Iatrogenic pulpat reactions to orthodontic extrusion Yehya A. Mostafa, BDS, MS, PhD,* Kameel G. Iskander, BDS, HDD, PhD,** and Nagwa Helmy EI-Mangoury, BDS, MS, PhD* Cairo, Egypt A careful review of the literature reveals an absence of studies about the reactions of dental pulp to orthodontic extrusion. The purpose of the present research investigation is to study the pulpal reactions and the sequence of histotogic events in human dental pulp after orthodontic extrusion. The sample consisted of 36 intact maxillary first premolars of young adult orthodontic subjects. The mean age of the subjects was 18 years. Eighteen maxillary first premolars were extruded, under controlled conditions with the aid of fixed edgewise orthodontic appliances, for either 1, 2, or 4 weeks. The contralateral maxillary first premolars were not extruded and were used as controls. Immediately after removal of the appliances, all the maxillary first premolars were extracted. The pulps were histologically examined in a double-blind experiment. The results obtained from this study indicate that certain characteristic pulpal reactions arise from orthodontic extrusion. These reactions involve circulatory disturbances with congested and dilated blood vessels, odontoblastic degeneration, vacuolization and edema of the pulp tissues, and (by the fourth week) manifestation of fibrotic changes. It is speculated that the vacuolization of the pulp tissues (which occurred after the application of extrusive orthodontic forces in young adult subjects) resulted from a prolapse of the pulp, made possible by the relatively wide apical foramina. However, the odontoblastic degeneration is most probably the result of a compromised blood supply. The authors believe that this study constitutes a building block for establishing a more complete biologic foundation for orthodontic tooth movement. Further studies are suggested to reach more definitive conclusions. (AM J ORTHOD DENTOFACORTHOP1991 ;99:30-4.)
A r c h i m e d e s , the Greek mathematician and inventor, stated: "Give me a firm place to stand, and I will move the earth." To paraphrase Archimedes, the contemporary orthodontist would say "Give me a firm biologic basis, and I will move the teeth." The effects of orthodontic forces on the oral tissues were examined by many investigators.t't8 The majority of these investigators t9"12'tT"t8were concerned with the reactions of the alveolar bone and periodontal ligament. Some researchers ~°'t''t3"~6 studied the pulp responses to orthodontic forces, particularly the intrusive type. No previous studies have been published on the reactions of the dental pulp to orthodontic extrusion. The purpose of the present research is to study histologically the iatrogenic pulpal reactions during orthodontic extrusion of human teeth.
MATERIALS AND METHODS A random sample of 1S adult orthodontic subjects was studied. All the subjects had intact (i.e., noncarious
*Associate Professors, Department of Orthodontics, Cairo University Faculty of Dentistry. **Professor, Department of Oral Pathology, Cairo University Faculty of Den-
tist~. 811118226
30
and nonrestored) maxillary right and left first premolars that had been recommended for extraction for orthodontic reasons. The mean age of the subjects was 18 years, with a range of 16 to 21 years. After written consents were obtained, a maxillary first premolar was extruded for each subject while its contralateral, which was not extruded, served as a control. The extrusion was done through the use of a fixed edgewise orthodontic appliance with an activated spring attached (Fig. I). The amount of activation was similar for all the subjects. The force of the activated spring was measured with a Correx stress and tension gauge on the first day, first week, second week, and fourth week after activation. Further, the subjects were fitted with maxillary bite plates. The subjects were divided randomly into three equal groups. Bilateral extractions of both right and left maxillary first premolars were done 1 week after activation for the first group, 2 weeks after activation for the second group, and 4 weeks after activation for the third group. In all, 36 teeth were histologically examined through a double-blind experiment) 9 Immediately after removal, the teeth were fixed in a neutral buffered formalin solution for 48 hours. They were decalcified in a 5.2% solution of formic acid and embedded in par-
Voh~me 99 Number 1
Pulpal reactions to extrusion
31
Fig. 1. Orthodontic appliance used. The spring was attached to a maxillary first molar and activated against a maxillary first premolar.
Fig. 2. Normal pulp tissues in a control specimen. (Magnification, x 200.)
affin. Serial sections 5 I-tm thick were cut longitudinally and stained with hematoxylin and eosin dye. RESULTS
The mean force of the activated spring was 57 gm for the first day, 54 gm for the first week, 52 gm for the second week, and 48 gm for the fourth week. Fig. 2 displays the appearance of normal pulp tissues. Figs. 3 through 5 show the coronal pulp of extruded teeth 1 week after activation, 2 weeks after activation, and 4 weeks after activation. At 1 week after activation,
marked vacuolization of the pulp tissues, congested blood vessels, and severe odontoblastic degeneration occurred (Fig. 3). Further, 2 weeks after activation, congested blood vessels, large vacuoles, and degeneration of the odontoblasts were obvious in the pulp tissues (Fig. 4). However, 4 weeks after activation, pulp fibrosis had appeared (Fig. 5). DISCUSSION
Researchers 2"9"t4'2°23 have shown that pulpal reactions differ according to the age of the subject and the
32 Mostafa, lskander, and EI-Mangouty
Am. J. Orthod. Dentofac. Orthop. January 1991
Fig. 3. Coronal pulp of an extruded tooth at 1 week after activation. A and B, Note the marked vacuolizationand degenerationof the odontoblastic layer and congested blood vessels. (Magnifications: A, x 100; B, x200.) C, Note severe odontob/astic degeneration and pulp vacuoIization. Dilated and congested blood vessels are also seen. (Magnification, x300.)
size of the apical foramen. To avoid any possible age effects, t4 the selected subjects were chosen from the same age bracket. Consequently, it was expected that the apical foramina were of nearly the same size. The appliances were carefully designed to deliver the same amount of force in all cases. To eliminate any possible traumatic occlusion during extrusion, maxillary bite plates were inserted. A double-blind experimental research design ~9was created to avoid false significant results. We attempted to study the sequence of histologic events occurring in the pulp after orthodontic extrusion of the maxillary first premolars in human beings. The purpose was to develop criteria for establishing a more complete biologic foundation for orthodontic tooth movement. A comparison between the extruded and nonextruded maxillary first premolars revealed characteristic pulpal reactions resulting from the orthodontic extrusion (Figs. 2 through 5). One of the earliest degenerative changes was the presence of vacuoles in the pulp tissues as well as in the odontoblastic layer (Figs. 3 and 4). This finding agrees with that of Anstendig and
Kronman." Further, the odontoblastic vacuolization was more pronounced coronally than apically. A similar histologic picture of odontoblastic vacuolization was reported to result from tooth intrusion. 2426 Circulatory disturbances were manifested as dilated and congested blood vessels (Figs. 3 and 4). The odontoblastic degeneration was most probably due to the compromised blood supply. It is known that the first premolars erupt when a child is 10 to 12 years of age. The roots are completely formed at 13 to 15 years of age. The subjects in the present sample were nearly 18 years old. At this age, the apical foramina are relatively wide. The extrustive forces, applied to the maxillary first premolars, seem to cause a topographic change in the pulp, or prolapse, made possible by the relatively large apical foramina. This prolapse may be responsible for the rupture or vacuolization appearing in the pulp tissues. This conclusion must be viewed as speculative, so further studies are suggested. Hamersky, Weimer, and Taintor 1' studied pulp respiration resulting from orthodontic forces. They reported a depression in the respiratory rate, which they
Voh~me 9 9 Number 1
P u l p a l reactions to extrusion
~,.
'.~.-
~,'~
.
-h"t
:
,"
33
~
.
Fig. 4. Coronal pulp of an extruded tooth at 2 weeks after activation. A and B, Observe the large vacuole (surrounded by odontoblasts). Vacuolization of the pulp tissues is obvious. (Magnification, x 200.) C, Higher magnification showing vacuolization of the pulp tissues, dilated and congested blood vessels, and degeneration of the odontoblasts. (Magnification, x 400.)
Fig. 5. Coronal pulp of an extruded tooth at 4 weeks after activation. Note that the pulp tissues show fibrosis (fibrous tissue reaction) and that the degree of vacuolization and blood congestion has decreased. (Magnification, x200.)
attributed to circulatory disturbances. One may raise the following question: What is the ultimate fate of these circulatory disturbances? The duration of these pathologic changes is controversial. Oppenheim 3 and Butcher and Taylora°'2~ obtained contradictory results, varying from temporary reversible degeneration to permanent irreversible de-
generation and ultimate necrosis of the dental pulp after orthodontic treatment. Fibrotic changes appeared 4 weeks after activation (Fig. 5). Stenvik and Mj6r '° were able to show signs of healing and scar tissue formation in a long-term intrusive study. It is known that the reparative properties of the pulp are extensive. However, the limit of toler-
34
Mostafa, Iskander, and EI.Mangoury
ance varies from person to person. The ultimate fate of these circulatory disturbances seems to be resolution through reparative processes. Additional studies are recommended for more definitive conclusions. SUMMARY AND CONCLUSIONS A r a n d o m sample o f 18 adult orthodontic subjects was studied. All the subjects had intact m a x i l l a r y right and left first premolars that had b e e n r e c o m m e n d e d for extraction for orthodontic reasons. T h e m e a n age o f the subjects was 18 years. E i g h t e e n m a x i l l a r y first premolars w e r e extruded for either 1, 2, or 4 w e e k s . T h e contralateral m a x i l l a r y first premolars s e r v e d as controis. T h e dental pulp was e x a m i n e d in a double-blind experiment. O n the basis o f the results obtained f r o m this research study, the f o l l o w i n g conclusions w e r e drawn: 1. Orthodontic extrusion causes certain characteristic reactions o f dental pulp, including odontoblastic d e g e n e r a t i o n , circulatory disturbances with congested b l o o d vessels, v a c u o l i z a t i o n and e d e m a o f the pulp tissues, and (by the 4th week) appearance o f fibrotic changes. 2. T h e odontoblastic d e g e n e r a t i o n is m o s t p r o b a b l y due to a c o m p r o m i s e d b l o o d supply. 3. T h e v a c u o l i z a t i o n o f the pulp tissues is b e l i e v e d to result f r o m a topographic c h a n g e , o r prolapse, o f the pulp, through the relatively w i d e apical foramina.
REFERENCES 1. Marshall JA. A study of bone and tooth changes incident to experimental tooth movement and its application to orthodontic practice. IN'r J OR'roOD 1933;19:1-17. 2. Orban B. Biologic problems in orthodontia. J Am Dent Assoc 1936;23:1849-79. 3. Oppenheim A. Biologic orthodontic therapy and reality. Angle Orthod 1936;6:5-38,69-116,153-83; 1937;7:58-9. 4. Stuteville OH. A summary review of tissue changes incident to tooth movement. Angle Orthod 1938;8:1-48. 5. Oppenheim A. Tissue response to orthodontic intervention. AM J ORTHOI9ORALSting 1942;28:263-301. 6. Reitan K. The initial tissue reaction incident to orthodontic tooth movement as related to the influence of function. Acta Odontol Scand 1951;supp 6. 7. Dellinger E. A histologic and cephalometric investigation of premolar intrusion in the Macaca speciosa monkey. AM J ORTHGD 1967;53:325-55. 8. Helmets CB. A microscopic study of orthodontic tooth movement in the dog. Master's thesis, Montgomery, Alabama: University of Alabama, 1967.
Am. J. Orthod. Oentofac. Orthop. January 1991
9. Kvam E. Tissue changes incident to movement of rat molars [Lic odont thesis]. Oslo, Norway: University of Oslo, 1967. 10. Stenvik A, Mj6r IA. Pulp and dentin reactions to experimental tooth intrusion--a histologic study of the initial changes. AM J OR'roOD 1970;57:370-85. I 1. Anstendig HS, Kronman JH. A histologic study of pulpal reaction to orthodontic tooth movement in dogs. Angle Orthod 1972;42:50-5. 12. Bondevik O. Tissue changes in the rat molar periodontium following application of intrusive forces. Eur J Orthod 1980; 2:41-9. 13. Guevara MJ, McClugage SG. Effects of intrusive forces upon the microvasculature of the dental pulp. Angle Orthod 1980; 50:129-34. 14. Hamersky PA, Weimer AD, Taintor JF. The effect of orthodontic force application on the pulpal tissue respiration rate in the human premolar. AM J ORTItOD 1980;77:368-78. 15. Reitan K. Biomechanical principles and reactions. In: Graber TM, Swain BF, eds. Orthodontics: current principles and techniques. St. Louis: CV Mosby, 1985:101-92. 16. Unsterseher RE, Nieberg LG, Weimer AD, Dyer JK. The response of human pulpal tissue after orthodontic force application. AM J ORTIIODDENTOFACORTttOP 1987;92:220-4. 17. Melsen B, Agerb~ek N, Eriksen J, Terp S. New attachment through periodontal treatment and orthodontic intrusion. AM J ORatOr) DEN'roFAcORaatOP 1988;94:104-16. 18. Murakami T, Yokota S, Takahama Y. Periodontal changes after experimentally induced intrusion of the upper incisors in Macaea fuscata monkeys. AMJ ORTItODDENTOFACORTHOP1989;95:11526. 19. Campbell DT, Stanley JC. Experimental and quasi-experimental designs for research. Chicago: Rand McNally College Publishing Company, 1966:34-64. 20. Butcher EO, Taylor AC. The effects ofdenervation and ischemia upon the teeth of the monkey. J Dent Res 1951;30:265-75. 21. Butcher EO, Taylor AC. The vascularity of the incisor pulp of the monkey and its alteration by tooth retraction. J Dent Res 1952;31:239-47. 22. Scheinin A, Pohto M, Luostarinen V. Defense reactions of the pulp with special reference to circulation--an experimental study in rats. Int Dent J 1967;17:461-75. 23. Ooshita M. The metabolism of radioactive succinate in stressed tooth supporting tissue. Bull Kanagawa Dent Coll 1975;3:1-11. 24. Ohman A. Healing and sensitivity to pain in young replanted human teeth. Odontol Tidskr 1965;73:165-227. 25. Luostarinen V, Pohto M, Scheinin A. Dynamics of repair in the pulp. J Dent Res 1966;45:519-25. 26. Nygaard-Ostby B. Pulpas og det apikale periodontiums patologi. In: Nordisk Klinisk Odontologi. Copenhagen: Forlaget for Fagliteratur, 1968:1-16. Reprint requests to: Drs. Y. A. Mostafa and N. H. EI-Mangoury 44 "A" Talaat Harb St. Cairo 11111, Egypt
A r c h i m e d e s , the Greek mathematician and inventor, stated: "Give me a firm place to stand, and I will move the earth." To paraphrase Archimedes, the contemporary orthodontist would say "Give me a firm biologic basis, and I will move the teeth." The effects of orthodontic forces on the oral tissues were examined by many investigators.t't8 The majority of these investigators t9"12'tT"t8were concerned with the reactions of the alveolar bone and periodontal ligament. Some researchers ~°'t''t3"~6 studied the pulp responses to orthodontic forces, particularly the intrusive type. No previous studies have been published on the reactions of the dental pulp to orthodontic extrusion. The purpose of the present research is to study histologically the iatrogenic pulpal reactions during orthodontic extrusion of human teeth.
MATERIALS AND METHODS A random sample of 1S adult orthodontic subjects was studied. All the subjects had intact (i.e., noncarious
*Associate Professors, Department of Orthodontics, Cairo University Faculty of Dentistry. **Professor, Department of Oral Pathology, Cairo University Faculty of Den-
tist~. 811118226
30
and nonrestored) maxillary right and left first premolars that had been recommended for extraction for orthodontic reasons. The mean age of the subjects was 18 years, with a range of 16 to 21 years. After written consents were obtained, a maxillary first premolar was extruded for each subject while its contralateral, which was not extruded, served as a control. The extrusion was done through the use of a fixed edgewise orthodontic appliance with an activated spring attached (Fig. I). The amount of activation was similar for all the subjects. The force of the activated spring was measured with a Correx stress and tension gauge on the first day, first week, second week, and fourth week after activation. Further, the subjects were fitted with maxillary bite plates. The subjects were divided randomly into three equal groups. Bilateral extractions of both right and left maxillary first premolars were done 1 week after activation for the first group, 2 weeks after activation for the second group, and 4 weeks after activation for the third group. In all, 36 teeth were histologically examined through a double-blind experiment) 9 Immediately after removal, the teeth were fixed in a neutral buffered formalin solution for 48 hours. They were decalcified in a 5.2% solution of formic acid and embedded in par-
Voh~me 99 Number 1
Pulpal reactions to extrusion
31
Fig. 1. Orthodontic appliance used. The spring was attached to a maxillary first molar and activated against a maxillary first premolar.
Fig. 2. Normal pulp tissues in a control specimen. (Magnification, x 200.)
affin. Serial sections 5 I-tm thick were cut longitudinally and stained with hematoxylin and eosin dye. RESULTS
The mean force of the activated spring was 57 gm for the first day, 54 gm for the first week, 52 gm for the second week, and 48 gm for the fourth week. Fig. 2 displays the appearance of normal pulp tissues. Figs. 3 through 5 show the coronal pulp of extruded teeth 1 week after activation, 2 weeks after activation, and 4 weeks after activation. At 1 week after activation,
marked vacuolization of the pulp tissues, congested blood vessels, and severe odontoblastic degeneration occurred (Fig. 3). Further, 2 weeks after activation, congested blood vessels, large vacuoles, and degeneration of the odontoblasts were obvious in the pulp tissues (Fig. 4). However, 4 weeks after activation, pulp fibrosis had appeared (Fig. 5). DISCUSSION
Researchers 2"9"t4'2°23 have shown that pulpal reactions differ according to the age of the subject and the
32 Mostafa, lskander, and EI-Mangouty
Am. J. Orthod. Dentofac. Orthop. January 1991
Fig. 3. Coronal pulp of an extruded tooth at 1 week after activation. A and B, Note the marked vacuolizationand degenerationof the odontoblastic layer and congested blood vessels. (Magnifications: A, x 100; B, x200.) C, Note severe odontob/astic degeneration and pulp vacuoIization. Dilated and congested blood vessels are also seen. (Magnification, x300.)
size of the apical foramen. To avoid any possible age effects, t4 the selected subjects were chosen from the same age bracket. Consequently, it was expected that the apical foramina were of nearly the same size. The appliances were carefully designed to deliver the same amount of force in all cases. To eliminate any possible traumatic occlusion during extrusion, maxillary bite plates were inserted. A double-blind experimental research design ~9was created to avoid false significant results. We attempted to study the sequence of histologic events occurring in the pulp after orthodontic extrusion of the maxillary first premolars in human beings. The purpose was to develop criteria for establishing a more complete biologic foundation for orthodontic tooth movement. A comparison between the extruded and nonextruded maxillary first premolars revealed characteristic pulpal reactions resulting from the orthodontic extrusion (Figs. 2 through 5). One of the earliest degenerative changes was the presence of vacuoles in the pulp tissues as well as in the odontoblastic layer (Figs. 3 and 4). This finding agrees with that of Anstendig and
Kronman." Further, the odontoblastic vacuolization was more pronounced coronally than apically. A similar histologic picture of odontoblastic vacuolization was reported to result from tooth intrusion. 2426 Circulatory disturbances were manifested as dilated and congested blood vessels (Figs. 3 and 4). The odontoblastic degeneration was most probably due to the compromised blood supply. It is known that the first premolars erupt when a child is 10 to 12 years of age. The roots are completely formed at 13 to 15 years of age. The subjects in the present sample were nearly 18 years old. At this age, the apical foramina are relatively wide. The extrustive forces, applied to the maxillary first premolars, seem to cause a topographic change in the pulp, or prolapse, made possible by the relatively large apical foramina. This prolapse may be responsible for the rupture or vacuolization appearing in the pulp tissues. This conclusion must be viewed as speculative, so further studies are suggested. Hamersky, Weimer, and Taintor 1' studied pulp respiration resulting from orthodontic forces. They reported a depression in the respiratory rate, which they
Voh~me 9 9 Number 1
P u l p a l reactions to extrusion
~,.
'.~.-
~,'~
.
-h"t
:
,"
33
~
.
Fig. 4. Coronal pulp of an extruded tooth at 2 weeks after activation. A and B, Observe the large vacuole (surrounded by odontoblasts). Vacuolization of the pulp tissues is obvious. (Magnification, x 200.) C, Higher magnification showing vacuolization of the pulp tissues, dilated and congested blood vessels, and degeneration of the odontoblasts. (Magnification, x 400.)
Fig. 5. Coronal pulp of an extruded tooth at 4 weeks after activation. Note that the pulp tissues show fibrosis (fibrous tissue reaction) and that the degree of vacuolization and blood congestion has decreased. (Magnification, x200.)
attributed to circulatory disturbances. One may raise the following question: What is the ultimate fate of these circulatory disturbances? The duration of these pathologic changes is controversial. Oppenheim 3 and Butcher and Taylora°'2~ obtained contradictory results, varying from temporary reversible degeneration to permanent irreversible de-
generation and ultimate necrosis of the dental pulp after orthodontic treatment. Fibrotic changes appeared 4 weeks after activation (Fig. 5). Stenvik and Mj6r '° were able to show signs of healing and scar tissue formation in a long-term intrusive study. It is known that the reparative properties of the pulp are extensive. However, the limit of toler-
34
Mostafa, Iskander, and EI.Mangoury
ance varies from person to person. The ultimate fate of these circulatory disturbances seems to be resolution through reparative processes. Additional studies are recommended for more definitive conclusions. SUMMARY AND CONCLUSIONS A r a n d o m sample o f 18 adult orthodontic subjects was studied. All the subjects had intact m a x i l l a r y right and left first premolars that had b e e n r e c o m m e n d e d for extraction for orthodontic reasons. T h e m e a n age o f the subjects was 18 years. E i g h t e e n m a x i l l a r y first premolars w e r e extruded for either 1, 2, or 4 w e e k s . T h e contralateral m a x i l l a r y first premolars s e r v e d as controis. T h e dental pulp was e x a m i n e d in a double-blind experiment. O n the basis o f the results obtained f r o m this research study, the f o l l o w i n g conclusions w e r e drawn: 1. Orthodontic extrusion causes certain characteristic reactions o f dental pulp, including odontoblastic d e g e n e r a t i o n , circulatory disturbances with congested b l o o d vessels, v a c u o l i z a t i o n and e d e m a o f the pulp tissues, and (by the 4th week) appearance o f fibrotic changes. 2. T h e odontoblastic d e g e n e r a t i o n is m o s t p r o b a b l y due to a c o m p r o m i s e d b l o o d supply. 3. T h e v a c u o l i z a t i o n o f the pulp tissues is b e l i e v e d to result f r o m a topographic c h a n g e , o r prolapse, o f the pulp, through the relatively w i d e apical foramina.
REFERENCES 1. Marshall JA. A study of bone and tooth changes incident to experimental tooth movement and its application to orthodontic practice. IN'r J OR'roOD 1933;19:1-17. 2. Orban B. Biologic problems in orthodontia. J Am Dent Assoc 1936;23:1849-79. 3. Oppenheim A. Biologic orthodontic therapy and reality. Angle Orthod 1936;6:5-38,69-116,153-83; 1937;7:58-9. 4. Stuteville OH. A summary review of tissue changes incident to tooth movement. Angle Orthod 1938;8:1-48. 5. Oppenheim A. Tissue response to orthodontic intervention. AM J ORTHOI9ORALSting 1942;28:263-301. 6. Reitan K. The initial tissue reaction incident to orthodontic tooth movement as related to the influence of function. Acta Odontol Scand 1951;supp 6. 7. Dellinger E. A histologic and cephalometric investigation of premolar intrusion in the Macaca speciosa monkey. AM J ORTHGD 1967;53:325-55. 8. Helmets CB. A microscopic study of orthodontic tooth movement in the dog. Master's thesis, Montgomery, Alabama: University of Alabama, 1967.
Am. J. Orthod. Oentofac. Orthop. January 1991
9. Kvam E. Tissue changes incident to movement of rat molars [Lic odont thesis]. Oslo, Norway: University of Oslo, 1967. 10. Stenvik A, Mj6r IA. Pulp and dentin reactions to experimental tooth intrusion--a histologic study of the initial changes. AM J OR'roOD 1970;57:370-85. I 1. Anstendig HS, Kronman JH. A histologic study of pulpal reaction to orthodontic tooth movement in dogs. Angle Orthod 1972;42:50-5. 12. Bondevik O. Tissue changes in the rat molar periodontium following application of intrusive forces. Eur J Orthod 1980; 2:41-9. 13. Guevara MJ, McClugage SG. Effects of intrusive forces upon the microvasculature of the dental pulp. Angle Orthod 1980; 50:129-34. 14. Hamersky PA, Weimer AD, Taintor JF. The effect of orthodontic force application on the pulpal tissue respiration rate in the human premolar. AM J ORTItOD 1980;77:368-78. 15. Reitan K. Biomechanical principles and reactions. In: Graber TM, Swain BF, eds. Orthodontics: current principles and techniques. St. Louis: CV Mosby, 1985:101-92. 16. Unsterseher RE, Nieberg LG, Weimer AD, Dyer JK. The response of human pulpal tissue after orthodontic force application. AM J ORTIIODDENTOFACORTttOP 1987;92:220-4. 17. Melsen B, Agerb~ek N, Eriksen J, Terp S. New attachment through periodontal treatment and orthodontic intrusion. AM J ORatOr) DEN'roFAcORaatOP 1988;94:104-16. 18. Murakami T, Yokota S, Takahama Y. Periodontal changes after experimentally induced intrusion of the upper incisors in Macaea fuscata monkeys. AMJ ORTItODDENTOFACORTHOP1989;95:11526. 19. Campbell DT, Stanley JC. Experimental and quasi-experimental designs for research. Chicago: Rand McNally College Publishing Company, 1966:34-64. 20. Butcher EO, Taylor AC. The effects ofdenervation and ischemia upon the teeth of the monkey. J Dent Res 1951;30:265-75. 21. Butcher EO, Taylor AC. The vascularity of the incisor pulp of the monkey and its alteration by tooth retraction. J Dent Res 1952;31:239-47. 22. Scheinin A, Pohto M, Luostarinen V. Defense reactions of the pulp with special reference to circulation--an experimental study in rats. Int Dent J 1967;17:461-75. 23. Ooshita M. The metabolism of radioactive succinate in stressed tooth supporting tissue. Bull Kanagawa Dent Coll 1975;3:1-11. 24. Ohman A. Healing and sensitivity to pain in young replanted human teeth. Odontol Tidskr 1965;73:165-227. 25. Luostarinen V, Pohto M, Scheinin A. Dynamics of repair in the pulp. J Dent Res 1966;45:519-25. 26. Nygaard-Ostby B. Pulpas og det apikale periodontiums patologi. In: Nordisk Klinisk Odontologi. Copenhagen: Forlaget for Fagliteratur, 1968:1-16. Reprint requests to: Drs. Y. A. Mostafa and N. H. EI-Mangoury 44 "A" Talaat Harb St. Cairo 11111, Egypt
