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Associa ion be ween low- equency ul asound and hip ac u es - compa ison wi h
DXA-based BMD
Mää ä, Mikko; Moilanen, Pe o; Timonen, Jussi; Pulkkinen, Pasi; Ko pelainen, Raija;
Jämsä, Timo
Mää ä, M., Moilanen, P., Timonen, J., Pulkkinen, P., Ko pelainen, R., & Jämsä, T.
(2014). Associa ion be ween low- equency ul asound and hip ac u es -
compa ison wi h DXA-based BMD. BMC Musculoskele al Diso de s, 15(208).
h ps://doi.o g/10.1186/1471-2474-15-208
2014
RESEARCH ARTICLE Open Access
Associa ion be ween low- equency ul asound
and hip ac u es −compa ison wi h DXA-based
BMD
Mikko Mää ä
1,2*
, Pe o Moilanen
3
, Jussi Timonen
3
, Pasi Pulkkinen
1
, Raija Ko pelainen
1,4,5,6
and Timo Jämsä
1,6,7
Abs ac
Backg ound: New me hods o diagnosing os eopo osis and e alua ing ac u e isk a e being de eloped. We aim
o s udy he associa ion be ween low- equency (LF) axial ansmission ul asound and hip ac u e isk in a
popula ion-based sample o olde women.
Me hods: The s udy popula ion consis ed o 490 communi y-dwelling women (78–82 yea s). Ul asound eloci y
(V
LF
) a mid- ibia was measu ed in 2006 using a low- equency scanning axial ansmission de ice. Bone mine al
densi y (BMD) a p oximal emu measu ed using dual-ene gy x- ay abso p iome y (DXA) was used as he e e ence
me hod. The ac u e his o y o he pa icipan s was collec ed om Decembe 1997 un il he end o 2010.
Li es yle- ela ed isk ac o s and mobili y we e assessed a 1997.
Resul s: Du ing he o al ollow-up pe iod (1997–2010), 130 women had one o mo e ac u es, and 20 o hem
had a hip ac u e. Low V
LF
( he lowes qua ile) was associa ed wi h inc eased hip ac u e isk when compa ed
wi h V
LF
in he no mal ange (Odds a io, OR = 3.3, 95% con idence in e al (CI) 1.3-8.4). Howe e , V
LF
was no
ela ed o ac u e isk when all bone si es we e conside ed. Os eopo o ic emo al neck BMD was associa ed wi h
highe isk o a hip ac u e (OR = 4.1, 95% CI 1.6-10.5) and highe isk o any ac u e (OR = 2.4, 95% CI 1.6-3.8)
compa ed o he non-os eopo o ic emo al neck BMD. Dec eased V
LF
emained a signi ican isk ac o o hip
ac u e when combined wi h li es yle- ela ed isk ac o s (OR = 3.3, 95% CI 1.2-9.0).
Conclusion: Low V
LF
was associa ed wi h hip ac u e isk in olde women e en when combined wi h
li es yle- ela ed isk ac o s. Fu he de elopmen o he me hod is needed o imp o e he measu emen p ecision
and o con i m he esul s.
Keywo ds: Quan i a i e ul asound, Speed o sound, Os eopo osis, Hip ac u e, Co ical bone
Backg ound
Os eopo o ic ac u es possess a signi ican public heal h
p oblem ha is inc easing due o aging popula ion. A
he momen , he golden s anda d used in ac u e isk
assessmen is bone mine al densi y (BMD) measu emen s
using dual ene gy x- ay abso p iome y (DXA). Recen ly,
Wo ld Heal h O ganiza ion (WHO) in oduced FRAX®, a
ac u e isk calcula o ha combines easily ob ained clin-
ical in o ma ion and DXA-based emo al neck BMD, i
a ailable, o es ima e he 10-yea os eopo o ic ac u e
p obabili y [1].
Quan i a i e ul asound (QUS) has aised in e es as
an al e na i e me hod o x- ay-based imaging o meas-
u ing bone s a us. The e is a numbe o di e en QUS
me hods ha ha e been used o assess bone s a us and
o e alua e ac u e isk [2]. The ad an ages o ul asound
include a ela i ely low cos and a po able echnique wi h
no ionizing adia ion. The esul s o QUS measu emen s
ha e been shown o be associa ed wi h ac u e isk [3]. A
ques ion has a isen whe he QUS pa ame e s can se e
as a su oga e o DXA-based BMD o imp o e FRAX®
es ima e [4].
* Co espondence: [email p o ec ed]
1
Depa men o Medical Technology, Uni e si y o Oulu, Ins i u e o
Biomedicine, PO Box 5000, FI-90014 Oulu, Finland
2
In o ech Oulu, Uni e si y o Oulu, Oulu, Finland
Full lis o au ho in o ma ion is a ailable a he end o he a icle
© 2014 Mää ä e al.; licensee BioMed Cen al L d. This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e
Commons A ibu ion License (h p://c ea i ecommons.o g/licenses/by/2.0), which pe mi s un es ic ed use, dis ibu ion, and
ep oduc ion in any medium, p o ided he o iginal wo k is p ope ly c edi ed.
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208
h p://www.biomedcen al.com/1471-2474/15/208
A no el low- equency (LF) axial ansmission QUS
me hod o assessing he p ope ies o co ical bone has
been shown o e lec bone densi y and co ical hick-
ness [5-7]. A ela ionship be ween he LF ibial eloci y
(V
LF
) and geome y o p oximal emu in olde women
has also been sugges ed [8]. Howe e , he sui abili y o he
me hod o indi idual ac u e isk assessmen has no ye
been es ablished.
In his s udy we e alua ed he associa ion be ween he
LF axial ansmission ul asound me hod and ac u es
in a popula ion-based sample o olde women, using he
s anda d DXA as he e e ence me hod. We hypo he-
sized ha dec eased ul asound eloci y measu ed on
ibia is associa ed wi h inc eased hip ac u e isk in eld-
e ly emales. In ou p e ious popula ion based p ospec i e
s udy we assessed li e-s yle ela ed de e minan s o hip
ac u e in elde ly emales [9]. He e we analyzed how he
combina ion o low- equency ul asound and p e iously
de e mined li es yle- ela ed ac o s a e ela ed o he isk
o hip ac u e.
Me hods
Subjec s and clinical assessmen
The s udy popula ion consis ed o 490 women bo n be-
ween 1924 and 1927, o iginally ec ui ed in 1997 as a
popula ion-based coho o s udy he isk ac o s o
os eopo osis and ac u es [10]. All hose s ill ali e belong-
ing o he o iginal coho we e in i ed o clinical measu e-
men s in 2006. A o al o 618 women a ended hese
measu emen s, and 490 we e measu ed using quan i a i e
ul asound. The ac u e his o y be ween Decembe 1,
1997 and Decembe 31, 2010 was collec ed om hospi al
discha ge egis e s. The ac u es we e con i med manu-
ally om medical eco ds o a oid he bias o eco ding
mul iple hospi aliza ions due o a single ac u e. Heal h
and li es yle in o ma ion, including medical his o y, age a
menopause, smoking habi s, alcohol and co ee consump-
ion, physical ac i i y and mobili y, calcium and i amin D
in akes, and ac u e his o y was collec ed a s udy base-
line in 1997 using sel -adminis a i e ques ionnai es and
in e iews. The assessmen o unc ional mobili y a base-
line was done using he “Timed Up & Go”(TUG) es
[11]. All subjec s ga e a w i en in o med consen and he
s udy p o ocol was app o ed by he E hics Commi ee o
he No he n Os obo hnia Hospi al Dis ic . The s udy
was done in acco dance wi h he Decla a ion o Helsinki.
Quan i a i e ul asound measu emen s
The speed o sound was eco ded in he medial mid-sha
o he le ibia using a scanning low- equency (LF) axial
ansmission de ice. The p inciple o he de ice and he
measu emen se up has been published p e iously [7,8].
In b ie , wo sepa a e ansduce s (
c
= 200 kHz) moun ed
on a ail scanned a 30 mm dis ance. The ime o ligh o
he i s a i ing signal (FAS) was de e mined using he
i s maximum. The appa en eloci y o he FAS (V
LF
)
was de e mined by measu ing he ime o ligh o a
numbe o sou ce- ecei e dis ances. The p ecision e o
was cha ac e ized by CV ms which was 3.2%. The s an-
da dized coe icien o a ia ion (SCV) [12] o he me hod
was 6.6%. Due o he lack o es ablished e e ence popula-
ion da a, we used he p esen s udy popula ion o de ine
he ange o SCV.
DXA measu emen s
A Hologic DXA de ice (Delphi QDR se ies, Hologic,
Bed o d, MA, USA) was used o ge he e e ence da a.
S anda d an e opos e io posi ioning was used o meas-
u e he emo al neck bone mine al densi y (BMD) o
he le p oximal emu .
S a is ical analysis
The subjec s o he s udy we e di ided in o h ee g oups
based on hei ac u e his o y (Figu e 1): a) women wi h-
ou ac u es (NF, con ols), b) women wi h any ac u e
(Fx), and c) women wi h a hip ac u e (Hip Fx). All he
hip ac u e pa ien s we e also included in g oup (b). The
ac u e da a o h ee di e en ime pe iods we e analyzed:
a) om he beginning o he ollow-up pe iod un il he
ime o bone measu emen s (1997–2006), b) om he
ime o he bone measu emen s un il he end o he
ollow-up pe iod (2006–2010), and c) he whole ollow-up
pe iod (1997–2010). The women wi h ac u es we e
compa ed o hose wi hou ac u es. Since he da a we e
no mally dis ibu ed he independen samples - es was
used o analyze he s a is ical signi icance o he di e -
ences be ween he NF, Fx, and Hip Fx g oups. The s udy
subjec s we e also classi ied in o no mal, os eopenic, and
os eopo o ic acco ding o hei emo al neck BMD T-
sco e in acco dance wi h he WHO de ini ion [13]. Due o
he lack o an es ablished e e ence popula ion, T-sco es
could no be calcula ed o low- equency ul asound el-
oci y (V
LF
). Thus, V
LF
esul s we e di ided in o h ee
g oups based on qua iles wi hin he s udy popula ion: a)
low V
LF
(0-25%), b) mode a e V
LF
(25-50% and 50-75%
combined), and c) high V
LF
(75-100%). C oss abula ion
and he χ
2
es we e used o compa e he dis ibu ion o
he subjec s wi h ac u es and hose wi hou ac u es
wi hin hese g oups. To u he analyze he s a is ical sig-
ni icance o he associa ion o bone measu emen esul s
(QUS/DXA) wi h he ac u e isk, a mul i a ia e logis ic
eg ession analysis was used. The esul s o hose analyses
a e epo ed as he odds a ios (OR) and 95% con idence
in e als (CI). The imaging modali y (QUS/DXA) used
was included in he model and he o wa d s epwise (like-
lihood a io) me hod was used o o m he inal models.
All models we e adjus ed wi h age and BMI. Fo he ac-
u es ha occu ed a e he measu emen s in 2006, he
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208 Page 2 o 8
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p edic i e abili y o each bone measu emen alue was
assessed using he Cox p opo ional haza ds model and
he co esponding haza d a ios (HR), and he 95% CIs
we e calcula ed. A simila p o ocol o logis ic eg ession
wasused.Inaddi ion,p e ious ac u es(1997–2006)
(yes, no) was added o models as co a ia es. The ollow-
up ime be ween he measu emen ime and he ime o
he i s ac u e, dea h, o end o he ollow-up pe iod
was eco ded. Logis ic eg ession models we e also
calcula ed o analyze he e ec o combining V
LF
and
p e iously de e mined [9] li es yle- ela ed isk ac o s
o hip ac u e. In ou p e ious popula ion based co-
ho s udy BMI, unc ional mobili y, physical ac i i y,
hype ension, co ee consump ion, and daily smoking
p edic ed hip ac u es in 1222 old women. These ac-
o s we e used as a co a ia es o de e mine he bes i
model o he cu en subpopula ion wi h ul asound
and DXA measu emen s.
Figu e 1 Conso cha . Numbe o women wi h and wi hou ac u es a di e en imepoin s.
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208 Page 3 o 8
h p://www.biomedcen al.com/1471-2474/15/208
Table 1 Dis ibu ion o ac u es (n (%)) acco ding o he ICD-10 code wi h selec ed subdi isions in a popula ion-based
sample o olde women (n = 490)
1997–2006 2006–2010 1997–2010
M80 Os eopo osis wi h pa hological ac u e 2 (2.6) 2 (1.1)
S12 F ac u e o neck 1 (1.3) 1 (0.6)
S22 F ac u e o ib(s), s e num and ho acic spine 3 (3.1) 3 (3.9) 6 (3.4)
S32 F ac u e o lumba spine and pel is
S32.0 F ac u e o lumba e eb a 9 (11.8) 9 (5.2)
O he 3 (3.1) 4 (5.3) 7 (4.0)
S42 F ac u e o shoulde and uppe a m 11 (11.2) 6 (7.9) 17 (9.8)
S52 F ac u e o o ea m
S52.5 F ac u e o lowe end o adius 29 (29.6) 22 (28.9) 51 (29.3)
O he 5 (5.1) 1 (1.3) 6 (3.4)
S62 F ac u e a w is and hand le el 7 (7.1) 5 (6.6) 12 (6.9)
S72 F ac u e o emu
S72.0 F ac u e o neck o emu 4 (4.1) 7 (9.2) 11 (6.3)
S72.1 Pe ochan e ic ac u e 1 (1.0) 4 (5.3) 5 (2.9)
S72.2 Sub ochan e ic ac u e 4 (4.1) 4 (2.3)
O he 3 (3.1) 6 (7.9) 9 (5.2)
S82 F ac u e o lowe leg, including ankle 26 (26.5) 5 (6.6) 31 (17.8)
S92 F ac u e o oo , excep ankle 2 (2.0) 1 (1.3) 3 (1.7)
To al numbe o ac u es 98 (100) 76 (100) 174 (100)
ICD-10 = In e na ional Classi ica ion o Diseases, 10
h
e ision. Time pe iods ep esen p e ious ac u es (1997–2006) and u u e ac u es (2006–2010) wi h espec
o he bone measu emen s, and all ac u es du ing he ollow-up pe iod (1997–2010).
Table 2 Cha ac e is ics o he women wi h di e en ac u e s a us (NF, Fx, and Hip Fx) in di e en ime pe iods
(1997–2006, 2006–2010, and 1997–2010) a he ime o he measu emen s (2006) (n = 490)
NF Fx 1997-2010 Hip Fx 1997-2010
n =360 n = 130 n = 20
Fx 1997-2006 Fx 2006-2010 Hip Fx 1997-2006 Hip Fx 2006-2010
n=81 n=61 n=9 n=11
Age [yea s] 79.9 (1.2) 80.0 (1.2) 80.0 (1.3)
79.7 (1.2) 80.3 (1.1)
*
79.3 (1.4) 80.5 (0.9)
Weigh [kg] 67.7 (11.3) 67.8 (12.2) 69.8 (15.7)
69.5 (12.3) 65.8 (12.2) 75.7 (10.2)
*
65.0 (18.2)
Heigh [cm] 155.2 (5.4) 155.6 (5.8) 158.9 (7.2)
*
156.6 (5.4)
*
154.5 (6.4) 160.7 (4.4)
*
157.4 (8.8)
BMI [kg/m
2
] 28.1 (4.5) 28.0 (4.7) 27.4 (4.6)
28.4 (4.8) 27.5 (4.6) 29.3 (3.6) 25.9 (4.9)
V
LF
[m/s] 3583 (193) 3547 (200) 3515 (245)
3534 (204)
*
3564 (203) 3500 (291) 3527 (215)
Femo al neck BMD [g/cm
2
] 0.654 (0.102) 0.606 (0.083)
*
0.589 (0.102)
*
0.609 (0.078)
*
0.605 (0.096)
*
0.611 (0.089) 0.570 (0.112)
*
Values a e Mean (SD).
*
Independen samples - es p- alue < 0.05 when compa ed o NF g oup.
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208 Page 4 o 8
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S a is ical analyses we e done using SPSS o Win-
dows (Release 18.0, SPSS Inc., Chicago, IL, USA). In all
es s, p- alues less han 0.05 we e conside ed s a is i-
cally signi ican .
Resul s
Du ing he i s ollow-up pe iod (1997–2006), 98 ac-
u es occu ed in 81 women (Figu e 1, Table 1). Be ween
2006 and 2010, 61 subjec s sus ained ac u es; in o al
76 di e en ac u es occu ed. Al oge he , be ween he
yea s 1997 and 2010, 174 di e en ac u es occu ed in
130 subjec s. W is ac u e was he mos common ac-
u e (n = 51). The e we e 9 hip ac u es be ween 1997
and 2006, and 11 hip ac u es a e he 2006 measu e-
men s, o aling in 20 hip ac u es du ing he whole
ollow-up pe iod. Thi y- i e subjec s died du ing he
ollow-up pe iod.
The cha ac e is ics o di e en ac u e g oups a e shown
in Table 2. The women wi h a hip ac u e we e alle han
he women wi hou ac u es (p < 0.05). Those wi h a p e-
ious ac u e (1997–2006) had a lowe V
LF
han he ones
wi hou ac u es (p < 0.05). Subjec s who sus ained a
ac u e du ing he ollow-up pe iod had a lowe emo al
neck BMD han hose in he NF g oup (p < 0.05), excep
when compa ing he Hip Fx 1997–2006 and NF g oups.
Di e ences be ween dis ibu ions in he NF and Hip
Fx g oups we e obse ed in bo h V
LF
and emo al neck
BMD (p < 0.05) (Table 3). Also, he e was a di e ence in
he dis ibu ion o subjec s based on emo al neck BMD
be ween he Fx and NF g oups.
Based on he eg ession analysis, low V
LF
was no as-
socia ed wi h p e ious ac u es (1997–2006) o wi h he
ac u es ha occu ed a e he measu emen s (2006–
2010) (Table 4). Dec eased emo al neck BMD, howe e ,
was associa ed wi h inc eased ac u e isk in all ollow-
up pe iods; es ima ed isks (odds and haza d a ios) a -
ied be ween 1.8 and 2.5 compa ed o he women wi h
emo al neck T-sco e > −2.5.
Dec eased V
LF
was associa ed wi h an inc eased isk o
hip ac u e occu ed be o e he measu emen s (1997–
2006) (OR = 6.3; Table 5). Addi ionally, ac oss he whole
ollow-up pe iod (1997–2010), low V
LF
was associa ed
wi h highe isk o hip ac u e compa ed o mode a e
o high V
LF
(OR = 3.3). An os eopo o ic emo al neck
BMD p edic ed hip ac u es a e he measu emen s
(2006–2010) wi h a haza d a io (HR) o 4.8 (95% CI
1.4-16.6) o subjec s wi h a T-sco e ≤−2.5 compa ed o
he women wi h no mal o os eopenic T-sco e. Low
emo al neck BMD was also associa ed wi h an inc eased
isk o hip ac u e (OR = 4.1, 95% CI 1.6-10.5) du ing
he whole ollow-up pe iod (1997–2010) compa ed o
women wi h no mal o os eopenic emo al neck BMD.
When V
LF
was combined wi h p e iously assessed [9]
hip ac u e isk ac o s eg ession model o he same
popula ion (Table 6), he inal model included V
LF
, low
physical ac i i y, and impai ed unc ional mobili y (p =
0.001, Table 6), V
LF
being he s onges independen ac-
o o hip ac u e (OR = 3.3, 95% CI 1.2–9.0). Femo al
neck BMD did no each s a is ical signi icance when in-
cluded in he eg ession analyses along wi h li es yle-
ela ed isk ac o s.
Table 3 The dis ibu ion o women wi h and wi hou a
ac u e and hip ac u e acco ding o he V
LF
and BMD
alues
NF Fx 1997–2010
Hip Fx
1997–2010
(n = 360) (n = 130) (n = 20)
V
LF
Highes 25% 101 (28) 24 (18) 5 (25)
*
25% o 75% 170 (47) 69 (53) 5 (25)
Lowes 25% 89 (25) 37 (28) 10 (50)
Femo al
neck BMD
No mal 73 (20) 11 (8)
*
2 (10)
*
Os eopenic 206 (57) 65 (50) 8 (40)
Os eopo o ic 81 (23) 54 (42) 10 (50)
Values a e n (%).
*
Dis ibu ion o he g oup is di e en han ha o he NF
g oup (p- alue o χ
2
es < 0.05).
Table 4 Associa ion o low V
LF
and os eopo o ic emo al neck BMD wi h ac u es ha occu ed du ing di e en
ollow-up pe iods
Fx 1997-2006 Fx 2006-2010 Fx 1997-2010
NF n = 409, Fx n = 81 NF n = 429, Fx n = 61 NF n = 334, Fx n = 121*
n OR (95% CI) p HR (95% CI) p OR (95% CI) p
V
LF
Mode a e o high (25-100%) 364
Low (0-25%) 126 1.6 (0.9 - 2.6) 0.088 0.8 (0.4 - 1.4) 0.359 1.3 (0.8 - 2.0) 0.326
Femo al neck BMD T-sco e > −2.5 355
T-sco e ≤−2.5 135 1.8 (1.1 - 3.0) 0.019 2.4 (1.4 - 3.9) 0.001 2.5 (1.6 - 3.9) <0.001
All eg ession models we e adjus ed by age and BMI. In Cox eg ession p e ious ac u e (du ing 1997–2006) was also used as a co a ia e. NF = non- ac u ed
g oup, Fx = ac u ed g oup, n = numbe o subjec s, OR = odds a io o logis ic eg ession, HR = haza d a io o Cox eg ession, CI = con idence in e al, p = p- alue
o he co a ia e in he model. *Subjec s who died du ing he ollow-up we e excluded (NF n = 26, Fx n = 9).
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208 Page 5 o 8
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Discussion
In his popula ion-based s udy, we used a low- equency
ul asound scanne o assess he associa ion be ween
dec eased ul asound eloci y and ac u e isk. To ou
knowledge, his is he i s ime ha low- equency axial
ansmission ul asound is being used in a popula ion-
based coho o olde women. The epo ed esul s show
ha dec eased ul asound eloci y (V
LF
) was associa ed
wi h highe isk o hip ac u e compa ed o mode a e o
high V
LF
. DXA and LF ul asound yielded simila esul s
when compa ing he hip ac u e and non- ac u e g oups.
Ou indings a e in line wi h ea lie s udies on he
ac u e-disc imina ion abili y o simila axial ansmis-
sion ul asound de ices. Using he Omnisense (Sunligh ,
BeamMed L d, Pe ah Tik a, Is ael) de ice, ope a ing a a
cen e equency o 1.25 MHz, Nguyen e al. [14] epo ed
ha dec eased ibial SOS is associa ed wi h inc eased ac-
u e isk independen ly o BMD and age wi h an odds a-
io (OR) o 1.75. The co esponding OR as de e mined o
he emo al neck BMD he e was 2.11. Damilakis e al. [15]
ound no di e ence using he Omnisense de ice in he
ibial SOS o heal hy subjec s and subjec s wi h os eopo -
o ic ac u e. Ne e heless, hey epo ed inc eased os eo-
po o ic ac u e ORs o ul asound measu emen s on he
adius and phalanx (ORs be ween 1.7 and 2.7). In o he
s udies wi h an Omnisense de ice, SOS measu ed on he
adius has been shown o disc imina e subjec s wi h hip
ac u e om con ols wi h no ac u es (ORs a ying be-
ween 1.9 and 2.7) [16-18]. Ano he axial ansmission
QUS de ice, My iad Soundscan (My iad Ul asound sys-
ems, Is ael) uses a cen e equency o 250 kHz which is
close o ha used in his s udy. Using his de ice,
S egman e al. [19] epo ed a low-ene gy appendicula
ac u e OR o 1.4 o he ibial SOS. This obse a ion is
in good ag eemen wi h he p esen s udy, whe e we
ound a simila end in he e ospec i e pa o he s udy.
Auga e al. [20] ound an inc eased OR o 1.7 o he ib-
ial SOS o subjec s who sus ained hip ac u e compa ed
o non- ac u e con ols. The co esponding OR o he
emo al neck BMD was 3.5 in hei s udy. This SOS OR is
somewha lowe han hose obse ed in he p esen s udy
o hip ac u es. Also, Talman e al. [21] s udied he ac-
u e disc imina ion abili y o a 1 MHz bidi ec ional ul a-
sonome e . They epo ed a ac u e OR o 1.8 o he
adius SOS and o 2.1 o he emo al neck BMD. Di ec
compa ison be ween he ul asound me hods used is
di icul due o di e ences in he ul asound me hod-
ology and measu emen se up. Also, he bone si e and
ype o ac u e, as well as he s udy popula ions, a ec
he esul s. Howe e , he majo i y o he s udies imply
ha axial ansmission ul asound is capable o asses-
sing ac u e isk.
Some s udies ha e assessed he combining clinical isk
ac o s and QUS pa ame e s [22-24]. In he cu en s udy
low V
LF
emained a signi ican isk ac o o hip ac u e
when included in he li es yle- ela ed isk ac o model ob-
se ed in ou p e ious s udy wi h he same popula ion [9].
Howe e , he li es yle- ela ed isk ac o s we e collec ed a
baseline whe eas QUS measu emen s we e made a eigh
Table 5 Associa ion o low V
LF
and os eopo o ic emo al neck BMD wi h hip ac u es ha occu ed du ing di e en
ollow-up pe iods
Hip Fx 1997-2006 Hip Fx 2006-2010 Hip Fx 1997-2010
NF n = 409, Hip Fx n = 9 NF n = 429, Hip Fx n = 11 NF n = 334, Hip Fx n = 19*
n OR (95% CI) p n HR (95% CI) p n OR (95% CI) p
V
LF
Mode a e o high (25-100%) 313 324 260
Low (0-25%) 105 6.3 (1.5 - 25.5) 0.010 116 1.7 (0.5 - 5.7) 0.415 93 3.3 (1.3 - 8.4) 0.012
Femo al neck BMD T-sco e > −2.5 311 325 267
T-sco e ≤−2.5 107 1.5 (0.4 - 6.0) 0.593 115 4.8 (1.4 - 16.6) 0.013 86 4.1 (1.6 –10.5) 0.003
All eg ession models we e adjus ed by age and BMI. In Cox eg ession p e ious ac u e (du ing 1997–2006) was also used as a co a ia e. NF = non- ac u ed
g oup, Hip Fx = hip ac u e g oup, n = numbe o subjec s, OR = odds a io o logis ic eg ession, HR = haza d a io o Cox eg ession, CI = con idence in e al,
p = p- alue o he co a ia e in he model. *Subjec s who died du ing he ollow-up we e excluded (NF n = 26, Hip Fx n = 1).
Table 6 Logis ic eg ession models wi hou and wi h V
LF
o ha ing a hip ac u e in a popula ion-based sample o
olde women
OR (95% CI) p- alue
Li es yle- ela ed isk ac o s
1
0.002
*
TUG ≥11 s s. less ( e e en ) 3.4 (1.2 - 9.9) 0.026
Low PA s. mode a e o high ( e e en ) 2.8 (1.0 - 7.5) 0.046
Co ee consump ion > 3 cups/day s.
less ( e e en )
0.3 (0.1 - 1.0) 0.051
Li es yle- ela ed isk ac o s and V
LF2
0.001
*
Low V
LF
(0-25%) s. Mode a e o high
(25-100%) ( e e en )
3.3 (1.2 - 9.0) 0.018
Low PA s. mode a e o high ( e e en ) 3.1 (1.1 - 8.5) 0.028
TUG ≥11 s s. less ( e e en ) 3.1 (1.0 - 8.9) 0.042
Odds a ios (OR) a e calcula ed compa ed o he NF g oup. TUG “Timed Up &
Go” es , PA physical ac i i y, CI con idence in e al. The numbe o subjec s in
he analyses was Hip Fx n = 18, NF n = 296.
1
Age, BMI, TUG, PA, hype ension,
co ee consump ion, and smoking we e included in he analysis o o m he
bes model,
2
The bes model a e including V
LF
in he analysis,
*
p- alue o
he ull model.
Mää ä e al. BMC Musculoskele al Diso de s 2014, 15:208 Page 6 o 8
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yea s om baseline. Thus, he esul s need o be con-
i med in u u e p ospec i e s udies.
In he p esen s udy ul asound eloci y was measu ed a
mid- ibia. E en hough os eopo osis is a sys emic disease,
he deg ee o changes in bone s uc u e a ies be ween
bone si es. In weigh -bea ing si es (e.g. he ibia) bone loss
is no as big as in non-weigh -bea ing si es (e.g. he adius
and phalanx) [25]. Thus, e en i he ibia is an easily ac-
cessible si e o axial ul asound measu emen s, i may no
be hemos esponsi esi e oos eopo o icchanges.Re-
cen ly, we ha e epo ed ha LF axial- ansmission ul a-
sound in he adius is able o e ospec i ely disc imina e
pos menopausal women wi h ac u es om age-ma ched
con ols wi h no ac u es using an imp o ed e sion o
he LF ul asound de ice used he e [26].
The s eng h o he p esen s udy was he use o a
popula ion-based coho o olde women. The o he
s eng h was he ela i ely long ollow-up ime be o e
and a e he bone measu emen s. Howe e , his s udy
also had some limi a ions. One majo limi a ion was he
limi ed measu emen p ecision o he cu en p o o ype
de ice. The bulky mechanical scanning se up limi s he
posi ioning accu acy and does no enable p ope co ec-
ion o he impac s o o e lying so issue [8]. As a e-
sul , he in i o p ecision (CV
ms
)waslimi ed.Du ing
he ollow-up pe iod o he s udy, signi ican mechanical
imp o emen s we e implemen ed in he de ice, and a
CV o 0.5% could be achie ed wi h he la es de ice e -
sion [5,26]. Ob iously, his aluable in o ma ion a ailable
a e he de ice imp o emen canno e ospec i ely im-
p o e he quali y o he esul s p esen ed he e. The o he
limi a ion is he e ospec i e na u e o he s udy. I is
possible ha he ac u e e en s be o e he measu emen s
caused he changes in bone p ope ies (e.g. ia al e ed
loading condi ions) and a ec ed on ou come o he mea-
su emen . Also, he numbe o hip ac u es was ela i ely
low, which signi ican ly limi ed he s a is ical eliabili y o
he esul s. Addi ionally, a mino limi a ion was he lack
o e e ence da a o young and heal hy popula ion, which
disabled he de e mina ion o he T-sco e. Ins ead, we
used qua iles o de ine he subjec s wi h low V
LF
alues.
Conclusions
In conclusion, dec eased low- equency ul asound e-
loci y was associa ed o inc eased hip ac u e isk despi e
he limi ed measu emen p ecision. The esul s epo ed
he e can be used o u he imp o e he measu emen
p ecision o he me hod so as o eliably p edic u u e
ac u es. To his end ca e ully planned ollow-up s udies
a e needed.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Au ho s’con ibu ions
MM pa icipa ed in he ac u e da a collec ion, ca ied ou he main
analyses, and d a ed he manusc ip . PM pa icipa ed in he analyses and
in e p e a ion o ul asound da a and manusc ip w i ing. JT and PP made
a con ibu ion o he design o he s udy and e ising he manusc ip .
RK and TJ pa icipa ed in s udy concep ion and design, da a in e p e a ion
and made subs an ial con ibu ions o he manusc ip . RK also pa icipa ed
signi ican ly o collec ion o li es yle- ela ed isk ac o s da a. All au ho s ha e
ead, e ised, and gi en hei inal app o al o he e sion o be published.
Acknowledgemen s
The wo k done is a pa o he Os eopo o ic F ac u e Risk s udy suppo ed
by he Finnish Funding Agency o Technology and Inno a ion (Tekes,
p ojec s no. 40463/05, 40403/06). The wo k was also suppo ed by he
Academy o Finland. MM was suppo ed by Tauno Tönning Founda ion
and Finnish Cul u al Founda ion.
Au ho de ails
1
Depa men o Medical Technology, Uni e si y o Oulu, Ins i u e o
Biomedicine, PO Box 5000, FI-90014 Oulu, Finland.
2
In o ech Oulu, Uni e si y
o Oulu, Oulu, Finland.
3
Depa men o Physics, Uni e si y o Jy äskylä,
Jy äskylä, Finland.
4
Depa men o Spo s and Exe cise Medicine, Oulu
Deaconess Ins i u e, Oulu, Finland.
5
Ins i u e o Heal h Sciences, Uni e si y o
Oulu, Oulu, Finland.
6
Medical Resea ch Cen e Oulu, Oulu Uni e si y Hospi al
and Uni e si y o Oulu, Oulu, Finland.
7
Depa men o Diagnos ic Radiology,
Oulu Uni e si y Hospi al, Oulu, Finland.
Recei ed: 28 Augus 2013 Accep ed: 10 June 2014
Published: 16 June 2014
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doi:10.1186/1471-2474-15-208
Ci e his a icle as: Mää ä e al.:Associa ion be ween low- equency
ul asound and hip ac u es −compa ison wi h DXA-based BMD. BMC
Musculoskele al Diso de s 2014 15:208. Submi you nex manusc ip o BioMed Cen al
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