Pressure-specifying sensory device: quantitative sensory measurement in the oral cavity and oropharynx of normal adults.

Abstract

We conducted a study to quantitatively determine the pressure perception thresholds in the oral cavity and oropharynx of a normal population with the Pressure-Specifying Sensory Device (PSSD). The PSSD measured pressure perception thresholds for both static and moving one-and two-point discrimination modalities at a variety of sites in the oral cavity and oropharynx as well as in the forearm of 11 adults. We also evaluated the ability of the PSSD to enhance sensory discrimination in four of these subjects by the process of sensory re-education for 11 days over a 15-day period. We found that the buccal mucosa and the tongue tip were the most sensitive sites in the oral cavity and oropharynx and that the floor of the mouth and the soft palate were the least sensitive. Sensory discrimination in the oral cavity was enhanced in all four subjects who underwent sensory re-education, although it returned to baseline levels over time after re-education was discontinued. The degree of intra- and intertester variability was minimal. Our data can be used as an aid in the development of techniques to surgically restore sensation in the oral cavity and oropharynx.

Introduction

The normal anatomy and function of the oral cavity and oropharynx are severely compromised following ablative surgery and radiotherapy to treat cancer in this area. In such patients, an alteration of the anatomy, a loss of motor function, a lack of lubrication, and the presence of anesthesia or hypoesthesia can lead to functional deficits. (l,2) As a result of advances in microvascular reconstructive surgery, restoration of the soft-tissue and bony anatomy in such patients can be achieved in a very precise and predictable fashion, (3,4) although restoration of motor function and lubrication is not yet possible. Re-establishment of sensation has been addressed through the use of sensate (reinnervated) microneurovascular free-tissue transfer, in which a microneural repair is performed between a sensory nerve of the free flap and a recipient nerve in the head and neck. (5-9)

To determine the success of surgery for sensory restoration, a quantitative assessment of sensory recovery at the reconstructed area is crucial. The first step toward this goal is to obtain an accurate measurement of sensation in different parts of the oral cavity and oropharynx in a normal population. In earlier studies of sensory discrimination in the oral cavity, authors have examined the tip, dorsum, and ventral aspect of the tongue and the floor of the mouth. (10-19) However, their techniques were not quantitative or completely comprehensive.

Sensory re-education is a method or combination of techniques that helps the patient with a sensory impairment learn to reinterpret the altered profile of normal impulses that reach the conscious level during neural regeneration. Sensory re-education improves the perception of sensory information that arises from receptors, and it increases the responsiveness of neurons in the somatosensory cortex. (20,21) In a study of the sensory potential of free-flap donor sites, Brown et al showed that the process of sensory re-education at these sites resulted in enhancement of sensory perception. (22) Their findings suggest that a 3-week course of sensory re-education can improve moving and static two-point discrimination in selected surface areas of the human body.

We undertook a study to quantitatively determine the pressure perception thresholds for both static and moving one- and two-point discrimination (s1PD, s2PD, m1PD, and m2PD) modalities in the oral cavity and oropharynx of a normal population with the Pressure-Specifying Sensory Device ([PSSD] NK Biotechnical Corp.; Minneapolis). This instrument has previously been used by hand surgeons to measure sensory thresholds in the upper extremities, and it has proven to be a reliable and accurate tool for the objective and quantitative measurement of sensation. (23) We also sought to evaluate the ability of this device to enhance sensory discrimination in the oral cavity by sensory re-education.

Materials and methods

Equipment. Pressure perception thresholds were quantified by the PSSD. This device consists of two prongs with hemispheric ends (figure 1). Both prongs are mounted on force transducers that are housed within the device. The distance between the prongs (interprong distance) can be altered to obtain two-point discrimination readings at various sites. These transducers record the amount of force that is applied during determination of s1PD, s2PD, m1PD, and m2PD. The cross-sectional area of the hemispheric ends is 0.9 [mm.sup.2]. By dividing the force of application (in grams) by the cross-sectional area, one can calculate the pressure ([g/mm.sup.2]) at which the sensation is perceived. The PSSD is computer-linked, which allows for real-time data display, retrieval, and analysis.

[FIGURE 1 OMITTED]

Testing methods'. To determine s1PD, s2PD, m1PD, and m2PD values in the oral cavity and oropharynx, we tested 11 normal volunteers--six men and five women, aged 27 to 51 years (mean: 34 [+ or -] 5)--who had no known neurologic impairment, history of radiation, or lesions in the oral cavity or oropharynx. Sensory testing was performed in a quiet, distraction-free room. Each subject sat comfortably in a chair with the head immobilized on a headrest. The examiner showed the instrument to each subject and explained the testing concept and then conducted one practice session on the forearm. During each test, the examiner calibrated the instrument for gravity. The examiner then informed the volunteer that the actual test was to commence and slowly brought the prongs of the PSSD into contact with the skin or mucosa. The pressure was slowly but steadily increased until the subject indicated perception of the stimulus by pressing a response button. The button was connected to the computer, which immediately displayed each value on the screen; information on the screen could not be seen by the subjects. The lowest threshold of s2PD was determined at various interprong distances. Mucosal blanching or indentation was avoided during all testing. Each of the four discrimination determinations was made five times.

After the data were reviewed on the computer screen, the highest and lowest values were discarded, and the mean of the remaining three values was recorded as the threshold for each determination. All tests were conducted at nine sites in the same sequence: forearm, lower lip, upper lip, buccal mucosa, floor of the mouth, tongue tip, lateral tongue, hard palate, and soft palate. All tests to establish normative data were performed by the same examiner. Static and moving one- and two-point discrimination thresholds were determined on the right and left sides separately. All four modalities were tested at all nine sites.

Four of the 11 subjects underwent sensory re-education. This was performed by touching the floor of the mouth with both prongs fixed at a distance of 13 mm. The s2PD thresholds were determined every day for 11 consecutive days, excluding weekends. These four subjects returned for re-evaluation 2 weeks following the end of testing. The floor of the mouth was selected because normative data showed that this is the least sensitive site in the oral cavity. The interprong distance was fixed at 13 mm because the threshold was maximum at this distance.

Statistical analysis. To evaluate intratester variability, the 11 subjects were studied by one of the testers for the pressure sensitivity threshold measurements. Two measurements (right and left sides) were performed at all nine sites. Correlation coefficients and 95% confidence intervals (CIs) were determined between the right and left sides of the oral cavity and forearm. The results were reported as the mean ([+ or -] SD) of the total number of sites measured by each modality.

Intertester variability was determined by measuring the thresholds of s2PD by two experienced testers at two sites--the forearm and the floor of the mouth--in eight of the 11 subjects. Each of these eight subjects was evaluated by both testers, one after the other, without any period of rest. The means ([+ or -] SD), correlation coefficients, and 95% CIs were reported for both sites. A compact variable was created between the right and left sides for all analyses of oral cavity sites and the forearm, split by modality. The most and least sensitive areas of the oral cavity were determined by a paired t test between each variable and every other variable. Because this resulted in 28 comparisons, a Bonferoni correlation was applied to establish the more appropriate probability level (0.05/28 = 0.0017). Therefore, statistical significance was defined as p [less than or equal to] 0.0017. A repeated measures analysis of variance (ANOVA) was performed to determine individual subject variability over time.

Results

We found a highly significant correlation between the right and left sides of the oral cavity and the forearm for all moralities. The correlation coefficients and 95% CIs revealed good reproducibility between the right and left sides, suggesting strong intratester reliability (table 1). Likewise, the mean ([+ or -] SD) results, correlation coefficients, and 95% CIs demonstrated very reproducible results and good intertester variability for forearm and floor of the mouth recordings performed during the s2PD modality (table 2). The results of the point discrimination thresholds were reported by oral cavity sites, forearm, and modality (table 3). The buccal mucosa and the tongue tip were found to be the most sensitive areas of the oral cavity, and the floor of the mouth and the soft palate were found to be the least sensitive (figure 2).

[FIGURE 2 OMITTED]

Initially, all four subjects who participated in the sensory re-education component of the investigation experienced significant improvement in their sensitivity at the floor of the mouth under the s2PD modality, but 2 weeks following discontinuation of the stimulus, pressure thresholds in all four returned to baseline levels (figure 3).

[FIGURE 3 OMITTED]

Discussion

The various modalities that have been used to assess sensation in other parts of the body (the hand in particular) are pain, touch, temperature, stereognosis, proprioception, and vibration. Pain is assessed by applying a needle to the skin, and it is quantitatively measured by an algesimeter. (24) Proprioception is evaluated by physically moving the anatomic structure and assessing the subject's ability to detect the direction of movement. Touch threshold can be quantified by the Semmes-Weinstein monofilament pressure esthesiometer, (25) although an engineering analysis (26) of this device revealed that it has several limitations. For example, variations in buckling stress generated within the monofilaments are difficult to avoid because changes in temperature and humidity can cause variations in the elastic modules of the monofilament. Also, even slight changes in the method of application can grossly skew the results of this discontinuous measurement. Finally, this instrument is extremely awkward to use in the oral cavity and oropharynx.

Stereognosis is the term used for the tactile recognition of objects, and it can be quantitatively assessed by two-point discrimination testing. (27) Of all the tests that measure sensation, two-point discrimination is believed to be the best at measuring functional sensation. (28,29) Functional sensation is the term used to connote the ability of the anatomic area being tested to perform a basic task. The s2PD determination is an evaluation of the innervation density of the slowly adapting fiber receptor system, and the m2PD determination is an evaluation of the rapidly adapting fiber receptor system. The results of our study suggest that the PSSD can accurately measure pressure perception in the oral cavity and oropharynx for both of these fiber-receptor systems.

An important feature of the PSSD is that it provides data points for each test from a continuous scale, and these points are recorded and stored by a computer program. In our study, the degree of intra- and intertester variability was minimal. To overcome the anatomic and technical constraints of measuring sensation in the oral cavity and oropharynx, the instrument was modified by the senior author (U.K.S.), who extended the length of the prongs so that quantitative measurement of sensation in hard-to-reach areas such as the soft palate and lateral pharyngeal wall could be obtained. Even so, the PSSD has three limitations in particular: it is expensive, it requires two examiners and a cooperative patient, and testing all sites takes approximately 30 minutes.

Recovery of functional sensation is often not satisfactory after nerve transection and repair because of several peripheral and central nervous system factors. Four problems in particular are encountered at the periphery: (1) the higher the level of the initial injury is, the greater is the retrograde damage to the cell body, (2) regenerating axons must successfully cross the site of nerve repair, (3) regenerating axons must locate an endoneural sheath that once housed a sensory axon, and (4) regenerating axons must successfully reinnervate a sensory end organ.

A variety of cortical changes has been observed in animals following the transection of a peripheral nerve. (7,30) These cortical changes may be partly responsible for the diminished sensory recovery following nerve repair and regeneration in humans because (1) regenerated nerves may reactivate only a fraction of their normal cortical space, (2) enlarged cortical representation of adjacent skin territories suggests a possible compensatory hypersensitivity of these areas, and (3) discontinuous and patchy cortical representation can lead to false localization.

Despite the peripheral and cortical disorganization, experimental and clinical evidence strongly suggests that the level of functional sensation can be improved after nerve repair. (31) Based on the results of their clinical studies, Parry and Salter (32) and Dellon (33) concluded that sensory re-education--as measured by long-term improvements in localization, tactile gnosis, and two-point discrimination--is possible in the adult following nerve repair. Sensory re-education can improve the sensory function of uninjured fingertips; such a benefit is seen when a blind person learns braille. Omer reported that the normal value for two-point discrimination was 3 to 5 mm in a sighted control group and 1.5 to 2 mm among a group of blind braille readers. (34) The value of sensory re-education was further reinforced by Brown et al. (22) The results of their study suggest that a 3-week course of sensory re-education with the Disk-Criminator can improve s2PD and m2PD in selected regions of the human body. Our study showed that improvement of sensation in the oral cavity among normal subjects through sensory training is certainly possible. However, the durability of that enhanced sensory discrimination is questionable in light of the return to baseline that occurred once the training regimen was halted. However, the loss of improvement in the normal state cannot necessarily be extrapolated to the diseased or rehabilitated state, because the level of sensation for diseased patients at the outset of training is lower than that of normals.

In our study, the PSSD provided an accurate and objective analysis of sensory discrimination in the oral cavity and oropharynx. A great deal of further investigation needs to be undertaken to ascertain the range of sensory perception in normal subjects. Studies should also be conducted in patients with neurologic, infectious, and neoplastic diseases that affect the entire sensory pathway, from the sensory receptor to the central nervous system. The impact of therapeutic intervention in this region must also be determined so that we might better understand the effect of ablative and reconstructive surgery as well as radiation and chemotherapy. It is only through quantitative analysis of the sensory thresholds that we can hope to determine the impact of anesthesia and hypoesthesia on the function of this region. Our preliminary work represents a critical step toward designing new surgical and rehabilitative strategies for restoring a higher level of function than what is currently possible.

Table 1. Intratester variability: Comparison of right and left sides

                  Total               Total
Modality        right side          left side       r value

s1PD        0.71 [+ or -] 0.43  0.72 [+ or -] 0.40   0.80
s2PD        0.82 [+ or -] 0.48  0.79 [+ or -] 0.45   0.78
m1PD        0.58 [+ or -] 0.30  0.58 [+ or -] 0.36   0.64
m2PD        0.63 [+ or -] 0.31  0.60 [+ or -] 0.35   0.87

                     Lower    Upper
Modality    p value  95% CI  95% CI

s1PD        <0.0001   0.72    0.86
s2PD        <0.0001   0.69    0.85
m1PD        <0.0001   0.50    0.75
m2PD        <0.0001   0.80    0.91

s1PD = static one-point discrimination; s2PD = static two-point
discrimination; m1PD = moving one-point discrimination; m2PD =
moving two-point discrimination; r = coefficient of linear
correlation; CI = confidence interval.

Table 2. Intertester variability for s2PD

Site             Tester 1            Tester 2       r value

Forearm     0.71 [+ or -] 0.34  0.76 [+ or -] 0.42   0.96
Floor of    0.69 [+ or -] 0.48  0.54 [+ or -] 0.27   0.94
 the mouth

                      Lower    Upper
Site        p value   95% CI  95% CI

Forearm     <0.0001    0.81    0.99
Floor of    <0.0001    0.72    0.99
 the mouth

s2PD = static two-point discrimination; r = coefficient
of linear-correlation; CI = confidence interval.

Table 3. Pressure discrimination thresholds
(g/[mm.sup.2]) for combined right and left sides

Site                    s1PD                 s2PD

Forearm          1.10 [+ or -] 0.50   1.17 [+ or -] 0.60
Lower lip        0.60 [+ or -] 0.28   0.76 [+ or -] 0.47
Upper lip        0.63 [+ or -] 0.21   0.65 [+ or -] 0.29
Buccal mucosa    0.44 [+ or -] 0.10   0.55 [+ or -] 0.25
Floor of mouth   1.06 [+ or -] 0.42   1.06 [+ or -] 0.40
Tongue tip       0.41 [+ or -] 0.09   0.41 [+ or -] 0.09
Lateral tongue   0.63 [+ or -] 0.37   0.62 [+ or -] 0.27
Hard palate      0.56 [+ or -] 0.22   0.74 [+ or -] 0.38
Soft palate      1.04 [+ or -] 0.49   1.29 [+ or -] 0.39

Site                    m1PD                 m2PD          IPD (mm)

Forearm          0.81 [+ or -] 0.31   0.84 [+ or -] 0.24     13
Lower lip        0.43 [+ or -] 0.15   0.56 [+ or -] 0.26      2
Upper lip        0.47 [+ or -] 0.20   0.53 [+ or -] 0.32      2
Buccal mucosa    0.43 [+ or -] 0.13   0.39 [+ or -] 0.14      4
Floor of mouth   1.00 [+ or -] 0.48   0.85 [+ or -] 0.24     12
Tongue tip       0.33 [+ or -] 0.06   0.41 [+ or -] 0.14      2
Lateral tongue   0.47 [+ or -] 0.21   0.47 [+ or -] 0.16      6
Hard palate      0.60 [+ or -] 0.30   0.49 [+ or -] 0.18     11
Soft palate      0.80 [+ or -] 0.32   1.12 [+ or -] 0.37     12

s1PD = static one-point discrimination; s2PD = static two-point
discrimination; m1PD = moving one-point discrimination; m2PD =
moving two-point discrimination; IPD = interprong distance.

References

(1.) Matloub HS, Larson DL, Kuhn JC, et al. Lateral arm free flap in oral cavity reconstruction: A functional evaluation. Head Neck 1989;11:205-11.

(2.) Urken ML, Buchbinder D, Weinberg H, et al. Functional evaluation following microvascular oromandibular reconstruction of the oral cancer patient: A comparative study of reconstructed and nonreconstructed patients. Laryngoscope 1991;101:935-50.

(3.) Urken ML. Composite free flaps in oromandibular reconstruction. Review of the literature. Arch Otolaryngol Head Neck Surg 1991;117:724-32.

(4.) Baker SR. Microvascular free flaps in soft-tissue augmentation of the head and neck. Arch Otolaryngol Head Neck Surg 1986;112: 733-7.

(5.) Irons GB, Wood MB, Schmitt EH III Experience with one hundred consecutive free flaps. Ann Plast Surg 1987;18:17-23.

(6.) Shaw WW. Microvascular free flaps. The first decade. Clin Plast Surg 1983;10:3-20.

(7.) Wall JT, Kaas JH, Sur M, et al. Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: Possible relationships to sensory recovery in humans. J Neurosci 1986;6:218-33.

(8.) Boyd B, Mulholland S, Gullane P, et al. Reinnervated lateral antebrachial cutaneous neurosome flaps in oral reconstruction: Are we making sense? Plast Reconstr Surg 1994;93:1350-9; discussion 1360-2.

(9.) Urken ML. The restoration or preservation of sensation in the oral cavity following ablative surgery. Arch Otolaryngol Head Neck Surg 1995;121:607-12.

(10.) Sherrington CS. Cutaneous sensations. In: Schaefer EA, ed. Textbook of Physiology. Vol. 2. London: Young J. Pentland, 1900:934-9.

(11.) Grossman RC. Methods for evaluating oral surface sensation. J Dent Res 1964;43:301-3.

(12.) Grossman RC, Hattis BF, Ringel RL. Oral tactile experience. Arch Oral Biol 1965;10:691-705.

(13.) Ringel RL, Ewanowski SJ. Oral perception: I. Two-point discrimination. In: Bosma JF, ed. Symposium on Oral Sensation and Perception. Springfield, Ill.: Charles C. Thomas, 1967:389-98.

(14.) Henkin RE, Banks V. Tactile perception on the tongue palate and the hand of normal man. In: Bosma JF. ed. Symposium on Oral Sensation and Perception. Springfield. Ill.: Charles C. Thomas, 1967:182-7.

(15.) Bosma JF. Human infant oral function. In: Bosma JF, ed. Symposium on Oral Sensation and Perception. Springfield, Ill.: Charles C. Thomas, 1967:98-110.

(16.) Rutherford D, McCall G. Testing oral sensation and perception in persons with dysarthria. In: Bosma JF, ed. Symposium on Oral Sensation and Perception. Springfield. Ill.: Charles C. Thomas, 1967:118-201.

(17.) Lass NL, Kotchek CL, Deem JF. Oral two-point discrimination: Further evidence of asymmetry on right and left sides of selected oral structures. Percept Mot Skills 1972;35:59-67.

(18.) Maeyama T, Plattig KH. Minimal two-point discrimination in human tongue and palate. Am J Otolaryngol 1989;10:342-4.

(19.) Aviv JE, Hecht C, Weinberg H, et al. Surface sensibility of the floor of the mouth and tongue in healthy controls and in radiated patients. Otolaryngol Head Neck Surg 1992;107:418-23.

(20.) Lundhorg G. Peripheral nerve injuries: Pathophysiology and strategies for treatment. J Hand Ther 1993;6:179-88.

(21.) Dellon AL. Evaluation of Sensibility and Re-education of Sensation in the Hand. Baltimore: Williams and Wilkins, 1981.

(22.) Brown CJ, Mackinnon SE, Dellon AL, Bain JR. The sensory potential of free flap donor sites. Ann Plast Surg 1989;23:135-40.

(23.) Dellon ES, Mourey R, Dellon AL, Human pressure perception values for constant and moving one- and two-point discrimination. Plast Reconstr Surg 1992;90:112-17.

(24.) Dellon AL. Evaluation of Sensibility and Re-education of Sensation in the Hand. Baltimore: John D. Lucas, 1988:4-13.

(25.) Semmes L Weinstein S, Ghent L, Telber HL. Somatosensory Changes after Penetrating Brain Wounds in Man. Cambridge. Mass.: Harvard University Press, 1960.

(26.) Levin S. Pearsall G. Ruderman RJ. Von Frey's method of measuring pressure sensibility in the hand: An engineering analysis of the Weinstein Semmes pressure aesthesiometer. J Hand Surg 1978;3:211-16.

(27.) Dellon AL. Evaluation of Sensibility and Re-education of Sensation in the Hand. Baltimore: John D. Lucas, 1988:123-39.

(28.) Moberg E. Criticism and study of methods for examining sensibility of the hand. Neurology 1962;12:8-9.

(29.) Flynn JE, Flynn WF. Median and ulnar nerve injuries. Ann Surg 1962:156:1002-9.

(30.) Merzenich MM, Jenkins WM. Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience. J Hand Ther 1993;6:89-104.

(31.) Vinograd A, Taylor E, Grossman S. Sensory retraining of the hemiplegic hand. Am J Occup Ther 1962;5:246-51.

(32.) Parry CB, Salter M. Sensory re-education after median nerve lesions. Hand 1976;8:250-7.

(33.) Dellon AL. Sensory recovery in replanted digits and transplanted toes: A review. J Reconstr Microsurg 1986;2:123-9.

(34.) Omer GE. Sensory evaluation by the pickup test. In: Jewett DL, McCarroll HR, Jr., eds. Nerve Repair and Regeneration: Its Clinical and Experimental Basis. St. Louis: Mosby, 1980.

From the Department of Otolaryngology-Head and Neck Surgery, Keck School of Medicine, University of Southern California, Los Angeles (Dr. Sinha), the Department of Otolaryngology-Head and Neck Surgery. Medical College of Wisconsin, Milwaukee (Dr. Rhee), and the Department of Otolaryngology-Head and Neck Surgery, Mount Sinai School of Medicine, New York City (Dr. Alcaraz and Dr. Urken).

Reprint requests: Uttam K. Sinha, MD, LAC-USC Medical Center, 1200 N. State St., Box 795, Los Angeles, CA 90033. Phone: [phone]; fax: [phone]; e-mail: [e-mail]