In e na ional Jou nal o
En i onmen al Resea ch
and Public Heal h
A icle
E ec s o he Manual The apy App oach o Segmen s C0-1 and
C2-3 in he Flexion-Ro a ion Tes in Pa ien s wi h Ch onic Neck
Pain: A Randomized Con olled T ial
Jacobo Rod íguez-Sanz 1,*, Miguel Malo-U iés2, Ma ía O osia Lucha-López 2, Albe Pé ez-Bellmun 1,
Andoni Ca asco-U iba en 1, Pablo Fanlo-Mazas 2, Jaime Co al-de-To o 2and Césa Hidalgo-Ga cía2


Ci a ion: Rod íguez-Sanz, J.;
Malo-U iés, M.; Lucha-López, M.O.;
Pé ez-Bellmun , A.; Ca asco-
U iba en, A.; Fanlo-Mazas, P.;
Co al-de-To o, J.; Hidalgo-Ga cía, C.
E ec s o he Manual The apy
App oach o Segmen s C0-1 and C2-3
in he Flexion-Ro a ion Tes in
Pa ien s wi h Ch onic Neck Pain: A
Randomized Con olled T ial. In . J.
En i on. Res. Public Heal h 2021,18,
753. h ps://doi.o g/10.3390/
ije ph18020753
Recei ed: 3 Janua y 2021
Accep ed: 15 Janua y 2021
Published: 17 Janua y 2021
Publishe ’s No e: MDPI s ays neu al
wi h ega d o ju isdic ional claims in
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Copy igh : © 2021 by he au ho s.
Licensee MDPI, Basel, Swi ze land.
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A ibu ion (CC BY) license (h ps://
c ea i ecommons.o g/licenses/by/
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1Facul y o Medicine and Heal h Sciences, Uni e si a In e nacional de Ca alunya, C/Josep T ue a s/n,
San Cuga del Vallés, 08195 Ba celona, Spain; [email p o ec ed] (A.P.-B.); [email p o ec ed] (A.C.-U.)
2
Depa amen o de Fisia ía y En e me ía, Unidad de In es igación en Fisio e apia, Facul ad de Ciencias de la
Salud, Uni e sidad de Za agoza, C/Domingo Mi al, s/n, 50009 Za agoza, Spain;
malom@uniza .es (M.M.-U.); o olucha@uniza .es (M.O.L.-L.); p anlo@uniza .es (P.F.-M.);
[email p o ec ed] (J.C.-d.-T.); hidalgo@uniza .es (C.H.-G.)
*Co espondence: j [email p o ec ed]; Tel.: +34-636-13-67-89
Abs ac :
Backg ound: Flexion- o a ion es p edominan ly measu es o a ion in C1-2 segmen . Re-
s ic ion in lexion- o a ion may be due o di ec limi a ion in C1-2, bu also o a p ema u e igh ening
o he ala ligamen as a esul o lack o mo emen in C0-1 o C2-3. The aim o his s udy was
o compa e he e ec o a 20-min single ce ical exe cise session, wi h o wi hou manual he apy
o C0-1 and C2-3 segmen in lexion- o a ion es , in pa ien s wi h ch onic neck pain and posi i e
lexion- o a ion es . Me hods: Randomized con olled clinical ial in 48 subjec s (24 manual he -
apy+exe cise/24 exe cise). Range o mo ion and pain du ing lexion- o a ion es , neck pain in ensi y
and ac i e ce ical ange o mo ion we e measu ed be o e and a e he in e en ion. Resul s: Sig-
ni ican di e ences we e ound in a ou o he manual he apy g oup in he lexion- o a ion es :
igh (p< 0.001) and le o a ion (p< 0.001); pain du ing he lexion- o a ion es : igh (p< 0.001)
and le o a ion (p< 0.001); neck pain in ensi y: (p< 0.001); ce ical lexion (p< 0.038), ex ension
(
p< 0.010
), igh side-bending (p< 0.035), le side-bending (p< 0.002), igh o a ion (p< 0.001), and
le o a ion (p< 0.006). Conclusions: Addi ion o one C0-C1 and C2-C3 manual he apy session o
ce ical exe cise can immedia ely imp o e lexion- o a ion es and ce ical ange o mo ion and
educe pain in ensi y.
Keywo ds: manual he apy; neck pain; exe cise; es ic ion
1. In oduc ion
Mobili y es ic ions o he uppe ce ical spine ha e been associa ed wi h neck pain
and headaches [
1
,
2
]. Mos o a ional mo emen o he uppe ce ical spine occu s a he
C1-2 segmen [
3
]. The lexion- o a ion es is he mos used es o assess he ange o
mo emen (ROM) in he ans e se plane o he uppe ce ical spine, and i is a alid
and eliable es [
4
–
7
]. This es is an easily applied me hod o manual examina ion ha
localizes he p esence o join dys unc ion a C1-2 le el [
8
]. Du ing he lexion- o a ion es ,
he head and neck a e placed in maximal lexion, and he head and neck a e u ned le
and igh [
3
]. The usual ROM is 45
◦
o each side [
9
]. The lexion- o a ion es is posi i e i
he ange is less han 33◦ o one side o i he e is a di e ence o 10◦be ween sides [8,9].
Al hough i is conside ed a es o assess he o a ion o he C1-2 segmen , he p esence
o pain ul join s in he lowe ce ical spine educed he a ailable ange in he lexion-
o a ion es o 37.5
◦
[
10
]. This indica es ha lowe ce ical spine pain may educe he
ROM eco ded du ing he lexion- o a ion es [11].
Takasaki e al. [
5
] ec ui ed 19 subjec s and examined he measu emen eliabili y o
segmen al uppe ce ical mo emen s using magne ic esonance imaging. They in es iga ed
In . J. En i on. Res. Public Heal h 2021,18, 753. h ps://doi.o g/10.3390/ije ph18020753 h ps://www.mdpi.com/jou nal/ije ph
In . J. En i on. Res. Public Heal h 2021,18, 753 2 o 14
he con en alidi y o he lexion- o a ion es compa ing ce ical o a ion ROM o each
segmen om a neu al and a maximally lexed posi ion o he neck. These esea che s
ound 1.7
◦
(1.9%) o mo emen in C0-1, 65
◦
(73.5%) in C1-2, 2.6
◦
(3%) in C2-3, and 19.1
◦
(21.6%) be ween C3 and C7 du ing he lexion- o a ion es . Smi h e al. [
12
] de e mined
ha age, gende and li es yle ac o s did no in luence he lexion- o a ion es . In u n,
Hall e al. [13]
ound an in e se ela ion be ween se e i y o symp oms and lexion- o a ion
es ROM. Ch onic neck pain al e s he ec ui men o he neck muscles [
14
], which can
lead o dec eased ange o mo emen [
15
]. Mechanisms a e no clea bu i has been ela ed
o a educ ion o he exci abili y o bo h co ical and spinal mo o neu ones [16].
Some s udies ha e in es iga ed he e ec i eness o ea ing uppe ce ical spine
es ic ion in he lexion- o a ion es wi h join mobiliza ion and manipula ion. These
s udies used join manipula ion and mobiliza ion ha was applied di ec ly o he C1-2
segmen s a he end o he ce ical o a ion ROM [
2
,
17
,
18
]. This ea men is no wi hou
con o e sy wi hin he li e a u e. This is due o he unique ROM cha ac e is ics and e -
eb al a e y angula ion a he C1-2 mo ion segmen . The po ion o he e eb al a e y
be ween C1-2 is conside ed by some o be he mos ulne able si e o inju y [
19
], especially
du ing o a ional manipula ion [
20
] and in addi ion o slow and epea ed mobiliza ion [
21
].
The e is con o e sy o e whe he ad e se e en s can be a ibu ed o he uppe ce ical
o a ion. The e o e, he In e na ional Fede a ion o O hopedic Manual Physical The a-
pis s (IFOMPT) ecommended ha end- ange o a ion and ex ension posi ions should be
a oided du ing ce ical spine mobiliza ion and manipula ion [
22
]. Al e na i e he apeu ic
s a egies p oposed in he li e a u e o a oid he di ec mobiliza ion o C1-C2 a e: ho acic
spine h us manipula ion, exe cise and pa ien educa ion [
23
–
25
] and he mobiliza ion o
C0-C1 [1,3] and C2-C3 [6].
Two p e ious s udies ha e shown ha he mobiliza ion o he C0-1 segmen p oduced
an imp o emen in lexion- o a ion es [
1
,
3
]. Hidalgo-Ga cía e al. [
26
,
27
] explained ha
he uppe ce ical spine is a unc ional elemen om C0 o C3. The es ic ion o ROM in
he lexion- o a ion es , in some pa ien s, could be explained by a p ema u e igh ening o
he ala ligamen as a esul o lack o mo emen in he C0-C1 [
26
] and C2-3 segmen s [
27
].
Howe e , he e a e no s udies ha ha e analysed he immedia e e ec o he manual
he apy ea men o he C0-1 and C2-3 segmen o imp o e he mobili y in a es ic ed
lexion- o a ion es , wi hou ea ing he C1-2 segmen .
Cleland e al. sugges in di e en a icles [
23
–
25
] ha du ing he ini ial ea men
sessions, he e is a subs an ial p obabili y o imp o ed pa ien ce ical ROM wi h indi ec
ea men , o example, when ho acic manipula ion is coupled wi h ce ical ac i e ROM
exe cises [
22
]. This app oach allows he he apis o obse e he pa ien ’s esponse o
ea men , and heo e ically minimizes he isks associa ed wi h di ec ce ical manipula-
ion in C1-2 segmen , in he p esence o ce ical ascula diso de [
22
]. Mo eo e , apa
om he biomechanical e ec s (inc ease ROM, dec ease passi e and ac i e s i ness), join
mobiliza ion and manipula ion ha e shown neu ophysiological e ec s as changes in spinal
exci abili y and in mo o unc ion, dec ease in co ical exci abili y and ac i a ion in b ain
pain p ocessing a eas, inc ease ac i a ion in inhibi o y pa hways and changes in es ing
s a e b ain unc ional connec i i y [28].
Finally, ce ical exe cise is e ec i e in educing pain [
29
] and inc easing ce ical
ROM in pa ien s wi h neck pain [
30
]. Speci ically, he low-load exe cise on deep ce ical
lexo muscles has demons a ed e ec i eness in imp o ing i s muscula pa ame e s
compa ed o o he ce ical exe cise p og ams [
31
] and neu omuscula coo dina ion [
32
].
This speci ic aining is ele an as app oxima ely 70% o pa ien s wi h ch onic neck pain
exhibi decline in s eng h and endu ance o hese muscles [
33
]. Fu he mo e, apa om he
neu ophysiological e ec s, exe cise may educe kinesiophobia and ea o mo emen [
34
].
Howe e , he immedia e e ec o exe cise wi hou associa ing manual he apy is no ye
ully desc ibed.
Ou hypo hesis was ha a one-session ea men o segmen s C0-1 and C2-3 can
immedia ely imp o e he lexion- o a ion es . The aim was o compa e he e ec , in he
In . J. En i on. Res. Public Heal h 2021,18, 753 3 o 14
lexion- o a ion es , o a 20-min session o manual he apy in C0-1 and C2-3 segmen
accompanied by ce ical exe cise, wi h he e ec o a 20-min session o ce ical exe cise
solely, in pa ien s wi h ch onic neck pain and posi i e lexion- o a ion es .
2. Ma e ials and Me hods
2.1. S udy Design
A p ospec i e, longi udinal, andomized (simple 1:1), and con olled assesso -blind
clinical ial was conduc ed. A esea che no in ol ed in he s udy andomized he in e -
en ion o each pa ien using compu e so wa e (www. andom.o g). The andomiza ion
esul s we e placed in a concealed opaque en elope, and pa icipan s we e assigned o
in e en ion g oups.
The s udy was ca ied ou in he acili ies o he Uni e si y o Za agoza, Spain
(Clinical ials.go numbe : NCT04406753)
. This s udy complied wi h he e hical p inciples
o esea ch on human beings as pe he Decla a ion o Helsinki (Fo aleza, B azil, Oc o-
be 2013). I was app o ed by he local e hics commi ee (Comi é É ico de In es igación
Clínica en A agón “CEICA”) in i s Reco ds n
◦
13/2018 on 4 July 2018. All pa icipan s we e
equi ed o p o ide w i en and in o med consen o pa icipa e. This s udy ollowed all
CONSORT c i e ia.
2.2. Sample Size Calcula ion
The p ima y a iable used o sample size calcula ion was he lexion- o a ion es
ROM [
2
], ob aining a o al sample o 48 subjec s (24 subjec s pe g oup). The common
s anda d de ia ion (7.15
◦
) and he minimum di e ence o be de ec ed be ween he g oups
(5.9
◦
) we e de e mined using he ou comes o Dunning e al. [
2
]. The sample size was
calcula ed using he GRANMO 7.12 p og am, wi h an
α
isk o 0.05, es wo-side, and a
β
isk o 0.20.
2.3. Subjec s
Fo y-eigh p ima y ca e subjec s (12 men and 36 women) we e included in he s udy.
The inclusion c i e ia comp ised: medical diagnosis o ch onic neck pain wi h mo e han
h ee mon hs o e olu ion [
35
], a posi i e esul in he lexion- o a ion es (less han 33
◦
o a di e ence o 10
◦
o mo e be ween he wo o a ions) [
6
,
8
,
9
] and loss o mobili y in
C0-1 and/o C2-3 spine segmen s ound h ough manual assessmen acco ding o Zi o
e al. and Kal enbo n [36,37]. Subjec s we e also equi ed o be o e 18 yea s old and sign
he in o med consen . The exclusion c i e ia we e: con aindica ions o manual he apy
o exe cise, p esen ing wa ning signs o ha ing su e ed a ele an neck auma, ha ing
pa icipa ed in exe cise o manual he apy p og ams in he las h ee mon hs [
22
], an
inabili y o main ain supine posi ion, he use o pacemake s, an inabili y o pe o m he
lexion- o a ion es , language di icul ies and pending li iga ion o lawsui s [38].
2.4. Measu emen s
The p ima y ou come measu e in his s udy was he ROM in he lexion- o a ion
es . Seconda y ou comes measu es we e neck pain in ensi y, pain in ensi y du ing he
lexion- o a ion es , and ce ical ROM.
The me hodology p oposed by Hall e al. [
9
] was ollowed o measu e he lexion-
o a ion es . In o de o pe o m i , he subjec was placed in supine posi ion, and he
e alua o passi ely mo ed he pa ien ’s ce ical spine o i s maximum lexion. Then he
head was o a ed o he igh and le sides wi h he occipu es ing agains he e alua o ’s
abdomen. The mo emen s opped when ei he he subjec p esen ed symp oms, o he
e alua o ound a i m end eel, whiche e si ua ion occu ed i s [
1
,
9
]. I any pain
appea ed du ing he es , i was eco ded by a e bal nume ic pain a ing scale (NPRS)
(scale: 0 = no pain/10 = wo s pain) o each o a ion [
39
]. A Ce ical Range o Mo ion
(CROM) de ice ( loa ing compass; Plas imo Ai guide, Inc., Bu alo G oo e, IL, USA) was
In . J. En i on. Res. Public Heal h 2021,18, 753 4 o 14
used, and h ee measu emen s we e aken o each o a ion. The esul was he mean o he
h ee measu emen s [38]. The eliabili y o his es is excellen , ICC = 0.93–0.96 [4,40].
Fo cu en neck pain in ensi y a he ime o e alua ion, he NPRS was used (scale:
0 = no pain/10 = wo s pain) [
41
]. NPRS has shown high eliabili y, wi h ICC = 0.76, in
pa ien s wi h ch onic neck pain [42].
Ac i e ce ical ROM was measu ed in all ca dinal planes o he assessmen o ce ical
mobili y. Fo ac i e mobili y es ing, pa ien s we e asked o si s aigh ahead, and o
mo e hei head as a as hey could wi hou pain in he di e en ca dinal planes o
mo emen [
43
]. A CROM de ice ( loa ing compass; Plas imo Ai guide, Inc.) was used and
h ee measu emen s we e aken o each mo emen . The esul was he mean o he h ee
measu emen s [38]. These measu emen s ha e high eliabili y (ICC = 0.98) [44].
A esea che specialized in manual he apy, wi h mo e han 5 yea s’ expe ience in
physical he apy, pe o med he measu es be o e and a e he in e en ion. This esea che
was blinded o he alloca ion g oup o each pa ien h oughou he p ocess.
2.5. In e en ion
In e en ion was ca ied ou by a di e en esea che wi h mo e han 5 yea s’ expe i-
ence in physical he apy. The in e en ion was p o ided indi idually in he acili ies a he
Uni e si y o Za agoza. Pa icipan s in bo h g oups ecei ed a single 20-min session.
2.6. Exe cise G oup
A e baseline assessmen s, pa ien s began he ce ical exe cise. They we e augh
o pe o m he con ac ion o deep neck lexo muscles (longus capi is and longus colli)
using he S abilize P essu e Bio eedback Uni (Cha anooga, TN, USA) in supine [
45
,
46
]
(Figu e 1)
. The exe cise was always ca ied ou wi hou pain because pain can be an
inhibi o o muscle con ac ion [
47
]. This exe cise was chosen because i has been ob-
se ed ha pa ien s wi h ch onic neck pain show educed ac i a ion o he deep ce ical
lexo muscles, which a e conside ed impo an o con ol o s abili y o he spinal ele-
men s, which canno be eplica ed by he mo e supe icial an e io muscles aining can
success ully add ess impai ed [14].
In . J. En i on. Res. Public Heal h 2021, 18, 753 5 o 14
Figu e 1. Deep neck lexo . Subjec s we e ins uc ed o “gen ly nod hei head as hough hey we e
saying ‘yes’”. Con ibu ion om he supe icial muscles was moni o ed using obse a ion and
palpa ion. Then, he subjec s we e augh o pe o m a slow and con olled deep neck lexo exe -
cise.
2.7. Manual The apy + Exe cise G oup
The Manual The apy+Exe cise g oup (MT + E g oup) ca ied ou a 20-min session o
ea men . The manual he apy echniques we e applied depending on he clinical ind-
ings in each pa ien , and he objec i e was o es o e he mobili y o C0-1 and C2-3 seg-
men s be o e applying ce ical exe cises. Manipula ion (high- eloci y low ampli ude)
and/o mobiliza ion (low- eloci y high ampli ude) echniques o C0-1 and C2-3 segmen s
we e applied [1,3,48,49] (Figu e 2). Manipula ions we e in he di ec ion o ac ion, wi h
he head in a neu al posi ion [50]. A maximum o wo ials a each le el on each side was
pe o med, yielding 2–8 h us s [51]. Mobiliza ion was pe o med epea ing cycles o 45 s
o mobiliza ion and 15 s o es [1,3]. The execu ion o he echniques is de ailed in Figu e
2. The ce ical exe cise pe o med by his g oup ollowed he same dose as he Exe cise
g oup, he only di e ence was ha ins ead o pe o ming 40-s es be ween each exe cise
epe i ion, his g oup ook 30-s. This was done in o de o ha e 3 min o ime o apply he
manual he apy echniques be o e he exe cise.
Figu e 2. Manual he apy in e en ions. (a) C0-1 T ac ion Manipula ion in he Res ing Posi ion. Pa ien was placed in
supine wi h neck in a neu al posi ion. The he apis gen ly cupped he pa ien ’s chin wi h hei hand while hei a m was
c adled a ound he head. The o he hand placed he adial side o he index inge unde he mas oid p ocess and aligned
he o ea m in he line o d i e poin ing c anially. Then, he he apis applied a c anial h us ; (b) C2-3 T ac ion Manipu-
la ion in he Res ing Posi ion. The same handling p ocedu e was pe o med, bu he g ip was eloca ed in C3 e eb ae;
(c) C0-1 Do sal Mobiliza ion. Pa ien was posi ioned in supine, wi h neck in a neu al posi ion. The he apis placed a hand
do sally a he le el o he e eb al a ch o C1 wi h he me aca pophalangeal and adial bo de o he index inge . The
o he hand was placed pos e io ly unde he occipu , wi h he shoulde posi ioned an e io ly on he pa ien ’s o ehead.
The mobiliza ion o ce was di ec ed do sally om he shoulde un il he he apis el a ma ked esis ance, and hen
sligh ly mo e p essu e was applied o pe o m a s e ching mobiliza ion.
All he manipula ion and mobiliza ion echniques used in his ial ollow IFOMPT
ecommenda ions o educe he isk o ad e se e en s [22].
Figu e 1.
Deep neck lexo . Subjec s we e ins uc ed o “gen ly nod hei head as hough hey we e
saying ‘yes’”. Con ibu ion om he supe icial muscles was moni o ed using obse a ion and
palpa ion. Then, he subjec s we e augh o pe o m a slow and con olled deep neck lexo exe cise.
I is assumed ha his al e ed ec ui men pa e n is a con ibu ing ac o o he
ch oni ica ion o neck pain. T aining deep neck lexo muscles achie es he imp o emen
o neu omuscula coo dina ion and no o he s eng h and endu ance, so a single session
can ob ain changes in he mo o pa e n [32].
The Exe cise g oup ca ied ou one 20-min session, composed o 2 blocks o 10 epe i-
ions. They held each epe i ion o 10 s [
47
], and had a 40-s es be ween each epe i ion
and 2 min be ween blocks.
In . J. En i on. Res. Public Heal h 2021,18, 753 5 o 14
2.7. Manual The apy + Exe cise G oup
The Manual The apy+Exe cise g oup (MT + E g oup) ca ied ou a 20-min session o
ea men . The manual he apy echniques we e applied depending on he clinical indings
in each pa ien , and he objec i e was o es o e he mobili y o C0-1 and C2-3 segmen s
be o e applying ce ical exe cises. Manipula ion (high- eloci y low ampli ude) and/o
mobiliza ion (low- eloci y high ampli ude) echniques o C0-1 and C2-3 segmen s we e
applied [
1
,
3
,
48
,
49
] (Figu e 2). Manipula ions we e in he di ec ion o ac ion, wi h he
head in a neu al posi ion [
50
]. A maximum o wo ials a each le el on each side was
pe o med, yielding 2–8 h us s [
51
]. Mobiliza ion was pe o med epea ing cycles o 45 s
o mobiliza ion and 15 s o es [
1
,
3
]. The execu ion o he echniques is de ailed in
Figu e 2
.
The ce ical exe cise pe o med by his g oup ollowed he same dose as he Exe cise
g oup, he only di e ence was ha ins ead o pe o ming 40-s es be ween each exe cise
epe i ion, his g oup ook 30-s. This was done in o de o ha e 3 min o ime o apply he
manual he apy echniques be o e he exe cise.
In . J. En i on. Res. Public Heal h 2021, 18, 753 5 o 14
Figu e 1. Deep neck lexo . Subjec s we e ins uc ed o “gen ly nod hei head as hough hey we e
saying ‘yes’”. Con ibu ion om he supe icial muscles was moni o ed using obse a ion and
palpa ion. Then, he subjec s we e augh o pe o m a slow and con olled deep neck lexo exe -
cise.
2.7. Manual The apy + Exe cise G oup
The Manual The apy+Exe cise g oup (MT + E g oup) ca ied ou a 20-min session o
ea men . The manual he apy echniques we e applied depending on he clinical ind-
ings in each pa ien , and he objec i e was o es o e he mobili y o C0-1 and C2-3 seg-
men s be o e applying ce ical exe cises. Manipula ion (high- eloci y low ampli ude)
and/o mobiliza ion (low- eloci y high ampli ude) echniques o C0-1 and C2-3 segmen s
we e applied [1,3,48,49] (Figu e 2). Manipula ions we e in he di ec ion o ac ion, wi h
he head in a neu al posi ion [50]. A maximum o wo ials a each le el on each side was
pe o med, yielding 2–8 h us s [51]. Mobiliza ion was pe o med epea ing cycles o 45 s
o mobiliza ion and 15 s o es [1,3]. The execu ion o he echniques is de ailed in Figu e
2. The ce ical exe cise pe o med by his g oup ollowed he same dose as he Exe cise
g oup, he only di e ence was ha ins ead o pe o ming 40-s es be ween each exe cise
epe i ion, his g oup ook 30-s. This was done in o de o ha e 3 min o ime o apply he
manual he apy echniques be o e he exe cise.
Figu e 2. Manual he apy in e en ions. (a) C0-1 T ac ion Manipula ion in he Res ing Posi ion. Pa ien was placed in
supine wi h neck in a neu al posi ion. The he apis gen ly cupped he pa ien ’s chin wi h hei hand while hei a m was
c adled a ound he head. The o he hand placed he adial side o he index inge unde he mas oid p ocess and aligned
he o ea m in he line o d i e poin ing c anially. Then, he he apis applied a c anial h us ; (b) C2-3 T ac ion Manipu-
la ion in he Res ing Posi ion. The same handling p ocedu e was pe o med, bu he g ip was eloca ed in C3 e eb ae;
(c) C0-1 Do sal Mobiliza ion. Pa ien was posi ioned in supine, wi h neck in a neu al posi ion. The he apis placed a hand
do sally a he le el o he e eb al a ch o C1 wi h he me aca pophalangeal and adial bo de o he index inge . The
o he hand was placed pos e io ly unde he occipu , wi h he shoulde posi ioned an e io ly on he pa ien ’s o ehead.
The mobiliza ion o ce was di ec ed do sally om he shoulde un il he he apis el a ma ked esis ance, and hen
sligh ly mo e p essu e was applied o pe o m a s e ching mobiliza ion.
All he manipula ion and mobiliza ion echniques used in his ial ollow IFOMPT
ecommenda ions o educe he isk o ad e se e en s [22].
Figu e 2.
Manual he apy in e en ions. (
a
) C0-1 T ac ion Manipula ion in he Res ing Posi ion. Pa ien was placed in
supine wi h neck in a neu al posi ion. The he apis gen ly cupped he pa ien ’s chin wi h hei hand while hei a m
was c adled a ound he head. The o he hand placed he adial side o he index inge unde he mas oid p ocess and
aligned he o ea m in he line o d i e poin ing c anially. Then, he he apis applied a c anial h us ; (
b
) C2-3 T ac ion
Manipula ion in he Res ing Posi ion. The same handling p ocedu e was pe o med, bu he g ip was eloca ed in C3
e eb ae; (
c
) C0-1 Do sal Mobiliza ion. Pa ien was posi ioned in supine, wi h neck in a neu al posi ion. The he apis
placed a hand do sally a he le el o he e eb al a ch o C1 wi h he me aca pophalangeal and adial bo de o he index
inge . The o he hand was placed pos e io ly unde he occipu , wi h he shoulde posi ioned an e io ly on he pa ien ’s
o ehead. The mobiliza ion o ce was di ec ed do sally om he shoulde un il he he apis el a ma ked esis ance, and
hen sligh ly mo e p essu e was applied o pe o m a s e ching mobiliza ion.
All he manipula ion and mobiliza ion echniques used in his ial ollow IFOMPT
ecommenda ions o educe he isk o ad e se e en s [22].
2.8. S a is ical Analysis
S a is ical analysis was conduc ed wi h he SPSS 23.0 package (IBM,
A monk, NY, USA
).
The e was no loss o ollow-up in he s udy. The mean, con idence in e al and s anda d
de ia ion we e calcula ed o each a iable. The Kolmogo o –Smi no es was used o
de e mine a no mal dis ibu ion o quan i a i e da a (p> 0.05). Ou lie s we e examined. No
alue was excluded because ex eme alues did no cause any signi ican bias. Wi hin- and
be ween-g oup di e ences we e analyzed using epea ed measu es o ANOVA and one-way
ANOVA. I he assump ion o sphe ici y was iola ed, he G eenhouse-Geisse co ec ion was
u ilized o in e p e a ion [
51
]. E ec sizes we e calcula ed using Cohen’s d coe icien [
52
]. An
e ec size >0.8 was conside ed la ge; a ound 0.5, in e media e; and <0.2, small [
52
]. Exclusions
a e andomiza ion a e explained in Figu e 3. All subjec s en olled o iginally we e included in
he inal analysis as planned. Thus, pa icipan s we e analyzed as pe p o ocol (by in en ion- o-
ea ). The le el o signi icance was se a p< 0.05.

In . J. En i on. Res. Public Heal h 2021,18, 753 6 o 14
In . J. En i on. Res. Public Heal h 2021, 18, 753 6 o 14
2.8. S a is ical Analysis
S a is ical analysis was conduc ed wi h he SPSS 23.0 package (IBM, A monk, NY,
USA). The e was no loss o ollow-up in he s udy. The mean, con idence in e al and
s anda d de ia ion we e calcula ed o each a iable. The Kolmogo o –Smi no es was
used o de e mine a no mal dis ibu ion o quan i a i e da a (p > 0.05). Ou lie s we e ex-
amined. No alue was excluded because ex eme alues did no cause any signi ican bias.
Wi hin- and be ween-g oup di e ences we e analyzed using epea ed measu es o
ANOVA and one-way ANOVA. I he assump ion o sphe ici y was iola ed, he G een-
house-Geisse co ec ion was u ilized o in e p e a ion [51]. E ec sizes we e calcula ed
using Cohen’s d coe icien [52]. An e ec size >0.8 was conside ed la ge; a ound 0.5, in-
e media e; and <0.2, small [52]. Exclusions a e andomiza ion a e explained in Figu e 3.
All subjec s en olled o iginally we e included in he inal analysis as planned. Thus, pa -
icipan s we e analyzed as pe p o ocol (by in en ion- o- ea ). The le el o signi icance
was se a p < 0.05.
Figu e 3. CONSORT. (Consolida ed S anda ds o Repo ing T ial) low diag am.
The demog aphic cha ac e is ics o he sample a e summa ized in Table 1. No ad-
e se e en s o side-e ec s we e epo ed in any pa icipan .
Table 1. Baseline Fea u es o Bo h G oups.
E G oup (n = 24) MT + E G oup (n = 24)
Clinical ea u es
Age (yea s) 54.71 ± 14.59 49.17 ± 14.24
Sex ( emale) 19 (79.2%) 17 (70.8%)
Du a ion o Symp oms (mon hs) 141.67 ± 157.27 91.88 ± 85.51
NPRS (0–10) 4.34 ± 2.65 4.13 ± 1.70
Flexion- o a ion es
Righ (°) 16.93 ± 10.17 22.11 ± 10.35
Le (°) 18.97 ± 10.26 24.06 ± 9.33
Righ (NPRS) 5.08 ± 2.32 3.67 ± 2.35
Figu e 3. CONSORT. (Consolida ed S anda ds o Repo ing T ial) low diag am.
The demog aphic cha ac e is ics o he sample a e summa ized in Table 1. No ad e se
e en s o side-e ec s we e epo ed in any pa icipan .
Table 1. Baseline Fea u es o Bo h G oups.
E G oup (n= 24) MT + E G oup (n= 24)
Clinical ea u es
Age (yea s) 54.71 ±14.59 49.17 ±14.24
Sex ( emale) 19 (79.2%) 17 (70.8%)
Du a ion o Symp oms (mon hs) 141.67 ±157.27 91.88 ±85.51
NPRS (0–10) 4.34 ±2.65 4.13 ±1.70
Flexion- o a ion es
Righ (◦) 16.93 ±10.17 22.11 ±10.35
Le (◦) 18.97 ±10.26 24.06 ±9.33
Righ (NPRS) 5.08 ±2.32 3.67 ±2.35
Le (NPRS) 4.75 ±2.67 2.34 ±2.37
Ce ical ROM (◦)
Flexion 47.08 ±10.77 47.38 ±11.50
Ex ension 50.71 ±13.44 54.54 ±14.56
Righ Side-Bending 26.92 ±8.91 32.29 ±9.95
Le Side-Bending 28.00 ±9.17 30.13 ±9.63
Righ Ro a ion 52.29 ±12.48 57.34 ±16.02
Le Ro a ion 54.58 ±12.40 60.25 ±15.61
Abb e ia ions: NPRS. Nume ical Pain Ra ing Scale; ROM. Range o mo ion; E. Exe cise; MT + E. Manual
The apy + Exe cise.
In . J. En i on. Res. Public Heal h 2021,18, 753 7 o 14
3. Resul s
Be ween June 2020 and July 2020, 81 olun ee s we e ec ui ed. Fo y-eigh pa ic-
ipan s (12 men and 36 women) wi h a mean age o 51.9 (14.5) yea s old me all eligi-
bili y c i e ia and ag eed o pa icipa e. Then, 24 pa icipan s we e andomly assigned
o each g oup, ecei ed hei assigned ea men , and we e analyzed o in en ion- o-
ea
(Figu e 3).
En ollmen and exclusions a e andomiza ion a e in he low diag am,
see Figu e 3.
3.1. Flexion-Ro a ion Tes ROM and NPRS
No s a is ically signi ican changes we e ound in he wi hin-g oup analysis
(Table 2)
o he exe cise g oup. In he MT + E g oup, signi ican inc ease was ound in he lexion-
o a ion es in igh o a ion (p< 0.001; d = 1.14) and le o a ion (p< 0.001; d = 1.09) ROM.
A s a is ically signi ican dec ease in NPRS was also obse ed du ing bo h o a ions ( igh
NPRS o a ion (p< 0.001; d = 0.89); le NPRS o a ion (p< 0.001; d = 0.76)).
Table 2. P e- and pos - ea men in NPRS and lexion- o a ion es ou comes.
Ou come G oup P e-T ea men Pos -T ea men Wi hin-G oup †Be ween-G oup ‡
NPRS (0–10)
E G oup 4.34 ±2.65
(3.2, 5.5)
4.50 ±2.49
(3.5, 5.6)
p> 0.709
p< 0.001
d = 1.30
d = 0.06
MT + E G oup 4.13 ±1.70
(3.4, 4.8)
1.75 ±1.68
(1.0, 2.5)
p< 0.001
d = 1.41
Flexion- o a ion
es (R) (◦)
E G oup 16.93 ±10.17
(12.6, 21.2)
16.21 ±10.56
(11.8, 20.7)
p> 0.090
p< 0.001
d = 1.72
d = 0.07
MT + E G oup 22.11 ±10.35
(17.7, 26.5)
33.15 ±9.06
(29.3, 37.0)
p< 0.001
d = 1.14
Flexion- o a ion
es (L) (◦)
E G oup 18.97 ±10.26
(14.6, 23.3)
17.98 ±10.43
(13.1, 22.2)
p>0.221
p< 0.001
d = 1.65
d = 0.10
MT + E G oup 24.06 ±9.33
(20.3, 28.2)
34.17 ±9.16
(30.2, 37.9)
p< 0.001
d = 1.09
Flexion- o a ion
es (R) (NPRS
0–10)
E G oup 5.08 ±2.32
(4.1, 6.1)
5.50 ±2.27
(4.5, 6.5)
p> 0.135
p<0.001
d = 1.74
d = 0.18
MT + E G oup 3.67 ±2.35
(2.7, 4.7)
1.67 ±2.12
(0.8, 2.6)
p< 0.001
d = 0.89
Flexion- o a ion
es (L) (NPRS
0–10)
E G oup 4.75 ±2.67
(3.6, 5.9)
4.92 ±2.54
(3.9, 6.0)
p> 0.548
p< 0.001
d = 1.41
d = 0.07
MT + E G oup 3.34 ±2.37
(2.3, 4.3)
1.67 ±2.04
(0.8, 2.5)
p< 0.001
d = 0.76
Abb e ia ions: R. igh ; L. le ; NPRS. Nume ical Pain Ra ing Scale E. Exe cise; MT + E. Manual The apy + Exe cise.
†,
alue is epea ed
measu es ANOVA. ‡, alue is one-way ANOVA. p alues ≤0.05 a e s a is ically signi ican . d. Cohen d e ec size.
In he be ween-g oup analysis (Table 2), s a is ically signi ican di e ences we e ound
in a o o he MT + E g oup in igh o a ion (p< 0.001; d = 1.72) and le o a ion
(p< 0.001
;
d = 1.65) ROM, and in igh NPRS o a ion (p< 0.001; d = 1.74) and in le NPRS o a ion
(p< 0.001; d = 1.41).
3.2. Neck Pain In ensi y (Nume ic Pain Ra ing Scale)
In he wi hin-g oup analysis (Table 2) o he exe cise g oup, no s a is ically signi ican
changes we e ound a any ime du ing he s udy. In he MT + E g oup, signi ican
imp o emen was ound (p< 0.001; d = 1.41).
In . J. En i on. Res. Public Heal h 2021,18, 753 8 o 14
In he be ween-g oup analysis (Table 2), s a is ically signi ican di e ences we e ound
in a ou o he MT + E g oup (p< 0.001; d = 1.30).
3.3. Ce ical ROM
In he wi hin-g oup analysis (Table 3) o exe cise g oup, a s a is ically signi ican
dec ease was ound in lexion (p< 0.008; d = 0.37), ex ension (p< 0.012; d = 0.26), and le
side-bending (p< 0.030; d = 0.20). In he MT + E g oup, a signi ican inc ease was ound
only in le side-bending (p< 0.001; d = 0.43).
Table 3. P e- and pos - ea men in ce ical ange o mo ion ou comes.
Ou come/G oup P e-T ea men Pos -T ea men Wi hin-G oup †Be ween-G oup ‡
Flexion (◦)
E G oup 47.08 ±10.77
(42.5, 51.6)
43.67 ±10.82
(39.1, 48.2)
p< 0.008
p< 0.038
d = 0.62
d = 0.37
MT + E G oup 47.38 ±11.50
(42.5, 52.2)
49.83 ±9.13
(46.0, 53.7)
p> 0.148
d = 0.24
Ex ension (◦)
E G oup 50.71 ±13.44
(45.0, 56.4)
47.46 ±11.31
(42.7, 52.2)
p< 0.012
p< 0.010
d = 0.77
d = 0.26
MT + E G oup 54.54 ±14.56
(48.4, 60.7)
56.79 ±12.81
(51.4, 62.2)
p> 0.171
d = 0.16
Side-bending (Righ ) (◦)
E G oup 26.92 ±8.91
(23.2, 30.7)
26.54 ±8.46
(23.0, 30.1)
p> 0.531
p< 0.035
d = 0.63
d = 0.04
MT + E G oup 32.29 ±9.95
(28.1, 36.5)
32.04 ±9.04
(28.2, 35.9)
p> 0.846
d = 0.03
Side-bending (Le ) (◦)
E G oup 28.00 ±9.17
(24.1, 31.9)
26.25 ±8.68
(22.6, 29.9)
p< 0.030
p< 0.002
d = 0.93
d = 0.20
MT + E G oup 30.13 ±9.63
(26.1, 34.2)
33.79 ±7.47
(30.6, 36.9)
p< 0.001
d = 0.43
Ro a ion (Righ ) (◦)
E G oup 52.29 ±12.48
(47.0, 57.6)
50.58 ±12.45
(45.3, 55.8)
p> 0.063
p< 0.006
d = 0.84
d = 0.14
MT + E G oup 57.34 ±16.02
(50.6, 64.1)
61.13 ±12.75
(55.7, 66.5)
p> 0.168
d = 0.26
Ro a ion (Le ) (◦)
E G oup 54.58 ±12.40
(49.4, 59.8)
52.67 ±12.26
(47.5, 57.8)
p> 0.163
p< 0.001
d = 1.03
d = 0.16
MT + E G oup 60.25 ±15.61
(53.7, 66.8)
64.75 ±11.15
(60.0, 69.5)
p> 0.082
d = 0.33
Abb e ia ions: E. Exe cise; MT + E. Manual The apy+Exe cise.
†,
alue is epea ed measu es ANOVA.
‡,
alue is one-way ANOVA.
p alues ≤0.05 a e s a is ically signi ican . d. Cohen d e ec size.
In he be ween-g oup analysis (Table 3), s a is ically signi ican di e ences we e ound
in a o o he MT + E g oup in lexion (p< 0.038; d = 0.62), ex ension (p< 0.010; d = 0.77),
In . J. En i on. Res. Public Heal h 2021,18, 753 9 o 14
igh side-bending (p< 0.035; d = 0.63), le side-bending (p< 0.002; d = 0.93), igh o a ion
(p< 0.006; d = 0.84), and le o a ion (p< 0.001; d = 1.03).
4. Discussion
This s udy ound an immedia e inc ease in ROM on he lexion- o a ion es in he
MT + E g oup
. The imp o emen in he lexion- o a ion es obse ed in he MT + E
g oup was supe io o he minimal de ec able change (4.7
◦
o igh o a ion and 7.0
◦
o le o a ion) desc ibed by Hall e al. [
40
]. This g oup managed o o e come he
clinically ele an imp o emen (10
◦
o mo e) o he lexion- o a ion es p omo ed by
o he au ho s [
8
,
9
]. In con as , he exe cise g oup did no expe ience any s a is ically
signi ican change in his a iable.
Excep o he C1-2 segmen , he e is li le in o ma ion ega ding he e ec s o he
ea men o o he ce ical segmen s on uppe ce ical o a ion ROM examined wi h he
lexion- o a ion es [1,3].
The e is e idence ha neck pain, ROM, and disabili y may be imp o ed by ea men
o segmen s and spinal egions emo e om he symp oma ic segmen [
24
]. Hidalgo-
Ga cía e al. [
3
] and Malo-U iés e al. [
1
] ound an inc ease in he lexion- o a ion es
when applying a mobiliza ion in C0-1 segmen . Ca asco-U iba en e al. [
50
] e alua ed he
lexion- o a ion es , and applied a p o ocol o ac ion manipula ion in he es ing posi ion
in C0-1, C1-2 and C2-3 segmen s, ob aining simila esul s o hose obse ed in his s udy.
A possible explana ion o hese esul s in he MT + E g oup in ou s udy may be
due o he ela ionship be ween he a icula , muscula , and ligamen ous issue be ween
C0-1, C1-2 and C2-3 segmen s [
3
], pa icula ly, by ala ligamen s. C1-2 o a ion is limi ed
by he ala ligamen sys em and occipi al, and C2 a e he main bony a achmen s o ala
ligamen s. Some au ho s ha e p oposed ha C0-1 [
1
,
3
] and/o C2-3 [
50
] dys unc ion may
inhibi he no mal o a ional mobili y o C1-2 [
53
]. The MT + E g oup ecei ed a ailo ed
manual he apy ea men acco ding o he C0-1 and C2-3 dys unc ion o each pa ien . This
could be a po en ial explana ion o he esul s o his s udy. Also, o he non-biomechanical
mechanisms such as spinal co d and cen al ne ous sys em mechanisms may accoun o
his imp o emen [3].
In ou s udy, we ound a signi ican educ ion in NPRS o bo h o a ions du ing he
lexion- o a ion es in he MT + E g oup. The e is only one p e ious s udy ha eco ds
NPRS du ing he lexion- o a ion es [
39
], bu he design o his s udy and he selec ion o
he sample do no allow us o con as ou esul s.
A signi ican dec ease in NPRS was ound in MT + E g oup. In con as , he exe cise
g oup did no expe ience any s a is ically signi ican change in neck pain in ensi y. Se e al
s udies ound immedia e imp o emen s wi h manual he apy and exe cise [
54
,
55
], wi h
isola ed manual he apy [56] o wi h isola ed exe cise [55,57].
Bialosky JE e al. [
58
] exposes he hypoalgesic e ec o manual he apy and exe cise
h ough a model ha is based on a mechanical s imulus ini ia ing a chain o spinal neu o-
physiological e en s, pe iphe al e en s, and/o sup aspinal e en s ha would p oduce his
hypoalgesia. Ne e heless, hese neu ophysiological e ec s would depend on he s imulus
and he dose [
58
,
59
]. The uppe ce ical egion is cha ac e ized by ha ing a g ea numbe
o mechano ecep o s, especially in he suboccipi al egion [
60
]. The e o e, his egion has
a high capaci y o ansmi mechanical inpu s om manual echniques, esul ing in a de-
c ease in neck pain in ensi y in MT + E g oup. The e is a non-signi ican inc ease in NPRS
in he exe cise g oup. This may be due o issue i i a ion p ocesses because o exe cising
deep ce ical muscles h ough uppe ce ical spine lexion wi hou a p ope ROM. The e
a e s udies ha sugges ed ha i i a ion o he suboccipi al issues can cause an inc ease
in muscle s e ch e lex, including in adjacen muscles, gene a ing an inc ease in issue
sensi i i y [
61
–
63
]. Because hese pa ien s had a o a o y es ic ion in he uppe ce ical
spine, he i i a ion could a ec cen al p ocesses p oduced by ac i a ion o segmen al
inhibi o y pa hways, spinal co d pa hways, o descending inhibi o y pa hways om he
b ains em gene a ing an inc ease in pain [
64
,
65
]. Al hough deep ce ical lexo exe cises