from osseoperception to implant-mediated sensory-motor

11
Review Article From osseoperception to implant-mediated sensory-motor interactions and related clinical implications* R. JACOBS & D. VAN STEENBERGHE 1 Laboratory of Oral Physiology, Department of Periodontology, Faculty of Medicine, Catholic University of Leuven, Leuven, Belgium SUMMARY Osseointegration of implants in the jaw bone has been studied thoroughly, dealing with various aspects such as bone apposition, bone qual- ity, microbiology, biomechanics, aesthetics, etc. A key issue that has received much less attention is the physiologic integration of the implant(s) and the associated prosthesis in the body. The latter aspect is however very important to obtain new insights in oral functioning with implant-supported pros- theses. Amputated patients rehabilitated with a lower limb prosthesis anchored to the bone by means of an osseointegrated implant, have reported that they could recognize the type of soil they were walking on. Clinical observations on patients with oral implants, have confirmed a special sensory perception skill. The underlying mechanism of this so-called ‘osseoperception’ phenomenon remains a matter of debate, because extraction of teeth involves elimination of the extremely sensitive periodontal ligaments while functional reinnerva- tion around implants is still uncertain. Histological, neurophysiological and psychophysical evidence of osseoperception have been collected, making the assumption more likely that a proper peripheral feedback pathway can be restored when using osseointegrated implants. This implant-mediated sensory-motor control may have important clinical implications, because a more natural functioning with implant-supported prostheses can be attemp- ted. It may open doors for global integration in the human body. KEYWORDS: osseoperception, dental implant, jaw, trigeminal nerve, tactile function, physiology Accepted for publication 1 January 2006 Introduction Sensory feedback plays an essential role in fine tuning of limb motor control. Thus, it is clear that amputation of a limb will not only involve destruction of an important part of the peripheral feedback pathways, but also hamper fine motor control. Conventional socket prostheses do not carry enough sensory information to restore the necessary natural feedback pathways for motor function (1). Comparable observations can be made after extraction of teeth. The periodontal liga- ment harbours a very rich innervation, carrying refined mechanoreceptive properties by an intimate contact between collagen fibres and Ruffini-like endings (2). The role of periodontal neural feedback is well-known (3, 4). After extraction of teeth however, this feedback pathway may be damaged as periodontal ligament receptors are eliminated. Thus, the impact of tooth extraction on the sensory feedback pathway seems considerable (3–6). Dentures can be compared with socket prostheses and are not able to fully compensate for normal tooth loading and force transfer. The peripheral feedback mechanisms are more limited as the mucosal mechanoreceptor function is less efficient than the periodontal ligament function. Consequently, oral function remains impaired (4). *Based on the Journal of Oral Rehabilitation Summer School 2005 in Bavagna, Italy. Kindly sponsored by Blackwell Munksgaard and Nobel Biocare. 1 Holder of the P-I Bra ˚ nemark Chair in Osseointegration ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd doi: 10.1111/j.1365-2842.2006.01621.x Journal of Oral Rehabilitation 2006 33; 282–292

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  • Review Article

    From osseoperception to implant-mediated sensory-motor

    interactions and related clinical implications*

    R. JACOBS & D. VAN STEENBERGHE1 Laboratory of Oral Physiology, Department of Periodontology, Faculty of

    Medicine, Catholic University of Leuven, Leuven, Belgium

    SUMMARY Osseointegration of implants in the jaw

    bone has been studied thoroughly, dealing with

    various aspects such as bone apposition, bone qual-

    ity, microbiology, biomechanics, aesthetics, etc. A

    key issue that has received much less attention is

    the physiologic integration of the implant(s) and the

    associated prosthesis in the body. The latter aspect is

    however very important to obtain new insights in

    oral functioning with implant-supported pros-

    theses. Amputated patients rehabilitated with a

    lower limb prosthesis anchored to the bone by

    means of an osseointegrated implant, have reported

    that they could recognize the type of soil they were

    walking on. Clinical observations on patients with

    oral implants, have confirmed a special sensory

    perception skill. The underlying mechanism of this

    so-called osseoperception phenomenon remains a

    matter of debate, because extraction of teeth

    involves elimination of the extremely sensitive

    periodontal ligaments while functional reinnerva-

    tion around implants is still uncertain. Histological,

    neurophysiological and psychophysical evidence of

    osseoperception have been collected, making the

    assumption more likely that a proper peripheral

    feedback pathway can be restored when using

    osseointegrated implants. This implant-mediated

    sensory-motor control may have important clinical

    implications, because a more natural functioning

    with implant-supported prostheses can be attemp-

    ted. It may open doors for global integration in the

    human body.

    KEYWORDS: osseoperception, dental implant, jaw,

    trigeminal nerve, tactile function, physiology

    Accepted for publication 1 January 2006

    Introduction

    Sensory feedback plays an essential role in fine tuning

    of limb motor control. Thus, it is clear that amputation

    of a limb will not only involve destruction of an

    important part of the peripheral feedback pathways, but

    also hamper fine motor control. Conventional socket

    prostheses do not carry enough sensory information to

    restore the necessary natural feedback pathways for

    motor function (1). Comparable observations can be

    made after extraction of teeth. The periodontal liga-

    ment harbours a very rich innervation, carrying refined

    mechanoreceptive properties by an intimate contact

    between collagen fibres and Ruffini-like endings (2).

    The role of periodontal neural feedback is well-known

    (3, 4). After extraction of teeth however, this feedback

    pathway may be damaged as periodontal ligament

    receptors are eliminated. Thus, the impact of tooth

    extraction on the sensory feedback pathway seems

    considerable (36). Dentures can be compared with

    socket prostheses and are not able to fully compensate

    for normal tooth loading and force transfer. The

    peripheral feedback mechanisms are more limited as

    the mucosal mechanoreceptor function is less efficient

    than the periodontal ligament function. Consequently,

    oral function remains impaired (4).

    *Based on the Journal of Oral Rehabilitation Summer School 2005 in

    Bavagna, Italy. Kindly sponsored by Blackwell Munksgaard and Nobel

    Biocare.1Holder of the P-I Branemark Chair in Osseointegration

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd doi: 10.1111/j.1365-2842.2006.01621.x

    Journal of Oral Rehabilitation 2006 33; 282292

  • It has been assumed that by anchoring prosthetic

    limbs directly to the bone via osseointegrated implants,

    partial sensory substitution can be realized (1, 5, 6). If

    the feedback pathway can be restored, such concept of

    bone-anchored limb prostheses would signify an

    important step towards global integration of a pros-

    thesis in the body. Amputated as well as edentulous

    patients, rehabilitated with a bone-anchored prosthesis,

    report a specific feeling around endosseous implants.

    Psychophysical threshold determination studies con-

    firmed that patients may perceive mechanical stimuli

    exerted on osseointegrated implants in the bone

    (1, 5, 6). This phenomenon has raised questions. Would

    this special feeling result from a changed impact force

    through the rigid implantbone interface, in contrast to

    the cushioning effect of the skin or mucosa under the

    socket prosthesis? Or would intra-osseous or periosteal

    neural endings be involved?

    The latter observations brings along the discussions of

    which receptor groups are responsible for this so-called

    osseoperception phenomenon. New insights and more

    objective non-invasive approaches may help clarifying

    this question. First, Somatosensory Evoked Potentials

    (SEPs), which are routinely used to screen for neuro-

    logical disorders, could assist localizing the origin of

    sensory phenomena observed upon implant stimula-

    tion. For trigeminal SEPs, thorough signal analyses are

    needed rather than visual inspection, to obtain reliable

    data on the SEP signals and enable further interpret-

    ation on the receptors activated upon implant stimula-

    tion (7, 8). A most promising approach is the use of

    functional Magnetic Resonance Imaging (fMRI), which

    has the advantage of being a static and/or dynamic

    imaging technique, without the drawback of exposure

    to ionizing radiation (9). This fMRI might help visual-

    izing activity centres on the pathway from the stimu-

    lation site to the cortex. Both non-invasive approaches

    offer new perspectives for osseoperception research and

    may try linking the anatomical and histological back-

    ground to the clinical observations. If such link is

    present, osseoperception might help in physiologic and

    functional integration of implants in the body.

    The present review attempts to provide arguments

    and scientific evidence to support this hypothesis.

    Neurovascularization of the jaw bones

    The jaws are richly supplied by neurovascular struc-

    tures. This needs to be carefully considered when

    performing surgical procedures in the jaw, such as

    inserting implants. Pre-surgical localization of neuro-

    vascular structures is essential to guarantee an

    uneventful outcome (10). On the other hand, the rich

    jaw bone innervation may help to sense mechanical

    deformation during loading of oral implant and thus

    contribute to restore peripheral feedback after tooth

    extraction and implant placement. Even in the anterior

    jaw bone, where the presence and functional signifi-

    cance of neurovascularization was somewhat neglected

    in the past, recent studies on a variety of human

    cadaver material have confirmed a rich innervation

    with clear sensory nerve characteristics (1012)

    (Fig. 1). The neurovascular content of a well-defined

    mandibular incisive and lingual canal and a maxillary

    nasopalatine canal structure may explain a number of

    altered sensations after anterior implant placement

    (Fig. 2).

    Histological background

    Tooth extraction results in damage of a large number of

    sensory nerve fibres and corresponds to an amputation,

    where the target organ and peripheral nervous struc-

    tures have been destroyed (13). After extraction of

    teeth, the myelinated fibre content of the inferior

    alveolar nerve is reduced by 20% (14). This finding

    indicates that fibres originally innervating the tooth and

    periodontal ligament are still present in the inferior

    alveolar nerve. Linden and Scott (15) succeeded to

    stimulate nerves of periodontal origin in healed extrac-

    tions sockets, which implies that some nerve endings

    remain functional. Nevertheless, most of the surviving

    mechanoreceptive neurons represented in the mesen-

    cephalic nucleus may lose some functionality (15).

    These experiments have been the basis for a further and

    long-lasting debate on the presence and potential

    function of sensory nerves fibres in the bone and

    peri-implant environment. Histological evidence indi-

    cates that there may be some reinnervation around

    osseointegrated implants (16, 17). Indeed, it has been

    shown that endosseous implants may lead to degener-

    ation of environing neural fibres by surgical trauma.

    Soon however, sprouting of new fibres is observed and

    the number of free nerve endings close to the bone-to-

    implant interface gradually increases during the first

    weeks of healing (18). Amore recent study in the dog has

    succeeded to partially regenerate the periodontal liga-

    ment on an implant surface (19). Whether such regen-

    O S S EO P E R C E P T I O N AND S E N SOR Y -MO TOR I N T E RA C T I O N S 283

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • eration might also induce restoration of the peripheral

    feedback pathway has however not been studied.

    On the other hand, existing mechanoreceptors in the

    periosteum may also play a role in tactile function upon

    implant stimulation. It is evident that oral implants

    offer another type of loading and force transfer than

    teeth, considering an intimate bone-to-implant contact

    with elastic bone properties instead of the characteristic

    viscoelasticity of the periodontal ligament. Thus, forces

    applied to osseointegrated implants are directly trans-

    ferred to the bone and bone deformation may lead to

    receptor activation in the peri-implant bone and the

    neighbouring periosteum (20).

    Cortical plasticity after tooth extraction

    The cortex of the brain reveals a somatotopically ordered

    representational map for movements that resembles a

    distorted cartoon of the body (21). After limb amputa-

    tion, the regions of the cortex deprived of a target acquire

    new targets. Remodelling takes place at a cortical or

    subcortical level (22). The potential cortical adaptation

    and/or plasticity that might occur after tooth extraction

    and implant placement has not yet been fully explored.

    A very interesting study was recently carried out on

    mole-rats (23). Henry et al. (23) extracted the lower right

    incisor in mole-rats. Five to 8 months afterwards, the

    oro-facial representation in S1 was considerably reor-

    ganized. Neurons in the cortical lower tooth representa-

    tion were responsive to tactile inputs from surrounding

    oro-facial structures. This studymay indicate that cortical

    representation of teeth may significantly restructure

    after tooth loss. These data parallel findings after deaf-

    ferentation in the somatosensory hand area of primates

    where tactile inputs from the chin and upper arm may

    activate the hand cortical area.

    Unfortunately, until now, similar evidence in

    humans has not yet been produced. Future research

    should therefore try to visualize cortical plasticity after

    Fig. 2. Placement of implants in the anterior mandible may

    present some risk for neurovascular damage. In the present cross-

    sectional image of a cone beam CT of the anterior mandible, the

    intimate contact between a canine osseointegrated implant and

    the incisive nerve becomes obvious.

    (a)

    (b)

    Fig. 1. Histological section (a) and high resolution MRI image (b)

    show one bony canal branching into two canals. Figure (a)

    visualizes two branches (arrow) of the canal on a histological

    section. Figure (b) is an horizontal MRI section showing one bony

    canal (grey arrow) branching into two canals (black arrows).

    [Reprinted from Dentomaxillofacial Radiology, vol.34, Liang X,

    Jacobs R, Lambrichts I, Vandewalle G, van Oostveldt D, Schepers

    E, Adriaensens P, Gelan J. Microanatomical and histological

    assessment of the content of superior genial spinal foramen and its

    bony canal, pp 362368, Copyright 2005, with permission from

    the British Institute of Radiology].

    R . J A COB S & D . V AN S T E E N B E RGH E284

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • tooth extraction and further functional rehabilitation

    with implants. It should be considered that an imme-

    diate extraction and implant rehabilitation protocol

    might induce a different cortical remodelling than a

    traditional two-stage implant rehabilitation protocol.

    An interesting phenomenon with respect to sensory-

    motor integration of osseointegrated implants, may be

    the so-called phantom tooth (after extraction) or

    phantom limb (after amputation), allowing perception

    of lost body parts (24). In fact, it could be assumed that

    such a phantom feeling of the lost limb may overlap

    with or enforce the feeling of a bone-anchored pros-

    thetic limb (1, 5). In this way, phantom sensations

    might contribute to physiological integration of a bone-

    anchored prosthesis in the human body (5).

    Neurophysiological versus psychophysicaldata

    Information on oral tactile function can be examined by

    neurophysiological as well as psychophysical methods.

    Neurophysiological investigations on the sensory func-

    tion of the trigeminal system in man are scarce.

    Afferent nerve recordings of the human trigeminal

    nerve require skilful performance and only few studies

    have been reported so far (2527). [see also review by

    Trulsson (28)].

    Evidence can also be found by non-invasive approa-

    ches for evaluation of oral tactile function. The first

    approach is the recording of the so-called trigeminal

    somatosensory evoked potentials (TSEP) after stimula-

    tion of receptors in the oral cavity (7, 8). This set-up has

    the advantage of obtaining information on the cortical

    response of the trigeminal afferent system upon non-

    invasive stimulation of oral receptors. Another non-

    invasive method to assess sensory function is the

    visualization of brain activities by fMRI (9). It is a very

    promising technique, which has so far received hardly

    any attention in relation to tactile function of teeth and

    implants.

    Conversely, psychophysical studies on the oral sen-

    sory function are numerous (4). A major advantage of

    this type of studies is that these are simple non-invasive

    techniques that may be performed in a clinical

    environment. Psychophysics includes a series of well-

    defined methodologies to help determining the thresh-

    old level of sensory receptors in man. Psychophysical

    methods allow connecting the psychological response

    of the patient to the physiological functions of the

    receptors involved. When performed meticulously and

    under standardized conditions, these studies may reveal

    nearly as precise information as neurophysiological set-

    ups (3, 4, 29).

    Regardless of the tests used, one must keep in mind

    that many variables contribute to the subjective nature

    of psychophysical sensory testing. Some variables are

    manageable, others are more difficult to deal with. The

    influencing factors are found in the different compo-

    nents of the experimental set-up (environmental influ-

    ence, psychophysical approach, patient-related factors,

    etc.) (3, 4, 29).

    Environmental factors should be well-controlled as

    background noise is distracting to patient and examiner.

    Tominimize the effect of noise, testing should be done in

    a quiet room with stable background illumination (29).

    Different psychophysical procedures have been des-

    cribed in order to reliably assess tactile function (30).

    Adaptive methods are generally recommended for

    threshold level determination, as these seem very

    effective and consistent. Such approaches are called

    adaptive as the subsequent stimulus value depends on

    the subjects response in the preceding trials. In the

    staircase method, the stimulus value is changed by a

    constant amount. When the answer shifts from one

    answer to another, the stimulus direction is changed. The

    threshold is then determined by averaging the peaks and

    valleys throughout all runs. Some patients may imagine

    a stimulus when there is none. Others admit feeling a

    sensation only if they are absolutely positive that it was

    felt. The inclusion of false alarms (implying that no

    stimulus is presented in the specified time interval) may

    exclude response bias and a guessing strategy of the

    subject. A thorough and standardized instruction to all

    subjects is important in this perspective.

    Other patient-related factors that should be consid-

    ered are of physical origin and include age, gender,

    dental status, and dexterity. Age is an important

    variable with respect to implant physiology, consider-

    ing the fact that edentulous patients are usually found

    amongst the elderly. In general, motor changes occur

    with age leading to impairment of balance and

    unsteadiness of motion. Besides, a deterioration of

    most sensory modalities in the distal extremities occurs

    (31). A decline in oral sensory function is also

    established. After the age of 80, the ability to differ-

    entiate tactile and vibratory stimuli on the lip decrea-

    ses and two-point discrimination deteriorates on the

    upper lip, on the cheeks and on the lower lip, but not

    O S S EO P E R C E P T I O N AND S E N SOR Y -MO TOR I N T E RA C T I O N S 285

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • on the tongue and the palate (32). The stereognostic

    ability also declines with age (33, 34). It is clear that

    this age-effect should be considered in experimental

    studies.

    In contrast to age, the existence of some gender effect

    remains a matter of debate. Taking into account the

    important inter-individual variability, clear-cut gender

    differences are not easily discerned with regard to oral

    sensory function. There is no marked gender effect on

    stereognostic ability or vibrotactile function (35, 36).

    The tactile sensory systems of men and women seem to

    operate similarly at both threshold and suprathreshold

    levels of stimulation (37, 38). However, females seem to

    have greater ability to discern subtle changes in lip,

    cheek and chin position than males (38). Dexterity is

    another patient-related variable. Although there is

    some relation between masticatory performance and

    dexterity (39), this is the case for neither tactile

    function nor stereognosis (29, 40).

    Tactile function of oral implants

    Periodontal neural receptors play an essential role in

    oral tactile function (3). Most receptors can be found in

    the periodontal ligament, which is evidently lacking

    around permucosal oral implants. In that case, remain-

    ing receptors in gingiva, alveolar mucosa and periost-

    eum may take over part of the normal exteroceptive

    function.

    It seems attractive to explain the observed tactile

    sensitivity of endosseous implants, coined osseopercep-

    tion, by the surrounding endosseous and periosteal

    neural endings. To prove it, part of the evidence is

    provided by a series of psychophysical and neurophys-

    iological experiments in man (4, 5). Neurophysiological

    evidence can be found in some experiments evoking

    TSEPs upon implant stimulation. By triggering sweeps

    in the electroencephalogram by means of an implant

    stimulation device and by cumulating and advanced

    analysis of the sweeps, one can finally note significant

    waves. The experiments indicate that it is indeed

    endosseous and/or periosteal receptors around the

    implants, which convey the sensation (8, 41).

    Psychophyscial testing has been performed by active

    and passive (vibro)tactile detection and discrimination

    tasks as well as by oral stereognosis (4, 29). During

    active threshold determination, subjects are asked

    detecting foils placed in between the teeth. During

    passive threshold level assessment, the concentrated

    patient is undergoing an external force applied to the

    implant (Fig. 3). As soon as the subject detects the foil

    or the force, he has to signal it (29). From several

    studies, it has been established that the oral tactile

    function is influenced by tooth position and dental

    status (3, 4, 6, 29). The tactile function of teeth is

    primarily determined by the presence of periodontal

    ligament receptors. Vital or non-vital teeth show a

    comparable tactile function (4) (Table 1). However,

    when periodontal ligament receptors are reduced in

    numbers or eliminated (e.g. periodontitis, chewing,

    extraction, anaesthesia, etc.), tactile function is

    impaired (4). This clinically implies that the patients

    ability to detect occlusal inaccuracies is decreased in

    these situations. Indeed, exteroceptors inform the

    nervous system on the characteristics of the stimulus,

    which then allows modulation of the motoneuron pool

    to avoid overloading. Elimination of these exterocep-

    tors by tooth extraction may reduce the tactile function

    to an important extent (4, 6, 42, 43). Even after

    rehabilitation with a prosthesis, the tactile function

    remains impaired. The inappropriate exteroceptive

    feedback may thus present a risk for overloading the

    Fig. 3. Set-up of passive threshold determination of a maxillary

    front tooth by applying axial pushing forces against the tooth.

    Table 1. Factors influencing the tactile function of teeth (6, 28,

    41, 42)

    Dental status

    Active detection

    threshold (lm)Passive detection

    threshold (g)

    Vital tooth 20 2

    Non-vital tooth 20 2

    Removable prosthesis 150 150

    Implant-supported

    prosthesis

    50 100

    R . J A COB S & D . V AN S T E E N B E RGH E286

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • prosthesis (1, 5). In comparison with the tactile func-

    tion of natural dentitions, the active threshold is seven

    to eight times higher for dentures but only three to five

    times higher for implants (42) (see Table 1). For the

    passive detection of forces applied to upper teeth,

    thresholds for dentures are 75 times increased and for

    implants 50 times (43) (see Table 1). The large discrep-

    ancies between active and passive thresholds can be

    explained by the fact that several receptor groups may

    respond to active testing, while the passive method

    selectively activates periodontal ligament receptors. The

    latter are eliminated after extraction, which may

    explain the reduced tactile function in edentulous

    patients. After rehabilitation with a bone-anchored

    prosthesis however, edentulous patients seem to func-

    tion quite well. These patients perceive mechanical

    stimuli exerted on osseointegrated implants in the jaw

    bone (43). If subjects are followed up after implant

    placement, there is a noticeable improvement in tactile

    function with oral implants following a 3-months

    healing period (44). Some people rehabilitated with

    osseointegrated implants even note a special sensory

    awareness with the bone-anchored prosthesis, coined

    osseoperception (1, 5). The existence of this phenom-

    enon could imply that the feedback pathway to the

    sensory cortex is partly restored with an hypothetical

    representation of the prosthesis in the sensory cortex

    allowing a more appropriate modulation of the moto-

    neuron pool leading to a more natural functioning and

    avoiding overload.

    Oral mechanoreceptors activated duringoral tactile function

    When performing psychophysical testing, various types

    of oral mechanoreceptors may be activated. Mecha-

    noreceptors in the oral region may be located in

    the periodontal ligament, oral mucosa, gingiva, bone,

    periosteum, and tongue. Mechanoreceptors in the

    periodontal ligament contribute to the very high

    sensitivity of teeth to mechanical stimuli (3, 4). The

    periodontal ligament is richly supplied with mecha-

    noreceptors, with the majority being identified histo-

    logically as Ruffini-like endings (2). During passive

    threshold determination, these receptors will be acti-

    vated. The assessment of the active tactile threshold

    level however is not solely based on activation of

    periodontal mechanoreceptors. Temporomandibular

    joint (TMJ) receptors are found to play only a minor

    role but muscular receptors are important in the

    discriminatory ability for mouth openings of 5 mm

    and more (45). In the oral mucosa, different types of

    mechanoreceptors can be identified including Meiss-

    ners corpuscules, glomerular endings, Merkel cells,

    Ruffini-like endings, and free nerve endings. The

    number of nerve fibres per unit area is greater in

    the anterior areas of the oral cavity, making this region

    the most sensitive part of the oral mucosa (46).

    The gingiva contains round and oval lamellar cor-

    puscles (2). These receptors respond to mechanical

    stimuli and are involved in the co-ordination of lip and

    buccal muscles during mastication (25, 26). Cutaneous

    mechanoreceptors in the facial skin are activated by

    skin stretching or contraction of facial muscles and may

    operate as proprioceptors involved in facial kinaesthesia

    and motor control (47).

    The periosteum contains free nerve endings, complex

    unencapsulated and encapsulated endings. The free

    nerve endings are activated by pressure or stretching of

    the periosteum through the action of masticatory

    muscles and the skin (20). When applying forces to

    osseointegrated implants in the jaw bone, it might be

    assumed that the pressure build-up in the bone is

    sometimes large enough to allow deformation of the

    bone and its surrounding periosteum (43). The involve-

    ment of bone innervation in mechanoreception

    remains however a matter of debate (48).

    Oral stereognosis and osseointegration

    Another functional test is the so-called stereognosis.

    The stereognostic ability is defined as the ability to

    recognize and discriminate different forms presented as

    a stimulus (49). While touch may obtain information

    on the mechanoreceptors activated by simple detection

    or discrimination of mechanical stimuli, stereognosis is

    a more complex process. It is a function of both

    peripheral receptors (touch and kinaesthetic) and cen-

    tral integrating processes (49). It may give an idea on

    daily functioning and may be applied to measure

    sensory impairment because of the presence of general

    or local pathology (speech pathology, blindness, deaf-

    ness, cleft lip and palate, temporary sensory ablations,

    etc.).

    A change in the oral cavity by means of partial or

    complete loss of the dentition certainly creates certain

    changes to the oral sensory function. In dentate

    subjects, the role of periodontal neural receptors

    O S S EO P E R C E P T I O N AND S E N SOR Y -MO TOR I N T E RA C T I O N S 287

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • and of the tongue seems essential. After a bilateral

    mandibular block, the stereognostic ability decreases

    with about 20% (50). When comparing teeth with full

    dentures, a far better stereognostic ability is noted for

    natural teeth when freely manipulating the test pieces

    (49, 50). When removing the denture(s) in complete

    denture wearers, a considerable reduction in stereo-

    gnostic ability is noted (50). An interesting observation

    is that edentulous subjects showing a lot of problems

    and a low satisfaction level after insertion of their new

    denture demonstrate higher levels of oral stereognostic

    ability than those subjects having few or no problems

    (51), but this could not be confirmed by Muller et al.

    (34).

    Lundqvist (52) demonstrated an improvement of

    the stereognostic ability after rehabilitation with oral

    implants. Jacobs et al. (53) compared different pros-

    thetic superstructures and noted no significantly

    different stereognostic ability with implant-supported

    fixed or removable prostheses, even when elimin-

    ating the involvement of tongue- and lip receptors

    (Fig. 4).

    Oral mechanoreceptors activated duringoral stereognosis

    To assess the stereognostic ability, test pieces are

    inserted in the oral cavity and in most experimental

    set-ups free manipulation of the test pieces is allowed.

    The latter implies activation of a large number of

    receptor groups (periodontal, mucosal, muscular, arti-

    cular, etc.]. As the tip of the tongue is one of the most

    densely innervated areas of the human body, it plays an

    important role in stereognosis of objects inserted in the

    mouth (49). Based on studies involving anaesthesia of

    the tongue, the palate or the absence of teeth, it could

    be stated that oral stereognostic ability is determined

    mostly by receptors in the tongue mucosa, the palate

    and to a lesser extent the periodontal ligament (49).

    A major modification to the experimental set-up is the

    insertion of a toothpick in each test piece to eliminate

    the involvement of lip and tongue receptors, to allow

    easy handling and standardized placement in between

    two antagonistic teeth (53) (Fig. 5).

    The role of the TMJ receptors is less clear. In fact, in

    studies on tactile function, an interocclusal thickness of

    5 mm and more seems able to activate receptors in the

    TMJ and the jaw muscles (4, 45). In the stereognostic

    ability tests, pieces are mostly manipulated inside the

    mouth and seldom kept between two antagonistic

    teeth, which excludes very often the need for a mouth

    opening of 5 mm or even more.

    Stereognostic ability testing is not designed to detect

    specific receptor groups, it rather reflects an overall

    sensory ability. A good result in a stereognosis test

    should indicate that the subject receives full and

    accurate information about what is going on in the

    mouth. Even if manipulation is allowed to identify the

    0

    10

    20

    30

    40

    50

    60

    70

    80

    90

    100%

    Cor

    rect

    iden

    tific

    atio

    ns

    Fixed

    prost

    hesis

    on im

    plants

    Over

    dentu

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    impla

    nts

    Full d

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    with p

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    Fig. 4. Average of correct identifica-

    tions out of 10 for all the groups in

    the oral test. [Reprinted from Clinical

    Oral lnvestigations, vol. 1, Stereo-

    gnosis with teeth and implants: a

    comparison between natural

    dentition, implant-supported fixed

    prostheses and overdentures on

    implants, pp 8994, Copyright 1997:

    with kind permission of Springer

    Science and Business Media].

    R . J A COB S & D . V AN S T E E N B E RGH E288

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • test piece, identification itself is a sensory rather than a

    motor accomplishment (49). It is an indicator of

    functional sensibility including synthesis of numerous

    sensory inputs in higher brain centres (49).

    From osseoperception to implant-mediated sensory motor interactions

    During the last few decades, millions of patients have

    already been rehabilitated by means of osseointegrated

    implants. Although part of the peripheral feedback

    mechanism is lost after tooth extraction, edentulous

    patients seem to function quite well, especially when

    rehabilitated with a prosthesis retained by or anchored

    to osseointegrated implants (5). These findings corres-

    pond well to the observation in amputees rehabilitated

    with a bone-anchored prosthesis rather than a socket

    prosthesis. During skeletal reconstruction, psychophys-

    ical testing reveals an improved tactile and vibrotactile

    capacity with an osseointegrated implant and the bone-

    anchored prosthetic limb (Fig. 6). Furthermore, both

    edentulous patients and amputees seem to report an

    improved awareness and special feeling with the

    implant-supported prosthesis, allowing a partial restor-

    ation of the peripheral feedback pathway with a

    hypothesized potential representation of the artificial

    limb feeling in the sensory cortex. If that could be

    confirmed, osseointegrated implants in the jaw or

    other skeletal bones might contribute to an implant-

    mediated sensory-motor control allowing physiological

    Fig. 5. The stereognostic ability is defined as the ability to

    recognize and discriminate different forms presented as a stimulus.

    (a) To eliminate the involvement of lip and tongue receptors, as

    well as to allow easy handling and standardized placement in

    between two antagonistic teeth, a toothpick is inserted in each test

    piece. (b) As soon as the subject has identified the form of the test

    piece, he has to indicate it on a chart visualizing the various forms

    presented in the mouth.

    (a)

    (b)

    Fig. 6. Vibrotactile testing of a lower arm (a) and a lower leg (b)

    prosthesis yields superior functioning with such bone-anchored

    prosthetic limbs as compared with conventional socket prostheses.

    [Reprinted from Prosthetics and Orthotics International, vol. 24,

    JacobsR,BranemarkR,OlmarkerK,RydevikB, vanSteenbergheD,

    Branemark P-I. Evaluation of the psycho-physical detection

    threshold level for vibrotactile and pressure stimulation of prosthe-

    tic limbs using bone anchorage or soft tissue support, pp 133142,

    Copyright 2000, with permission from Taylor and Francis].

    O S S E O P E R C E P T I O N AND S E N SOR Y -MO TOR I N T E RA C T I O N S 289

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

  • integration of the implant in the human body. The

    phenomenon of the so-called osseoperception might

    contribute to physiological integration and more nat-

    ural functioning. Originally, osseoperception has been

    defined as the conscious perception of external stimuli

    transmitted via a bone-anchored prosthesis by activa-

    tion of neural endings and/or receptors in the peri-

    implant environment such as the bone and more likely

    the periosteum (5). To put stress on the incorporation

    of the tactile function in a series of sensory-motor

    interactions, a recent consensus statement on osseo-

    perception added the aforementioned sensory-motor

    interactions to the definition, yielding: (i) the sensation

    arising from mechanical stimulation of a bone-

    anchored prosthesis, transduced by mechanoreceptors

    that may include those located in muscle, joint,

    mucosal and periosteal tissues; together with (ii) a

    change in central neural processing in maintaining

    sensorimotor function (54). The present review sug-

    gests keeping the original definition of osseoperception,

    but consider this phenomenon as part of an overall

    sensory-motor integration of the endosseous implants

    in the human body.

    Clinical implications of implant-mediatedsensory-motor interaction

    Psychophysical testing on various bone-anchored pros-

    theses confirm an improved tactile function leading to a

    better physiological integration of the limb. If percep-

    tion upon implant stimulation is working well, periph-

    eral feedback mechanism may be restored and help

    tuning fine motor control. This implant-mediated

    sensory-motor interaction may thus help to achieve a

    more natural function with the bone-anchored pros-

    thesis (1, 5). Osseointegrated thumb prostheses even

    allow patients to perform the activities of daily life

    without any problem (55).

    Considering the increased tactile threshold level for

    oral implant stimulation, one should however consider

    a few clinical implications. During rehabilitation by

    means of implant-supported prostheses, dentist should

    not rely on the patients perception of occlusion. In this

    respect, one should also be aware of gradually increas-

    ing tactile function during the healing period after

    implant placement. This may be of particular import-

    ance when dealing with immediate loading protocols.

    To avoid any overloading related to suboptimal feed-

    back mechanisms, patients should be encouraged to

    limit chewing forces by soft food intake during the

    healing period. Furthermore, parafunctional habits

    such as grinding or clenching, might have a negative

    impact during the implant healing phase. Bruxism has

    therefore been defined as a relative contra-indication

    for immediate loading protocols (56). [see also Review

    by Lobbezoo (57)].

    Conclusions

    Endosseous implants are routinely used to rehabilitate

    amputations of limbs or teeth. In order to reach

    satisfactory clinical function with such bone-anchored

    prostheses, physiological as well as psychological integ-

    ration of the implant(s) should take place. Clinical

    observations on patients with oral implants indicate the

    presence of sensory perception after some time. The

    underlying mechanism of this so-called osseopercep-

    tion phenomenon remains a matter of debate. In any

    case, scientific evidence allows to state that implant-

    mediated sensory-motor interactions may offer poten-

    tials for physiological integration of the implant in the

    human body. The latter might help restoring the

    peripheral feedback pathways and attempt a more

    natural functioning. It could even be assumed that

    such physiological integration might lead to better

    acceptance and improved psychological integration.

    This is a step forward towards total implantbody

    integration. However, further research is required to

    make practical use of osseoperception in the design of

    novel bone-anchored prosthetic appliances and bionic

    limbs.

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    Correspondence: Reinhilde Jacobs, Laboratory of Oral Physiology,

    Department of Periodontology, Faculty of Medicine, Catholic Univer-

    sity of Leuven, Kapucijnenvoer 7, 3000 Leuven, Belgium.

    E-mail: [email protected]

    R . J A COB S & D . V AN S T E E N B E RGH E292

    2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd