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Received: 18 January 2022 Revised: 2 April 2022 Accepted: 12 April 2022

DOI: 10.1111/cid.13094

ORIGINAL ARTICLE

A comparative evaluation of neurophysiological activity, active


tactile sensibility and stereognostic ability of complete denture
prosthesis, and implant-supported prosthesis wearer—A
pilot study

Bappaditya Bhattacharjee BDS1 | Ritu Saneja MDS1 | Atul Bhatnagar MDS1 |


Ashish Verma PhD, DNB2 | Romesh Soni MDS1 | Ankita Singh MDS1 |
Pavan Dubey MDS1

1
Department of Prosthodontics, Faculty of
Dental Sciences, Banaras Hindu University, Abstract
Varanasi, Uttar Pradesh, India Aim: The study aimed to evaluate the effect of implant-supported prosthesis in
2
Department of Radiodiagnosis and Imaging,
completely edentulous participants in terms of osseoperception ability, neural activ-
Institute of Medical Sciences, Banaras Hindu
University, Varanasi, Uttar Pradesh, India ity, and stereognostic ability in comparison to removable prosthetic options.
Materials and Methods: A total sample of 18 patients, irrespective of gender and age
Correspondence
Atul Bhatnagar, Department of were allocated into three groups according to the three-treatment protocol (upper
Prosthodontics, Faculty of Dental Sciences,
and lower complete denture, upper complete denture opposing lower implant-
Banaras Hindu University, Varanasi 221005,
Uttar Pradesh, India. retained overdenture, implant-supported fixed prosthesis in both arches). Four weeks
Email: atuldent@hotmail.com
after completion of the treatment procedure active tactile sensibility (ATS) was
Funding information checked by using varying thicknesses (12, 40, 80, 100, 200 μ) of articulating foils and
Indian Council of Medical Research
papers. Functional magnetic resonance imaging (fMRI) was performed to record neu-
rophysiological activity in cerebral cortex in all the participants. Various forms of test
pieces (heat cure acrylic resin) were used to evaluate stereognostic ability. Data
regarding the neurophysiological activity were analyzed by using Krushkal–Wallis
test and p ≤ 0.05 was considered to be statistically significant. Data from
stereognostic ability test procedure and ATS were compared by using chi-squared
test and p ≤ 0.05 was considered to be statistically significant.
Results: Statistically significant difference was found in between the articulating foils
in terms of true negative responses as the foil thickness increased in participants
wearing complete denture in both the arches (p = 0.004) and implant-supported
fixed prosthesis in both the arches (p = 0.010). Participants in implant-supported
fixed prosthesis group showed significantly more activation in primary motor cortex
(right side), somatosensory cortex (left side), angular gyrus (both sides), temporal lobe
(left) compared to other groups. No significant difference found in thalamus and
premotor cortex region in between the participants of different groups. No statisti-
cally significant difference found in between the groups in terms of true responses
identifying correct shapes. Mean number of correct responses in stereognostic ability
test were 4.16 (83.33%), 3.5 (70%), 3.83 (76.66%) for participants of complete

Clin Implant Dent Relat Res. 2022;1–12. wileyonlinelibrary.com/journal/cid © 2022 Wiley Periodicals LLC. 1
2 BHATTACHARJEE ET AL.

denture group, upper complete denture opposing lower implant retained overdenture
group, and implant-supported fixed prosthesis group, respectively.
Conclusion: Primary motor cortex, somatosensory cortex, and other regions of brain
were diffusely activated in participants wearing implant-supported fixed prosthesis in
both the arches. Less number of false responses were recorded in participants of
implant-supported fixed prosthesis group and upper complete denture opposing
lower implant-retained overdenture group in ATS test compared to participants
wearing complete denture in both the arches.

KEYWORDS
edentulous mandible, fixed implant prosthesis, overdenture

Summary Box

What is known
• Progressive recovery of osseoperception occurs around implant-supported prosthesis.
• Recent studies have showed implant-supported prosthesis used to activate different regions
of cerebral cortex.
• Little is known on the stereognostic ability of different combination of prosthesis.

What this study adds


This comparative study evaluated active tactile sensibility, neurophysiological activity and
stereognostic ability in different types of prosthesis wearer and aimed to generate scientific evi-
dence on this topic.

1 | I N T RO DU CT I O N prosthesis undergoes integration with the stomatognathic system similar


to natural dentition. Perception level of implant-supported prosthesis is
Oral function and quality of life are dependent on number and condition quite similar to natural antagonists.9,10,11 It is quite evident that cerebral
of functional tooth units which influence the functioning of masticatory cortex and sensory homunculus in the brain undergoes some structural
apparatus of an individual.1,2 Various implant-supported prosthetic and functional changes to adapt with altered sensory perception in rela-
options (implant-retained overdentures, implant-supported fixed pros- tion to any part of human body.12 This phenomenon of structural and
thesis, and all-on-four prosthesis) have become available in recent times functional adaptation of human brain has been termed as “Neuro-
to rehabilitate edentulous ridges. Sensory perception of implant- plasticity.”13 Various factors like critical developmental periods of brain,
supported prosthetic options may play a role in its longevity and choice neuromodulatory inhibitors, and other factors like age, sex, and diseases
of loading protocol.3 The presence of mechanoreception observed after affecting brain can modify neuroplasticity phenomenon of human
4
loading of the implant is termed as osseoperception. Patient's percep- brain.13 Extraction of teeth and rehabilitation of edentulous space with
tion level in response to mechanical stimuli may reduce complications dental implant show changes in cerebral cortex of brain.14
for and around dental implants. Complications may further be reduced Evaluation of activated regions in the brain can be done through
through optimal occlusal contact and appropriate loading protocols.3,5 various imaging systems. Positron emission tomography (PET) was
The oral perception sensibility of dental implants can be tested widely used in past to evaluate the activated regions. However, due
either by having the test persons bite on thin test bodies (active tactile to its low temporal and spatial resolution and invasive nature of the
sensibility [ATS]) or by passively applying pressure on the occlusal sur- procedure newer imaging systems have evolved. Functional magnetic
face of the implant (passive tactile sensibility).6,7 How the sensory signals resonance imaging (fMRI) techniques make it possible to explore, non-
reach the cerebral cortex and how it remodels after extraction of teeth is invasively, the neuroplasticity in humans using BOLD (blood oxygen
a common research question of oral neuroscience in recent times. level dependent) method that measures blood flow changes in the
Batista and colleagues evaluated mean threshold of sensory perception brain, and uses these changes to determine brain areas activity during
of different combination of prosthesis in a comparative study. Study a specific task.15 Oral stereognosis (OS) is the neurosensorial ability of
showed threshold of sensory perception of implant-supported prosthesis the oral mucous membrane to recognize and discriminate the forms of
was quite high (10–14 μ) compared to complete denture wearers objects in the oral cavity. Temporal lobe of the cerebral cortex is the
(92 μ).8 Various studies have also reported that implant-supported higher center for discriminating size, shapes, and stereognostic
BHATTACHARJEE ET AL. 3

ability.16 Proper masticatory function generally improves when the • Participants rehabilitated with implant-supported fixed prosthesis
texture and shape of the particles can be adequately felt by an individ- were allocated in Group 3.
ual. These sensory signals are transmitted to the second and third
order neurons which relay in the cerebral cortex to generate the
chewing force and modulate three-dimensional movement of
mandible.17 2.3 | Clinical procedures
There is sizable evidence of progressive osseoperceptive recovery
after dental implant placement. However, there appears to be meager Complete dentures were fabricated using conventional technique and
number of studies exploring neuroplastic and stereognostic changes by following selective pressure impression technique. Teeth setting
occurring in brain and oral cavity in response to altered oral environ- were done in semi-adjustable articulator and bilateral-balanced occlu-
ment. There seems to be a lack of clarity on relationship of sion was used as an occlusal scheme. In participants of second group
osseoperception and neurosensory feedback pathways with neuro- two bone level-tapered implants (Touareg-S, Adin Dental Implant Sys-
plasticity. It is aimed with this pilot study to evaluate the correlation tem Ltd., Afula, Israel) with alumina oxide blasted/acid etched surface
between the neurophysiological activity through fMRI images, ATS, were placed in mandibular canine region (Figure 1). Standard surgical
and stereognostic ability of participants wearing implant-supported protocol and strict asepsis was maintained during the implant
fixed prosthesis, implant-retained overdenture opposing complete placement.
denture, and complete denture opposing complete denture.
TABLE 1 Inclusion and exclusion criteria

Inclusion criteria Exclusion criteria


2 | MATERIALS AND METHODS
1. Healthy patients with good 1. Patients with uncontrolled
oral hygiene systemic disorders
2.1 | Clinical data 2. Patients without any history 2. Patients with smoking habit
of temporomandibular joint and history of alcoholism
Completely edentulous patients were selected from departmental disorders, psychiatric 3. Patients with claustrophobia
disorders or on 4. Patients with implanted device
OPD by convenience sampling method due to COVID-19 pandemic
neurophysiology modifying (cardiac pacemakers, MRI
from February 2020 to July 2021. The edentulous participants who medication incompatible prosthetic heart
were willing to undergo with removable complete denture or fixed 3. Completely edentulous valves) that can affect the
implant-supported prosthesis or implant-supported overdenture were patients who were willing fMRI findings
included in this study. The study adopted parallel arm study design. for rehabilitation with 5. Patients with parafunctional
removable prosthesis disorders like clenching,
The study aimed to evaluate the effect of implant-supported pros-
4. Completely edentulous bruxism, tongue thrusting, etc.
thesis in completely edentulous participants in terms of osseoperception patients with bilateral severe 6. Patients with recent history of
ability, neural activity, and stereognostic ability in comparison to remov- pneumatization of maxillary undergoing radiotherapy
able prosthetic options. Participants were appraised in detail on study sinuses 7. Indifferent and poorly
5. Completely edentulous motivated patients
procedures, bi-lingual consent was obtained from all the participants.
patients with less vertical 8. Patients who were not willing
Ethical clearance was obtained from Banaras Hindu University bone height available in to appear in the follow-up visit
(Dean/2020/EC/1919) dated January 21, 2020. Trial was registered maxillary and mandibular due to other reasons.
in Clinical Trial Registry of India with reference number posterior region

CTRI/2020/11/029169. Abbreviation: fMRI, functional magnetic resonance imaging.

2.2 | Sample size and allocation

A total sample of 18 patients, irrespective of gender and age were


selected for study in accordance to the inclusion and exclusion criteria
(Table 1). Participants were allocated into three groups with each
group containing six participants. Individual groups were created
according to the treatment protocol.

• Edentulous participants rehabilitated with complete denture were


allocated in Group 1.
• Edentulous participants rehabilitated with maxillary complete den-
ture and two-implant-retained overdenture in mandibular arch F I G U R E 1 Postoperative radiographic view after placement of
were allocated in Group 2. implants in participants of Group 2
4 BHATTACHARJEE ET AL.

F I G U R E 2 Postoperative radiographic view


after placement of implants in participants of
Group 3

Lignocaine hydrochloride 2% with adrenaline (1:100 000) was


used through infiltration during surgery. Complete denture of the par-
ticipants was duplicated and used as a custom-made surgical guide.
Osteotomy was done under copious irrigation after elevating full-
thickness muco-periosteal flap by giving a midcrestal incision. After
completion of healing phase of 3 months, a second stage surgery was
performed and healing abutments were placed. After a healing period
of 2 weeks, ball abutments were placed. Acrylic resin was removed
from the intaglio surface of the mandibular denture and a space was
created for metal housing. Metal housing along with plastic sleeve was
placed on the ball abutment and self-cure acrylic resin was filled in the
previously made gap in the intaglio surface of the denture. Direct pick
up was taken. Proper seating of denture was then evaluated. Occlusal
evaluation and interferences were checked and corrected. FIGURE 3 Articulating foils and papers used in the study
In implant-supported fixed prosthesis group some participants
were rehabilitated with all-on-four treatment protocol as proposed by Patients of fixed implant-supported prosthesis group were reha-
Malo and colleagues18 and some participants were rehabilitated with bilitated with either screw-retained hybrid prosthesis/metal-ceramic
conventional implant-supported fixed prosthesis. In case of all-on-four prosthesis after evaluating the crown-height space. Participants reha-
treatment protocol in maxilla, initial osteotomy was started posteriorly bilitated with implant-supported metal-ceramic prosthesis were not

from second premolar/first molar region with pilot drill in a 30–45 included in this study due to chance of procedural complications dur-
angulation parallel to anterior wall of maxillary sinus. In the anterior ing functional MRI.
region, osteotomy were done in a parallel manner upto a sufficient
length to engage the nasal cortex. Subsequently osteotomy was
enlarged with drills of specific diameter and final implant placement 2.4 | Evaluation of data
(Touareg-S, Adin Dental Implant System Ltd.) were done.
In mandible initial, osteotomy was done in a tilted manner so that 2.4.1 | Active tactile sensibility
the apex of osteotomy remained a safe distance from mental foram-
ina. Posterior implants were inserted at tilted angulation (30–45 ). In the psychophysical approach, ATS of participants were checked
Anteriorly two implants were placed in axial manner with appropriate 4 weeks after the completion of treatment procedure. Varying thick-
length and diameter (Figure 2). nesses (12, 40, 80, 100, 200 μ) of articulating foils and papers were
In case of fixed implant-supported prosthesis, implant number introduced in between the occluding surfaces (maximum intercuspal
was decided depending on the available bone, arch form, and mastica- position) for five times (Figure 3).
tory dynamics of the patient. Key implant position (Canine and molar Each foil was tested between the occluding teeth, following a ran-
region) and other rules of implant placement for fixed prosthesis were dom order of true and false insertions. Soon after participants
followed. Implant diameter was selected depending on the available occluded in maximum intercuspation of teeth, the subject responses
bucco-lingual width of bone and length was determined depending on (yes or no) concerning sensation of presence of foil was recorded. If
height of bone available maintaining a safe distance from anatomical response was “yes” then the subject was asked to show thumb up
structures. and if response was no then the subject was asked to show thumb
BHATTACHARJEE ET AL. 5

down. True positive and false negative responses were recorded and
score was given according to the maximum number of responses. Sim-
ilarly, five times false placement of artifoils and papers was done and
true negative and false positive responses were recorded.

2.5 | Neurophysiological activity

fMRI was performed to record neural activity in cerebral cortex


4 weeks after the completion of rehabilitation procedure.
Subjects were instructed to lie comfortably with their eye closed
in a supine position. Head of the participants was immobilized with
vacuum-pads, ear-plugs were inserted to reduce the foreign noise and FIGURE 4 Stereognostic test pieces used in the study
they were advised to practice clenching.
In a single session, 25 contiguous axial slice comprising the entire diameter. Five forms were used to prevent fatigue. Heat cure acrylic
brain (each slice 3 mm thick, with no gap) were acquired using a single resin was used to fabricate the test pieces (Figure 4). After each use
shot echo planner image T2-sensitive sequence with repetition time test pieces were autoclaved. Participants were blindfolded and test
(TR) = 3560 ms and echo time (TE) = 50 ms, and 176 slide per slab pieces were placed in the participant's mouth. Participants were
and field of view 192 mm. For display purpose, a high-resolution shown a chart containing drawing of all the test pieces to identify the
T1-weighted structural MRI was acquired for each subject using correct form.
three-dimensional FLASH SEQUENCE (1 mm thick, no gap, TR/TE/ Test was performed 4 weeks after the completion of treatment
Fractional Anisotropy (FA) = 1900 ms/3.37 ms/256 mm). procedure in a calm quite environment after instructing them to com-
The task paradigm was an alteration between 25 s of clenching fortably lying in a dental chair. Test pieces were placed in mid-dorsum
(on) and 25 s of rest (off). This procedure was repeated four times in of tongue in a blindfolded position and participants were asked to
each scanner run. Before each functional scan, an 8 mm whole brain manipulate the test forms inside the oral cavity. A chart corresponding
three-dimensional anatomic image scanning procedure was to all the test pieces was shown to the participants to identify the cor-
performed. rect shape.
Activation of different regions of brain was examined by obtaining A two-point scale (0, 1) was used for recording the oral
functional MRI images by instructing the participants to perform inter- stereognostic analysis score. The scale used was as follows: 0—for not
cuspal clenching task in a blindfolded position. Six different regions of identifying the test sample, 1—for correct identification of the test
brain (primary motor cortex, somatosensory cortex, premotor cortex, sample, if all answers were correct, a full five points was scored. Thus,
angular gyrus, thalamus, temporal lobe) were mainly compared in the higher the score, the better is an individual's stereognostic ability.
between the groups. These regions have been shown to be activated Five different shapes (circle, oval, rectangle, square, and triangle)
during clenching and action of masticatory muscles according to the were used.
previous literature. Apart from this, other activated regions of brain
were also evaluated. Group 1 was considered as complete denture
treatment protocol, Group 2 was considered to be implant-retained 2.7 | Statistical analysis used
overdenture, Group 3 was considered to be implant-supported fixed
prosthesis treatment protocol. Codings used in this section to indicate Data from the results were compared in between the groups by apply-
activity in a regional part of brain were: (0) means no activity in a partic- ing chi-squared test and p ≤ 0.05 was considered to be statistically sig-
ular region of brain. (1) means slight activity in a particular region of nificant. Intra-group comparison of ATS of different articulating papers
brain (light yellow color in a particular region in image). (2) means mod- was done through Cochran's-Q test and p ≤ 0.05 was considered to be
erate activity in a particular region of brain (reddish yellow color in a statistically significant. Data regarding the neurophysiological activity
particular region in image). were analyzed by using Krushkal–Wallis test and p ≤ 0.05 was consid-
ered to be statistically significant. Data from stereognostic ability test
procedure were compared by using chi-squared test and p ≤ 0.05 was
2.6 | Stereognostic ability considered to be statistically significant.

The various forms used to evaluate stereognostic ability were square,


rectangle, triangle, circle, and oval. These test forms were chosen in 3 | RE SU LT S
accordance with the guidelines provided by the National Institute of
Dental Research which developed a range of 20 shapes to assess Demographic characteristics of all the 18 participants have been men-
OS. The test forms used were of 5 mm in thickness and 10 mm in tioned in Table 2. True positive and true negative responses were
6 BHATTACHARJEE ET AL.

TABLE 2 Demographic characteristics of the participants T A B L E 3 Intra-group comparison of active tactile sensibility in
relation to different articulating papers in Group 1
Overall
Age and sex of demographic Absence of articulating foil False positive True negative
Group the participants characteristics
12 μ 2 4
Group 1 (complete 55 female Mean age—61 years
40 μ 3 3
denture) 63 male Female 4
59 female Male 2 80 μ 3 3
65 female 100 μ 0 6
67 male
200 μ 1 5
57 female
Cochran Q = 5.231; p = 0.264 (Not significant)
Group 2 (implant- 63 male Mean age—
retained 58 male 59.83 years Presence of articulating foil False negative True negative
overdenture) 65 male Male 4 12 μ 6 0
58 male Female 2
40 μ 5 1
61 female
54 female 80 μ 3 3

Group 3 (implant- 63 male Mean age— 100 μ 1 5


supported fixed 64 female 61.33 years 200 μ 0 6
prosthesis group) 55 female Male 4
Cochran Q = 15.294; p = 0.004 (Significant)
59 male Female 2
62 male
65 male
T A B L E 4 Intra-group comparison of active tactile sensibility in
relation to different articulating papers in group 2

Absence of articulating foil False positive True negative


12 μ 1 5
40 μ 2 4
80 μ 2 4
100 μ 1 5
200 μ 1 5
Cochran Q = 1.091; p = 0.896 (Not significant)
Presence of articulating foil False negative True negative
12 μ 5 1
40 μ 4 2
F I G U R E 5 Bar chart showing comparison of active tactile
sensibility between different groups on absence of different 80 μ 2 4
thicknesses of articulating foils 100 μ 1 5
200 μ 1 5
Cochran Q = 9.429; p = 0.051 (Not significant)

supported fixed prosthesis with 40 and 80 μ articulating papers


(Figures 5 and 6). No statistically significant difference was found in
between the groups due to limited number of sample size and low
study duration period owing to COVD-19 pandemic. Statistically sig-
nificant difference was found in between the articulating foils in terms
of true negative responses as the foil thickness increased in partici-
pants of Group 1 (p = 0.004) and Group 3 (p = 0.010) (Tables 3–5).
Participants in implant-supported fixed prosthesis showed signifi-
F I G U R E 6 Bar chart showing comparison of active tactile
cantly more activation in primary motor cortex (right side), somatosen-
sensibility between different groups on presence of different
thicknesses of articulating foils sory cortex (left side), angular gyrus (both sides), temporal lobe (left)
compared to other groups (Tables 6 and 7) (Figures 7–9). No signifi-
cant difference found in thalamus and premotor cortex region in
more with correct identification of artifoils in case of implant- between the participants of different groups. Participants in all the
supported fixed prosthesis compared to other two treatment options. groups showed activation pattern in other regions also which are
Number of false responses were comparatively low in implant- mentioned in Table 8.
BHATTACHARJEE ET AL. 7

T A B L E 5 Intra-group comparison of active tactile sensibility in No statistically significant difference found in between the
relation to different articulating papers in group 3 groups in terms of true responses identifying correct shapes. Mean
Absence of articulating foil False positive True negative number of correct responses were 4.16 (83.33%), 3.5 (70%), 3.83

12 μ 0 6 (76.66%) for participants of Groups 3, 2, and 1, respectively.


Highest correct responses were recorded in identifying triangle and
40 μ 2 4
lowest correct responses were recorded in identifying rectangle
80 μ 1 5
and oval after evaluation of the data from all the participants
100 μ 2 4
(Table 9) (Figure 10).
200 μ 1 5
Cochran Q = 3.111; p = 0.539 (Not significant)
Presence of articulating foil False negative True negative 4 | DI SCU SSION
12 μ 4 2
40 μ 1 5 Sensory homunculus or the topographic representation of body sur-
80 μ 0 6 faces in somatosensory cortex is closely linked with the neuroplastic
100 μ 0 6 changes in brain. Studies have shown that chewing activates various
200 μ 0 6 region in human brain-like sensorimotor cortex, supplementary motor

Cochran Q = 13.333; p = 0.010 (Significant) area, thalamus, and cerebellum.19,20

TABLE 6 Inter group comparison of activity in primary motor cortex, somatosensory cortex and prefrontal cortex region

Primary motor Primary motor Somatosensory Somatosensory Premotor cortex Premotor


Group Score cortex (right) cortex (left) cortex (right) cortex (left) (right) cortex (left)
Group 1 0 4 2 3 3 3 3
1 2 4 3 3 3 3
2
Group 2 0 2 1 1 2 1
1 5 4 5 4 4 5
2 1 1
Group 3 0 1 1 1
1 4 2 4 4 5 3
2 2 3 2 2 2
p = 0.013 p = 0.171 (Not p = 0.046 p = 0.074 (Not p = 0.492 (Not p = 0.194 (Not
(Significant) significant) (Significant) significant) significant) significant)

TABLE 7 Inter group comparison of activity in angular gyrus, thalamus, and temporal lobe region

Group Score Angular gyrus (right) Angular gyrus (left) Thalamus Temporal lobe (right) Temporal lobe (left)
Group 0 3 3 4 3 5
1
1 3 2 3 1
2 1 2
Group 0 2 4 3 2 2
2
1 4 2 1 3 4
2 2 1
Group 0 1 1
3
1 3 4 3 4 2
2 3 2 2 2 3
p = 0.026 p = 0.049 p = 0.567 (Not p = 0.098 (Not p = 0.031
(Significant) (Significant) significant) significant) (Significant)
8 BHATTACHARJEE ET AL.

TABLE 8 Other activated regions in different groups

Group 1 Group 2 Group 3


Midbrain— Insular cortex—three Insular cortex—more
moderate out of six activation in four
activation two participants participants out of
participants Midbrain—three out six
among six of six participants Midbrain—more
(Substantia nigra, Supramarginal activation
crus cerebri in gyrus—four out of amygdala,
one, red nucleus, six participants hippocampal body,
subthalamic Lateral occipito and
nucleus in one) temporal gyrus— parahippocampal
Cerebellum— four out of six gyrus region
F I G U R E 7 Neurophysiological activity in a participant of Group (moderate in participants Cerebellum—Bilateral
1 (complete denture) two, greater in Hippocampal body— activation in five
one) three two out of six participants out of
participants participants six participants
among six Cerebellum—three Supramarginal gyrus
Orbital gyrus— out of six and lateral
Bilateral in one, participants occipitofrontal
left in one gyrus showed
Occipital gyrus— more activation
three than other groups
participants
Lateral occipital
temporal gyrus—
three
participants

F I G U R E 8 Neurophysiological activity in a participant of Group center and form an inteconnected network.19 Studies based on PET
2 (maxillary complete denture opposing mandibular implant retained imaging showed that cerebral blood flow increases during mastication.
overdenture) Mastication can increase blood flow in the primary sensorimotor areas
by 25%–28% in the supplementary motor areas and insulae by 9%–
17%, and in the cerebellum and striatum by 8%–11% according to a
study.20
Kimoto and colleagues studied the changes in brain activities in
completely edentulous individuals by transforming their complete
denture to implant-retained overdentures. Results showed that
implant overdenture suppressed chewing induced brain activity in
prefrontal cortex, sensorimotor cortex, and cerebellum. Group com-
parison did not show any change in activity in supplementary motor
area, thalamus, and insula in between the groups.21
In an animal study, it has been clearly shown that sensory cortex
can reorganize itself after extraction of tooth in naked mole-rats.22
Another functional MRI-based study showed that osseointegrated
F I G U R E 9 Neurophysiological activity in a participant of Group thumb prosthesis-improved activation in primary motor cortex and
3 (implant-supported fixed prosthesis in both the arches) bilateral activation in sensory cortex in a patient compared to preop-
erative situation.23
Yan and colleagues24 also suggested that implant-supported pros-
Previously, one study explored the functional neural networks thesis play a role in restoring sensory and motor feedback to the cen-
during teeth tapping in old dentulous and edentulous patients through tral nervous system. Blood oxygen level-dependent signals were
functional MRI-based study. Psychophysiological interaction analysis elevated in the primary sensorimotor cortex in patients with implant-
in between edentulous patients wearing dentures and nondenture supported fixed prosthesis in this study. Prefrontal cortex, Brocas
wearers showed that subcortical and cortical structures, such as pri- area, premotor cortex, supplementary motor area, superior temporal
mary motor cortex, sensory cortex, supplementary motor cortex, gyrus, insular, basal ganglion, and hippocampus were also activated.
insula cortex, basal ganglia, and cerebellum are likely to be functional Then, activation signals in primary sensorimotor cortex signified the
BHATTACHARJEE ET AL. 9

TABLE 9 Inter-group comparison of stereognostic ability

Circle Oval Square Rectangle Triangle

False True False True False True False True False True
Group response response response response response response response response response response
Group 1 1 (16.7%) 5 (83.3%) 3 (50%) 3 (50%) 1 (16.7%) 5 (83.3%) 2 (33.3%) 4 (66.7%) 0 (0%) 6 (100%)
Group 2 1 (16.7%) 5 (83.3%) 2 (33.3%) 4 (66.7%) 2 (33.3%) 4 (66.7%) 4 (66.7%) 2 (33.3%) 1 (16.7%) 5 (83.3%)
Group 3 0 (0%) 6 (100%) 2 (33.3%) 4 (66.7%) 0 (0%) 6 (100%) 1 (16.7%) 5 (83.3%) 0 (0%) 6 (100%)
p = 0.570 (Not p = 0.792 (Not p = 0.301 (Not p = 0.195 (Not p = 0.347 (Not
significant) significant) significant) significant) significant)

group and implant-supported fixed prosthesis group. In case of


100 and 200 μ articulating papers, all the participants in each group
showed maximum number of true positive and true negative
responses. Overall, the result of this study added scientific evidence
that osseoperceptive ability of implant-supported fixed prosthesis is
much greater than any removable prosthesis and mean threshold of
detecting articulating foils is also lower than removable options. Bet-
ter tactile perception can improve the survival rate of dental implants
by preventing undue overload and rhythmic neuromuscular coordina-
tion during functional activities.

F I G U R E 1 0 Bar-chart showing comparison of stereognostic In terms of neurophysiological activity, implant-supported fixed


ability in between different groups prosthesis showed statistically significant more activation in primary
motor cortex and somatosensory cortex on right side compared to
implant overdenture and complete denture. On the left side no sta-
correlation of the improved tactile, stereognostic ability, mastication tistically significant differences were found although number of
functions, and underlying mechanism of osseoperception.24 moderate activations in these regions were more in case of implant-
In the current study, response of the participants were checked supported treatment modalities. Studies have shown that somato-
both in presence and absence of foils to crosscheck the perceptive sensory cortex and motor cortex play a role in jaw movement and
ability. Blindfolding of the participants and application of white noise orofacial functions in natural dentition.25,26 Moderate activations of
were done to reduce the bias of the confounding factors during the primary motor cortex (right), somatosensory cortex (both side) were
study. Each participant was checked 4 weeks after the completion of present in two patients in implant-supported group, whereas moder-
treatment to provide sufficient time to adapt with prosthesis. None of ate activation was not seen in any of patients with complete den-
the patients had monoplane teeth in the prosthesis, cusped, sem- ture. Only one patient in implant overdenture group showed
ianatomic teeth were used in complete denture and implant over- moderate activation in somatosensory cortex (left side) and primary
denture group. Implant-supported fixed prosthesis showed greater motor cortex (right side). Premotor cortex which is an important
number of true positive and true negative responses during applica- region for cognitive learning did not show significant changes in
tion and nonapplication of articulating paper, respectively. There were terms of activation between the groups. Most of the patients in all
no statistically significant differences found in between the groups the groups showed slight or no activation in premotor region. Mod-
due to limited sample size and shorter study duration period. Progres- erate activation found in only two patients with implant-supported
sive recovery of osseoperception could not be observed due to lesser fixed prosthesis. Somatosensory, motor, premotor, and supplemen-
number of patient appointments and shortened follow-up periods due tary cortex forms a circuit through which planning and execution of
to COVID-19. In complete denture and in implant-supported fixed movements occur. Increased activation in implant-supported treat-
prosthesis group, there was statistically significant difference found in ment option may be due to adaptability of cerebral cortex and its
detecting the presence of articulating papers as the thickness association with increased density of the mechanoreceptors in peri-
increased. Denture base movement and reduced mechanoreceptor implant region that transmit the sensory inputs to central nervous
density around prosthesis may contribute toward more false systems.
responses in complete denture group, apart from this patient satisfac- Angular gyrus was bilaterally activated in most of the patients in
tion, psychological integration might also play a role. There was an group 3 (three patients in implant-supported fixed prosthesis) and sta-
increased number of correct responses in identifying 40 and 80 μ tistically significant difference found compared to other group of
articulating papers showed by participants in implant overdenture patients. Thalamus showed moderate activation in two patients in all
10 BHATTACHARJEE ET AL.

the groups and no significant difference was present in between the oval and rectangular test pieces were the difficult ones to identify.
groups. Temporal lobe which has a distinct role in long-term memory Inter-participant variability and coordination of receptors present in
and declarative memory showed significantly more activation in left tongue, palate, and periodontium generally modulate the result of
side in implant-supported group. stereognostic ability. Decreased prosthesis movement and psycholog-
Other regions of brain like cerebellum which controls the fine ical benefit were believed to be the most important reasons for better
rhythmic movements showed moderate activation in five out of six stereognostic ability score in implant-supported fixed prosthesis. Pre-
patients in implant-supported group. Hippocampus and para- vious study on stereognostic ability of maxillary implant-supported
hippocampal region showed activation in two patients in both implant overdenture compared to complete denture also did not find any
overdenture and implant-supported fixed prosthesis group. Hippo- significant changes similar to the current study.28 All the partici-
campal region is mainly associated with learning and memory which is pants in Group 2 had complete dentures in upper arch so no major
very much needed for fine tuning of movements in oro-mandibular variability was found in terms of movement of tongue around the
region. Insular cortex and supramarginal gyrus were the other promi- palate which was covered by acrylic (both in Groups 1 and 2).
nent regions that got activated implant-supported treatment modality. Slightly less overall number of score in participants of Group 2 may
In complete denture, Group 2 patients showed moderate activation in be found due to inter-participant variability and neuromuscular
midbrain (substantia nigra) and Group 3 patients showed activation in coordination. Retentive mechanism of implant retained over-
lateral occipito-temporal gyrus. dentures had no significant relation with this finding. Omission of
Somatic sensory system has two pathways in human being, one palatal part of prosthesis in implant-supported fixed group may had
for detection of mechanical stimuli (light touch, vibration, pressure, contributed to report more number of correct responses in case of
and cutaneous tension) and another for detection of pain and temper- Group 3.
ature. A question arises, how is this information from external sur- Current study was conducted in a parallel arm design with differ-
faces or oral cavity processed in the thalamus and cortex in order to ent participants in all the study groups, in future edentulous partici-
identify objects, and how is this information used in guiding and for- pants previously rehabilitated with complete denture can be
mulating motor control? There are various mechanorecptors like transitioned into implant-supported fixed prosthesis to evaluate all
pacinian corpuscles, ruffini nerve endings; merkel cells are present in the test procedures to form a more conclusive evidence. Three differ-
the soft tissue regions of mouth and in external surfaces also. Peri- ent test procedures were applied in the study to get a correlation of
odontal ligaments of teeth, dental pulp also contain mechanorecep- various perspectives of neuromuscular control. As per author's knowl-
tors. These receptors are responsible for conducting touch and other edge, previously no studies have been done on three different treat-
tactile perceptions in the higher centers of brain.16,17,27 OS is con- ment modalities evaluating three different test procedures in this
trolled by various mechanoreceptors in the oral cavity but predomi- topic. ATS was given importance in this study instead of passive tac-
nant role is played by receptors present in tongue, palate, and tile sensibility because ATS show direct activation of receptors around
16
periodontium. peri-implant region compared to passive tactile sensibility tests. Limi-
Only one study has been found till now in literature regarding tations of the study were low sample size and less number of follow-
stereognostic ability in implant-supported prosthesis. Ikbal and col- up periods owing to pandemic situation. Inter-patient variables and
leagues28 conducted a study in which three group of participants occlusal contacts may have also influence in the result despite of
were compared in terms of stereognostic ability. Group 1 comprised checking occlusal contacts with specific thickness of articulating
of dentate individuals, Group 2 consisted of complete denture papers for different prosthesis. Concurrent evaluation of electroen-
patients and in Group 3 patients were rehabilitated with implant- cephalogram (EEG) and real time functional MRI can also be done to
supported fixed prosthesis in upper arch. Statistically significant dif- generate dynamic activity of cerebral cortex with better temporal and
ference was found in perception of stereognostic patterns in between spatial resolution in future which can help us to get a clearer picture
participants of control group and other groups (p < 0.001). The partici- about the feedback pathway during oral functions with these
pants wearing implant-supported dentures (Group 3) perceived pyra- prosthesis.
mid and drop shapes (round shapes tested: circle, pyramid, window, There is appreciable scope present in future to conduct further
drop, and cone) statistically significantly earlier in comparison to study on this topic to overcome the limitations of this study. Sam-
Group 2 (p < 0.001). Participants of Group 3 perceived the shapes sta- ple size can be increased to evaluate the effect in larger population.
tistically significantly earlier (except for circles and drops) than Group Equilibration of occlusal contacts can be done in a more systematic
2 without dentures. manner by the use of digital technologies like T-scan occlusal
In current study, patients with implant-supported fixed prosthesis device so that correlation can be drawn intensity of occlusal con-
showed highest number of correct responses and implant retained tacts and brain activity. Treatment modality variation can be done
overdenture group of patients scored lowest mean score in in a single patient to reduce the effect of confounding factors. Spa-
stereognostic ability test. There was no statistically significant differ- tial and temporal resolution of the images can be improved by
ence in between the groups in terms of correct response. Identifica- applying concurrent electroencephalogram recordings and Func-
tion ability of triangular test piece was highest due to distinct shape, tional MRI reading.
BHATTACHARJEE ET AL. 11

5 | C O N CL U S I O N 6. Mericske-Stern R, Hofmann J, Wedig A, Geering AH. In vivo mea-


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ACKNOWLEDGMENTS for learning and recovery. Front Psychol. 2017;8:1657.
Indian Council of Medical Research (ICMR). 14. Jacobs R, Van Steenberghe D. From osseoperception to implant-
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CONF LICT OF IN TE RE ST
15. Pauling L, Coryell CD. The magnetic properties and structure of
No conflict of interest. hemoglobin, oxyhemoglobin and carbonmonoxyhemoglobin. Proc
Natl Acad Sci U S A. 1936;22:210-216.
AUTHOR CONTRIBUTIONS 16. Jacobs R, Wu CH, Goossens K, Van Loven K, Van Hees J, Van Steen-
berghe D. Oral mucosal versus cutaneous sensory testing: a reviewof
Concept/design—Bappaditya Bhattacharjee, Ritu Saneja, Atul Bhatnagar.
the literature. J Oral Rehabil. 2002;29(10):923-950.
Data analysis/interpretation—Bappaditya Bhattacharjee, Atul Bhatnagar, 17. Daroff R, Aminoff M. Encyclopedia of the neurological sciences. 2nd ed.
Ashish Verma. Drafting article—Bappaditya Bhattacharjee, Ritu Burlington, Elsevier Science; 2014.
Saneja. Critical revision of article—Romesh Soni, Ankita Singh, 18. Malo  P, Rangert B, Nobre M. "all-on-four" immediate-function con-
cept with Brånemark system implants for completely edentulous
Pavan Dubey. Approval of article—Atul Bhatnagar. Statistics—
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Ashish Verma, Bappaditya Bhattacharjee. Data collection— 2003;5(suppl 1):2-9.
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network involved in teeth tapping in elderly adults. Front Aging Neu-
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Bappaditya Bhattacharjee https://orcid.org/0000-0001-6823-1188 regional cerebral blood flow in humans examined by positron-
Atul Bhatnagar https://orcid.org/0000-0001-7091-5132 emission tomography with 15O-labelled water and magnetic reso-
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