopo-

rosis may lead to serious disability. Frail patients would

certainly benefit from a treatment regimen which could

increase skeletal muscle and bone strength.

We have developed an experimental animal model6,7

to study the ability of a growth hormone secretagogue

(GHS) to counteract glucocorticoid (GC) effects on

skeletal musculature and bone. In animal experiments,

a decrease in muscle protein synthesis,8muscle mass

and muscle strength has been observed in GC-treated

rats,9,10 as well as a reduction in bone mass and

strength.11,12

Growth hormone (GH) administration increases

muscle fibre size,13,14 leading to increased skeletal

muscle mass,15 which is accompanied by a propor-

tionate increase in muscle strength.7Furthermore, GH

1096–6374/01/050266+07 $35.00/0 C°2001 Harcourt Publishers Ltd

GHS counteracts GC-induced effects on bone 267

stimulates bone formation and increases bone

mass.15,16, 17 Growth hormone secretagogue may also

increase the bone mineral content of young rats18

and promote muscle function. Lieber et al.19 reported

an increase in muscle strength and fibre size in dogs

treated with GHS during remobilization.

Growth hormone administration may counteract the

GC-induced catabolic effects on muscle and bone

mass.11,20 GHS may reverse GC suppression of GH

secretion.21,22 At present it is not known, however,

to what extent GHS can counteract the catabolic ef-

fects of GC. The GHS, Ipamorelin, is a pentapeptide

selective for GH release similar to that displayed by

growth hormone releasing hormone.23 In short-term

studies, Ipamorelin increases BW gain, in GC-treated

animals24 and increases longitudinal growth in young

rats.25

The effects of the GHS, Ipamorelin, and GC admin-

istration, alone and in combination, were investigated

on muscle strength, muscle mass, bone mass, bone for-

mation rate and bone strength.

MATERIALS AND METHODS

Seventy female Wistar Hannover 8-month-old rats,

from Møllegaard Breeding and Research Centre

(Ll. Skensved, Denmark) were randomly divided into

five groups with 14 rats in each group. Group A

was killed at the start of the experiment. Group B

was injected daily with saline. Group C was injected

with GC 9 mg/kg/day (Solumedrol, Upjohn, Puurs,

Belgium). Group D was injected with GHS, 100 μg/kg

(Ipamorelin, Novo Nordisk A/S, Gentofte, Denmark)

three times daily. Group E was injected with a combi-

nation of GC and GHS in the above mentioned doses.

Injections were given subcutaneously in the nape of

the neck daily for 3 months. The animals had free ac-

cess to drinking water and normal pellet diet (Altromin,

Chr. Pedersen, Ringsted, Denmark), in a 12 hours light,

12 hours of darkness cycle. All rats were injected subcu-

taneously with 20 mg tetracycline/kg (Sigma Chemical

Co., St. Louis, MO, USA) 25 days before killing, and with

15 mg/kg of calcein (Sigma Chemical Co., St. Louis, MO,

USA) 5 days before killing. The study was approved by

the Danish Animal Experiment Inspectorate.

Maximum tetanic tension of skeletal muscles

The maximal tetanic tension (MTT) and time course of

tetanic tension of the calf musculature (m. soleus, m.

plantaris and m. gastrocnemius together) were studied

in vivo using a previously described method.7The rats

were anesthetized with pentobarbital 60 mg/kg in-

traperitoneally. The proximal end of the three mus-

cles was kept in position by a 0.7 mm steel wire

through a 1 mm transverse canal drilled through the

centre of the femur condyles. The distal tendons of

the muscles were fixed with a pin to maintain nat-

ural in situ length, and the calcaneus was then cut

and the distal end of the tendons was clamped and

fixed to the movable cross-head of a materials test-

ing machine. The femur epicondyles were fixed by

the steel wire to the load cell of the materials test-

ing machine (TCT5, Lorentzen & Wettre, Stokholm,

Sweden). The muscle tension was measured continu-

ously by means of the load cell, the direct signals fed

to a load-time recorder (Philips PM 8272, Eindhoven,

Netherlands).

The muscles were stimulated to contraction through

n. ischiadicus on the back of the thigh. The elec-

trical stimulus was given through steel electrodes

(diameter 1.2 mm, electrode distance 1 mm) which

were connected to a stimulator (Anapulse stimulator,

model 302-T, W-P Instruments, New Haven, CO, USA).

The electrodes were isolated from the surrounding tis-

sue with parafilm to avoid activation of adjacent mus-

cles and nerves. During the experiment the rats were

placed on a small electric blanket to maintain constant

body temperature.

At the beginning of the experiment, the muscles

were strained until a tension of 4 N was obtained.

The first two stimulations were single stimulations

(30 V for 4 ms) and were given to ensure a correct local-

ization of the electrodes. Then two stimulations of 1-s

duration (30 V, impulse-duration 4 ms, a frequency of

100 Hz) were given to induce maximal tetanic contrac-

tion force. The final stimulation was 30 s in duration

(30 V, impulse-duration 4 ms, a frequency of 100 Hz).

Maximal tetanic tension of each rat was calculated as

the mean value of the maximal tetanic tension obtained

in the last three contractions. The endurance of the

muscles was studied by following the time course of

the tetanic tension during 30 s stimulation. The rats

were killed by exsanguination, under anaesthesia. The

blood was centrifuged and serum was stored at −20◦C

until analysis.

Skeletal muscle mass

The hind legs were exarticulated in the hip joints. The

calf muscles were dissected free from the hind legs,

defatted for 7 days in three changes of acetone, freeze-

dried for 3 days and weighed (dry defatted weight =

DDW). The tibia bone length was measured from facies

articularis condylus medialis to facies articularis infe-

rior with a sliding caliper.

268 N.B. Andersen et al.

Mechanical three-point bending analysis

of cortical bone

The Strength of the femur diaphyses were assessed in

a materials testing machine (Alwetron 250, Lorentzen

& Wettre, Stockholm, Sweden), using a standardized

procedure,15,17, 26 The femurs were placed on the pos-

terior surface on two rounded supporting bars with a

distance of 15.1 mm between the bars. A third rounded

bar was then lowered onto the anterior surface, load-

ing the bone diaphysis. The loading point was at a dis-

tance of 55% of the total length of the femur from the

top of the caput femoris. The femur was deflected at

a constant speed of 5 mm/min until failure and load-

deflection curves were registered simultaneously on

an x-y-recorder by transducers coupled to measuring

bridges. The ultimate breaking load (bending strength)

was calculated.

Bone formation and histomorphometry

Two 300 μm transverse sections were cut from both

femurs 2 mm below the loading point by means

of a precision bone saw (Eksakt-Apparatebau, Otto

Hermann, Norderstedt, Germany). One of the sections

was placed on a slide and projected onto a screen by

means of a projection microscope, magnification 20x.

The outer and inner circumferences were drawn and

scanned into a computer. Circumferences and cross-

sectional areas were calculated using the SigmaScan

program (Jandel Scientific Software, St. Rafael, CA,

USA). The other section was embedded in acylacetate

(Entellan, Merck, Darmstadt, Germany) on a glass

slide and used for determination of mineral apposi-

tion rates and bone formation rates by fluorescence

microscopy.15,27 A translucent star-shaped grid was

placed on top of the section with the centre of the star

in the mid-point of the marrow cavity and 16 lines

radiating from the centre point. Since only the cen-

tre of the star was fixed, the 16 radiating lines inter-

sected the periosteal and endocortical surface at ran-

dom. At the point of intersection, the distance between

the middle of the tetracycline label and the middle

of the calcein label was measured at a magnification

200x. An aspect with no labelling was classified as a

point of no mineral apposition. No distance between

the tetracycline and calcein labels was classified as a

point of no measureable mineral apposition, i.e. zero

mineral apposition. The mineral apposition rate was

calculated by dividing the distance between the two

labels by the interlabelling period in days. The lower

limit for detection of a distance between the tetracy-

cline and calcein labels was 5μm, corresponding to a

mineral apposition rate of 0.25 μm per day. The bone

formation rate was the mean mineral apposition rate ×

circumference.

Total serum IGF-I

This was determined by a RIA-assay.28

Statistical analyses

For analysis of differences between the groups the

Kruskal–Wallis test was applied; in case of difference,

the Mann–Whitney U-test was used. P< 0.05 (two-

tailed) was considered statistically significant.29 In the

tables, lower-case letters indicate significance levels at

P<0.05, but >0.01; upper-case letters significance

levels at P<0.01. The following comparisons were

made: 1, the saline-injected group was compared with

the GC-injected group; 2, GHS-injected rats were com-

pared with saline-injected rats; 3, GC-injected rats

were compared with the combined GC +GHS treated

rats; 4, the start control group was compared with

the saline group to delineate changes in the param-

eters in relation to the base line, i.e. start control

group.

RESULTS

GC vs saline

The GC-injected rats had a 4% decrease in BW during

the experimental period (Table 1), and their final

body weight was 14% lower than that of the saline

group. GC had no significant effect on the tibia length

during the experiment (Table 1). A 54% increase in

IGF-I was found in the GC-injected animals compared

with the saline group (Table 1). The DDW of the calf

musculature was reduced by 19% in the GC-injected

rats compared with the saline injected (Table 2), and

the MTT of the calf musculature was reduced by 28%

in the GC-injected rats [Fig. 1(A)]. When the MTT was

normalized to the DDW of the calf musculature a de-

crease was still observed in GC-treated compared with

saline-injected rats [Fig. 1(B)]. No change was found

in the time course of the tetanic tension during 7.5 or

15 seconds of stimulation (Table 2). The GC-injections

resulted in a near total arrest of bone formation rate

[Fig. 2(A)], and a decrease in the periosteal mineralizing

surface [Fig. 2(B)]. The breaking strength was found to

be at the level of the start control group, but did not

differ significantly from the breaking strength of the

saline group (Table 3).

GHS counteracts GC-induced effects on bone 269

Table 1 BW at start, final BW, body weight change, tibia length and total serum IGF-I in 8-month-old female rats injected with growth

hormone secretagogue (GHS) and/or glucocorticoids (GC) for 3 months

Start BW Final BW Change in BW Tibia length Serum IGF-I

Groups n(g) (g) (g) (mm) (ng/ml)

Start control 14 264 ±4−−38.2 ±0.2 497 ±19

Saline 14 264 ±4 294 ±4A30 ±3 38.5 ±0.2 386 ±21A

GC 14 264 ±4 254 ±8a,B −10 ±4B38.2 ±0.2 596 ±51B

GHS 14 264 ±4 313 ±6A,b 49 ±3B38.7 ±0.3 475 ±28b

GC +GHS 14 263 ±4 270 ±6D9±3c,D 38.2 ±0.2 568 ±18D

a: P< 0.05, A: P< 0.01 against the start control group, b: P< 0.05, B: P< 0.01, against the saline injected group, c: P< 0.05 against

the GC-injected group, D: P< 0.01 against the GHS-injected group.

Effect of GHS in normal animals

Injections with GHS increased the body weight by 19%

and the final BW 7% greater than the saline group. The

IGF-I concentrations were increased by 21% compared

with the saline group. GHS had no effect on muscle

mass (DDW) or in tibia length. Likewise, the maximal

tetanic tension [Fig. 1(A)] and the time course of tetanic

tension (Table 2) were unchanged compared with the

saline group. The bone formation rate at the femur

mid-diaphyseal periosteum [Fig. 2(A)] was three times

that of the saline group and there was a small non-

statistically significant increase in mineralizing surface

[Fig. 2(B)]. No significant changes were found in fe-

mur mid-diaphyseal cross-sectional area or breaking

strength (Table 3).

Effect of GHS in GC-injected animals

The group injected with GC and GHS in combina-

tion had a small BW gain in contrast to the group in-

Table 2 Dry defatted weight of the calf musculature and time

course of the tetanic tension during the first 15 seconds of

stimulation in 8-month-old female rats injected with growth

hormone secretagogues (GHS) and/or glucocorticoid (GC) for

3 months. Tetanic tension is given as a percentage of maximal

tetanic tension (MTT)

Tetanic tension Tetanic tension

after stimulation after stimulation

Dry defatted for 7.5 s for 15 s

Groups: nweight (mg) (% of MTT) (% of MTT)

Start Control 14 364 ±10 31.0 ±3.8 12.5 ±1.5

Saline 14 363 ±8 38.7 ±4.6 13.5 ±1.2

GC 14 295 ±8A, B 36.2 ±2.7 16.6 ±1.6

GHS 14 373 ±8 38.5±3.8 15.7 ±1.6

GC +GHS 14 318 ±9D34.8 ±2.8 14.6 ±0.9

A: P< 0.01 against the start control group, B: P< 0.01 against the

saline-injected group, D: P< 0.01 against the GHS-injected group.

jected with GC alone, which had a significant BW loss

(Table 1). The tibia length remained at the same level as

in the start control group. The DDW of the calf muscu-

lature was lower than that of the GHS-infected group

(Table 2). The MMT of animals injected with GC +GHS

in combination was decreased compared with the

saline and GHS treated groups, but increased signifi-

cantly compared with the GC-treated group [Fig. 1(A)].

When the MTT was corrected for differences in mg

DDW of the calf musculature, no difference was found

compared with the saline group [Fig. 1(B)]. No change

was observed in the time course of tetanic tension

(Table 2). The mid-diaphyseal periosteal bone forma-

tion rate was lower compared with the start control

group and the group injected with GHS, but four-fold

higher than the group injected with GC alone [Fig. 2(A).

Likewise, the periosteal mineralizing surface of animals

injected with GC +GHS was clearly increased com-

pared with the rats injected with GC alone [Fig. 2(b)].

This did not, however, result in a significant increase in

the breaking strength of the femur (Table 3). The IGF-I

concentration of the GC +GHS was not significantly

different from that of the GC group (Table 1).

DISCUSSION

Growth hormone secretion decreases with age; after

the age of 60, many elderly subjects have low levels

of GH and IGF-I.30,31 Muscle strength, muscle mass,

bone strength and mass also decrease with aging, and

these losses are further exacerbated by glucocorticoid

treatment. Rudman et al.32 hypothesized that replac-

ing GH in elderly subjects with low levels of serum

GH and serum IGF-I might result in improvements of

physical function; they treated elderly men who had

low serum IGF-I values with GH and found an in-

crease in serum IGF-I, lean body mass and a reduc-

tion in body fat mass.32 Several studies have shown

270 N.B. Andersen et al.

Fig. 1 Maximum tetanic tension (MMT) (A) and MTT normalized to

dry defatted weight (DDW) (B) of the calf muscles in 8-month-old

female rats injected with growth hormone secretagogue (GHS)

and/or glucocorticoid (GC) for 3 months. Mean values with SEM. N:

newton. A: P< 0.01 against the start control group; B: P< 0.01

against the saline group; c: P< 0.05 against the GC-injected

group; D: P< 0.01 against the GHS-injected group.

similar changes in body composition, but it has been

difficult to demonstrate improvements in skeletal mus-

cle strength as a result of the GH treatment.33, 34 Welle

et al.35 found, however, an increase in skeletal muscle

strength after GH treatment for 3 months. GHSs might

have an advantage compared with GH, because some

GHS-preparations can be given orally and some have

been shown to stimulate pulsatile GH secretion.36

In the present study, the GHS-preparation , Ipamore-

lin, injected subcutaneously in rats increased the to-

tal serum concentration of IGF-I by 23% and BW by

7% compared with the saline-injected group, without

significant effect on tibial length. Ipamorelin did not

change skeletal muscle mass or MTT compared with

the saline group. The bone formation rate was clearly

increased in the Ipamorelin-injected rats. The amount

of new bone which corresponded to a 0.1 mm increase

in the thickness of the diaphyseal bone was not suf-

ficient to significantly change the breaking strength

of the bone. In the present study, however, a signifi-

cant stimulation of longitudinal growth was not found.

In the dose–response study of Johansen et al.,25 longi-

tudinal bone growth of 4-month-old rats was signifi-

cantly stimulated by Ipamorelin. In the present study,

the rats were 8–11 months old and had passed the

period of longitudinal growth, even though the epi-

physeal growth plate is still cartilaginous in rats at

that age.

Total serum-IGF-I increased with GC treatment, sup-

porting previous observations.11,37 However, Skjærbæk

et al.38 found a reduced amount of free IGF-I, al-

though the total amount of IGF-I was unchanged or

Fig. 2 Periosteal bone formation rate (A) and mineralizing surface

(B) at the femur mid-diaphysis in 8-month-old female rats injected

with growth hormone secretagogue (GHS) and/or glucocorticoid

(GC) for three months. Mean values with SEM. a: P< 0.05, A:

P< 0.01 against the start control group; B: P< 0.01 against the

saline group; C: P< 0.01 against the GC-injected group; D:

P< 0.01 against the GHS-injected group.

GHS counteracts GC-induced effects on bone 271

Table 3 Mid-diaphyseal cross-sectional area, medullary area and

breaking strength of the femur of 8-month-old female rats injected

with growth hormone secretagogue (GHS) and/or glucocorticoid

(GC) for 3 months

Cortical bone

cross-sectional Medullary Breaking

Groups narea (mm2) area (mm2) strength (N)

Start control 14 6.2 ±0.1 2.7 ±0.1 165 ±6

Saline 14 6.2 ±0.1 2.9 ±0.1 182 ±6

GC 14 6.1 ±0.1 2.5 ±0.1 166 ±6

GHS 14 6.3 ±0.1 2.5 ±0.1 180 ±5

GC +GHS 14 6.1 ±0.1 2.6 ±0.1 175 ±4

increased during GC-treatment. In rats, about 5% of the

IGF-I is free.39 The change in weight induced by GC-

treatment was significantly correlated with free IGF-I

and not with total IGF-I.38 GC-treatment influences

the relationship between IGF-I and its binding pro-

teins. In the present experiment, even though the total

serum IGF-I was increased, the free serum IGF-I may

well be reduced, resulting in reduced IGF-I biological

activity.

The present study supports a possible therapeu-

tic role for GHSs in patients receiving catabolic glu-

cocorticoids and is in agreement with Gertz et al.21

who demonstrated that a GH secretagogue given i.v.

to young men partially reversed glucocorticoid sup-

pression of GH secretion. Likewise, it supports the

study of Lieber et al.19 who immobilized a hind

limb of dogs; GHS given during the remobilization

phase increased muscle strength markedly. Concern-

ing bone, oral administration of GHSs has been shown

to increase markers of bone turn-over in young obese

males40 and in elderly adults.41 A partial attenua-

tion of the GH response to GHS has been shown

i.e. desensitization.25,40,42 The mechanism behind this

phenomenon is not yet clear, but could be due to

negative feedback by GH or IGF-I or to down regu-

lation of the GHS receptor. Despite the decrease in

serum GH, serum IGF-I was increased during these

studies and the desensitization seemed to be partial and

reversible.40 Whether coadministration of GC changes

the desensitization mechanism is unclear. It might be

speculated that the production of immunoglobulins

against Ipamorelin could be lowered with coadminis-

tration of GC possibly affecting its half-life. The normal

half-life of Ipamorelin is 30–60 min in rats after i.v.

administration.43

In conclusion, the decrease in bone formation found

in GC-injected rats can be counteracted by administra-

tion of GHS.

ACKNOWLEDGEMENTS

Novo Nordisk A/S, The Danish Health Research Coun-

cil, grants no. 9500922 (Centre for Molecular Gerontol-

ogy), 9503023 and 9600822 (Aarhus University-Novo

Nordisk Centre for Research in Growth and Regener-

ation), Aarhus University Research Foundation, Novo

Nordisk Foundation. The skilled technical assistance

of C. Knæhus, J. Utoft, E. K. Mikkelsen and linguistic

revision of M. Fischer are gratefully acknowledged.

REFERENCES

1. Askari A, Vignos PJ, Moskowitz RW. Steroid myopathy in

connective tissue disease. Am J Med 1976; 61: 485–492.

2. Horber FF, Scheidegger JR, Grunig BE, Frey FJ. Evidence that

prednisone-induced myopathy is reversed by physical training.

J Clin Endocrinol Metabol 1985; 61: 83–88.

3. Seene T. Turnover of skeletal muscle contractile proteins in

glucocorticoid myopathy. J Steroid Biochem Mol Biol 1994; 50:

1–4.

4. Adinoff AD, Hollister JR. Steroid-induced fractures and bone loss

in patients with asthma. N Engl J Med 1983; 309: 265–268.

5. Lukert B. Glucocorticoid-induced osteoporosis. In: Marcus R,

Feldman D, Kelsey J (eds). Osteoporosis. San Diego: Academic

Press, Inc., 1996: 801–820.

6. Ørtoft G. The effect of glucocorticoid and growth hormone on

the skeletal system in young growing rats. Faculty of Health

Sciences, University of Aarhus, Denmark. Thesis 2000: 1–48.

7. Andersen NB, Andreassen TT, Ørskov H, Oxlund H. Growth

hormone and mild exercise in combination increases markedly

muscle mass and tetanic tension in old rats. Eur J Endocrinol

2000; 143: 409–418.

8. McGrath JA, Goldspink DF. Glucocorticoid action on protein

synthesis and protein breakdown in isolated skeletal muscles.

Biochem J 1982; 206: 641–645.

9. Ruff RL, Martyn D, Gordon AM. Glucocorticoid-induced atrophy

is not due to impared excitability of rat muscle. Am J Physiol

1982; 243: E512–E521.

10. Moore BJ, Miller MJ. Diaphragm atrophy and weakness in

cortisone-treated rats. J Appl Physiol 1989; 67: 2420–2426.

11. Ørtoft G, Grønbæk H, Oxlund H. Growth hormone

administration can improve growth in glucocorticoid-injected

rats without affecting the lymphocytopenic effect of the

glucocorticoid. Growth Horm IGF Res 1998; 8: 251–264.

12. Ørtoft G, Andreassen TT, Oxlund H. Growth hormone increases

cortical and cancellous bone mass in young growing rats with

glucocorticoid-induced osteopenia. J Bone Miner Res 1999; 14:

710–721.

13. Ullman M, Oldfors A. Effects of growth hormone on skeletal

muscle. I. Studies on normal adult rats. Acta Physiol Scand 1989;

135: 531–536.

14. Florini JR, Ewton DZ. Skeletal muscle fibre types and myosin

ATPase activity do not change with age or growth hormone

administration. J Gerontol 1989; 44: B110–117.

15. Andreassen TT, Jørgensen PH, Flyvbjerg A, Ørskov H, Oxlund H.

Growth hormone stimulates bone formation and strength of

cortical bone in aged rats. J Bone Miner Res 1995; 10: 1057–

1067.

16. Andreassen TT, Melsen F, Oxlund H. The influence of growth

hormone on cancellous and cortical bone of the vertebral body

in aged rats. J Bone Miner Res 1996; 11: 1094–1102.

272 N.B. Andersen et al.

17. Oxlund H, Andersen NB, Ørtoft G, Ørskov H, Andreassen TT.

Growth hormone and mild exercise in combination markedly

enhance cortical bone formation and strength in old rats.

Endocrinology 1998; 139: 1899–1904.

18. Svensson I, Lall S, Dickson SL, et al. The GH secretagogues

ipamorelin and GH-releasing peptide-6 increase bone mineral

content in adult female rats. J Endocrinol 2000; 165: 569–577.

19. Lieber RL, Jacks TM, Mohler RL, et al. Growth hormone

secretagogue increases muscle strength during remobilization

after canine hindlimb immobilization. J Orthop Res 1997; 15:

519–527.

20. Kovacs G, Fine RN, Worgall S, et al. Growth hormone prevents

steroid-induced growth depression in health and uremia. Kidney

Int 1991; 40: 1032–1040.

21. Gertz BJ, Sciberras DG, Yogendran L, et al. L-692,429, a

nonpeptide growth hormone (GH) secretagogue, reverses

glucocorticoid suppresion of GH secretion. J Clin Endocrinol

Metab 1994; 79: 745–749.

22. Voltz DM, Piering AW, Magestro M, Giustina A, Wehrenberg W B.

Effect of GHRP-6 and GHRH on G H secretion in rats following

chronic glucocorticoid treatment. Life Sci 1995; 56: 491–497.

23. Raun K, Hansen BS, Johansen NL, Thøgersen H, Madsen K,

Andersen PH. Ipamorelin, the first selective growth hormone

secretagogue. Eur J Endocrinol 1998; 139: 552–561.

24. Malml ̈

of K, Haahr P-M, Johansen PB, Wilken M, Oxlund H.

Methylprednisolone does not inhibit the release of growth

hormone after intravenous injection of a novel growth hormone

secretagogue in rats. Growth Horm IGF Res 1999; 9: 445–450.

25. Johansen PB, Nowak J, Skjærbæk C, et al. Ipamorelin, a new

growth-hormone-releasing peptide, induces longitudinal bone

growth in rats. Growth Hormone IGF Res 1999; 9: 106–113.

26. Ørtoft G, Oxlund H, Jørgensen P H, Andreassen TT.

Glucocorticoid treatment or food deprivation counteract the

stimulating effect of growth hormone on rat cortical bone

strength. Acta Paediatr 1992; 81: 912–917.

27. Oxlund H, Ejersted C, Andreassen TT, Tørring O, Nilsson MHL.

Parathyroid hormone (1–34) and (1–84) stimulate cortical bone

formation both from periosteum and endosteum. Calcif Tissue

Int 1993; 53: 394–399.

28. Flyvbjerg A, Orskov H. Kidney tissue insulin-like growth factor I

and initial renal growth in diabetic rats: relation to severity of

diabetes. Acta Endocrinol (Copenhagen) 1990; 122: 374–378.

29. Sokal RR, Rohlf FJ. Biometry. San Francisco: WH Freeman & Co.

1981.

30. Zadik Z, Chalew SA, McCarter RJ, Meistas M, Kowarski A A. The

influence of age on the 24-hour integrated concentration of

growth hormone in normal individuals. J Clin Endocrinol Metab

1985; 60: 513–516.

31. Juul A, Bang P, Hertel NT, et al. Serum insulin-like growth

factor-I in 1030 healthy children, adolescents, and adults:

relation to age, sex, stage of puberty, testicular size, and body

mass index. J Clin Endocrinol Metab 1994; 78: 744–752.

32. Rudman D, Feller AG, Nagraj HS, et al. Effects of human growth

hormone in men over 60 years old. N Engl J Med 1990; 323:

1–6.

33. Taaffe DR, Pruitt L, Reim J, et al. Effects of recombinant human

growth hormone on the muscle strength response to resistance

exercise in elderly men. J Clin Endocrinol Metab 1994; 79:

1361–1366.

34. Yarasheski KE, Zachwieja JJ, Cambell JA, Bier D. Effect of growth

hormone and resistance exercise on muscle growth and strength

in older men. Am J Physiol 1995; 268: E268–E276.

35. Welle S, Thornton C, Statt M, McHenry B. Growth hormone

increases muscle mass and strength but does not rejuvenate

myofibrillar protein syntesis in healthy subjects over 60 years

old. J Clin Endocrinol Metab 1996; 81: 3239–3243.

36. Chapman IM, Bach MA, Van Cauter, et al. Stimulation of the

growth hormone (GH)-insulin-like growth factor I axis by daily

oral administration of a GH scretagogue (MK-677) in healthy

elderly subjects. J Clin Endocrinol Metab 1996; 81: 4249–4257.

37. Luo JM, Murphy LJ. Dexamethasone inhibits growth hormone

induction of insulin like growth factor-I (IGF-I) messenger

ribonucleic acid (mRNA) in hypophysectomized rats reduces

IGF-I mRNA abundance in the intacts rat. Endocrinology 1989;

125: 165–171.

38. Skjærbæk C, Frystyk J, Grøfte T, et al. Serum free insulin-like

growth fatctor-I is dose-dependently decreased by

metylprednisolone and related to body weight changes in rats.

Growth Horm IGF Res 1999; 9: 74–80

39. Frystyk J, Skjaerbaek C, Dinesen B, Orskov H. Free insulin-like

growth factors (IGF-I and IG F-II) in human serum. FEBS Lett

1994; 348: 185–191.

40. Svensson J, L ̈

onn L, Jansson J O, et al. Two-month treatment of

obese subjects with oral growth hormone (GH) secretagogue

MK-677 increases GH secretion, fat-free mass, and energy

expenditure. J Clin Endocrinol Metab 1998; 83: 362–369.

41. Murphy MG, Plunkett LM, Gertz BJ, et al. MK-677, an orally

active growth hormone secretagogue, reverses diet-induced

catabolism. J Clin Endocrinol Metab 1998; 83: 320–325.

42. Rahim A, O’Neill PA, Shalet SM. Growth hormone status during

long-term hexarelin therapy. J Clin Endocrinol Metab 1998; 83:

1644–1649.

43. Johansen PB, Hansen KT, Andersen JV, Johansen NL.

Pharmacokinetic evaluation of ipamorelin and other peptidyl

growth hormone secretagogues with emphasis on nasal

absorption. Xenobiotica 1998; 28: 1083–1092.

... Malmlöf et al., using similar steroid doses (5 mg  kg À1  d À1 ) and Ipamorelin (0.4 or 1.6 mg  kg À1  d À1 ), observed that Ipamorelin normalized GH secretion and IGF-I levels in steroid treated rats [29].The observation that Ipamorelin did not increase IGF-I may indicate GH resistance in the liver as also observed in diabetic mice [28]. In a recent study Ipamorelin was found to counteract the decrease in bone formation by glucocorticoid, and in that study there was no difference in serum IGF-I between the groups studied, either [30]. We did not measure GH levels, though it might have enlightened this observation, as GH may stimulate local IGF-I production which may in turn exert autocrine and paracrine effects. ...

Niels Kristian Aagaard

Thorbjørn Grøfte Jacob Greisen

Hendrik Vilstrup

Growth hormone (GH) reduces the catabolic side effects of steroid treatment via effects on the amino-nitrogen metabolism. Ipamorelin is a synthetic peptide with GH releasing properties. We wished to study the metabolic effects of Ipamorelin and GH on selected hepatic measures of alpha-amino-nitrogen conversion during steroid-induced catabolism. Five groups of rats were included: (1) free-fed controls (2) pair-fed controls (3) prednisolone (delcortol, 4 mg x kg(-1) x day(-1)) (4) prednisolone and GH (1 mg x kg(-1) x day(-1)) (5) prednisolone and Ipamorelin (0.5 mg x kg(-1) x day(-1)). After seven days the hepatic capacity of urea-N synthesis (CUNS) was determined in parallel with measurements of liver mRNA levels of urea cycle enzymes, whole-body N-balance, and N-contents of various organs. Compared to pair-fed controls, prednisolone increased CUNS (p<0.01) as well as the expression of urea cycle genes (p<0.01), and decreased N-balance (p<0.01) as well as organ N-contents (p<0.05). Compared to prednisolone treated animals, co-administration of GH reduced CUNS by 33% (p<0.01), normalized urea cycle gene expression, improved N-balance 2.5-fold, and normalized or improved organ N-contents. In prednisolone treated rats Ipamorelin reduced CUNS by 20% (p<0.05), decreased the expression of urea cycle enzymes, neutralised N-balance, and normalized or improved organ N-contents. Accelerated nitrogen wasting in the liver and other organs caused by prednisolone treatment was counteracted by treatment with either GH or its secretagogue Ipamorelin, though at the doses given less efficiently by the latter. This functional study of animals confirms that the GH secretagogue exerts GH related metabolic effects and may be useful in the treatment of steroid-induced catabolism.

Cory Mayfield

Ioanna K Bolia

Cailan Feingold

Alexander Weber

Background Therapeutic peptides are short-chain amino acids that regulate cellular functions and facilitate biochemical processes. In recent years, there has been significant growth in the global market for therapeutic peptides and thus its popularity among patients. Given the increase in the development of peptides and increased marketing to patients for orthopaedic injuries, it is critical for orthopaedic surgeons to understand the current evidence behind these therapeutic peptides. Purpose To evaluate the current evidence and applications of injectable peptide therapy, focusing on its potential in regenerative medicine and sports performance, to help orthopaedic providers better understand the current state of different therapeutic peptide approaches. Study Design Narrative review. Methods A comprehensive literature search was conducted using PubMed to identify biochemical and clinical studies on the most popular types of injectable peptide therapy. Key peptides evaluated included BPC-157, TB-4, TB-500, CJC-1295 + ipamorelin, tesamorelin, and GHK-Cu. Results BPC-157 demonstrated potential benefits in tendon and muscle repair, but these findings are largely unvalidated in human trials. A single human case series reported improvements in pain after intra-articular knee injections of BPC-157, although significant methodological flaws and a lack of controls limit its applicability and reliability. TB-4 and its derivative TB-500 promoted angiogenesis and tissue repair in preclinical models, but human orthopaedic data are lacking, and both remain banned substances in sports. CJC-1295 combined with ipamorelin showed significantly improved maximum tetanic tension in murine models with glucocorticoid-induced muscle loss, but these findings are limited to animal studies. Tesamorelin, approved for treating HIV-associated lipodystrophy, has no supporting orthopaedic evidence. GHK-Cu showed promise in wound healing and anti-inflammatory effects, but no clinical data support its use for musculoskeletal conditions. Conclusion While peptide therapy may possess significant therapeutic and regenerative potential, it is critical that orthopaedic and sports medicine providers understand the current lack of evidence to support the clinical use of these peptides. Importantly, information regarding the indications, dosing, frequency, and duration of treatment remains unknown. Despite the popularity of these peptides in mainstream media and among patients, significant research regarding the safety and efficacy of these therapeutic methods is required before definitive recommendations can be made to patients.

Philip A Carpino

The 28 amino acid polypeptide, ghrelin, is a novel neuroendocrine hormone synthesised primarily in the stomach. It stimulates growth hormone (GH) secretion, increases food intake and appetite and promotes body weight gain by decreasing fat mass metabolism, particularly in rodent models. The pharmacological properties of this peptide are mediated by the type 1a growth hormone secretagogue receptor (GHS-R1a), a G-protein-coupled receptor localised predominantly in the pituitary gland and hypothalamus. The discovery of new agents that either mimic or modulate the actions of ghrelin via the GHS-R1a has attracted considerable interest in recent years. Many peptidyl and peptidomimetic GHS-R1a agonists such as growth hormone-releasing peptides (GHRPs) and growth hormone secretagogues (GHSs) that stimulate GH secretion and increase plasma levels of insulin-like growth factor-1 (IGF-1) have been identified. First generation GHSs have undergone extensive clinical evaluation in humans, but have shown disappointing results in the treatment of diseases such as frailty, the age-related decline in body composition. Several of these compounds were found to increase adiposity in rodent models. Second generation dipeptidyl and third generation small molecule GHSs have recently been profiled in various animal models. A third generation of GHS with partial agonist activity at the GHS-R1a showed anabolic activity in rodent models, increasing fat-free (muscle) mass rather than fat mass. A few GHS-R1a receptor antagonists have been disclosed, although these compounds have exhibited poor selectivities or weak affinities for the receptor. Since endogenous ghrelin appears to play an important role in the long-term regulation of energy balance, GHS-R1a antagonists may be useful in the prevention of weight gain, following weight loss, or in the treatment of obesity, a pathological condition characterised by excess adiposity. This review describes the pharmacology of select ghrelin receptor modulators and highlights new ghrelin receptor agonists and antagonists that have appeared in the literature from 1999 – 2002.

Ernest A. Adeghate

Abdul S Ponery

To examine the effect of ipamorelin (IPA), a novel pentapeptide with a strong growth hormone releasing potency, on insulin secretion from pancreatic tissue fragments of normal and diabetic rats. Diabetes mellitus was induced by streptozotocin (60 mg kg(-1)). Four weeks after the induction of diabetes, pancreatic tissue fragments of normal and diabetic rats were removed and incubated with different concentrations (10(-12) - 10(-6) M) of IPA. Insulin release from the pancreas was measured by radioimmunoassay. Ipamorelin evoked significant (p<0.04) increases in insulin secretion from the pancreas of normal and diabetic rats. Either diltiazem or yohimbine or propranolol or a combination of atropine, propranolol and yohimbine inhibited IPA-evoked insulin secretion significantly (p<0.03) from the pancreas of normal and diabetic rats. Atropine caused a significant (p<0.007) reduction in the IPA-induced insulin secretion in diabetic but not in normal rats. IPA stimulates insulin release through the calcium channel and the adrenergic receptor pathways. This is the first study to examine the effect of ipamorelin on insulin secretion in the pancreas.

A Juul Peter Bang

Niels Thomas Hertel N E Skakkebaek

Serum levels of insulin-like growth factor-I (IGF-I) increase with age and pubertal development. The large variation in circulating IGF-I levels in adolescence makes it difficult to use the IGF-I value of a single child in the assessment of his growth status. In addition, the interference of IGF-binding proteins in many IGF-I assays contributes to this problem. We measured IGF-I in acid-ethanol-extracted serum from 1030 healthy children, adolescents, and adults, employing a RIA that reduces interference of IGF-binding proteins by using monoiodinated Tyr31-[125I]des-(1-3)IGF-I as radioligand. Mean serum IGF-I concentrations increased slowly in prepubertal children from 80-200 μgs/L with a further steep increase during puberty to approximately 500 μgs/L. After puberty, a subsequent continuous fall in circulating IGF-I levels was apparent throughout adulthood to a mean of 100 μgs/L at the age of 80 yr (P < 0.0001). Girls had maximal IGF-I levels at 14.5 yr of age, whereas boys had peak IGF-I levels 1 yr later. This is almost 2 yr later than average peak height velocity. The large variation in serum IGF-I levels during puberty was diminished when data were separated according to sex and Tanner stage of puberty. Interestingly, we found a significant variation with age within the Tanner stages; there was an increase in serum IGF-I concentrations with age in the early pubertal stages and a decrease in the late stages (P < 0.05). Serum IGF-I increased concomitantly with increasing testicular volume. Multiple regression analysis revealed that serum IGF-I levels predicted height velocity in the following year (r = 0.33; P < 0.0001). Body mass index did not correlate significantly with serum IGF-I in prepubertal children in a multiple regression analysis. In conclusion, there was a significant variation in serum IGF-I levels with age within a given Tanner stage of puberty in addition to the well known increase with increasing age or pubertal stage. Accordingly, the effects of sex, age, and puberty on serum IGF-I cannot be separated into simple additive components when studying 1030 children in a cross-sectional design. Thus, the age-, sex-, and puberty-corrected IGF-I values may, in fact, improve the use of serum IGF-I as a diagnostic tool to distinguish between a child with retarded puberty and a GH-deficient individual.

Ian Chapman

Mark Bach

Eve Van Cauter

Michael O Thorner

Aging is associated with declining activity of the GH axis, possibly contributing to adverse body composition changes and increased incidence of cardiovascular disease. The stimulatory effects on the GH-insulin-like growth factor I (IGF-I) axis of orally administered MK-677, a GH-releasing peptide mimetic, were investigated. Thirty-two healthy subjects (15 women and 17 men, aged 64-81 yr) were enrolled in a randomized, double blind, placebo-controlled trial. They received placebo or 2, 10, or 25 mg MK-677, orally, once daily for 2 separate study periods of 14 and 28 days. At baseline and on day 14 of each study period, blood was collected every 20 min for 24 h to measure GH, PRL, and cortisol. Attributes of pulsatile GH release were assessed by 3 independent algorithms. MK-677 administration for 2 weeks increased GH concentrations in a dose-dependent manner, with 25 mg/day increasing mean 24-h GH concentration 97 +/- 23% (mean +/- SE; P < 0.05 vs. baseline). This increase was due to an enhancement of pree...

Stephen Welle

Colleen Thornton M Statt B McHenry

The rate of synthesis of myofibrillar proteins is slower in muscle of healthy subjects over 60 yr old than it is in young adults. Previous research suggests that reduced activity of the GH/insulin-like growth factor-I system could be a determinant of this slowing of protein synthesis. To test the hypothesis that GH could rejuvenate the rate of myofibrillar protein synthesis, we studied healthy subjects over 60 yr old, after a single injection (0.03 mg/kg.sc) of recombinant human GH (n = 6 males/2 females) or placebo (n = 6 males/2 females), or after 3 months of either GH (0.03 mg/kg, sc, 3 x /week, n = 5 males) or placebo (n = 5 males) treatment. Myofibrillar protein synthesis and whole-body protein metabolism were evaluated with the tracer L-[1-13C]leucine. GH reduced whole-body leucine oxidation by 36% (P < 0.01) in the single injection study. There was no effect of GH on whole-body protein breakdown or synthesis, or on myofibrillar protein synthesis in the quadriceps, either acutely or after 3 months of treatment. GH treatment for 3 months increased lean body mass (3.3 +/- 0.7 kg, P < 0.01, as evaluated by 40K counting), muscle mass (3.3 +/- 1.1 kg, P < 0.02, as evaluated by urinary creatinine excretion), and thigh strength (14 +/- 5%, P < 0.05, as evaluated by isokinetic dynamometry). We conclude that GH can increase muscle mass and strength in healthy men over 60 yr old, but does not restore a youthful rate of myofibrillar protein synthesis.

H. Oxlund

The effects of a combination of mild exercise and GH injections on bone were studied in old female rats. Biosynthetic human GH, 2.7 mg/kg/day, was injected sc for 73 days. Exercised rats ran 8 m/min on a treadmill for 1 h/day. All rats (age 21 months old) were labeled with a tetracycline injection 56 days and a calcein injection 11 days before killing. The GH injections resulted in an 11-fold increase in femoral middiaphyseal bone formation rate and a 12% increase in cross-sectional area compared with the saline-injected group. The mild exercise doubled the mineralizing surface but did not influence the bone formation rate significantly. The combination of GH injections plus exercise, however, resulted in a further increase of 39% in bone formation rate, primarily at the anterolateral aspects, and an increase of 5% in cross-sectional area compared with the group injected with GH only. The femur ultimate breaking load was increased by 37% and the stiffness by 42% in the group injected with GH compared with the saline-injected group. Exercise alone did not influence the femur mechanical properties. The combination of GH injections plus exercise induced a 4% further increase in ultimate breaking load and 7% further increase in stiffness compared with the group injected with GH alone. The GH injections induced a 117% increase in serum insulin-like growth factor I. The GH-insulin-like growth factor I axis stimulates recruitment of osteoblast precursor cells, resulting in increased bone formation at the periosteal surface. GH injections and mild excercise in combination modulate and increase further the formation and strength of cortical bone in old female rats.

J Svensson

Growth hormone (GH) is of importance for normal bone remodelling. A recent clinical study demonstrated that MK-677, a member of a class of GH secretagogues (GHSs), increases serum concentrations of biochemical markers of bone formation and bone resorption. The aim of the present study was to investigate whether the GHSs, ipamorelin (IPA) and GH-releasing peptide-6 (GHRP-6), increase bone mineral content (BMC) in young adult female rats. Thirteen-week-old female Sprague-Dawley rats were given IPA (0.5 mg/kg per day; n=7), GHRP-6 (0.5 mg/kg per day; n=8), GH (3.5 mg/kg per day; n=7), or vehicle administered continuously s.c. via osmotic minipumps for 12 weeks. The animals were followed in vivo by dual X-ray absorptiometry (DXA) measurements every 4th week. After the animals were killed, femurs were analysed in vitro by mid-diaphyseal peripheral quantitative computed tomography (pQCT) scans. After this, excised femurs and vertebrae L6 were analysed by the use of Archimedes' principle and by determinations of ash weights. All treatments increased body weight and total tibial and vertebral BMC measured by DXA in vivo compared with vehicle-treated controls. However, total BMC corrected for the increase in body weight (total BMC:body weight ratio) was unaffected. Tibial area bone mineral density (BMD, BMC/area) was increased, but total and vertebral area BMDs were unchanged. The pQCT measurements in vitro revealed that the increase in the cortical BMC was due to an increased cross-sectional bone area, whereas the cortical volumetric BMD was unchanged. Femur and vertebra L6 volumes were increased but no effect was seen on the volumetric BMDs as measured by Archimedes' principle. Ash weight was increased by all treatments, but the mineral concentration was unchanged. We conclude that treatment of adult female rats with the GHSs ipamorelin and GHRP-6 increases BMC as measured by DXA in vivo. The results of in vitro measurements using pQCT and Archimedes' principle, in addition to ash weight determinations, show that the increases in cortical and total BMC were due to an increased growth of the bones with increased bone dimensions, whereas the volumetric BMD was unchanged.

Leland Graves

Barbara Lukert

Glucocorticoid-induced osteoporosis is the leading cause of medication-induced osteoporosis. The fracture incidence after 1 yr of glucocorticoid therapy has been found to be 17% and observational studies suggest that fractures eventually occurin 30 to 50% of chronic glucocorticoid-treated patients. An increased risk of fracture develops within as quickly as 3 mo, and with doses of prednisone as low as 2.5 mg daily. Despite effective methods of prevention and treatment, only 50% of chronic glucocoriticoid-treated patients undergo any evaluation for osteoporosis and less than one in four receives treatment. This article addresses the various issues the clinician faces in managing patients receiving chronic glucocorticoids. It begins and ends with a case perspective. Evidence-based information is used to outline the current best strategy for the prevention and treatment of glucocorticoid-induced osteoporosis.

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