7
Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross- sectional multicenter study Frauke Mu ¨ller Marta Hernandez Linda Gru ¨tter Luis Aracil-Kessler Dieter Weingart Martin Schimmel Authors’ affiliations: Frauke Mu ¨ller, Martin Schimmel, Division of Gerodontology and Removable Prosthodontics, University of Geneva, Geneva, Switzerland Frauke Mu ¨ller, Department of Rehabilitation and Geriatrics, University Hospitals of Geneva, Thonex, Switzerland Marta Hernandez, Luis Aracil-Kessler, Department of Periodontology, Oral Surgery, Oral Medicine, University Complutense Madrid, Madrid, Spain Marta Hernandez, Dieter Weingart, Department of Maxillofacial Surgery, Plastic Surgery and Centre of Oral Implantology, Katharinen Hospital, Stuttgart, Germany Linda Gru ¨tter, Division of Fixed Prosthodontics and Occlusion, University of Geneva, Geneva, Switzerland Corresponding author: Martin Schimmel, Dr Med Dent, MAS Oral Biol Division of Gerodontology and Removable Prosthodontics University of Geneva 19, Rue Barthe ´lemy-Menn CH-1205 Geneva Switzerland Tel.: þ 41 22 379 4060 Fax: þ 41 22 379 4052 e-mail: [email protected] Key words: implant-supported fixed dental prostheses, implant-supported overdenture, masseter muscle thickness, masticatory efficiency, maximum voluntary bite force, ultrasound Abstract Objectives: Edentulous patients may be restored with conventional dentures (C/C), implant-supported overdentures (IOD) or implant-supported fixed dental prostheses (IFDP). Null-hypotheses: chewing efficiency, maximum voluntary bite force (MBF) and masseter muscle thickness (MMT) are lower in patients with C/IOD compared with the patients with bimaxillary IFDPs. Both groups perform better than C/C and are inferior to fully dentate controls. Material and methods: Ethical approval was obtained. For this multicenter cross-sectional study, 80 patients were recruited. Four groups of different dental states comprised of either implant-supported prostheses (C/IOD and IFDP/IFDP) or served as control-groups (C/C and fully dentate D/D). Chewing efficiency was assessed with a two-colour mixing ability test. MBF was measured bilaterally with a force gauge. Two dimensional ultrasonography was used to measure MMT bilaterally. Results: Chewing efficiency in C/IOD and IFDP/IFDP (difference NS) was better than in C/C, but not as good as in D/D. MBF in C/IOD was lower than in IFDP/IFDP. Chewing efficiency and MBF were significantly lower in IFDP/IFDP, who had experienced chipping or fracture of the prosthetic superstructure. Median MMT of patients with implant-supported prostheses was between those with C/C and fully dentate participants. There was no significant difference in MMT between C/IOD and IFDP/IFDP. Conclusion: Supporting complete prostheses with oral implants seems to have positive effects on the thickness of the masseter muscle, maximum bite force as well as chewing efficiency. The type of implant-supported prostheses may have an influence on the magnitude of the effect. Compared with conventional complete dentures, implant-supported overdentures (IOD) and im- plant-supported fixed dental prostheses (IFDP) seem to offer substantial psycho-social and func- tional benefits to the edentulous individuals (Feine et al. 1994a; Brennan et al. 2010). Once all teeth are lost, the stabilization of the lower denture with two implants placed in the inter- foraminal region was recommended as treatment of first choice (Thomason et al. 2009). The improvements of orofacial functions with IOD comprises of increased bite force (van der Bilt et al. 2010a), larger chewing cycles, better coordi- nation of the chewing sequence (Benzig et al. 1994) as well as improved masticatory efficiency and ability (van Kampen et al. 2004). In addition, they seem to provide better oral health-related quality of life (Rashid et al. 2011) and might even be more cost effective (Emami et al. 2009) than conventional full dentures. Also, dental implants seem to slow down the peri-implant alveolar bone loss in the edentulous mandible and thus show tertiary preventive properties (Behneke 1994). The patient’s age and years of the edentulism have a negative impact on the macro- and micro- scopic structure of the chewing muscles (Raustia et al. 1996). The cross-sectional area as well as radiographic density of the masseter and medial pterygoid muscle decrease with age and these effects are significantly aggravated by edentulism (Newton et al. 1993). In an animal model the change from a hard to a soft texture diet reduced the weight of the masseter muscle significantly. Mice fed with a soft diet lost 19% of the muscle weight within 1 week (Urushiyama et al. 2004). Date: Accepted 31 March 2011 To cite this article: Mu ¨ ller F, Hernandez M, Gru ¨ tter L, Aracil-Kessler L, Weingart D, Schimmel M. Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross- sectional multicenter study. Clin. Oral Impl. Res. 23, 2012 144–150 doi: 10.1111/j.1600-0501.2011.02213.x 144 © 2011 John Wiley & Sons A/S . ;

Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

Embed Size (px)

Citation preview

Page 1: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

Masseter muscle thickness, chewingefficiency and bite force in edentulouspatients with fixed and removableimplant-supported prostheses: a cross-sectional multicenter study

Frauke MullerMarta HernandezLinda GrutterLuis Aracil-KesslerDieter WeingartMartin Schimmel

Authors’ affiliations:Frauke Muller, Martin Schimmel, Division ofGerodontology and Removable Prosthodontics,University of Geneva, Geneva, SwitzerlandFrauke Muller, Department of Rehabilitation andGeriatrics, University Hospitals of Geneva, Thonex,SwitzerlandMarta Hernandez, Luis Aracil-Kessler, Department ofPeriodontology, Oral Surgery, Oral Medicine,University Complutense Madrid, Madrid, SpainMarta Hernandez, Dieter Weingart, Department ofMaxillofacial Surgery, Plastic Surgery and Centre ofOral Implantology, Katharinen Hospital, Stuttgart,GermanyLinda Grutter, Division of Fixed Prosthodontics andOcclusion, University of Geneva, Geneva, Switzerland

Corresponding author:Martin Schimmel, Dr Med Dent, MAS Oral BiolDivision of Gerodontology and RemovableProsthodonticsUniversity of Geneva19, Rue Barthelemy-MennCH-1205GenevaSwitzerlandTel.: þ 41 22 379 4060Fax: þ 41 22 379 4052e-mail: [email protected]

Key words: implant-supported fixed dental prostheses, implant-supported overdenture,

masseter muscle thickness, masticatory efficiency, maximum voluntary bite force, ultrasound

Abstract

Objectives: Edentulous patients may be restored with conventional dentures (C/C), implant-supported

overdentures (IOD) or implant-supported fixed dental prostheses (IFDP). Null-hypotheses: chewing

efficiency, maximum voluntary bite force (MBF) and masseter muscle thickness (MMT) are lower in

patients with C/IOD compared with the patients with bimaxillary IFDPs. Both groups perform better

than C/C and are inferior to fully dentate controls.

Material and methods: Ethical approval was obtained. For this multicenter cross-sectional study, 80

patients were recruited. Four groups of different dental states comprised of either implant-supported

prostheses (C/IOD and IFDP/IFDP) or served as control-groups (C/C and fully dentate D/D). Chewing

efficiency was assessed with a two-colour mixing ability test. MBF was measured bilaterally with a

force gauge. Two dimensional ultrasonography was used to measure MMT bilaterally.

Results: Chewing efficiency in C/IOD and IFDP/IFDP (difference NS) was better than in C/C, but not as

good as in D/D. MBF in C/IOD was lower than in IFDP/IFDP. Chewing efficiency and MBF were

significantly lower in IFDP/IFDP, who had experienced chipping or fracture of the prosthetic

superstructure. Median MMT of patients with implant-supported prostheses was between those with

C/C and fully dentate participants. There was no significant difference in MMT between C/IOD and

IFDP/IFDP.

Conclusion: Supporting complete prostheses with oral implants seems to have positive effects on the

thickness of the masseter muscle, maximum bite force as well as chewing efficiency. The type of

implant-supported prostheses may have an influence on the magnitude of the effect.

Compared with conventional complete dentures,

implant-supported overdentures (IOD) and im-

plant-supported fixed dental prostheses (IFDP)

seem to offer substantial psycho-social and func-

tional benefits to the edentulous individuals

(Feine et al. 1994a; Brennan et al. 2010). Once

all teeth are lost, the stabilization of the lower

denture with two implants placed in the inter-

foraminal region was recommended as treatment

of first choice (Thomason et al. 2009). The

improvements of orofacial functions with IOD

comprises of increased bite force (van der Bilt et

al. 2010a), larger chewing cycles, better coordi-

nation of the chewing sequence (Benzig et al.

1994) as well as improved masticatory efficiency

and ability (van Kampen et al. 2004). In addition,

they seem to provide better oral health-related

quality of life (Rashid et al. 2011) and might even

be more cost effective (Emami et al. 2009) than

conventional full dentures. Also, dental implants

seem to slow down the peri-implant alveolar

bone loss in the edentulous mandible and thus

show tertiary preventive properties (Behneke

1994).

The patient’s age and years of the edentulism

have a negative impact on the macro- and micro-

scopic structure of the chewing muscles (Raustia

et al. 1996). The cross-sectional area as well as

radiographic density of the masseter and medial

pterygoid muscle decrease with age and these

effects are significantly aggravated by edentulism

(Newton et al. 1993). In an animal model the

change from a hard to a soft texture diet reduced

the weight of the masseter muscle significantly.

Mice fed with a soft diet lost 19% of the muscle

weight within 1 week (Urushiyama et al. 2004).

Date:Accepted 31 March 2011

To cite this article:Muller F, Hernandez M, Grutter L, Aracil-Kessler L,Weingart D, Schimmel M. Masseter muscle thickness,chewing efficiency and bite force in edentulous patients withfixed and removable implant-supported prostheses: a cross-sectional multicenter study.Clin. Oral Impl. Res. 23, 2012 144–150doi: 10.1111/j.1600-0501.2011.02213.x

144 © 2011 John Wiley & Sons A/S

.;

Page 2: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

These findings are particularly relevant for com-

plete denture wearers who often compensate the

lack of masticatory ability by changing to a softer

diet (Millwood & Heath 2000). The observed

atrophy of the muscle tissues in edentulous

patients with conventional complete dentures

may therefore be caused by a ‘‘de-training’’ effect.

Newton et al. (2004) have demonstrated that

overdentures supported by natural roots seem to

counteract atrophy of the jaw closing muscles.

For implant-supported dental prostheses evidence

on their effect on masticatory muscle atrophy

remains scarce (Schimmel et al. 2010). Also, it

remains unclear if IFDP provide better function

and show a superior effect on the macroscopic

structure of the jaw closing muscles than IOD

(Feine et al. 1994b). Such findings would under-

line the preventive value of placing fixed implant-

supported restorations rather than removable

IODs.

The aim of the study was to test the hypoth-

eses: Edentulous patients who were restored with

maxillary complete dentures and mandibular

IOD show lower masticatory efficiency (first

H0), lower maximum voluntary bite force

(MBF) (second H0) and reduced masseter muscle

thickness (MMT) (third H0) compared with pa-

tients with upper and lower IFDP.

Concerning these investigated parameters,

both implant-born reconstructions perform better

than controls with conventional complete den-

tures (fourth H0) and are inferior to volunteers

with a natural dentition (fifth H0).

Materials and methods

Approval was obtained from the ethics commit-

tees of the University Hospitals of Geneva,

Switzerland (Ref.: 08-162/Psy 08-020) and the

Medical Association of Baden-Wurttemberg,

Germany (Ref.: 2009-084-f-z). Written informed

consent was obtained before the experiments.

Subjects

For this multicenter cross-sectional study, 80

patients with similar age were recruited (four

sites: two clinics, two private practices). Inclu-

sion criteria comprised of edentulism and the

provision of maxillary complete dentures and

mandibular implant-supported overdentures (C/

IOD), upper and lower implant-supported fixed

dental prostheses (IFDP/IFDP) or conventional

complete dentures (C/C, first control-group) at

least 1 year before the experiments. Furthermore,

participants were selected to be similar in gender,

wearing period of the current prostheses and the

time of edentulism. The second control-group

(D/D) consisted of fully dentate participants.

Exclusion criteria were history of neuromuscular

disease, radiotherapy and clinically relevant TMJ

dysfunction.

Chewing efficiency

Chewing efficiency was evaluated with a pre-

viously described two-colour mixing ability test

(Schimmel et al. 2007). Commercially available

chewing gum in azure and pink colour (The Wrig-

ley Company Ltd, Plymouth, Devon, UK) served

as test food. The specimen (30 � 18 � 3mm) was

placed on the tongue and the participant was asked

to masticate the gum for 20 chewing cycles on his/

her preferred chewing side. It was then retrieved

from the oral cavity, placed into a transparent

plastic bag and flattened to a 1-mm-thick wafer.

The wafer was scanned with a flatbed scanner and

the images subsequently copied into a template of

fixed size. Using the ‘‘magic wand tool’’ and

‘‘histogram’’ function (Adobe Photoshop Elements

2.0, Adobe Systems Inc., San Jose, CA, USA) the

total number of pixels of unmixed azure colour was

evaluated and subsequently, the ratio of azure pixels

to the total pixels of the original template was

calculated (unmixed fraction [UF]).

UF shows characteristics of a logarithmic func-

tion (log10) on the base of chewing cycles and will

decrease for two reasons: a higher degree of colour

mixture (lower ratio of unmixed azure) and a

reduction in volume of the specimen due to

sweetener extraction (Schimmel et al. 2007,

2011). Both are measures for chewing efficiency

(Anastassiadou & Heath 2001; van der Bilt et al.

2010b); thus the smaller the UF, the higher is the

individual chewing efficiency.

MBF

The Occlusal Force-Meter GM 10s

(Nagano Keiki

Co. Ltd; 1-30-4 Higashimagome, Ohta-ku, To-

kyo, Japan) was utilized (Nakatsuka et al. 2006). It

is a digital force gauge with an 8.6-mm-thick bite

element. MBF was assessed bilaterally between

the upper and lower first molar. The participant

was asked to bite as hard as possible on the force

gauge, but to stop clenching when she/he started

feeling uncomfortable. The mean of six recordings

(3 � right, 3 � left) was used for analysis. Further-

more, participants with IFDP/IFDP were asked if

they had experienced a fracture of the framework

and/or chipping of the veneering material since

their prosthesis had been provided.

MMT

MMT was evaluated bilaterally with real time

ultrasound scanners (FALCO 100 [PieMedical,

Imaging BV, Maastricht, The Netherlands] or

MyLab25 [Esaote, Genova, Italy]) and linear array

transducers (6–8 or 4–13 MHz, respectively). The

two examiners (M. H., M. S.) had been calibrated

by the experienced operator, who had developed

the method (Kiliaridis & Kalebo 1991). The parti-

cipants sat upright with no head support. The

anterior border and subsequently the origin as

well as insertion of the masseter muscle were

palpated to locate the thickest part of the muscle

as site for the measurement. To avoid compression

of the muscle a generous amount of ultrasound

contact gel was applied to the probe (Kendall

Meditec, Mirandola (MO), Italy). The transducer

was oriented perpendicular to the mandibular ra-

mus to avoid oblique scanning, as this would result

in artificially elevated readings (Fig. 1). The probe

was then tilted until the reflection of the bone was

depicted as a sharp white line. The thickest part of

the muscle close to the occlusal plane level was

measured (distance between ramus and fascia,

resolution of 0.1 mm). For MMT the mean of the

four readings in contracted muscle condition

(2 � right, 2 � left) was used for analysis. The

error of the method ranged from 0.2 to 0.4 mm

(Kiliaridis & Kalebo 1991; Botteron et al. 2009).

Statistical analysis

Categorical variables were compared using w2-

tests or Fisher’s exact test. A priori comparisons

Fig. 1. Example of an image of a masseter muscle obtained with ultrasonography. The distance between the thickest part of

the muscle between ramus mandibularis and muscle fascia (white arrow) in contracted muscle condition was used for

evaluation of masseter muscle thickness.

Muller et al �Masseter muscle thickness and bite force

© 2011 John Wiley & Sons A/S 145 | Clin. Oral Impl. Res. 23, 2012 / 144–150

Page 3: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

between C/IOD and IFDP/IFDP were performed

using Mann–Whitney U-tests to assess the first,

second and third H0. Continuous data of all

investigated groups of different dental state were

then compared using Kruskal–Wallis tests to

investigate the fourth and fifth H0; post hoc tests

were performed with adjusted P-values for multi-

ple comparisons between groups (Siegel & Cas-

tellan 1988). Non-parametric 95% confidence

intervals (95% CI) for the difference between

medians of two groups C/IOD and IFDP/IFDP

(point estimate of shift: y¼pop2�pop1) was

computed using the Hodges–Lehmann estimates

of shift parameters. The level of significance for

type 1 errors was set at ao0.05. Hypothetical

sample size calculation was performed for type 2

errors with a power of 1�b40.9 using GnPower

3.1 (Faul et al. 2009). All statistical tests were

performed using Stata Statistical Software release

11 (Stata Corporation, College Station, TX,

USA). Figures were drawn with StatView for

Windows 5.0 (SAS Institute Inc., Carry, NC,

USA).

Results

Subjects

The four groups were not significantly different

regarding gender (P¼0.85, Fisher’s exact test),

time of edentulism (P¼0.557, Kruskall–Wallis)

and wearing period of the present prosthesis

(P¼0.334, Kruskall–Wallis) (Table 1). All pa-

tients were satisfied with their prostheses to the

degree that they did not actively seek dental

treatment.

In the C/IOD-group all participants wore max-

illary conventional complete dentures, six had

mandibular IOD with bar-attachments on four

implants, and further 14 presented with ball or

Locators

attachments on two implants. All IODs

were placed on Straumanns

implants (Basel,

Switzerland). The IFDP/IFDP-group comprised

one patient with 16 implants, 10 patients with

14 implants, six patients with 12 implants, one

patient with 13 implants, one patient with 10

implants and one patient with eight implants.

Seven patients presented with composite ve-

neered bridges and further 13 had ceramic-fused

metal prostheses. Of the 20 IFDP/IFDP patients,

13 were restored with single-unit prostheses,

whereas seven patients presented with three to

six unit restorations. Six patients had Nobel

Biocares

(Gothenburg, Sweden) and further 14

Straumanns

implants.

Chewing efficiency

Chewing efficiency as evaluated with the two-

colour mixing ability test was significantly dif-

ferent between the four groups (P¼0.0001, Krus-

kal–Wallis). The lowest chewing performance

was found in the conventional complete denture

control-group with the highest ratio of unmixed

colour and the highest efficiency in the fully

dentate control-group. The groups with im-

plant-supported restorations showed median

chewing efficiencies between the control-groups

(Fig. 2). No difference was found between C/IOD

and IFDP/IFDP (P¼0.339, Mann–Whitney,

y¼ �0.01055: 95% CI for y: [�0.0264,

0.0093]). In each of the groups with implant-

supported restorations C/IOD and IFDP/IFDP a

sample size of n¼536 (total n¼1072) would

have to be realized to demonstrate a significant

difference (a¼0.05, power¼0.9, m1¼0.05706,

m2¼0.0507, SD1¼0.028532, SD2¼0.035315,

n2/n1¼1). The dentate control-group (D/D)

showed a significantly better masticatory effi-

ciency than all other groups except for IFDP/

IFDP. The conventional complete denture wear-

ers chewed significantly less efficient than all

other groups (Fig. 3).

MBF

MBF was significantly different between groups

(P¼0.0001, Kruskal–Wallis). The lowest forces

were found in the C/C-group, the highest values

were measured in the D/D-group. The partici-

pants, who were restored with C/IOD, showed

significantly lower forces than those with IFDP/

IFDP (P¼0.0002, Mann–Whitney, y ¼118.165:

95% CI for y: [70.33, 196.84]). The IFDP/IFDP-

group showed a lower median MBF than the fully

dentate control-group, however, this difference

was not significant. The mean MBF in the C/C-

group was only 69.7% of the mean MBF in the

C/IOD-group, but again the difference was not

significant (Fig. 4).

Fracture experience in IFDP/IFDP and itsinfluence on UF and MBF

Of the 20 participants with IFDP/IFDP, 10 had

experienced a chipping of the veneering material

or fracture of the bridge framework of their

prosthetic superstructure during time in function.

The participants with such fracture occurrence

showed a significantly lower chewing efficiency

(with fracture: UF¼mean 0.074 � 0.035, with-

out fracture: UF¼mean 0.03 � 0.02, P¼0.004,

Mann–Whitney) as well as a significantly lower

MBF (with fracture: mean 176.4 � 112.57 N,

without fracture: mean 363.6 � 249.85 N,

P¼0.041, Mann–Whitney).

MMT

There was a significant difference in MMT be-

tween the four groups (P¼0.002, Kruskal–

Table 1. Descriptive of the study population: maxillary complete dentures and mandibular implant-supported overdentures (C/IOD), bimaxillary implant-supported fixed dental prostheses (IFDP/IFDP),complete full dentures (C/C), fully dentate (D/D)

C/IOD IFDP/IFDP C/C D/D

N 20 20 20 20Age (years � SD) 68.1 � 4.6 61.5 � 8.3 68.2 � 6.2 66.4 � 8Gender 9#, 11~ 8#, 12~ 6#, 14~ 8#, 12~Edentulous since (years � SD) 7.3 � 5.9 7.6 � 6.5 9 � 11.2 NAProstheses in function (years � SD) 4 � 2.6 3.89 � 2.1 3.3 � 3 NA

NA, not applicable.

0.001

0.01

0.1

10 5 10 20 30 50

log UF

Chewing cycles

C/CC/IODIFDP/IFDPD/D

Fig. 2. Nomogram of 20 fully dentate, healthy, young adults: data taken from a previous study (Schimmel et al. 2007). The

unmixed fraction (UF) of azure colour follows an almost logarithmic function on the base of chewing cycles and is thus a

measure for chewing efficiency. A high UF correlates to a low chewing performance and vice versa. Complete denture wearers

(C/C: UF¼0.106 � 0.041, n¼20) showed the lowest and dentate participants (D/D: UF¼0.028 � 0.014, n¼20) the

highest chewing efficiency. Participants with maxillary complete dentures and mandibular implant-supported overdentures

(C/IOD: UF¼0.057 � 0.029, n¼20) were not different from participants with bimaxillary implant-supported fixed dental

prostheses (IFDP/IFDP: UF¼0.051 � 0.035, n¼20, P¼0.339, Mann–Whitney).

Muller et al �Masseter muscle thickness and bite force

146 | Clin. Oral Impl. Res. 23, 2012 / 144–150 © 2011 John Wiley & Sons A/S

Page 4: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

Wallis). The thinnest masseter muscles were

found in the C/C-group, the thickest muscles

in the D/D-group. The results for MMT in the C/

IOD-group were statistically not different from

those in the IFDP/IFDP-group (P¼0.536, Mann–

Whitney, y¼0.3625002: 95% CI for y: [�1.075,

1.925]). To each group C/IOD and IFDP/IFDP a

sample size of n¼271 (total n¼542) would have

to be attributed in order to demonstrate a sig-

nificant difference (a¼0.05, power ¼0.9,

m1¼13.2875, m2¼13.9039, SD1¼2.07162,

SD2¼2.34623, n2/n1¼1). MMT in the two

groups with implant-supported dental prostheses

was higher than in the control-group of edentu-

lous participants with conventional full dentures,

nevertheless this result was not significant when

the P-value for significance was adjusted for

multiple comparisons between the groups (Krus-

kal–Wallis, adjusted P¼0.004). Furthermore,

MMT in the IFDP/IFDP-group were not signifi-

cantly different from those in the fully dentate

control-group (Fig. 5).

Discussion

The benefits of stabilizing complete dentures by

means of oral implants are largely documented

(Thomason et al. 2009). Fixed implant-supported

dental prostheses seem to be a valid treatment

option especially for younger patients, yet the

clinical effort and cost are considerably higher

(Feine et al. 1994a; Lambert et al. 2009). Little is

known if fixed restorations offer superior func-

tional and structural benefits to IOD (Brennan et

al. 2010, Carlsson & Lindquist 1994).

Chewing efficiency

As expected, study participants with conven-

tional full dentures showed the lowest chewing

efficiency and fully dentate ones the highest.

This result is intuitive and corresponds to evi-

dence from the literature (Manly & Braley 1950;

Ikebe et al. 2010). However, no difference be-

tween edentulous patients with C/IOD and

IFDP/IFDP was found. Statistically this may be

explained either by the absence of a difference or a

lack of power of the current study. As post hoc

power analyses are subject to controversial dis-

cussion (Thomas 1997) a hypothetical sample

size calculation, to avoid type II errors on the

basis of the current results, was performed. In

each implant-group a sample size of 536 partici-

pants would have to be included to demonstrate a

significant difference with a power of 90%. It can

thus be concluded that, if there were a difference,

it would be extremely small and of no clinical

relevance. The first null-hypothesis must there-

fore be rejected. Chewing with removable pros-

theses may be limited by a displacement or

loosening of the denture during unfavourable

loading or food getting caught underneath the

denture base. When the upper complete denture

and the posterior parts of the lower denture are

mucosa-born, chewing forces may be limited by

pain from the denture bearing tissues. Removable

denture wearers may further chew more cau-

tiously, as they may be aware that the denture

resin can fracture while chewing hard food-stuffs.

However, the total occlusal surface area is sig-

nificantly correlated with chewing efficiency

(Bourdiol & Mioche 2000); and removable den-

tures frequently replace the second molars and

restore the posterior denture teeth in their full

oro-vestibular dimension. The total occlusal sur-

face available for chewing may therefore be larger

in C/IOD than in patients with fixed reconstruc-

tions. These opposed effects may have finally

eliminated any differences in UF between C/IOD

and IFDP/IFDP participants in the present study.

Reports in the literature on the masticatory

efficiency of bimaxillary implant-supported pros-

theses are scarce. Carlsson and Lindquist com-

0

100

200

300

400

500

600

700

800

900

MB

F [

N]

[p<0.0001]

[p<0.0001]

[p=0.129]

[p<0.0001]

[p=0.0002*]

[p=0.181]

Fig. 4. Abbreviations as in Fig. 2. Box plot of maximum voluntary bite force measured in the four groups of participants.

(nMann–Whitney test for second H0, all other P-values: Kruskall–Wallis for multiple comparisons between groups, adjusted P-

value for significance: 0.004, each group n¼20, mean values with standard deviation below group descriptive.)

0

.02

.04

.06

.08

.1

.12

.14

.16

.18

.2

UF

[p=0.00006]

[p=0.0006]

[p=0.011]

[p<0.0001]

[p=0.339*]

[p=0.001]

C/IOD0.057±0.029

IFDP/IFDP0.051±0.035

C/C0.106±0.041

D/D0.028±0.014

Fig. 3. Abbreviations as in Fig. 2. Box plot of unmixed fraction (UF), which is a measure for chewing efficiency. A high UF

correlates to a low chewing performance and vice versa. (nMann–Whitney test for first H0, all other P-values: Kruskall–Wallis

for multiple comparisons between groups, adjusted P-value for significance: 0.004, each group n¼20, mean values with

standard deviation below group descriptive.)

Muller et al �Masseter muscle thickness and bite force

© 2011 John Wiley & Sons A/S 147 | Clin. Oral Impl. Res. 23, 2012 / 144–150

Page 5: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

pared in a 10 year follow-up study patients with

maxillary complete dentures/mandibular IFDP to

those with bimaxillary IFDP. In their study, no

difference in masticatory efficiency between

those two groups was found which is in agree-

ment with the results of the current study.

Interestingly, the subjective perception of masti-

catory function was significantly higher in pa-

tients with bimaxillary IFDP, so that the gain for

such treatment may mainly be psychological

(Carlsson & Lindquist 1994).

MBF

Albeit a similar chewing efficiency, in the pre-

sent study MBF was significantly lower in parti-

cipants with C/IOD than with IFDP/IFDP. Both

groups lack periodontal receptors in the surround-

ings of the dental implants and subsequently

projections on the primary sensory and motor

cortex (Abarca et al. 2006). But in contrast to the

fixed restorations the C/IOD provide a close

contact of the denture base with the underlying

mucosa. Previous experiments with complete

dentures showed, that a good retention of a lower

denture and thus an intimate contact between

the denture base and the denture bearing tissues

allows for a higher inter-occlusal tactile sensitiv-

ity than in edentulous patients with poor lower

denture retention (Muller et al. 1995). It is likely

that the quantity and/or quality of stimuli to the

mechanoreceptors in the mucosa account for this

finding. The higher MBF in patients restored

with IFDP/IFDP may therefore be related to a

reduced peripheral input, which is necessary to

tune muscle force during oral function. Harald-

son (1983) reported that the reduction of muscle

force during a chewing sequence along with the

softening of the food bolus was less in patients

with fixed implant-bridges than in dentate indi-

viduals. There seems to be unique activation

patterns of the jaw closing muscles in patients

with oral implants which implies a less graduated

contraction of the jaw closing muscles if biting is

performed on implant-supported prostheses

(Gartner et al. 2000). In the current study, the

fixed implant-supported dental restorations var-

ied with regard to the number of implants and

type of the superstructures used. This implies

differences in the total implant–bone contact

surface between the patients who might have

influenced the inter-occlusal perception and con-

sequently the fine motor control. If osseopercep-

tion is caused by vibration (Klineberg et al. 2005),

the different damping characteristics of the ve-

neering materials (ceramic/composite) would

have influenced the results.

Although in the current study MBF in patients

with C/IOD proved higher than patients with

conventional full dentures, the difference was not

significant which contrasts with previous find-

ings reported in the literature (van der Bilt et al.

2010a). This result may be related to the applied

measuring technique as MBF was assessed uni-

laterally with an 8.6-mm-thick gauge. The use of

thinner pressure sensitive foils would have re-

duced the gape and allowed for higher MBF in

both groups (Proschel et al. 2008). Higher forces

might have possibly accentuated a possible dif-

ference in MBF between the C/C and C/IOD

groups.

A further interesting finding is the discrepancy

in chewing efficiency and MBF between partici-

pants who experienced a fracture of their fixed

dental prostheses and those who did not. These

fractures may have resulted from an impaired

mechanosensation with IFDP/IFDP (Luraschi

2009) and consequently a poor motor control

(Trulsson & Gunne 1998). Another possible ex-

planation would be technical shortcomings of the

reconstructions as clear differences in fracture

prevalence had occurred between the different

centres. Thus particular attention should be

paid to technical execution and occlusion of

implant-supported prostheses. Patients might

have also lost confidence in the durability of

their IFDPs and consequently avoided applying

maximum forces when asked during the experi-

ments; a presumption confirmed qualitatively by

several participants with fracture experience.

MMT

In the current study, MMT was assessed with

ultrasound as described by Kiliaridis & Kalebo

(1991). The method shows only small errors (in

contracted muscle condition 0.2–0.4 mm), does

not use electromagnetic radiation like computed

tomography and does not necessitate supervision

and interpretation of a specialist radiologist. For

this multicenter study, which also included pa-

tients from private practice an added advantage

was the portability of the ultrasound equipment.

Although atrophy of the masseter and medial

pterygoid muscles related to age and edentulism

is well documented (Newton et al. 1993), there is

little evidence on the morphological effects of

dental prostheses on the masticatory muscles.

Newton et al. (2004) had demonstrated that the

retention of natural roots covered by overdentures

was associated with less atrophied chewing mus-

cles than in subjects with conventional full den-

tures. Schimmel et al. (2010) had described the

case of a patient who had regained MMTafter the

stabilization of the lower denture with two im-

plants. The current study demonstrated, with the

conceptual limitations of any cross-sectional

study, the positive structural effects of mastica-

tory muscles of implant placement in edentulous

patients. Because of the cross-sectional study

design, it remains unclear if the placing of im-

plants prevented atrophy of the masseter muscles

or if the patients regained muscle mass through

improved function.

Prolonged low activity of muscles will result in

atrophy both on a macroscopic and microscopic

level. Consequently, the cross-sectional area of

the masticatory muscles is reduced in edentulous

8

10

12

14

16

18

20

22

MM

T [

mm

]

C/IOD13.29±2.07

IFDP/IFDP13.90±2.35

C/C11.98±1.84

D/D15.05±2.68

[p=0.011]

[p=0.021]

[p=0.082]

[p<0.0001]

[p=0.536*]

[p=0.043]

Fig. 5. Abbreviations as in Fig. 2. Box plot of masseter muscle thickness measured in the four groups of different dental state.

(nMann–Whitney test for third H0, all other P-values: Kruskall–Wallis for multiple comparisons between groups, adjusted P-

value for significance: 0.004, each group n¼20, mean values with standard deviation below group descriptive.)

Muller et al �Masseter muscle thickness and bite force

148 | Clin. Oral Impl. Res. 23, 2012 / 144–150 © 2011 John Wiley & Sons A/S

Page 6: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

patients compared with dentate subjects, regard-

less of their age (Newton et al. 1993), a finding

that was confirmed by the current study. Also,

the radiographic density of these muscles is

reduced after a long wearing time of conventional

full dentures (Raustia et al. 1996). On a micro-

scopic level ageing muscle tissue shows a de-

creased fibre diameter, a degenerated sarcoplasm

and a replacement of muscle fibres by fat and

connective tissue (Larsson 1995). Temporal mus-

cle type II fibres in denture wearers, who rate

their dentures as insufficient, are smaller than

the corresponding fibres in the dentate patients

(Ringqvist 1974). She suggested that the low

percentage and small size of these fibres in

denture wearers might be attributed to reduced

functional demands. The described studies may

only in part explain the age- and function-related

changes in the masticatory muscles. Findings

from other muscles may not apply to the chewing

muscles as their functioning, their embryo-ge-

netic origin and the fibre composition are unique

in the human body (Monemi et al. 1998).

Edentulous patients benefit from an improved

muscle activity by stabilizing the lower denture

with two implants, but there seems to be no

further improvement of these parameters by

providing bimaxillary IFDPs (Ferrario et al.

2004; Heckmann et al. 2009). The current study

confirmed these results on a morphological level.

The third null-hypothesis must be rejected, as

MMT between the two implant-groups was not

statistically different. Patients with implant-sup-

ported dental prostheses showed thicker masseter

muscles than edentulous patients with conven-

tional full dentures, although the result was no

longer significant when the statistical test was

corrected for multiple comparisons between

groups.

Summary and conclusion

Although the stabilization of conventional man-

dibular dentures with dental implants improves

chewing efficiency significantly, the effect might

not be improved further by providing edentulous

patients with bimaxillary implant-supported

fixed prostheses.

A fracture experience with the dental recon-

struction may limit the functional benefit.

In edentulous patients, supporting or stabiliz-

ing dental prostheses by placing oral implants

seems to have positive effects on the training

level and dimension of the masseter muscle.

The type of implant prostheses may have an

influence on the magnitude of the effect. The

functional advantages of implant reconstructions

and their tertiary preventive properties on the

masseter muscle should be considered in treat-

ment planning.

Acknowledgements: The study was

supported by the ITI Foundation (grant no.

552_2008). The contributions of Prof Dr Jean-

Pierre Bernard, Prof Dr Urs Belser and Dr

German Gallucci (University of Geneva,

Switzerland), Dr Manfred Imsand (Sion,

Switzerland), Dr Kamel Salem (Morges,

Switzerland), Leonard Brazzola (Lausanne,

Switzerland) and the staff of the Divisions of

fixed and removable Prosthodontics of the

University of Geneva to the clinical care and

recruitment of study participants is greatly

acknowledged. Furthermore the authors want

to express their gratitude to Priv. Doc. Dr

Francois R Herrmann, MPH (University

Hospitals of Geneva, Switzerland) for his help

with the statistical analysis. Thanks are also

due to Prof Dr Stavros Kiliaridis (University of

Geneva, Switzerland) for teaching the

ultrasound method and calibrating the two

examiners of the study.

References

Abarca, M., Van Steenberghe, D., Malevez, C. & Jacobs,

R. (2006) The neurophysiology of osseointegrated oral

implants. A clinically underestimated aspect. Journal

of Oral Rehabilitation 33: 161–169.

Anastassiadou, V. & Heath, M.R. (2001) The develop-

ment of a simple objective test of mastication suitable

for older people, using chewing gums. Gerodontology

18: 79–86.

Behneke, N. (1994) Klinische Erfahrungen mit enossa-

len Implantaten im zahnlosen Unterkiefer. Dr Med

Dent Habil Thesis, Johannes Gutenberg-University,

Mainz, Germany.

Benzig, U., Weber, H., Simonis, A. & Engel, E. (1994)

Changes in chewing patterns after implantation in the

edentulous mandible. The International Journal of

Oral & Maxillofacial Implants 9: 207–213.

Botteron, S., Verdebout, C.M., Jeannet, P.Y. & Kiliar-

idis, S. (2009) Orofacial dysfunction in Duchenne

muscular dystrophy. Archives of Oral Biology 54:

26–31.

Bourdiol, P. & Mioche, L. (2000) Correlations between

functional and occlusal tooth-surface areas and food

texture during natural chewing sequences in humans.

Archives of Oral Biology 45: 691–699.

Brennan, M., Houston, F., O’Sullivan, M. & O’Connell,

B. (2010) Patient satisfaction and oral health-related

quality of life outcomes of implant overdentures and

fixed complete dentures. The International Journal of

Oral & Maxillofacial Implants 25: 791–800.

Carlsson, G.E. & Lindquist, L.W. (1994) Ten-year long-

itudinal study of masticatory function in edentulous

patients treated with fixed complete dentures on

osseointegrated implants. International Journal of

Prosthodontics 7: 448–453.

Emami, E., Heydecke, G., Rompre, P.H., de Grand-

mont, P. & Feine, J.S. (2009) Impact of implant

support for mandibular dentures on satisfaction, oral

and general health-related quality of life: a meta-

analysis of randomized-controlled trials. Clinical

Oral Implants Research 20: 533–544.

Faul, F., Erdfelder, E., Buchner, A. & Lang, A.G. (2009)

Statistical power analyses using Gnpower 3.1: tests for

correlation and regression analyses. Behavior Re-

search Methods 41: 1149–1160.

Feine, J.S., de Grandmont, P., Boudrias, P., Brien, N.,

LaMarche, C., Tache, R. & Lund, J.P. (1994a)

Within-subject comparisons of implant-supported

mandibular prostheses: choice of prosthesis. Journal

of Dental Research 73: 1105–1111.

Feine, J.S., Maskawi, K., de Grandmont, P., Donohue,

W.B., Tanguay, R. & Lund, J.P. (1994b) Within-

subject comparisons of implant-supported mandibular

prostheses: evaluation of masticatory function. Jour-

nal of Dental Research 73: 1646–1656.

Ferrario, V.F., Tartaglia, G.M., Maglione, M., Simion,

M. & Sforza, C. (2004) Neuromuscular coordination

of masticatory muscles in subjects with two types of

implant-supported prostheses. Clinical Oral Im-

plants Research 15: 219–225.

Gartner, J.L., Mushimoto, K., Weber, H.P. & Nishi-

mura, I. (2000) Effect of osseointegrated implants

on the coordination of masticatory muscles: a

pilot study. Journal of Prosthetic Dentistry 84:

185–193.

Haraldson, T. (1983) Comparisons of chewing patterns

in patients with bridges supported on osseointegrated

implants and subjects with natural dentitions. Acta

Odontology Scandinavica 41: 203–208.

Heckmann, S.M., Heussinger, S., Linke, J.J., Graef, F.

& Proschel, P. (2009) Improvement and long-term

stability of neuromuscular adaptation in implant-

supported overdentures. Clinical Oral Implants Re-

search 20: 1200–1205.

Ikebe, K., Matsuda, K., Murai, S., Maeda, Y. & Nokubi,

T. (2010) Validation of the Eichner index in relation to

occlusal force and masticatory performance. Interna-

tional Journal of Prosthodontics 23: 521–524.

Kiliaridis, S. & Kalebo, P. (1991) Masseter muscle

thickness measured by ultrasonography and its rela-

tion to facial morphology. Journal of Dental Research

70: 1262–1265.

Klineberg, I., Calford, M.B., Dreher, B., Henry, P.,

Macefield, V., Miles, T., Rowe, M., Sessle, B. &

Trulsson, M. (2005) A consensus statement on osseo-

perception. Clinical and Experimental Pharmacology

and Physiology 32: 145–146.

Lambert, F.E., Weber, H.P., Susarla, S.M., Belser, U.C.

& Gallucci, G.O. (2009) Descriptive analysis

of implant and prosthodontic survival rates with

fixed implant-supported rehabilitations in the

edentulous maxilla. Journal of Periodontology 80:

1220–1230.

Larsson, L. (1995) Motor units: remodeling in

aged animals. The Journals of Gerontology Series A:

Biological Sciences and Medical Sciences 50:

91–95.

Muller et al �Masseter muscle thickness and bite force

© 2011 John Wiley & Sons A/S 149 | Clin. Oral Impl. Res. 23, 2012 / 144–150

Page 7: Masseter muscle thickness, chewing efficiency and bite force in edentulous patients with fixed and removable implant-supported prostheses: a cross-sectional multicenter study

Luraschi, J. (2009) Mechanosensation in totally edentu-

lous persons rehabilitated by means of implant-sup-

ported fixed dental prostheses. Dr Med Dent, Thesis,

University of Geneva, Geneva, Switzerland.

Manly, R.S & Braley, L. (1950) Masticatory perfor-

mance and efficiency. Journal of Dental Research

29: 448–462.

Millwood, J. & Heath, M.R. (2000) Food choice by older

people: the use of semi-structured interviews with

open and closed questions. Gerodontology 17: 25–32.

Monemi, M., Eriksson, P.O., Eriksson, A. & Thornell,

L.E. (1998) Adverse changes in fibre type composition

of the human masseter versus biceps brachii muscle

during aging. Journal of the Neurological Sciences

154: 35–48.

Muller, F., Link, I., Fuhr, K. & Utz, K.H. (1995) Studies

on adaptation to complete dentures. Part ii: oral

stereognosis and tactile sensibility. Journal of Oral

Rehabilitation 22: 759–767.

Nakatsuka, K., Usui, T., Masuda, Y., Rugh, J. &

Kurihara, S. (2006) Accuracy and repeatability of the

GM10 occlusal force-meter. Nihon Kyosei Shika

Gakkai Taikai Puroguramu, Shorokushu 65: 336.

Newton, J., Yemm, R., Abel, R. & Menhinick, S. (1993)

Changes in human jaw muscles with age and dental

state. Gerodontology 10: 16–22.

Newton, J.P., McManus, F.C. & Menhenick, S. (2004)

Jaw muscles in older overdenture patients. Gerodon-

tology 21: 37–42.

Proschel, P.A., Jamal, T. & Morneburg, T.R. (2008)

Motor control of jaw muscles in chewing and in

isometric biting with graded narrowing of jaw gape.

Journal of Oral Rehabilitation 35: 722–728.

Rashid, F., Awad, M.A., Thomason, J.M., Piovano, A.,

Spielberg, G.P., Scilingo, E., Mojon, P., Muller, F.,

Spielberg, M., Heydecke, G., Stoker, G., Wismeijer,

D., Allen, F. & Feine, J.S. (2011) The effectiveness of

2-implant overdentures – a pragmatic international

multicentre study. Journal of Oral Rehabilitation 38:

176–184.

Raustia, A.M., Salonen, M.A. & Pyhtinen, J. (1996)

Evaluation of masticatory muscles of edentulous

patients by computed tomography and electromyo-

graphy. Journal of Oral Rehabilitation 23: 11–16.

Ringqvist, M. (1974) A histochemical study of temporal

muscle fibers in denture wearers and subjects with

natural dentition. Scandinavian Journal of Dental

Research 82: 28–39.

Schimmel, M., Christou, P., Herrmann, F. & Muller, F.

(2007) A two-colour chewing gum test for mastica-

tory efficiency: development of different assessment

methods. Journal of Oral Rehabilitation 34: 671–

678.

Schimmel, M., Leemann, B., Herrmann, F.R., Kiliar-

idis, S., Schnider, A. & Muller, F. (2011) Masticatory

function and bite force in stroke patients. Journal of

Dental Research 90: 230–234.

Schimmel, M., Loup, A., Duvernay, E., Gaydarov, N.

& Muller, F. (2010) The effect of lower denture

abstention on masseter muscle thickness in a 97

year-old patient: a case report. International Journal

of Prosthodontics 23: 418–420.

Siegel, S. & Castellan, N.J. (1988) Nonparametric

Statistics for the Behavioral Sciences. Singapore:

McGraw-Hill.

Thomas, L. (1997) Retrospective power analysis. Con-

servation Biology 11: 276–280.

Thomason, J.M., Feine, J., Exley, C., Moynihan, P.,

Muller, F., Naert, I., Ellis, J.S., Barclay, C., Butter-

worth, C., Scott, B., Lynch, C., Stewardson, D.,

Smith, P., Welfare, R., Hyde, P. & McAndrew, R.

(2009) Mandibular two implant-supported overden-

tures as the first choice standard of care for edentulous

patients-the York consensus statement. British Den-

tal Journal 207: 185–186.

Trulsson, M. & Gunne, H.S. (1998) Food-holding

and -biting behavior in human subjects lacking

periodontal receptors. Journal of Dental Research

77: 574–582.

Urushiyama, T., Akutsu, S., Miyazaki, J., Fukui, T.,

Diekwisch, T. & Yamane, A. (2004) Change from a

hard to soft diet alters the expression of insulin-like

growth factors, their receptors, and binding proteins in

association with atrophy in adult mouse masseter

muscle. Cell and Tissue Research 315: 97–105.

van der Bilt, A., Burgers, M., van Kampen, F.M. &

Cune, M.S. (2010a) Mandibular implant-supported

overdentures and oral function. Clinical Oral Im-

plants Research 21: 1209–1213.

van der Bilt, A., Mojet, J., Tekamp, F.A. & Abbink, J.H.

(2010b) Comparing masticatory performance and

mixing ability. Journal of Oral Rehabilitation 37:

79–84.

van Kampen, F.M., van der Bilt, A., Cune, M.S.,

Fontijn-Tekamp, F.A. & Bosman, F. (2004) Mastica-

tory function with implant-supported overdentures.

Journal of Dental Research 83: 708–711.

Muller et al �Masseter muscle thickness and bite force

150 | Clin. Oral Impl. Res. 23, 2012 / 144–150 © 2011 John Wiley & Sons A/S