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Experimental Dental Granulomas in Dogs*
E X P E R IM E N T A L
DENTAL
GRANULOM AS
IN
D OG S*
By THOMAS J. HILL, D.D.S., Cleveland, Ohio
H E experiments here detailed were conducted, first, to observe whether dental granulomas produced experi mentally in dogs were comparable to hu
T
m an dental granulom as; and, secondly, to compare the development of granulomas when the root canals have been infected w ith th at of granulomas adjacent to ster-
Fig. 1.— Appearance of section tw elve days after rem oval of pulp and infection of canal with streptococci. *From the Institute of Pathology, W estern Reserve University. *W ork aided by a grant from the Callahan M emorial A w ard Commission. *Read before the Section on Research and Biologic Sciences at the M idwinter Clinic of the Chicago Dental Society, Jan. 19, 1932.
Jour. A. D .A .,A u g u st, 1932
ile pulpless, unfilled roots. I t is evident th at the recovery of bacteria from mature granulomas does not prove their etiologic relationship because bacteria may be pres ent as the result of secondary invasion of necrotic tissue.
1389
1390
T h e Jou rn a l of th e A m erica n D e n t a l A ssociation
G ottlieb, S ch w arz and Stein1 and B oulger2 have studied the tissue reaction w hich occurs w hen root tips have been im planted in the muscles of rats. T hese w orkers have dem onstrated quite clearly th a t the tissue reaction in the presence of infected roots is different from the reac tion in the presence of im planted, un in fected teeth. T h ese conditions are not
reactions have a certain sim ilarity, it can not be assum ed th a t th e reaction of m us cle to the presence of a foreign body w ould be the same as the reaction of the periden ta l tissues if the same teeth w ere in the norm al position, i.e., in th e ir alveolar sockets. In th e im p lan tatio n of root tips in anim als, th ere is necessarily a loss of the p erid en tal m em brane and its attend-
Fig. 2.— Section of tooth twelve days after sterile pulp removal.
sim ilar to those present w hen the same teeth are in situ. W h ile , in a general way, it m ay be said th a t all inflam m atory tissue 1. Gottlieb, B ernh ard ; Schwarz, A. M., and Stein, G eorges: Das Problem der W urzelbe handlung, Ztschr. f. Stomatol, 26:1151, 1928. 2. Boulger, E. P .: Reaction of Rat Tissue to Im planted Root Ends, J.A.D.A., 18:988 (June) 1931.
ing stru ctu res. A tte n tio n has been called to the im portance of epithelial rests in the p eriden tal m em brane and th eir p a rt in the form ation of cysts. In th is respect, cystic areas th a t develop w hen root tips are im planted in the muscles of rats are not identical w ith the cystic areas th a t devel op at the apex of teeth in the alveolar bone.
H i l l — D e n t a l G ra nu lom as in D o g s
T h e conditions present in the develop m ent of dental granulom as in dogs ap proxim ate, b u t are n o t exactly like, the conditions present in hum an dental g ra n ulomas. T h e num ber of foram ina in dogs’ teeth is greater and the b ranch ing of canals occurs higher in the pulp cham ber th an in the average hum an tooth. T h ese anatom ic features m ay account for the fact th a t dental granulom as are pro
1391
pulps had been rem oved frequently showed fragm ents of th e odontoblasts adhering to the d en tin al w all. T h e second or th ird incisor teeth, upper and low er, w ere used. T h e pulps w ere re moved from the teeth and the dogs w ere killed on a schedule th a t w o u ld allow the study, in chronologic order, of these teeth from th e prim ary in ju ry to the m ature granulom as.
Fig. 3.— Section of tooth four weeks after sterile pulp removal.
duced m ore quickly and m ore easily in dogs th an in hum an beings. T h e w ork here reported w as conducted on forty-eight teeth in the m ouths of dogs. T h e cuspid teeth w ere n o t used because th eir length prevented proper rem oval of pulps w ith stan d ard root canal in stru m ents. A few cuspid teeth from w hich
T h e anesthetics w ere eth er o r m orphin and scopolam in. W h e n m orphin and scopolam in w ere employed, the dosage sug gested by N oyes3 w as used and a very satisfactory anesthetic w as produced. 3. Noyes, F. B., and Ladd, R. L .: Lymphatics of Dental Region, D. Cosmos, 71:1041 (Nov.) 1929.
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T h e Journal of the American D ental Association
A ll teeth were operated on under as strictly aseptic conditions as it was pos sible to obtain. In one series, the pulps were removed and the root canals were left unfilled, but the coronal ends were hermetically sealed w ith cement and amal gam. In another series, the pulps were removed and dressings consisting of ster ilized paper points infected w ith pure cultures of streptococci were inserted.
strain was a larger chain, nonhemolytic streptococcus. A ll teeth treated, either by infection of the root canal or by sterile removal of the pulp, developed granulomas if allowed to remain for a sufficient length of time. T h e teeth which were infected showed inflam m atory reaction and degenerative changes in the many fine branching canals w ithin a few days, and similar conditions ap
Fig. 4.— Osteoclastic activity in the formation of a dental granuloma.
These teeth were also sealed at the crowns with cement and amalgam. T w o strains of streptococci isolated from tw o granulomas removed from a hospitalized tuberculous patient were used. O ne strain was a small, short chain, Streptococcus hemolyticus; the other
peared in the periapical tissue soon after. Figure 1 is a photomicrograph of a tooth twelve days after removal of the pulp and infection of the canal w ith streptococci. I t shows one canal in which the tissue is vital and a second canal containing nec rotic material. T here is a polymorphonu
H ill— D ental Granulomas in Dogs
1393
clear and lym phocytic reaction around the apex. In teeth w hich w ere not infected, th e tissue w ith in the fine apical canals rem ained vital for a longer tim e. F ig ure 2 illustrates a sterile pulpless tooth tw elve days a fte r pulp rem oval. T h e tissues w ith in the m ore m inute
photom icrograph of a to o th fo u r weeks a fte r sterile pulp rem oval. T h e periden ta l m em brane is n ot detached from the root. T h is loose periapical stru ctu re g ra d ually becomes filled w ith lymphocytes, plasm a cells and connective tissue, which, in some areas, is very dense. A ccom pany
branches of the pulp canal are still vital. A fte r a period of quiescence, the periapi cal tissues of noninfected teeth show an extensive edem a involving the regions beyond the apex and an infiltratio n of a few scattered lymphocytes. F igure 3 is a
ing this condition is a m arked osteoclastic activity as illu strate d in F ig u re 4, w hich shows the rapid absorption of bone and the form ation of dense connective tissue adjacent to an area of edema. Connective tissue an d inflam m atory
1394
T h e Journal of the American D ental Association
Fig. 7.— Section of tooth four weeks after removal of pulp and infection of canal.
H ill— D ental Granulomas in Dogs cells gradually fill all edem atous areas. F ig u re 5 is a pulpless tooth five weeks a fte r sterile pulp rem oval. T h e re is in addition to the inflam m atory reaction an absorption of the root surface. T h is con dition is com mon on the roots of dogs’ teeth w ith granulom as. In advanced, m a tu re granulom as, large areas of the root become absorbed as is show n in F igure 6.
1395
thelial p ro liferatio n is com mon in g ra n ulom a of dogs, it does n ot appear to be constant in g ranulom as less th a n 3 m onths old. A reas of epithelial p ro liferatio n are sim ilar in th eir m orphologic aspects to hum an granulom as. S tran d s and islands are form ed as illu strated in F ig u re 8. F igure 9 shows a large epithelial island w ith necrotic center in a g ran u lo m a three
m stm
Fig. 8.—Epithelial proliferation in dental granuloma of dog.
F ig u re 7 illustrates the apex of a pulpless tooth four weeks afte r rem oval of the pulp and infection of the canal. T h is shows inflam m atory reaction w hich con sists of polym orphonuclear as w ell as plasm a cell and lym phocytic in filtration. E pithelial proliferation appears in the form ation of granulom as from four to six weeks afte r pulp rem oval. W h ile epi-
m onths afte r rem oval of th e pulp and in fection of the canal. B acteria are easily dem onstrable in all granulom as a fte r areas of necrosis have appeared. T h e teeth th a t w ere infected w ith streptococci and allow ed to remain for three m onths all gave positive cultures in dextrose-brain broth, and w h at ap peared to be the same organism used to
1396
T h e Journal of the American D ental Association
inoculate the tooth w as recovered, b u t never in pure culture. T w o incidental observations w ere m ade. O n e granulom a contained c a rti lage in its o u te r border, w hich w as the resu lt of connective tissue m etaplasia. (F ig . 10.) A bsorption of cem entum and dentin w ith rebuilding of new cem entum is frequently found on the sides of dogs’
stru ctu re of dogs’ teeth and th a t of hum an teeth shows a g reater b ranching of pulp canals in the form er. Because of this con dition and the atten d in g difficulties of com plete rem oval of organic m aterial, the production of dental granulom as m ay be m ore readily induced. In th eir m orphologic and histologic as pects, experim ental granulom as in dogs
Fig. 9.—Formation of cystic area w ithin proliferated epithelium.
teeth, even w hen these teeth w ere not u n d er treatm en t. F ig u re 11 is a photo m icrograph of a tooth adjacent to one u n d er treatm en t. SU M M A RY
A com parison betw een the anatom ic
are com parable to h um an granulom as. G ranulo m as may be produced on u n in fected roots. T h e type of reaction a t tending such granulom as suggests th a t the irrita tin g facto r is not caused by infec tion w hich has been introduced by w ay of
H ill— D ental Granulomas in Dogs
Fig. 11.—Absorption of cementum and dentin and form ation of new cementum.
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T h e Journal of the American D ental Association
the root canal, but may result from the accumulation of serous exudate in any open root canal. I t is possible that the serous exudate w ithin the pulp canal may become altered by its own enzymes or by some other agents which act as an irri tan t to the periapical tissues. A ll granu lomas produced on both infected and sterile teeth can be demonstrated to con
tain bacteria after necrosis has occurred. Histologic demonstration of bacteria could not be made in tissue surrounding the roots of uninfected teeth until after the appearance of necrosis. It would ap pear that, in many instances, the bacteria in dental granulomas are the result of secondary invasion.
CARIES: A RESUM E OF O U R KNOW LEDGE OF ITS A C T IO N , TO G ETH ER W IT H SOME OF T H E M ORE R E C EN T RESEARCH W ORK* By EDWARD H. H ATTON, B.L., M.D., Chicago, 111.
O state that recent research work has added nothing of importance to our knowledge of the action of dental caries may be radical. If one studies care fully the investigations and conclusions of M iller, Black and W illiams, no other deduction is possible. I t is also quite clear that, w ith perhaps only one exception, the present generation of investigators is either w ilfully or innocently ignorant of w hat seem to be crucial observations of the older school of workers in this field. T he latter were not only able to pro duce typical caries in extracted teeth in the test tube, but were also cognizant of the fact th at extracted teeth replaced in the m outh in prosthetic restorations were affected w ith caries in exactly the same way as teeth w ith vital pulps and em bedded in normal tooth sockets. They knew that caries occurred equally fre quently in both vital and pulpless teeth and that the same laws controlled the in cidence and distribution of caries in both of these groups of teeth, w ithout any'note-
T
w orthy difference. T hey were reasonably fam iliar with the fact that certain primi tive races such as the South Sea Islander, South African and Eskimo were remark ably resistant to dental decay. T hey and their contemporaries were just as sus picious of the modern diet and made just as radical statements as our contem poraries about the refinement and sophis tication of food. “ But when to please public taste the m anufacturer of super fine flour robs the w heat grain of fourfifths of this phosphate he is destroying the teeth of his customers.”1 “T h e introduction of bolts into flour ing mills may be regarded as a calam ity .”2 M iller, Black and W illiam s never wavered from the conviction that caries was caused by the acid produced by bac teria and confined to the tooth surfaces which were affected with caries. T he question which they asked then and which they could not answer still defies solution; namely, by what power is
*Read before the Section on Operative Den tistry at the M idw inter Clinic of the Chicago Dental Society, Jan. 20, 1932.
1. Chase, H enry S.: Missouri D. J., 1:115, 1869. 2. Wilson, I. P .: Missouri D. J., 1 :233, 1869.
Jour. A. D. A ., August, 1932
DENTAL
GRANULOM AS
IN
D OG S*
By THOMAS J. HILL, D.D.S., Cleveland, Ohio
H E experiments here detailed were conducted, first, to observe whether dental granulomas produced experi mentally in dogs were comparable to hu
T
m an dental granulom as; and, secondly, to compare the development of granulomas when the root canals have been infected w ith th at of granulomas adjacent to ster-
Fig. 1.— Appearance of section tw elve days after rem oval of pulp and infection of canal with streptococci. *From the Institute of Pathology, W estern Reserve University. *W ork aided by a grant from the Callahan M emorial A w ard Commission. *Read before the Section on Research and Biologic Sciences at the M idwinter Clinic of the Chicago Dental Society, Jan. 19, 1932.
Jour. A. D .A .,A u g u st, 1932
ile pulpless, unfilled roots. I t is evident th at the recovery of bacteria from mature granulomas does not prove their etiologic relationship because bacteria may be pres ent as the result of secondary invasion of necrotic tissue.
1389
1390
T h e Jou rn a l of th e A m erica n D e n t a l A ssociation
G ottlieb, S ch w arz and Stein1 and B oulger2 have studied the tissue reaction w hich occurs w hen root tips have been im planted in the muscles of rats. T hese w orkers have dem onstrated quite clearly th a t the tissue reaction in the presence of infected roots is different from the reac tion in the presence of im planted, un in fected teeth. T h ese conditions are not
reactions have a certain sim ilarity, it can not be assum ed th a t th e reaction of m us cle to the presence of a foreign body w ould be the same as the reaction of the periden ta l tissues if the same teeth w ere in the norm al position, i.e., in th e ir alveolar sockets. In th e im p lan tatio n of root tips in anim als, th ere is necessarily a loss of the p erid en tal m em brane and its attend-
Fig. 2.— Section of tooth twelve days after sterile pulp removal.
sim ilar to those present w hen the same teeth are in situ. W h ile , in a general way, it m ay be said th a t all inflam m atory tissue 1. Gottlieb, B ernh ard ; Schwarz, A. M., and Stein, G eorges: Das Problem der W urzelbe handlung, Ztschr. f. Stomatol, 26:1151, 1928. 2. Boulger, E. P .: Reaction of Rat Tissue to Im planted Root Ends, J.A.D.A., 18:988 (June) 1931.
ing stru ctu res. A tte n tio n has been called to the im portance of epithelial rests in the p eriden tal m em brane and th eir p a rt in the form ation of cysts. In th is respect, cystic areas th a t develop w hen root tips are im planted in the muscles of rats are not identical w ith the cystic areas th a t devel op at the apex of teeth in the alveolar bone.
H i l l — D e n t a l G ra nu lom as in D o g s
T h e conditions present in the develop m ent of dental granulom as in dogs ap proxim ate, b u t are n o t exactly like, the conditions present in hum an dental g ra n ulomas. T h e num ber of foram ina in dogs’ teeth is greater and the b ranch ing of canals occurs higher in the pulp cham ber th an in the average hum an tooth. T h ese anatom ic features m ay account for the fact th a t dental granulom as are pro
1391
pulps had been rem oved frequently showed fragm ents of th e odontoblasts adhering to the d en tin al w all. T h e second or th ird incisor teeth, upper and low er, w ere used. T h e pulps w ere re moved from the teeth and the dogs w ere killed on a schedule th a t w o u ld allow the study, in chronologic order, of these teeth from th e prim ary in ju ry to the m ature granulom as.
Fig. 3.— Section of tooth four weeks after sterile pulp removal.
duced m ore quickly and m ore easily in dogs th an in hum an beings. T h e w ork here reported w as conducted on forty-eight teeth in the m ouths of dogs. T h e cuspid teeth w ere n o t used because th eir length prevented proper rem oval of pulps w ith stan d ard root canal in stru m ents. A few cuspid teeth from w hich
T h e anesthetics w ere eth er o r m orphin and scopolam in. W h e n m orphin and scopolam in w ere employed, the dosage sug gested by N oyes3 w as used and a very satisfactory anesthetic w as produced. 3. Noyes, F. B., and Ladd, R. L .: Lymphatics of Dental Region, D. Cosmos, 71:1041 (Nov.) 1929.
1392
T h e Journal of the American D ental Association
A ll teeth were operated on under as strictly aseptic conditions as it was pos sible to obtain. In one series, the pulps were removed and the root canals were left unfilled, but the coronal ends were hermetically sealed w ith cement and amal gam. In another series, the pulps were removed and dressings consisting of ster ilized paper points infected w ith pure cultures of streptococci were inserted.
strain was a larger chain, nonhemolytic streptococcus. A ll teeth treated, either by infection of the root canal or by sterile removal of the pulp, developed granulomas if allowed to remain for a sufficient length of time. T h e teeth which were infected showed inflam m atory reaction and degenerative changes in the many fine branching canals w ithin a few days, and similar conditions ap
Fig. 4.— Osteoclastic activity in the formation of a dental granuloma.
These teeth were also sealed at the crowns with cement and amalgam. T w o strains of streptococci isolated from tw o granulomas removed from a hospitalized tuberculous patient were used. O ne strain was a small, short chain, Streptococcus hemolyticus; the other
peared in the periapical tissue soon after. Figure 1 is a photomicrograph of a tooth twelve days after removal of the pulp and infection of the canal w ith streptococci. I t shows one canal in which the tissue is vital and a second canal containing nec rotic material. T here is a polymorphonu
H ill— D ental Granulomas in Dogs
1393
clear and lym phocytic reaction around the apex. In teeth w hich w ere not infected, th e tissue w ith in the fine apical canals rem ained vital for a longer tim e. F ig ure 2 illustrates a sterile pulpless tooth tw elve days a fte r pulp rem oval. T h e tissues w ith in the m ore m inute
photom icrograph of a to o th fo u r weeks a fte r sterile pulp rem oval. T h e periden ta l m em brane is n ot detached from the root. T h is loose periapical stru ctu re g ra d ually becomes filled w ith lymphocytes, plasm a cells and connective tissue, which, in some areas, is very dense. A ccom pany
branches of the pulp canal are still vital. A fte r a period of quiescence, the periapi cal tissues of noninfected teeth show an extensive edem a involving the regions beyond the apex and an infiltratio n of a few scattered lymphocytes. F igure 3 is a
ing this condition is a m arked osteoclastic activity as illu strate d in F ig u re 4, w hich shows the rapid absorption of bone and the form ation of dense connective tissue adjacent to an area of edema. Connective tissue an d inflam m atory
1394
T h e Journal of the American D ental Association
Fig. 7.— Section of tooth four weeks after removal of pulp and infection of canal.
H ill— D ental Granulomas in Dogs cells gradually fill all edem atous areas. F ig u re 5 is a pulpless tooth five weeks a fte r sterile pulp rem oval. T h e re is in addition to the inflam m atory reaction an absorption of the root surface. T h is con dition is com mon on the roots of dogs’ teeth w ith granulom as. In advanced, m a tu re granulom as, large areas of the root become absorbed as is show n in F igure 6.
1395
thelial p ro liferatio n is com mon in g ra n ulom a of dogs, it does n ot appear to be constant in g ranulom as less th a n 3 m onths old. A reas of epithelial p ro liferatio n are sim ilar in th eir m orphologic aspects to hum an granulom as. S tran d s and islands are form ed as illu strated in F ig u re 8. F igure 9 shows a large epithelial island w ith necrotic center in a g ran u lo m a three
m stm
Fig. 8.—Epithelial proliferation in dental granuloma of dog.
F ig u re 7 illustrates the apex of a pulpless tooth four weeks afte r rem oval of the pulp and infection of the canal. T h is shows inflam m atory reaction w hich con sists of polym orphonuclear as w ell as plasm a cell and lym phocytic in filtration. E pithelial proliferation appears in the form ation of granulom as from four to six weeks afte r pulp rem oval. W h ile epi-
m onths afte r rem oval of th e pulp and in fection of the canal. B acteria are easily dem onstrable in all granulom as a fte r areas of necrosis have appeared. T h e teeth th a t w ere infected w ith streptococci and allow ed to remain for three m onths all gave positive cultures in dextrose-brain broth, and w h at ap peared to be the same organism used to
1396
T h e Journal of the American D ental Association
inoculate the tooth w as recovered, b u t never in pure culture. T w o incidental observations w ere m ade. O n e granulom a contained c a rti lage in its o u te r border, w hich w as the resu lt of connective tissue m etaplasia. (F ig . 10.) A bsorption of cem entum and dentin w ith rebuilding of new cem entum is frequently found on the sides of dogs’
stru ctu re of dogs’ teeth and th a t of hum an teeth shows a g reater b ranching of pulp canals in the form er. Because of this con dition and the atten d in g difficulties of com plete rem oval of organic m aterial, the production of dental granulom as m ay be m ore readily induced. In th eir m orphologic and histologic as pects, experim ental granulom as in dogs
Fig. 9.—Formation of cystic area w ithin proliferated epithelium.
teeth, even w hen these teeth w ere not u n d er treatm en t. F ig u re 11 is a photo m icrograph of a tooth adjacent to one u n d er treatm en t. SU M M A RY
A com parison betw een the anatom ic
are com parable to h um an granulom as. G ranulo m as may be produced on u n in fected roots. T h e type of reaction a t tending such granulom as suggests th a t the irrita tin g facto r is not caused by infec tion w hich has been introduced by w ay of
H ill— D ental Granulomas in Dogs
Fig. 11.—Absorption of cementum and dentin and form ation of new cementum.
1397
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T h e Journal of the American D ental Association
the root canal, but may result from the accumulation of serous exudate in any open root canal. I t is possible that the serous exudate w ithin the pulp canal may become altered by its own enzymes or by some other agents which act as an irri tan t to the periapical tissues. A ll granu lomas produced on both infected and sterile teeth can be demonstrated to con
tain bacteria after necrosis has occurred. Histologic demonstration of bacteria could not be made in tissue surrounding the roots of uninfected teeth until after the appearance of necrosis. It would ap pear that, in many instances, the bacteria in dental granulomas are the result of secondary invasion.
CARIES: A RESUM E OF O U R KNOW LEDGE OF ITS A C T IO N , TO G ETH ER W IT H SOME OF T H E M ORE R E C EN T RESEARCH W ORK* By EDWARD H. H ATTON, B.L., M.D., Chicago, 111.
O state that recent research work has added nothing of importance to our knowledge of the action of dental caries may be radical. If one studies care fully the investigations and conclusions of M iller, Black and W illiams, no other deduction is possible. I t is also quite clear that, w ith perhaps only one exception, the present generation of investigators is either w ilfully or innocently ignorant of w hat seem to be crucial observations of the older school of workers in this field. T he latter were not only able to pro duce typical caries in extracted teeth in the test tube, but were also cognizant of the fact th at extracted teeth replaced in the m outh in prosthetic restorations were affected w ith caries in exactly the same way as teeth w ith vital pulps and em bedded in normal tooth sockets. They knew that caries occurred equally fre quently in both vital and pulpless teeth and that the same laws controlled the in cidence and distribution of caries in both of these groups of teeth, w ithout any'note-
T
w orthy difference. T hey were reasonably fam iliar with the fact that certain primi tive races such as the South Sea Islander, South African and Eskimo were remark ably resistant to dental decay. T hey and their contemporaries were just as sus picious of the modern diet and made just as radical statements as our contem poraries about the refinement and sophis tication of food. “ But when to please public taste the m anufacturer of super fine flour robs the w heat grain of fourfifths of this phosphate he is destroying the teeth of his customers.”1 “T h e introduction of bolts into flour ing mills may be regarded as a calam ity .”2 M iller, Black and W illiam s never wavered from the conviction that caries was caused by the acid produced by bac teria and confined to the tooth surfaces which were affected with caries. T he question which they asked then and which they could not answer still defies solution; namely, by what power is
*Read before the Section on Operative Den tistry at the M idw inter Clinic of the Chicago Dental Society, Jan. 20, 1932.
1. Chase, H enry S.: Missouri D. J., 1:115, 1869. 2. Wilson, I. P .: Missouri D. J., 1 :233, 1869.
Jour. A. D. A ., August, 1932