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Bone and Mineral, 20 (1993) 125 -132 125

© 1993 Elsevier Scientific Publishers Irela nd L td. All r ights reserved. 0169-6009/93/ 06.00

B AM 00531

H i g h i n t e n s it y a c ti v it ie s in y o u n g w o m e n s it es p e c i f i c b o n e m a s s e f f e c t s a m o n g f e m a l e f i g u r e

s k a t e r s

Charles W Slemenda and C Conrad Johnston

I n d iana Un ive rs i ty Schoo l o f M edic ine D epa r tmen t o f Medicine, 702 Barnhill Drive, Indianapolis, IN 46202

USA )

(Received 10 March 1992)

(Accepted 8 September 1992)

Summary

W e c o m p a r e d y o u n g female f igure skaters , a ged 10-23, w ith non ath le t ic con tro l subjects to ascerta in

wh ethe r there we re differences in skeletal densities at va riou s sites. W e also compared other character i s t i c s

of body s ize, including height , w eight and percent body fat . Although the skaters were th inner and

s ignif icant ly mo re l ike ly to have o l igo- or am enorrhe a, they had s imilar skeletal densit ies at uppe r bodysites (spine, arms, ribs) a n d s i g n i f i c a n t l y greater densities in the p e l v i s a n d legs. These differences were

n o t e v i d e n t u n t i l the mid-teens, however, suggesting that there is l i t t l e l ike l ihood of se lec t ion bias as the

cause of th e observed d ifferences .

Key words: Bone densi ty ; In tense phys ica l ac t iv i ty ; A m e n o r r h e a

Introduction

Pat terns o f phys ica l ac t iv i ty in the deve lop ed cou ntr i es o f the wor ld have chan ged

m a r k e d l y o v e r t h e p a s t 2 0 - 3 0 y e a r s . A l t h o u g h t h e r e i s c o n s i d e r a b l e e v i d e n c e t h a t

the f itness leve l s o f ch ildren have , on average , dec l ined an d that ch ildren have

bec om e fa t t er [ l ] , there are subgro ups o f the pop ula t ion part i c ipat ing in ex tremely

in tense ac t iv i t i e s a t l eve l s not before contemplated . Among women, part i c ipat ion in

com pet i t ive d i s tance running , m ul t ip l e - sport event s b ia th lons , t r ia th lons) , gym -

nasti cs , swim ming a nd skat ing have a l l increased in recent years. T he long- t erm

ske le tal cons eque nces o f these t emp ora l chan ges in ac t iv i ty patt erns are not en ti re ly

unde rstood . W hereas, we have sh ow n that m oder ate ac t iv ity in ch ildren i s assoc ia ted

w ith increased ske letal m ass [2l and oth ers have repo rted that retrospectively ascer-

Correspondence to : Char les W. Slemenda, Dr .P.H. , I n d i a n a U n i v e r s i t y D e p a r t m e n t of Medicine, 702

B am hi l l Dr ive , Ind ianapo l i s, I N 46202, US A.

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t a i ned ch i l dhood ac t i v it y is a s soc i a ted w i th g r ea t e r bo ne m ass i n youn g wom en [3] ,

t he r e a r e a l so c l ea r r i sk s a s soc i a t ed w i th i n t ense ac t i v i t i e s i n young women when

these ac tiv i ties a re assoc ia ted wi th me ns t rua l d i s turba nces [4] . This con t ras t in the

e f fec t s o f exe rci s e on b one d em ons t r a t e t he need t o an swer a nu mb er o f ques t i ons

b e f o r e a r a t io n a l a p p r o a c h t o e x e rc is e r e c o m m e n d a t i o n s c a n b e m a d e . H o w m u c h

ac t iv i ty i s appropr ia te and benef ic ia l? What types of ac t iv i ty y ie ld the grea tes t

benef i t s? And which ske le ta l s i tes a re most a f fec ted by spec i f ic ac t iv i t ies? We have

a t t emp ted t o add re s s a spec t s o f t he se ques t i ons w i th t he s t udy de sc r ibed be low,

wh ich com pare s g roup s w i th s t a rk ly con t r a s t i ng ac t i v i t y pa t t e rn s - - f a i rl y s eden t a ry

you ng wom en and r eg iona l and i n t e rna t iona l c a l ibe r f ema le ic e ska t e rs .

Me t h o d s

opulationsAl l o f t he you ng wo men in t he se s t ud ie s we re be tween 10 and 23 yea r s o ld and cauca -

s ian. T he s eden t a ry g roup n = 22 ) was r ec ru it ed fo r a s t udy o f c a l c ium a bso rp t i onand we re aged 10 -23 when me asu red Tab l e 1 ). A l thoug h som e d id pa r t i c ipa t e i n

casua l a th le t ics , none was involved in in tense phys ica l t ra in ing .

The i ce ska t e rs n = 22) we re r ec ru it ed t h roug h the Ind i ana W or ld Ska t i ng

Academy , wh ich conduc t s eva lua t i on camps and t r a in ing p rog rams fo r a l l l eve l s o f

compet i t ive ska te rs , inc luding in te rna t iona l ca l iber compet i tors . The ska te rs involv-

ed in th i s s tudy were both reg iona l and na t iona l / in te rna t iona l leve l ska te rs , aged

11-2 3 an d d iv ided ab ou t equa l ly in the three sepa ra te ska t ing d isc ip lines : i ce

dancers , pa i r s ska te rs and indiv idua l compet i tors . The in te rna t iona l ca l iber ska te rs

t r a ined 25 -40 h pe r w eek on ave rage , nea r ly a l l o f th i s t ime be ing spen t i n we igh t-

bear ing ac t iv i ties on the ice . Da nce t ra in ing w as the only o ther ac t iv i ty to cont r ibu te

Tab l e

t -Tes t s compar ing ska t e r s t o non -a th l e t i c compar i son g roup

V a r i a b le S k a t e r s C o n t r o l s P - v a l u e

A g e ( y e a r s ) 1 7 .7 ± 3 .2 1 6 .0 ± 3 .4 0 .1 1

A g e ( f i r s t m e n s e s ) 1 3 .7 ± 2 .1 1 2 .6 ± 1 .1 0 .0 6

H e i g h t ( i n ) 6 2 .4 ± 2 .8 6 3 .0 ± 2 .8 0 .3 7W eig ht ( lbs ) 111 ± 16 117 ± 21 0 .22

B o d y f a t ( ) 1 8 .7 ± 5 .4 2 4 .3 ± 6 .0 0 .0 0 0 4

O l i g o m e n o r r h e i c a ( ) 2 0 0

A m e n o r r h e i c a ( ) 2 0 0 0 . 01

N o r m a l a ( ) 6 0 1 0 0

A r m s B M D 0 .8 1 ± 0 . 0 9 0 . 7 8 ± 0 . 0 9 0 . 1 2

R i b s B M D 0 . 7 0 ± 0 . 0 6 0 . 6 7 ± 0 . 0 8 0 . 0 8

S p i n e B M D 1 .0 7 ± 0 .1 5 1 .0 1 ± 0 .1 4 0 .0 8

T r u n k B M D 0 . 9 4 ± 0 . 0 9 0 . 8 7 ± 0 . 1 0 0 . 0 0 5

L e g s B M D 1 .2 1 ± 0 .1 4 1 .1 0 ± 0 .1 5 0 .0 0 5

P e l v i s B M D 1 .2 1 ± 0 .1 4 1 .0 6 ± 0 .1 3 0 .0 0 0 1

T o t a l b o d y B M D 1 .1 3 ± 0 .1 1 1 .0 7 ± 0 .1 1 0 .0 2

a E x c l u d e s p r e p u b e r t a l ( n = 2 s k a t e r s , n = 4 c o n t r o l s ) .

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more t han 2 h pe r week fo r any ska t e r ) . The t op - l eve l r eg iona l compe t i t o r s we re

s l igh t ly younger than the e l i t e ska te rs , bu t genera l ly asp i red to compete a t h igher

leve ls . The i r average t ra in ing t ime wa s ab ou t ha l f of the e l i te level ska te rs , bu t d id

not d i f fe r qua l i ta t ive ly ( i . e . v i r tua l ly a l l t ra in ing was ska t ing) .

Bone mass measurements

Tota l bo dy bone m ine ral dens i t y (TB BM D) wa s a s se s sed u s ing dua l- ene rgy x - ray

a b s o r p t i o m e t r y ( D X A ) o n a L u n a r I n s t r u m e n t s D P X - L ( L u n a r C o r p o r a t i o n ,

Madison , WI) . This scan a l so y ie lds va lues for sof t t i s sue , inc luding to ta l g rams of

fa t and lean t i ssue , perce nt bo dy fa t ( BF) and percent l ean t i s sue ( LT) . The prec i -

s i on e r ro r o f TB BM D ( r epea t ed s cans o f ind iv idua ls s epa ra t ed by ab ou t 1 week ) is

o f t he o rde r o f 1 ; p r ec i s ion e r ro r s f o r t o t a l g r ams o f f a t o r le an t i ssue a re som ewh a t

h igher (2-4 ) .

Each scan was ana lyzed and dens i t ies ca lcu la ted for head , a rm s , l egs , pe lv is , t runk ,

r ibs and sp ine . R el iab le re fe rence da ta do n ot ex is t for head o r r ibs . In addi t ion , head

dens it ie s c an be a f f ec t ed by t he p r e sence o f o r t hod on t i c app l i ances (wh ich s eve ra lpa r t i c i pan t s had ) and t he r e fo r e t he se two r eg ions a r e no t d i s cus sed fu r t he r .

Other measurements

All subjec ts were ques t io ned regard ing th e onse t (age a t fi r s t per iod ) and f requen-

cy o f menses ( cyc le s i n t he l a s t yea r ) and t he u se o f b i r th con t ro l med i ca t i ons (now,

ever , dura t ion of use) .

I n fo rma t ion r ega rd ing t r a i n ing pa t t e rn s was a l so co l l e c t ed f rom each a th l e t e ,

us ing ques t ionnai res spec i f ica l ly des igned to focus on the pr imary ac t iv i t i es of

ska te rs . Addi t iona l ques t ions regard ing dance , weight - t ra in ing and o ther ac t iv i t i es

were inc luded for a l l subjec ts . In addi t ion to the scans , an thropometr ic da ta werecol lec ted on the ska te rs . Su bsca pula r sk info ld th ickness , ca l f c i rcumference an d

b i ac romia l w id th we re measu red on each sub j ec t, u s ing s t anda rd me thods [5 ]. These

s i t e s we re s e l ec t ed ba sed on ou r pub l i shed work demons t r a t i ng i ndependen t and

s ignif icant assoc ia t ions be tw een each o f these measu rem ents an d ske le ta l dens i t ies

at mult iple s i tes [6] .

Ca l c ium in t ake w as a s ses sed u s ing a 14 -i tem fo od f r equency q ues t i onna i re wh ich

we have t e s t ed i n s eve ra l popu l a t i ons and shown to be r ep roduc ib l e and wh ich i s

mo de ra t e ly co r r e l a ted w i th 3 -day d i e t d i a r ie s [ 7 ] . M ean ca l c ium in t ake w as 976

mg /day , bu t it d id not cor re la te wi th B M D at any s ite ( -0 .12 < r < 0 .02) and i s

not fur ther d i scussed .

nalysis

Between -g roup compar i sons i n B M D w ere ma de u s ing unpa i r ed t - t es ts . Because

o f d i ff e r ences i n age and bod y we igh t , ad ju s t ed d i f f e rences i n B M D were ca l cu la t ed

f rom gene ra l li nea r mode l s wh ich i nc luded age , we igh t and w he the r o r n o t a p e r son

was a ska te r .

esults

Tab le 1 com pare s t he ska t e r s t o t he non -a th l e t i c g roup . The ska t e rs we re o lde r

(2 years ) ye t l igh te r , a l tho ugh no t s igni f icant ly so . The re w as a h ighly s igni f icant d i f-f e rence i n t he f r equency o f o l igo - and am enor rhea be tween the g roups , w i th 40 o f

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Table 2

Reg ress ion mod el s pred ic t ing ske le ta l dens i t i e s a t se lec ted s it es us ing age we ight

and skat ing status as predictors

Ske le t al s i te P red ic to r C oe f f i c i en t SE P-va lue

Ar ms Age 0 .032 0 .023 0 .16

Age x Age -0 .000 7 0 .0007 0 .32

W eigh t 0 .0023 0 .0004 0 .0001

Ska t ing 0 .0020 0 .0174 0 .91

Sp ine

Legs

Pelvis

Ag e 0.0768 0.0365 0.04

Age x Age -0 .0018 0 .0011 0 .10

W eig ht 0.0031 0.0006 0.0001

Sk at ing -0 .0001 0 .0279 0 .91

Age 0 .089 0 .037 0 .02Age x Age -0 .002 4 0 .0011 0 .03

W eig ht 0.0035 0.0006 0.0001

Sk at ing 0 .059 0 .027 0 .04

Ag e 0.081 0.036 0.03

Age x Age -0 .0022 0 .0011 0 .05

W eight 0 .0032 0 .0006 0 .0001

Ska t ing 0 .121 0 .028 0 .0001

t he ska t e r s hav ing some d i s t u rbance i n no rma l m ens t rua l pa t t e rn s (P < 0 .001 ) andthe ska t e rs expe ri enced mena rche on ave rage 1 yea r l a te r t han t he non - ska t e r s . BM D

was h igher am ong the ska te rs wi th d i f fe rences ranging be tw een 3 .8 (a rms ,

P = 0.12) and 14.1 (pelvis, P = 0.001), with genera l ly grea ter differenc es in the

lower pa r t o f t he ske l e ton .

Reg re s s ion mode l s we re then co ns t ruc t ed t o ad d re s s t he ques t i on o f whe the r t he r e

were s i gn if ic an t d i f fe r ences i n B M D a f t e r co r r ec t ion fo r t he a bove -no t ed d i f fe r ences

in age and weight ( see Table 2) . No s igni f icant e f fec t s of ska t ing were observed for

upp er bo dy s ites . Ho we ver , there remained a s ignif icant e f fec t of ska t ing on low er

bo dy dens i t ies ( leg and pe lv is ). A djus tm ents fo r d i f fe rences in percent b od y fa t , age

a t menarche or t ime s ince menarche , d id not a l te r these resu l t s . Table 3 shows the

Table 3

BMDs , ad ju s t ed fo r we igh t and age , i n ska t e r s and non -a th l e t i c compar i son g roup

Ske le t al s i te Ska te r s C on t ro l s P -va lue

Arm s B M D 0 .79 0 .79 n . s .

Spine BM D 1.03 1 .04 n .s .

Legs BM D 1.19 1 .14 0 .04Pelvis BM D 1.20 1 .08 0 .0001

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1 . 6

1.4

1.2

1 . 0

0 . 8

0 . 6

NON-ATHLETES, PELVIS

SKATERS, PELVIS

o o

o o

o

o

1.5-

1.4-

1.3-

1.2ci

m

1.1-tu-J

1.0 -~

0 . 9 =

0.8 -

0.7 -

1 1 1 1 1 1 1 1 1 8 1 1 2 110 11 12 13 14 15 16 17 1 19 20 1

AGE

B NON-ATHLETES, LEGS

SKATERS, LEGS

o

• o

oo o• ; o

@ • •

• : • • •

• • • •o

I I

22 23

I I I I I I I I I I I I I

10 11 12 13 14 15 16 17 18 19 20 21 22 23

AGE

Fig. i Values of A) pelvis and B) leg BM D by age for skaters dot ted l ine, open ci rcles , O) and

non -skaters sol id l ine, c losed ci rcles, O). Th e f i t ted l ines are the regression of B M D on age an d age 2,

determ ined separately for the skaters a nd no n-ath let ic controls .

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adjus ted BM D s for a rms , sp ine , l egs and pe lv is . A f te r ad jus tm ent for age and weigh t

(and/o r bo dy fa t ) , l eg and pe lv is B M D were s igni ficant ly h igher in the ska te rs

(5 .5 and 1 1 , respec tive ly). F igures la ,b show the ac tua l l eg and pe lv is B M D s for

the ska te rs and cont ro ls by age ( f i t t ed l ine i s the age and age-squared regress ion) .

At both s i tes the ska te rs appeared l i t t l e d i f fe ren t f rom the cont ro ls un t i l about age

15, a t which t ime the s lope for the ska te rs cont inues to increase whi le tha t for the

cont ro ls f la t tens .

We then examined f ac to r s wh ich migh t i n f l uence BMD among t he ska t e r s .

A l though t he ska t e r s w i th mens t rua l d i s t u rbances had l ower dens i t i e s ( abou t 2

depending on ske le ta l s i t e ) than normal ly mens t rua t ing ska te rs (pre-puber ta l sub-

jec t s were exc luded) , these d i f fe rences were not s ignif icant . W e were a l so no t ab le

to demons t ra te d i f fe rences be tween ska t ing d isc ip l ines (e .g . ind iv idua l vs . pa i r s

ska te r s) . How eve r , t he r e was a tr end t ow ard l ower BM Ds am ong t hose wh o t r a ined

mo re hou r s e ach week . Cor r e l a t i ons be tw een hou r s o f t r ai n ing and BM D were be -

tween r = -0 .40 and r = -0 .45 , depending on s i te . Af te r ad jus tments for age (and

age-squared ) there remaine d a s igni f icant nega t ive e ffec t of hours of t ra in ing on legand pe lv ic dens i t ies in the ska te rs , de sp i te the fac t tha t these were the tw o s i tes wi th

the grea tes t d i f fe rences favor ing the ska te rs . F ur th er a d jus tm ents fo r weight , percent

bod y f a t, mens t rua l f r eque ncy and o the r f a c to r s d id n o t subs t an t i a l ly d imin i sh t h is

assoc ia t ion .

iscussion

Thi s s t udy was unde r t aken t o add re s s conce rns r ega rd ing t he f r equency o f mens t rua l

i r regular i ti es am ong th i s gro up of e li t e a th le tes and the p rove n potent ia l o f such

dis turbances to d iminish ske le ta l in tegr i ty [4 ,8] . These ska te rs , however , demon-s t ra ted only smal l (ab ou t 2 ) nega t ive e f fec ts of m ens t rua l i r regular i t ies on the i r

ske le tons . Surpr i s ingly , ske le ta l dens i t ies among the ska te rs were s igni f icant ly

g rea t e r t han dens i ti e s in non - ska t e r s i n t he l ower pa r t o f the ske l e ton and no t

s igni ficant ly d i f fe ren t e l sewhere . A s imi la r l ack o f de t r imenta l e f fec t s in e l i te

oa r swo men wi th i r regu l a r m enses ha s been obse rved [9 ]. The l i ke li hood o f s el ec ti on

bias in observa t iona l s tud ies mus t a lways be cons idered , bu t in th i s case the d i f -

f e r ences be tween ska t e r s and con t ro l s a r e no t ev iden t among t he younge r ska t e r s ,

bu t s eem r a the r t o deve lop i n l a t e r ado l e scence and young adu l t hood . Th i s wou ld

sugges t tha t se lec t ion for ska te rs to be drawn f rom a po pu la t ion wi th grea te r ske le ta l

densi t ies is less l ikely, s ince al l of these skaters began training at very young ages.

The ska te rs a re smal le r and l igh te r than the non-ska te rs a t a l l ages .

The potent ia l mechanisms for increas ing ske le ta l dens i t ies in ice ska te rs inc lude

two prom inent poss ib il i ti es . The t ra in ing of these ska te rs is in tense and dom inated

by r epe t i ti ous p r ac t ic e o f e ach a spec t o f the i r p rog rams , i nc lud ing jum ps , sp in s and

other e lements . The jumps , which~are n ow the fo cus of com pet i t ive ska t ing , invo lve

cons ide r ab l e impac t upo n t he co mp le t i on o f e ach j ump , w i th d i s si pa t ion o f t he

ene rgy f rom such j um ps abso rbed m a in ly i n t he musc l e s o f t he uppe r l egs and h ip s.

S imilar ly , the t rans i t ion in to jum ps ( t ransfer r ing the energy of s t roking in to jum p-

ing ) a l so r equ i r e s t he u se o f t he se s ame musc l e g roups and may p roduce s imi l a r

forces on the ske le ton . S i te spec i fic pos i t ive e f fec t s on bo ne m ass in e l i t e a th le tes hav e

been r epo r t ed fo r t he fo r ea rms o f t enn is p l aye r s [ 10 ] and pa r a ll e l nega t ive e f f ec ts

have been obse rved i n hemip l eg i a , compar ing t he a f f ec t ed t o t he una f f ec t ed l imbs

[ i l l .

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I t is unc lea r w hy t he app a ren t ske le t a l bene fi t s o f ska ti ng d o n o t em erge un t il t he

mid - teens , s ince mo s t o f t he ska t e r s began com pe t ing a t qu i t e a yo ung age . A l though

th is is reassur ing in te rm s o f the ro le o f se lec t ion b ias in these da ta , one co uld

specu la t e t ha t t he bene f i t s o f ska t i ng on ly acc rue d u r ing t he r ap id g ro wth p roces s ,

pe rhaps by ex t end ing t he l eng th o f t ime du r ing wh ich ske le t a l mode l l ing occu r s . I f

i n tense ac t i v it y a f fec t s bone mass by s l owing r emode l i ng , t hen con t i nued ac t iv i t y a t

th i s l eve l m ay be necessary to m ain ta in the advan tages n oted . I t is a l so not c lear why

t h e r e w a s a t e n d e n c y t o w a r d l o w e r B M D s a m o n g t h o s e w h o s p e n t t h e g r e a t e s t

am oun t o f t ime t r a ining , a l t hough t h is l evel o f t ra i n ing m ay be a s soc i a t ed w i th more

subt le d i s turbances in gonadal func t ion [12] , o r a l te ra t ions in o ther sys tems which

we cou ld no t measu re .

The absence o f a s i gni fi c ant de t r imen t a l e f f ec t o f d i s t u rbed m ens t rua l p a t t e rn s o n

bon e m ass was surpr is ing . Th e smal l (ab ou t 2 ) def ic i t in those wi th mens t rua l

i r regular i ti es w ou ld not g enera l ly be cause for c linica l conc ern a nd sugges ts tha t in-

tense weight -bear ing ac t iv i t i es may d iminish the nega t ive e f fec t s of these i r regular -

i ti es on bone m ass. H owev e r , c au t i on i n th i s r ega rd i s r equ i red . Few w om en , o the rthan profess iona l a th le tes , have ac t iv i ty leve ls approaching those observed here .

Addi t iona l ly , s ta t i s t i ca l power to de tec t modes t d i f fe rences in BMD (e .g . 0 .05

g / cm 2 ) va r i ed cons ide r ab ly . A l thou gh t he r e was g r ea te r t han 70 pow er t o de t ec t

d i f fe r ences be tween amenor rhe i c ska t e r s and con t ro l s , t he r e was on ly 40 -50 pow er

to de tec t such d i ffe rences wi th in the sk a t ing group . M oreo ver , the f requ ency, in tens i -

t y and na tu r e o f t he ac t iv i ti e s o f the se ska t e r s a r e un ique and a r e ce r t a in ly no t pos s i-

b l e f o r t he va s t ma jo r i t y o f women . F ina l l y , we have obse rved ve ry l ow ske l e t a l

dens i t ies in o ther female a th le tes whose ac t iv i ty pa t te rns , whi le ex t remely in tense ,

d i f fe r in the ex ten t o f weigh t -bear ing (e.g. e l i te t r ia th le tes ), sugges t ing tha t there m ay

be charac te r i s t ics unique to ska t ing which y ie ld the apparent subs tan t ia l benef i t s tosom e ske le ta l si tes. A l thou gh these da ta a re reassur ing for th i s grou p of e l it e a th le tes ,

pers i s ten t mens t rua l i r regular i t i es in those wi th more modera te exerc i se habi t s

should s t i l l be cons idered a cause for concern and c l in ica l a t ten t ion .

cknowledgements

W e w o u l d l ik e t o a c k n o w l e d g e t h e c o o p e r a t i o n o f th e I n d i a n a W o r l d S k a t i ng

Academy and t he Un i t ed S t a t e s F igu re Ska t i ng Assoc i a t i on fo r t he i r a s s i s t ance i n

fac i l it a t ing the par t ic ipa t ion of the ska te rs in th i s s tudy . This wor k i s sup por te d b y

AG 05793 US Publ ic Heal th Serv ice .

References

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