_______ J ! * 0 ) A _______________ CLINICAL
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The use of infrared thermography in the evaluation of oral lesions B . A le x W hite, D D S P eter B. L ockhart, D D S Su san F. C o n n o lly , D M D S tep h en T . S o n is, D M D , D M S c
nfrared therm ography, a technique whereby infrared radiation is trans lated from the body surfaces into a th e r m a l p ic tu r e , h as b e e n u s e d medicine as a clinical diagnostic aid for many years. Lawson1 introduced infrared therm ography in 1956 for the evaluation o f breast lesions. Since th a t tim e, re searchers have used the technique as an adjunct to screen for and assess breast cancer2,8 and to diagnose and m anage m alignant m elanom a.7'9 T herm ography has been used to quantitate inflammation present in osteoarthritic joints10 and in the sacroiliac region.11 T he technique also has been used to evaluate oral tissues. Crandell and Hill12 studied therm ography and its ability to determ ine the vitality of teeth.
I
In addition, therm ography has been used to evaluate inflammation o f the oral tis sues in studies by Sukharev and others13 in and by Soffin and others.14 Two techniques exist by which infrared radiation emitted from the body surface can be detected and translated into visible lig h t. O n e m e th o d is e le c tro n ic , o r teletherm ographic. In this m ethod, in frared radiation em itted from the body, usually at wavelengths between 4 and 20 /xm, is captured by a detector and trans lated into visible light. T he image is sub sequ en tly p ro je cted o n to a television screen and photographed for a perm a nent record.15 T he second m ethod uses a Mylar plate em bedded with liquid crystals, which is placed in contact with the skin,
resulting in color visual im ages. Selfdeveloping color films often are used to obtain the final im age.16 This study evaluates the potential o f in frared therm ography in assessing normal versus abnormal oral mucosa by telether mography.
Methods and materials O n e subject with n o rm al o ral m ucosa (no visible oral lesions) and th re e subjects with o ral lesions w ere studied. T h e re was n o o ra l in ta k e fo r 30 m inutes b efore the study. E ach subject was e x am in ed w ith a th erm al video system (H u g h es Series 4000 PRO BEY E) using a n in fra re d im ag er a n d a m icroprocessor. In fra re d em issions fro m th e m ucosal tissue sur-
Fig 1 ■ Subject 1. Left, clinical photograph o f norm al tongue. Note the position o f the m axillary teeth, low er lip, an d buccal vestibule lateral to tongue and m edial to com m issures. R ight, therm ogram o f same patient. Cool areas (blue) represent anterior tongue (A) and m axillary teeth (B) and w arm er areas (green) represent posterior tongue (sm all arrows) and low er lip (large arrows). T h e w arm est area is intraoral and is represented as buccal vestibule (C).
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faces w ere d e te cte d by a h a n d -h eld scanner com p o sed o f six in fra re d d etectors, cooled to 87 K ( —186 C) by arg o n gas. T h e in fra re d ra d ia tion d e te cte d was c o n v erted in to electrical im pulses, a m p lifie d , p ro c essed , a n d p ro jec te d o n to a color television screen as a reconstruction of the in fra re d radiation. A 35-m m cam era was used to obtain a color p h o to g ra p h o f the televi sion m o n ito r a n d a clinical p h o to g ra p h o f each subject. M ultiple th erm o g ram s w ere taken and p h o to g ra p h e d at d iffe re n t tim es to d e te rm in e
w h e th er te m p e ra tu re re ad in g s could be d u p li cated a n d to test th e d e g ree o f accuracy o f each read in g . Subject 1 was a 27-year-old w hite m ale in good health w ith n o signs o r sym ptom s o f sys tem ic disease o r oral lesions (Fig 1). Subject 2 was a 31-year-old w hite fem ale with severe aplastic anem ia w ho h a d an ulceration o f the left labial m ucosa ad jacen t to th e first p re m o la r (Fig 2). T h e lesion, believed to be secon d a ry to trau m a a n d im m u n o su p p re ssio n , was
appro x im ately l x l cm a n d h a d a w hite n e crotic c en ter w ith a s u rro u n d in g 0.2-cm halo o f ery th em a. Subject 3 was a 60-year-old w hite m ale with ch em o th era p y -in d u c ed n e u tro p e n ia , secon dary to a d iffu se histiocytic lym p h o m a, w ho had an ulceration on the m id-dorsal su rface o f the to n g u e (Fig 3). T h e re was a s u rro u n d in g a re a o f appro x im ately 2.5 X 1.5 cm of d e n u d e d p apil lae. In the c en ter of this a re a was a n ulceration sh ap ed like a n u m b e r seven (7) w ith a yellow
Fig 2 ■ Subject 2. Left, clinical photograph o f neutropenic m ucosal breakdow n with a white necrotic center and su rro u n d in g erythem atous halo (small arrows). Swelling extends from the index finger at the top of the figure to the finger seen at th e extrem e bottom of th e fig ure (arrow). Right, therm ogram o f same patient. H and and fingers (large arrows) holding the low er lip show a range o f tem peratures from the teeth (A), w hich are blue-green, to the swollen, erythem atous low er lip (B). T he areas are separated by a very warm buccal vestibule (C). T he cooler area (D) in the center of the sw ollen lip is the plaque-covered ulcer seen in Figure 2, left. In the rin g o f w arm er (red) areii around the lesion, the cross hairs intersect (D). T he red band between the teeth (A) and the buccal vestibule rep resen ts p eriodontal inflam m ation.
Fig 3 ■ Subject 3. Left, clinical photograph of ulceration w ith superim posed thick yellow plaque shaped like a num ber seven (7) and su r ro u n d ed by raised, denuded, and erythem atous tongue tissue. Right, therm ogram o f sam e patient. Tongue (large arrow s) is progressively w arm er tow ard th e lesion (small arrow ). A slight distortion has occurred as a result o f th e angle from which the therm ogram was taken. As a resu lt, the ulceration in Figure 3, left, appears to be o ff center in Figure 3, right. T he warm est area is represented by the d enuded area to the left of the ulceration in Figure 3, left, and by the w hite area (C) in Figure 3, right.
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left) shows scattered ulcerations in th e c e n te r o f th e h a rd palate. T h e th e rm o g ra m (Fig 4, right) shows areas o f increased te m p e ra tu re (33.9 C) s u r ro u n d in g each lesion, w ith th e w arm est a reas in the c en tral area o f ulceration. T h e area betw een the ulcerations also has in creased te m p e ra tu re . T h e uninvolved areas, such as th e al veolar ridges a n d lateral palate, a re c ooler (31.5 C to 32.0 C). Several th e rm o g ra m s o f each subject w ere o btained. Each lesion show ed a core te m p e ra tu re th a t was re p ro d u c ib le to w ithin 0.2 C.
Discussion
Fig 4 ■ Subject 4. Left, clinical photograph o f m ultiple ulcerations on the h ard palate. T he lesions have varying am ounts of overlying plaque and significant erythem a is present. L etters indicate posi tions o f lesions represented in the therm ogram (Fig 4, right). R ight, therm ogram o f sam e patient. Note m ultiple areas o f increased heat (red), some o f w hich have w an n er (white) centers. As a resu lt o f the in ability to position the in frared cam era at a 90° angle to the palate, th e lesions appear in a slightly d iffer en t orientation than in the clinical photographs. T hus, various ulcers are lettered on both F igure 4, left and right, fo r orientation. T he cross hairs (arrow) are in th e cen ter of the warm est an d m ost denuded ulcer (A).
necrotic surface. Subject 4 was a 60-year-old w hite m ale with acute m yelogenous leukem ia w ho h a d palatal ulcerations secondary to cancer ch em o th era p y (Fig 4). T h ese lesions w ere shallow, irreg u larly sh ap ed , a n d scattered over m ost o f th e h a rd palate vault. T h e ulcers h a d d iffe re n t d eg rees o f d e n u d a tio n a n d associated necrotic covering. M o d e ra te in fla m m a tio n s u rro u n d e d th e le sions.
Results T h e results o f this study a re su m m arized in T ab le 1. T h e te m p e ra tu re ra n g e o f th e m ucosal surfaces stu d ied v aried betw een 30.0 C a n d 34.2 C, w ith a sensitivity in each case o f 0.2 C. T h e te m p e ra tu re scales fo r each th e rm o g ra p h are re p re se n te d above o r alo n g th e side o f each th e rm o g ra m , with blue re p re se n tin g th e coolest a re a s a n d w hite re p r e s e n tin g th e w a rm e st areas. T h e a rea indicated by the intersection o f th e vertical a n d h o rizontal lines o n each th e r m og ram was m ea su re d a n d is n o te d as th e core te m p e ra tu re . Subject 1 served as th e co n tro l (Fig 1, right). T h e a n te rio r th ird o f the to n g u e (A), w hich is covered by papillae, a n d the facial surfaces o f I he m axillary teeth (B) a re cooler (31.0 C to 31.5 ('.) th a n a re o th e r areas. T h e m iddle th ird o f th e to n g u e (small arrow s) a n d th e lips (large a r rows) a re slightly w a rm er (31.9 C) th a n is the facial surface o f th e teeth. T h e w arm est areas
(C) (33.0 C to 34.0 C) a re th e in tra o ra l areas m edial to the com m issures a n d lateral to the tongue. T h e clinical p h o to g ra p h o f subject 2 (Fig 2, left) shows an ulcerative lesion with a necrotic c en ter, su rro u n d e d by a n e ry th e m a to u s halo (small arrow s). T h e th e rm o g ra m fo r subject 2 (Fig 2, rig h t) shows th at th e coolest area s (D)
It is likely that the oral mucosal lesions in this study had varying thicknesses o f su r face epithelium , exudate, necrosis, and cellular debris. Changes in surface tem perature probably were related to the d e gree of inflammation because o f increased vascularity and blood flow.13,14 It is clear from a com parison o f the clinical and therm ographic pictures in this study that a direct relationship existed between the thickness o f the overlying plaque and the tem perature em itted by the lesion. T he degree o f vascularization and inflam m a tion was most decided in the d enuded areas (Fig 4) and in areas with thin his tological epithelium but without surface debris. Although the lesions in this study pro b ably were ulcerative in nature, infrared therm ography had potential value as an aid in determ ining the surface tem pera ture o f other oral lesions. Given that in creased tem perature is often a sign o f in flam m ation, a decrease in tem perature during a period may reflect a decrease in
; 'urther applications of infrared thermography may include the measurement of changes in the surface temperature of certain oral lesions before and after the administration of different anti-inflammatory agents.
(31.7 C) o f th e lesion w ere at its c e n te r, w ith the w arm er b an d (B) (32.0 C to 33.0 C) s u rro u n d ing th e ulceration. T h e clinical p h o to g ra p h o f subject 3 (Fig 3, left) shows an area o f d e n u d e d to n g u e w ith a c en tral necrotic ulceration. T h e th erm o g ram (F'ig 3, right) shows cooler areas w h ere th e p apil lae a re intact (large arrow s) a n d a progressively increased te m p e ra tu re tow ard th e c e n te r o f the lesion. T h e core a re a (C) o f th e u lceration was th e w arm est (33.7 C) a n d was su rro u n d e d by a b an d o f tissue (small arrow s) w ith increased te m p e ra tu re (33.9 C). T h e clinical p h o to g ra p h o f subject 4 (Fig 4,
inflammation. In this pilot study, it has been shown that differences in surface tem perature, which may reflect inflam m a tory changes associated with oral lesions, can be m easured accurately by the use of therm ography, fu r th e r applications o f in frare d th erm ography may include the m easurem ent o f effects o f different top ical and systemic anti-inflam m atory agents on certain oral lesions by m easuring the change in surface tem perature o f oral le sions before and after the agent has been adm inistered.
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Table 1 ■ Summary of the results of the study. Subject
T e m p e ra tu re ra n g e (C)
C o re te m p e ra tu re (C)
A reas co oler th a n c o re te m p e ra tu re
A reas sam e te m p e ra tu re as c o re te m p e ra tu re
A reas w a rm e r th a n c o re te m p e ra tu re
1
31.0 to 34.2
31.9
M iddle th ird o f dorsal s u rface o f to ngue C om m issures o f lips U p p e r lip
Buccal vestibules
2
30.0 to 33.2
31.7
A n te rio r th ird o f to n g u e Facial su rface o f m a n d ib u la r incisors S u p e rio r surface o f low er lip Facial su rface o f m a n d ib u la r incisors
M a n d ib u lar facial gingiva I n n e r su rfa c e o f low er lip
3
31.0 to 34.2
33.7
A re a s u rro u n d in g lesions Low er lip M an d ib u lar labial vestibule N o areas noticed
4
31.0 to 34.2
33.9
Summary
This study was conducted to quantitate the degree o f inflammation associated with oral lesions by using infrared therm og raphy. It was reasoned that the increased vascularity associated with inflamed tissue may result in m easurable increases in sur face tem perature. O ne subject with norm al oral mucosa and three subjects with oral lesions o f vary ing causes were studied with a therm al video system, using an infrared imager and m icroprocessor. A clinical p h o to graph o f each subject was obtained. Multi ple therm ogram s were made in a tem pera ture range o f 30.0 C to 34.2 C at a sensitiv ity o f 0.2 C. Photographs were taken on different occasions to determ ine w hether the tem perature readings could be dupli cated and to test the accuracy o f each reading. T h e norm al surface tem perature o f the control subject’s mucosa was significantly cooler than were the tem peratures o f the inflam ed areas in the subjects with le sions in d u c e d by ch em o th erap y . T h e tem perature o f the areas of stomatitis was consistent (subject 3, x = 33.7 C; subject 4, x = 33.9 C). T h e necrotic center o f a traum atic ulcer inhibited m easurem ent of an underlying inflamed base and, thus, was equivalent to the control in tem pera 786 ■ JA D A , V ol. 113, N ovem ber 1986
A n te rio r th ird o f d o rsa l su rface o f to n g u e L ateral b o rd e rs o f m id d le th ird o f d o rsa l su rface o f to n g u e L ateral d e n u d e d areas o f m id d le th ird o f to n g u e R in g a p p ro x im a te ly 0.2 cm in d ia m e te r s u rro u n d in g c e n te r o f lesion A lveolar ridges an d lateral areas o f h a rd palate R in g ap p ro x im ately 0.2 cm in d ia m e te r s u rro u n d in g c en tra l a re a o f each lesion
A re a 0.3 cm x 0.3 cm s u rro u n d in g a re a o f core te m p e ra tu re
C en tra l areas o f a d ja ce n t lesions
tu re (subject 1 (control), x = 31.9 C; sub ject 2 (necrotic lesion), x = 31.7 C). T h ese results suggest th at in fra re d therm ography may provide a means to quantitatively assess the degree o f mucosal inflammation. ---------------------- j m A -----------------------T h is stu d y was s u p p o rte d in p a rt by th e B righam Surgical G ro u p F o u n d a tio n a n d E. I. D u P o n t deN e m o u rs an d Co.
D r. W hite is g ra d u a te stu d e n t, d e p a rtm e n t o f h ealth policy a n d m an ag em en t, H a rv a rd U niversity School o f Public H ealth , B oston; an d was c h ie f re sid en t, division o f d e n tistry , B rig h am a n d W om en’s H ospital, B oston. D r. L o c k h a rt is d ire c to r, residency p ro g ra m in g e n eral d e n tistry , division o f d e n tistry , B rig h am a n d W o m en ’s H o sp ital, B oston. Dr. C onnolly is d ire c to r o f c o n tin u in g e d u c a tio n , division o f d e n tistry , B rig h a m a n d W o m en ’s H ospital, B oston. D r. Sonis is chief, d e n ta l service, division o f den tistry , B righam a n d W o m en ’s H o sp ital, 75 Francis Street, B oston, 02115. A ddress re q u e sts fo r re p rin ts to D r. Sonis. 1. Law son, R.N. T h e rm o g ra p h y : new tool in inves tig atio n o f b re a st lesions. C an Serv M ed J 13:517-524, 1957. 2. Is a rd , H .J., a n d o th e rs. B reast th e rm o g rap h y : th e m a m m a th e rm . Radiol C lin N o rth A m 12:167-188, 1974. 3. Isa rd , H .J., a n d o th e rs. B reast th e rm o g ra p h y a fte r fo u r years a n d 10,000 studies. A m J R oentgenol 115:811-821, 1974. 4. G a u th erie , J ., an d G ross, C.M . B reast th e rm o g ra p h y a n d c an c e r risk p re d ic tio n . C an c e r 45:51-56,
N o are as noticed
1980. 5. G a u th erie , M. T h e rm obiological assessm ent o f b e n ig n a n d m a lig n a n t b re a st diseases. A m J O bstet G ynecol 147(8):861-869, 1983. 6. D avison, T .W ., an d o th e rs. D etection o f b reast c a n c e r by liq u id c r y s ta l t h e r m o g r a p h . C a n c e r 29:1123-1132, 1972. 7. B o urjot, P.; G au th erie, M.; a n d G rosshans, E. D iagnosis, follow -up, a n d p ro g n o s is o f m a lig n a n t m elan o m a by th e rm o g ra p h y . Bibl R adiol 6:115-127, 1975. 8. H a rtm a n n , M., a n d K u rn ze, J . In f ra re d th e r m o g ra p h y fo r diagnosis a n d surveillance o f m a lig n a n t m elan o m a p atien ts A rch D erm atol Res 2 6 4 :1 2 0 ,1 9 7 9 . 9. H a rtm a n n , M.; K u rn a e , J.; a n d F riedel, S. T e le th e rm o g ra p h y in the diagnosis a n d m a n a g e m e n t o f m a lig n a n t m elanom a. J D erm atol S urg O ncol 3:213215, 1979. 10. R ing, E.F.; D rip p e , P.A .; a n d B acon, P.A. T h e th e rm o g ra p h ic assessm ent o f in flam m a tio n a n d a n ti in flam m ato ry d ru g s in osteo arth ritis. B r J C lin Pract 35(7-8):263-264, 1981. 11. G re e n e r, D.M ., an d Caygill, L. In f ra re d th e r m o g ra p h y in th e assessm ent o f sacroiliac in flam m a tion. R h eu m ato l an d R ehabil 21:81-87, 1982. 12. C ra n d ell, C.E., an d H ill, R.P. T h e rm o g ra p h y in d en tistry : a pilot study. O ral S u rg 21:316-320, 1966. 13. Sukharev, M .F.; Ivanova, R.P.; an d R eitsm an, D.M. T h e rm o g ra p h y in od o n to g e n ic in flam m a to ry process. Stom atologia 56:37-39, 1977. 14. Soffin, C .B ., an d o th e rs. T h e rm o g ra p h y a n d o ral in flam m ato ry conditions. O ral S u rg 56(3): 256262, 1983. 15. G a u th e rie , M ., a n d o th e rs . A c c u ra te m e a s u re m en ts o f skin te m p e ra tu re by in fra re d th e rm o g ra p h y . Pathol Biol 10:559, 1971. 16. G a u th erie , M.; Q uenneville, Y.; a n d G ross, C. L iquid crystal th e rm o g ra p h y : clinical, p h a rm a c o lo g i cal, a n d physiological application a n d c o m p a riso n w ith in fra re d th e rm o g ra p h y . Pathol Biol 22:553, 1974.