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Periodontal disease in the rice rat
Periodontia PERIODONTAL DISEASE IN THE RICE RAT II. Methods for the Evaluation of the Extent of Periodontal Disease Ch
P.
GIJPTA,
B.D.S., M.S.,
AND
JAMES
H.
SHAW,
PH.~).,
BOSTON,
JVLASS.
UMEROUS procedures have been reported for the evaluation of periodontal N disease in experimental animals. There are conflicting opinions as to whether an adequate appraisal of the extent of periodontal involvement can be made of soft tissue lesions alone, of alveolar bone resorption only, or whether both should be estimated. Mitchell’ has used a method based on evaluation ol’ t,he condition of the gingival tissues and the quantity of subgingival debris in forty designated areas around the molar teeth of hamsters. Scores from 0 t’o 3 were recorded for each area. Mitchell and Chernausek* further modified this procedure by omitting a consideration of the eight inte.rproximal areas and chose to express periodontal damage on the basis of whether or not there were lesions in the remaining thirty-two areas without reference to the size of the lesion. Rushton made histologic preparations from which the amount of downgrowth of the epithelial attachment was measured. The extent of periodont,al damage was estimated from these measurements coupled with the amount, of gingival plaque. Johansen has described a method for estimation of the cxtent of soft tissue involvement in living hamsters. This is essentially a modificat,ion of the procedure described by Mitchell1 and allows for a numerical evaluation of the lateral extent of periodontal pockets as well as the depth of the lesions. Costich5 recorded alveolar bone resorption in terms of a scale from 0 to 3+. However, he felt, that, this was inaderluate and described an alt.ernatr method in which the lesions were drawn on a chart. Tracings of t,he lesions were made on cellulose acetate paper. The areas representing bone resorption wtre cut out and weighed by quadrant or as the total per animal. Shourie, Driesinger, and Hein have proposed a roentgenographic method for use in living hamsters for estimation of the extent of periodontal lesions. Keyes and Oold7 have advocated use of a specially designed, graduated instrument for the measurement of alveolar crest resorption after the soft tissues were removed. From the Harvard School of Dental Medicine. This investigation was supported by a grant-in-aid from the Nutrition Ii’oUndation New York, N. Y.. and by a research grant, D-100, from the National Institute of Kesearch, of the National Institutes of Health, Public Health Service.
727
Inc. hcntai
7%
oM P. GTX’TA AND .JAMER H. ST-lb\%
The purpose of the present study was to develop a reasonably quantitative mctllod l’or the evaluation of 1he scvrritp 0I’ periodontal Icsions in the rice rat, whose susceptibility lo tllcsc Icsiorrs has bWi dosc~ribrd in an c~rlior article.” It was our purpose to ~mparc available methods and arjrivc at a procedure Orat would give an accurate, yet not undu1.v time-consuming, appraisal of the degree of periodontal involvrment with reproducible results in repeated observations of the same specirncns.
Methods Sevent.een rice rats with slight to severe periodontal lesions were selected as representative subjects to be evaluated by three different. procedures. Tl~sc animals had been maintained for twenty-three weeks after weaning on dirts that were slight modifications of purified, high-sucrose, cariogenic ration ‘700.” They had been housed singly in wire-bottom cages, and had been provided with ,4fter sacrifice and fixation of the heads f’or diet and tap water ad libitum. forty-eight, hours or more in 95 per cent alcohol, t,he oral Gssucs were cxaminrtl at, a magnification of X 30. Periodontal lesions were evaluated according to the following ‘three rnethods :
1. Extent of Soft Tissue Involvement.-For
reference purposes, in the evaluation process the tissues surrounding a molar were divided arbitrarily into as many areas as the nurnber of cusps in each tooth. Thus, there were seven areas on the lingual and seven on the buccal aspect of the teeth in each quadrant. of each jaw, a total of fifty-six areas. It was considered that the area adjacent to the mesiobuccal cusp of any molar extended from t,he center of thr rnrsial surface to the first sulcus on the buccal surface. Likewise, the area adjacent to the mesiodistal cusp of any molar extended from the center of t,he distal surface to the adjacent sulcus on the buccal surface. Similar defirritions were employed for the areas adjacent, to the mesial and distal cusps on thcl lingual surface of the molars. In this way, no scores pertained specificall) to the mesial and distal surfaces. The gingival lesions were assigned arbit,rary gradations on the basis of severity-O, l+, 2+, 3+, and &-which could be described as follows: 0 = No detectable abnormalit,irs. I+ = The gingival tissue showed slight changes in color, contour, a’ncl consistency. Usually there was a slight impaction of foreign matter. 2+ = A slight detachment, of the gingiva was commonly observed with moderate impaction of foreign rnattcr and early changes in rolor, contour, and consistency of t,he gingiva. 3~1~= A moderate detachment, and recession of the gingi\q were characteristic. In addition, the gingiva was flabby in consistency and
PERIODONTAL
DISEASE
IX
had lost its normal color and contour. impaction
of debris throughout
RICE
RAT.
7”2!!
II
These Icsions usnaIl>; showed
the cntircl gingival
SUES.
4: = These lesions were associated with severe detachment. of the gingiva with extreme recession. Commonly there were major impactions of foreign material in the spaces between the gingiva and the t,eeth. Teeth with lesions of this size Crrqucntly \v~re mobile and WI)arated by sizeable diastema. Examples of the size and nature of these lesions arc shown in Figs. 1. :L ,5, and T. The degree of involvement of the soft tissues for the cntirr> I!WU~~ was determined by adding the scorrs of thr fifty-six areas.
2. Evaluation
of Bone Resorption by the Method of Keyes and Goldq7-
After the examination and recording of soft, tissue lesions, the soft, tissues were removed. The fifty-six areas adjacent to the cusps were taken as ihe reference points; alveolar bone resorption was mc>asurcd in terms of tho distance that the alveolar bone had reccdcd from the cementoenamel junction. The measurements were made under a hinoeular dissecting microscope with 1hr help of a metal blade graduated at, 0.2 mm. intervals. The blade was hc~ltl against each area and the recession of’ alveolar bonc~ was recorded in trrms 01 the divisions on the blade. The records wore not kept directly in millimeters but in units, each unit being equal to 0.2 mm. The units of’ hone resorpt iott determined for the fifty-six areas we’re totaled as a means of expressing thy degree of periodontal disturbance in the clntire mouth.
3. Evaluation of Alveolar Bone Resorption by Assignment of Arbitrary Values.-In this case, the degree of alveolar resorption for t,hc salnc fifty-sis areas was recorded under arbitrary the following characteristics:
gradations--O,
14, ?A! :I-+; and 1 ~---with
0 = No detectable hone resorption. 11. = These areas had a minor amount of alveolar resorption one-fourth or less of the root exposed.
with
‘Lt = These lesions had an appreciable amount, of alveolar loss with one-fourth to one-halt’ of the root exposed.
horrta
with
3+ = These lesions had a moderately bet,wecn one-half and three-fourths
cxtcnsivc alveolar rrxorptio,t, of the root being visihll>.
4t- = These areas demonstrated the most severe alveolar resorption with essentially no remaining alveolar bone support for the root. Teeth with several areas of this size usually were mobile and separated by
diastema. Examples of the size and nature of these lesions are shown in $‘igs. 2, 4, 6, and 8. The scores for the fifty-six areas of the entire mout,h were totaled as a measure of the severity of periodontal disease. In order to test the reproducibi1it.y of the values obtained by the three methods, the seventeen heads were evaluated three times on different days by each method.
Figs. 1 to 8.-,Photograpbs of flxed preparations of rice rat jaws that were selected “,o,sil;;trate the ,appli~ation of the three procedures used for scormg the extent of periodontal . (Magmflcation, x15: reduced J/e.) The odd-numbered figures are photographs of the lingual aspects of mandibles with the Immediately above each of these figures are seven individual scores soft tissues in situ. as obtained for the seven lingual cuspal areas by the soft tissue evaluation procedure (Soft). The even-numbered figures are photographs of the lingual aspects of the same four mandibles after the soft tissues have been removed to reveal the amount of alveolar bone resorption. Immediately below each of these flgures are two horizontal rows, each of which The scores in the upper row in each case were obtained contains seven individual values. by the method of Keyes and Gold (K. & G.), while the values in the lower row of each pair were obtained by the method of assigning arbitrary values (Arb.) The values shown above for all three methods were the actual ones determined for Minor discrepancies appear to exist when the these jaws under laboratory circumstances. results are recorded adjacent to the appropriate regions of photographs. These discrepancies can be explained by the lack of the third dimension in the photographic reproductions. by differences in the occlusal planes of the molars, and by varying root lengths among the three molars. Figs. 1 and Z.-Lingual views of the left mandibular molars of a rice rat with mild lesions in the periodontal tiSSUSS. Figs. 3 and 4.-Lingual views of the right mandibular molars of a rice rat with a moderate involvement of the periodontal structures.
PERIODONTAL
DISEASE
.gs. Per views of the right Fi igs. 7 and 8.-Lingual ten sive de st ruction of the periodontal structurw
IS KtCE RAT. II
I‘i 1.E
Fi
SeY ‘et-e
nlnnilibular
molar’s of a rice
H
ith
732
OM
I’.
GUPT.4
1ND
JAMES
H.
SHAW
Results and Discussion In Table I are recorded the scores obtained by the three methods for the extent of periodontal disease in these rice rats. In this presentation of data, the individual rice rats have been arranged in increasing order of severity of disease manifestations as scored by the method of Keyes and Gola.’ The data in this table indicate that the standard deviation did not exceed 4 units per head either by Keyes and Gold’s method or by the method of assigning arbitrary values for the amount of alveolar bone resorption. However, the standard deviation of observations for a given animal by the method of soft tissue involvement was as high as _+7 units. TABLE I.
AVERAGE SCORES OF TRIPLICATE MEASUREMENTS OF THE EXTENT OF PERIODONTAL DISEASE IN RICE RATS OBTAINED BY THREE DIFFERENT METHODS I
RAT NO. 93 78 75 82
81 79 94 76
89
ALVEOLARBONERESORPTION METHODOF KEYESANDGOLD ARBITRARY METHOD AVERAGE* S.D.t (UNITS) (UNITS) AVERAGE 1 S.P. t 94 3 68+ 2+ 108 122 125 136 195 203 206 207 221 228 237 242 243 267 269 273
2 2 a 2 3 1 1 1
76+ 95+ 79+ 95+ 159+ 152+ 154t 162t
2c 2+ 1+ 1+ 0 2 2t 3t
170t
lt
154+ 174+ lF(O+ 186+ 183+ 200+
3t 4t 3+ 3+ 3+ 3t
1 190+ *One unit is equal to 0.2 mm. of bone loss. tstandard deviation.
3+
74 83 95 88 97 96 80 73
i 2 2 3 2 2
I SOFTTISSUE DESTRUCTION AVERAGE 1 S.D.t 0 0 0 0 7+ 127+ 96+
0 1+ 4+
1e9+
6t
127+ 123t 132+ 704t 148+ 171+ 152+ 157t 144t
3t 3+ 3t 7t 6+ 2t 2+ 2+ 2+
In this series of rice rats we observed that the scores in both the maxilla and the mandible had a high degree of bilateral symmetry. The extent of this bilaterality, as tested by both alveolar bone resorption methods, is presented in Table II. It was further observed that the scores of the lingual side were higher than the scores of the buccal side and that the mandibular scores were higher than the maxillary scores (Table II). Our findings clearly indicate that the evaluation of periodontal lesions in the rice rat could be limited to one-half of both jaws; however, both the lingual and buccal scores must be taken into consideration. The alveolar bone resorption method described by Keyes and Gold7 appeared to be the most exact method for the evaluation of bone resorption, albeit considerably more tedious and time consuming than t,he other methods. The method of assigning arbitrary values from 0 to 4+ for the extent of alveolar bone resorption was appreciably quicker and less tedious, without demonstrable sae-
-
93 78 73 82 Xl 79 94 76 89 74 83 95 88 9; 96 SO $3
ILIT so.
11.
37 50 62 6" 64 98 104 99 99 112 110 121 119 124 134 137 135
:z 71 97 99 10; 109 10s 11% I L6 123 119 133 132 13s
56 58
%9+ 38+ 4it 4oc 48+ 81t ii+ i3+ i6+ 8% ii* H6t 90H& X9+ 100~Rj-
40+ 40+ 4i+ 39i 47+ is+ 75, 81+ 83t 82+ iii Xir
I
55
38 46 49 4i 54 8" St5 87 8s 100 10.5 94 113 1 1 1'
41+
i-I+ 8% lix837 96+ ?,6-
104-i lO5*
27+ 37+ 41c 28+ 36~ 68t 62~ 6% ilf ix+ TO+
I no+ RS+ UXf 1OOf
54+ 51+ 59, 91+ 91+ 85+ Ml+ cl",w-c
41+
I
BONE RES~RPTIOX BY Two METHODS
COXlPARISONOFSCORESFOR BUCCALAA-D I.ISGUAL SURFACES hIETHoDOF ARBITRARY KEYESAXDGOLD*
h (:OJWAIWOX OF THE ESTEST OF QLYEOLAR OF Rrcz RAT JAWS AS DETERMINED
COMPARISOS OF SC'ORES FOR LEFT AEiD RIGHT Qr-ADRAS'TS METHOD OF , KEYES ANDGOLD" ARBlTRARY
TABLE
AREAS
CoMPARISONOFSCORESFOR MAXILLARP ASD S1a SDIBT-LARLESIONS XETHODOF ARBITRARY KEYES ASIJ GOLD" METHOD Jt.~SIl~l,AKY / hIANI1IBI-I~.ZK 39+ 29c 3" 61 5:3+ 25+ 67 ‘49+ 46+ 70 52, 27c 41+ 541 X2+ 'ii+ 73t is iOt XSL S-k+ ix84+ X6+ 847 'To* Sit Xi+ 9% 88+ 1o"t 84~ ')Y+ 83+ 94+ 105+ 86+ 104+
IS VARIOUS
734
OM
P.
GUPTA
AND
JAMES
H.
SHAW
rifice in the reproducibility of the results from one examination to another in the same specimen. However, fine shades of differences between animals were not defined as well by the latter procedure. Evaluation of periodontal disease on the basis of only soft tissue lesions was unquestionably much less satisfactory than either of the two methods for the evaluation of alveolar bone resorption. Among seventeen rice rats, there were four with no evidence of soft tissue involvement, but a readily demonstrable amount of bone loss was observed in each upon the removal of soft tissue. In addition, there was a much lower correlation between either of the alveolar bone resorption scores and the soft tissue scores in the other thirteen animals than the.re was between the two scores based on alveolar bone resorption. Hence, these findings suggested that soft, t,issue lesions did not give an adequate portrayal of the extent of periodontal disease in the rice rat More important still, however, the absence of soft tissue lesions in the presence of alveolar bone resorption suggested the operation of a significant systemic influence that, in the early stages at least, may have caused alveolar bone resorption, primarily, with secondary soft tissue destruction and debris impaction. On the basis of the inability of the soft tissue evalution procedure to detect the earlier stages of periodontal disease, when alveolar bone resorption was present without comparable soft tissue involvement, we consider the soft tissue method to be completely inadequat.e for use as the sole measure of the extent of periodontal disease. For most experiments, either one of the two alveolar bone resorption procedures is unquestionably superior for use alone. For out purposes, we prefer the suggested grading system from 0 to 4+ in terms of the approximate severity of bone loss in fifty-six standard areas, since it was three to four times less time consuming than the method of Keyes and Gold’ without a sufficient sacrifice in accuracy of differentiation between similar animals, However, the latter method did provide somewhat more precise differentiat,ion in those cases where small differences existed between animals or between groups of animals. For some experimental situations where t,he influence of systemic and external factors is being compared, the use of both a soft tissue evaluation procedure and an alveolar bone resorption evaluation on the same heads may be required. Summary Studies of periodontal disease in experimental animals are sufficiently recent that no evaluation system has been accepted as uniquely desirable by the various researchers in the field. Three methods of recording have been used to obtain the data discussed in this article. These are modifications of the three most commonly used methods adapted to the situation encountered in the rice rat. A method based solely on soft tissue lesions was insufficiently exacting to detect stages of alveolar bone resorption t,hat occurred prior to soft tissue destruction. However, this method is of potential value when used parallel to an alveolar bone resorption method to evaluate the possible extent of participation of a systemic influence in the disease process.
PERlODONTAL
DISEASE Ibi RICF. RAT. II
i$
The method for evaluating alveolar bone resorption developed by Keyet and &ld7 is particularly precise, although tedious and time consuming. The evaluation of the amount of alveolar bone resorption on the basis o! an arbitrary grading system from 0 to 4+ appeared to be particularly desirabh with an adequate degree of precision, while at the same time quickly and rcnro ducibly applied. Because of the high degree of bilateral symmetry of the lesions, the evaIua tion of the extent of periodontal disease involvement in the rice rat may ht based satisfactorily on the esaminat,ion of the huccal and lingual aspects o one maxilla and one mandible. We wish to express our appreciation to Marck & Company, Inc., Rahway, New Jersey for the supply of B complex vitamins and to Dr. Victor Schwentker, Tumblebrook Farm Brant Lake, New York, for his willingness to increase his stock colony of rice rats suffinieml: to permit a. variety of experimental studies with these animals.
References 1. Mitchell, D. F.:
The Production of Periodontal Disease in the Hamster as Related to Diet
Coprophagyand Maintenance Factors, J. D. Res. 29: 732, 1950.
2. MiteheR, D. F., and Chernausek, D. S.: Two Studies of Periodontal Disease in the Syria1 Hamster, J. D. l&s. 30: 802, 1951. 3. Rushton, M. A.: The Epithelial Downgrowth on the Molar Roots of Golden Hamst,rrr Brit. D. J. 90: 87, 1951. 4. Johansen,, E. : A System for Recording Oral Conditions and Dental Lesions in t,hc Liva Syrian Hamster, J. D. Res. 32: 578, 1953. 5. Costich, E.: Experimental Studies on Periodontal Disease in the Syrian Hamster: Thl Beneficial Effect of Copper and Fluorine, Thesis, TJniversity of Rorhester, Roehest,er New York, 1954. 6. Shourie, K. L., Driesinger, I?., and Hein, J. IV.: A Method for Taking Dental Rtwnt genographic Records of Live Hamsters, J. D. Res. 27: 746, 1948. 7. Keyes, P. H., and Gold, H. S.: Periodontai Lesions in the Syrian Hamster. I. :\ Metho< of Evaluating Alveolar Bone Resorption, OaAr, SVRG., ORAL MED., AXI 0~~1. p.4~~ 6 492, 1955.
8. Gupta, 0. P., and Shaw, J. H.: Periodontal Disease in the Rice Rat. I. Anatomic i~rlc Histopathologic Findings, ORAL SURG., ORAL MED., AND ORAL PATH. 9: 592, 1956. 9. Shaw, J. H.: Carious Lesions in Cotton Rat Molars. 1. The Role of Mechanical Factor! Studied hy the Extraction of Antagonistic Molars, J. D. Res. 26: 47, 1947.
P.
GIJPTA,
B.D.S., M.S.,
AND
JAMES
H.
SHAW,
PH.~).,
BOSTON,
JVLASS.
UMEROUS procedures have been reported for the evaluation of periodontal N disease in experimental animals. There are conflicting opinions as to whether an adequate appraisal of the extent of periodontal involvement can be made of soft tissue lesions alone, of alveolar bone resorption only, or whether both should be estimated. Mitchell’ has used a method based on evaluation ol’ t,he condition of the gingival tissues and the quantity of subgingival debris in forty designated areas around the molar teeth of hamsters. Scores from 0 t’o 3 were recorded for each area. Mitchell and Chernausek* further modified this procedure by omitting a consideration of the eight inte.rproximal areas and chose to express periodontal damage on the basis of whether or not there were lesions in the remaining thirty-two areas without reference to the size of the lesion. Rushton made histologic preparations from which the amount of downgrowth of the epithelial attachment was measured. The extent of periodont,al damage was estimated from these measurements coupled with the amount, of gingival plaque. Johansen has described a method for estimation of the cxtent of soft tissue involvement in living hamsters. This is essentially a modificat,ion of the procedure described by Mitchell1 and allows for a numerical evaluation of the lateral extent of periodontal pockets as well as the depth of the lesions. Costich5 recorded alveolar bone resorption in terms of a scale from 0 to 3+. However, he felt, that, this was inaderluate and described an alt.ernatr method in which the lesions were drawn on a chart. Tracings of t,he lesions were made on cellulose acetate paper. The areas representing bone resorption wtre cut out and weighed by quadrant or as the total per animal. Shourie, Driesinger, and Hein have proposed a roentgenographic method for use in living hamsters for estimation of the extent of periodontal lesions. Keyes and Oold7 have advocated use of a specially designed, graduated instrument for the measurement of alveolar crest resorption after the soft tissues were removed. From the Harvard School of Dental Medicine. This investigation was supported by a grant-in-aid from the Nutrition Ii’oUndation New York, N. Y.. and by a research grant, D-100, from the National Institute of Kesearch, of the National Institutes of Health, Public Health Service.
727
Inc. hcntai
7%
oM P. GTX’TA AND .JAMER H. ST-lb\%
The purpose of the present study was to develop a reasonably quantitative mctllod l’or the evaluation of 1he scvrritp 0I’ periodontal Icsions in the rice rat, whose susceptibility lo tllcsc Icsiorrs has bWi dosc~ribrd in an c~rlior article.” It was our purpose to ~mparc available methods and arjrivc at a procedure Orat would give an accurate, yet not undu1.v time-consuming, appraisal of the degree of periodontal involvrment with reproducible results in repeated observations of the same specirncns.
Methods Sevent.een rice rats with slight to severe periodontal lesions were selected as representative subjects to be evaluated by three different. procedures. Tl~sc animals had been maintained for twenty-three weeks after weaning on dirts that were slight modifications of purified, high-sucrose, cariogenic ration ‘700.” They had been housed singly in wire-bottom cages, and had been provided with ,4fter sacrifice and fixation of the heads f’or diet and tap water ad libitum. forty-eight, hours or more in 95 per cent alcohol, t,he oral Gssucs were cxaminrtl at, a magnification of X 30. Periodontal lesions were evaluated according to the following ‘three rnethods :
1. Extent of Soft Tissue Involvement.-For
reference purposes, in the evaluation process the tissues surrounding a molar were divided arbitrarily into as many areas as the nurnber of cusps in each tooth. Thus, there were seven areas on the lingual and seven on the buccal aspect of the teeth in each quadrant. of each jaw, a total of fifty-six areas. It was considered that the area adjacent to the mesiobuccal cusp of any molar extended from t,he center of thr rnrsial surface to the first sulcus on the buccal surface. Likewise, the area adjacent to the mesiodistal cusp of any molar extended from the center of t,he distal surface to the adjacent sulcus on the buccal surface. Similar defirritions were employed for the areas adjacent, to the mesial and distal cusps on thcl lingual surface of the molars. In this way, no scores pertained specificall) to the mesial and distal surfaces. The gingival lesions were assigned arbit,rary gradations on the basis of severity-O, l+, 2+, 3+, and &-which could be described as follows: 0 = No detectable abnormalit,irs. I+ = The gingival tissue showed slight changes in color, contour, a’ncl consistency. Usually there was a slight impaction of foreign matter. 2+ = A slight detachment, of the gingiva was commonly observed with moderate impaction of foreign rnattcr and early changes in rolor, contour, and consistency of t,he gingiva. 3~1~= A moderate detachment, and recession of the gingi\q were characteristic. In addition, the gingiva was flabby in consistency and
PERIODONTAL
DISEASE
IX
had lost its normal color and contour. impaction
of debris throughout
RICE
RAT.
7”2!!
II
These Icsions usnaIl>; showed
the cntircl gingival
SUES.
4: = These lesions were associated with severe detachment. of the gingiva with extreme recession. Commonly there were major impactions of foreign material in the spaces between the gingiva and the t,eeth. Teeth with lesions of this size Crrqucntly \v~re mobile and WI)arated by sizeable diastema. Examples of the size and nature of these lesions arc shown in Figs. 1. :L ,5, and T. The degree of involvement of the soft tissues for the cntirr> I!WU~~ was determined by adding the scorrs of thr fifty-six areas.
2. Evaluation
of Bone Resorption by the Method of Keyes and Goldq7-
After the examination and recording of soft, tissue lesions, the soft, tissues were removed. The fifty-six areas adjacent to the cusps were taken as ihe reference points; alveolar bone resorption was mc>asurcd in terms of tho distance that the alveolar bone had reccdcd from the cementoenamel junction. The measurements were made under a hinoeular dissecting microscope with 1hr help of a metal blade graduated at, 0.2 mm. intervals. The blade was hc~ltl against each area and the recession of’ alveolar bonc~ was recorded in trrms 01 the divisions on the blade. The records wore not kept directly in millimeters but in units, each unit being equal to 0.2 mm. The units of’ hone resorpt iott determined for the fifty-six areas we’re totaled as a means of expressing thy degree of periodontal disturbance in the clntire mouth.
3. Evaluation of Alveolar Bone Resorption by Assignment of Arbitrary Values.-In this case, the degree of alveolar resorption for t,hc salnc fifty-sis areas was recorded under arbitrary the following characteristics:
gradations--O,
14, ?A! :I-+; and 1 ~---with
0 = No detectable hone resorption. 11. = These areas had a minor amount of alveolar resorption one-fourth or less of the root exposed.
with
‘Lt = These lesions had an appreciable amount, of alveolar loss with one-fourth to one-halt’ of the root exposed.
horrta
with
3+ = These lesions had a moderately bet,wecn one-half and three-fourths
cxtcnsivc alveolar rrxorptio,t, of the root being visihll>.
4t- = These areas demonstrated the most severe alveolar resorption with essentially no remaining alveolar bone support for the root. Teeth with several areas of this size usually were mobile and separated by
diastema. Examples of the size and nature of these lesions are shown in $‘igs. 2, 4, 6, and 8. The scores for the fifty-six areas of the entire mout,h were totaled as a measure of the severity of periodontal disease. In order to test the reproducibi1it.y of the values obtained by the three methods, the seventeen heads were evaluated three times on different days by each method.
Figs. 1 to 8.-,Photograpbs of flxed preparations of rice rat jaws that were selected “,o,sil;;trate the ,appli~ation of the three procedures used for scormg the extent of periodontal . (Magmflcation, x15: reduced J/e.) The odd-numbered figures are photographs of the lingual aspects of mandibles with the Immediately above each of these figures are seven individual scores soft tissues in situ. as obtained for the seven lingual cuspal areas by the soft tissue evaluation procedure (Soft). The even-numbered figures are photographs of the lingual aspects of the same four mandibles after the soft tissues have been removed to reveal the amount of alveolar bone resorption. Immediately below each of these flgures are two horizontal rows, each of which The scores in the upper row in each case were obtained contains seven individual values. by the method of Keyes and Gold (K. & G.), while the values in the lower row of each pair were obtained by the method of assigning arbitrary values (Arb.) The values shown above for all three methods were the actual ones determined for Minor discrepancies appear to exist when the these jaws under laboratory circumstances. results are recorded adjacent to the appropriate regions of photographs. These discrepancies can be explained by the lack of the third dimension in the photographic reproductions. by differences in the occlusal planes of the molars, and by varying root lengths among the three molars. Figs. 1 and Z.-Lingual views of the left mandibular molars of a rice rat with mild lesions in the periodontal tiSSUSS. Figs. 3 and 4.-Lingual views of the right mandibular molars of a rice rat with a moderate involvement of the periodontal structures.
PERIODONTAL
DISEASE
.gs. Per views of the right Fi igs. 7 and 8.-Lingual ten sive de st ruction of the periodontal structurw
IS KtCE RAT. II
I‘i 1.E
Fi
SeY ‘et-e
nlnnilibular
molar’s of a rice
H
ith
732
OM
I’.
GUPT.4
1ND
JAMES
H.
SHAW
Results and Discussion In Table I are recorded the scores obtained by the three methods for the extent of periodontal disease in these rice rats. In this presentation of data, the individual rice rats have been arranged in increasing order of severity of disease manifestations as scored by the method of Keyes and Gola.’ The data in this table indicate that the standard deviation did not exceed 4 units per head either by Keyes and Gold’s method or by the method of assigning arbitrary values for the amount of alveolar bone resorption. However, the standard deviation of observations for a given animal by the method of soft tissue involvement was as high as _+7 units. TABLE I.
AVERAGE SCORES OF TRIPLICATE MEASUREMENTS OF THE EXTENT OF PERIODONTAL DISEASE IN RICE RATS OBTAINED BY THREE DIFFERENT METHODS I
RAT NO. 93 78 75 82
81 79 94 76
89
ALVEOLARBONERESORPTION METHODOF KEYESANDGOLD ARBITRARY METHOD AVERAGE* S.D.t (UNITS) (UNITS) AVERAGE 1 S.P. t 94 3 68+ 2+ 108 122 125 136 195 203 206 207 221 228 237 242 243 267 269 273
2 2 a 2 3 1 1 1
76+ 95+ 79+ 95+ 159+ 152+ 154t 162t
2c 2+ 1+ 1+ 0 2 2t 3t
170t
lt
154+ 174+ lF(O+ 186+ 183+ 200+
3t 4t 3+ 3+ 3+ 3t
1 190+ *One unit is equal to 0.2 mm. of bone loss. tstandard deviation.
3+
74 83 95 88 97 96 80 73
i 2 2 3 2 2
I SOFTTISSUE DESTRUCTION AVERAGE 1 S.D.t 0 0 0 0 7+ 127+ 96+
0 1+ 4+
1e9+
6t
127+ 123t 132+ 704t 148+ 171+ 152+ 157t 144t
3t 3+ 3t 7t 6+ 2t 2+ 2+ 2+
In this series of rice rats we observed that the scores in both the maxilla and the mandible had a high degree of bilateral symmetry. The extent of this bilaterality, as tested by both alveolar bone resorption methods, is presented in Table II. It was further observed that the scores of the lingual side were higher than the scores of the buccal side and that the mandibular scores were higher than the maxillary scores (Table II). Our findings clearly indicate that the evaluation of periodontal lesions in the rice rat could be limited to one-half of both jaws; however, both the lingual and buccal scores must be taken into consideration. The alveolar bone resorption method described by Keyes and Gold7 appeared to be the most exact method for the evaluation of bone resorption, albeit considerably more tedious and time consuming than t,he other methods. The method of assigning arbitrary values from 0 to 4+ for the extent of alveolar bone resorption was appreciably quicker and less tedious, without demonstrable sae-
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I
BONE RES~RPTIOX BY Two METHODS
COXlPARISONOFSCORESFOR BUCCALAA-D I.ISGUAL SURFACES hIETHoDOF ARBITRARY KEYESAXDGOLD*
h (:OJWAIWOX OF THE ESTEST OF QLYEOLAR OF Rrcz RAT JAWS AS DETERMINED
COMPARISOS OF SC'ORES FOR LEFT AEiD RIGHT Qr-ADRAS'TS METHOD OF , KEYES ANDGOLD" ARBlTRARY
TABLE
AREAS
CoMPARISONOFSCORESFOR MAXILLARP ASD S1a SDIBT-LARLESIONS XETHODOF ARBITRARY KEYES ASIJ GOLD" METHOD Jt.~SIl~l,AKY / hIANI1IBI-I~.ZK 39+ 29c 3" 61 5:3+ 25+ 67 ‘49+ 46+ 70 52, 27c 41+ 541 X2+ 'ii+ 73t is iOt XSL S-k+ ix84+ X6+ 847 'To* Sit Xi+ 9% 88+ 1o"t 84~ ')Y+ 83+ 94+ 105+ 86+ 104+
IS VARIOUS
734
OM
P.
GUPTA
AND
JAMES
H.
SHAW
rifice in the reproducibility of the results from one examination to another in the same specimen. However, fine shades of differences between animals were not defined as well by the latter procedure. Evaluation of periodontal disease on the basis of only soft tissue lesions was unquestionably much less satisfactory than either of the two methods for the evaluation of alveolar bone resorption. Among seventeen rice rats, there were four with no evidence of soft tissue involvement, but a readily demonstrable amount of bone loss was observed in each upon the removal of soft tissue. In addition, there was a much lower correlation between either of the alveolar bone resorption scores and the soft tissue scores in the other thirteen animals than the.re was between the two scores based on alveolar bone resorption. Hence, these findings suggested that soft, t,issue lesions did not give an adequate portrayal of the extent of periodontal disease in the rice rat More important still, however, the absence of soft tissue lesions in the presence of alveolar bone resorption suggested the operation of a significant systemic influence that, in the early stages at least, may have caused alveolar bone resorption, primarily, with secondary soft tissue destruction and debris impaction. On the basis of the inability of the soft tissue evalution procedure to detect the earlier stages of periodontal disease, when alveolar bone resorption was present without comparable soft tissue involvement, we consider the soft tissue method to be completely inadequat.e for use as the sole measure of the extent of periodontal disease. For most experiments, either one of the two alveolar bone resorption procedures is unquestionably superior for use alone. For out purposes, we prefer the suggested grading system from 0 to 4+ in terms of the approximate severity of bone loss in fifty-six standard areas, since it was three to four times less time consuming than the method of Keyes and Gold’ without a sufficient sacrifice in accuracy of differentiation between similar animals, However, the latter method did provide somewhat more precise differentiat,ion in those cases where small differences existed between animals or between groups of animals. For some experimental situations where t,he influence of systemic and external factors is being compared, the use of both a soft tissue evaluation procedure and an alveolar bone resorption evaluation on the same heads may be required. Summary Studies of periodontal disease in experimental animals are sufficiently recent that no evaluation system has been accepted as uniquely desirable by the various researchers in the field. Three methods of recording have been used to obtain the data discussed in this article. These are modifications of the three most commonly used methods adapted to the situation encountered in the rice rat. A method based solely on soft tissue lesions was insufficiently exacting to detect stages of alveolar bone resorption t,hat occurred prior to soft tissue destruction. However, this method is of potential value when used parallel to an alveolar bone resorption method to evaluate the possible extent of participation of a systemic influence in the disease process.
PERlODONTAL
DISEASE Ibi RICF. RAT. II
i$
The method for evaluating alveolar bone resorption developed by Keyet and &ld7 is particularly precise, although tedious and time consuming. The evaluation of the amount of alveolar bone resorption on the basis o! an arbitrary grading system from 0 to 4+ appeared to be particularly desirabh with an adequate degree of precision, while at the same time quickly and rcnro ducibly applied. Because of the high degree of bilateral symmetry of the lesions, the evaIua tion of the extent of periodontal disease involvement in the rice rat may ht based satisfactorily on the esaminat,ion of the huccal and lingual aspects o one maxilla and one mandible. We wish to express our appreciation to Marck & Company, Inc., Rahway, New Jersey for the supply of B complex vitamins and to Dr. Victor Schwentker, Tumblebrook Farm Brant Lake, New York, for his willingness to increase his stock colony of rice rats suffinieml: to permit a. variety of experimental studies with these animals.
References 1. Mitchell, D. F.:
The Production of Periodontal Disease in the Hamster as Related to Diet
Coprophagyand Maintenance Factors, J. D. Res. 29: 732, 1950.
2. MiteheR, D. F., and Chernausek, D. S.: Two Studies of Periodontal Disease in the Syria1 Hamster, J. D. l&s. 30: 802, 1951. 3. Rushton, M. A.: The Epithelial Downgrowth on the Molar Roots of Golden Hamst,rrr Brit. D. J. 90: 87, 1951. 4. Johansen,, E. : A System for Recording Oral Conditions and Dental Lesions in t,hc Liva Syrian Hamster, J. D. Res. 32: 578, 1953. 5. Costich, E.: Experimental Studies on Periodontal Disease in the Syrian Hamster: Thl Beneficial Effect of Copper and Fluorine, Thesis, TJniversity of Rorhester, Roehest,er New York, 1954. 6. Shourie, K. L., Driesinger, I?., and Hein, J. IV.: A Method for Taking Dental Rtwnt genographic Records of Live Hamsters, J. D. Res. 27: 746, 1948. 7. Keyes, P. H., and Gold, H. S.: Periodontai Lesions in the Syrian Hamster. I. :\ Metho< of Evaluating Alveolar Bone Resorption, OaAr, SVRG., ORAL MED., AXI 0~~1. p.4~~ 6 492, 1955.
8. Gupta, 0. P., and Shaw, J. H.: Periodontal Disease in the Rice Rat. I. Anatomic i~rlc Histopathologic Findings, ORAL SURG., ORAL MED., AND ORAL PATH. 9: 592, 1956. 9. Shaw, J. H.: Carious Lesions in Cotton Rat Molars. 1. The Role of Mechanical Factor! Studied hy the Extraction of Antagonistic Molars, J. D. Res. 26: 47, 1947.