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J Dent Res 82(1): 38-42, 2003
© 2003 International and American Associations for Dental Research

RESEARCH REPORT
Biomaterials & Bioengineering

Age Effect on Orthodontic Tooth Movement in Rats

Y. Ren, J.C. Maltha*, M.A. Van ’t Hof1, and A.M. Kuijpers-Jagtman

Department of Orthodontics & Oral Biology, and
1 Department of Preventive and Curative Dentistry, University Medical Centre Nijmegen, College of Dental Science, PO Box 9101, 6500 HB Nijmegen, The Netherlands;

*corresponding author, j.maltha{at}dent.umcn.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Orthodontic procedures seem to be more time-consuming in adults than in juveniles. This might be related to delay in the initial tissue response or to a slower turnover of the bone and periodontal ligament in adults. To study this problem, we studied orthodontic tooth movement in two groups of 30 rats, aged 6 wks and 9–12 mos, respectively. At one side of the maxilla, 3 molars together were moved mesially with a standardized orthodontic appliance delivering a force of 10 cN. The other side served as a control. The results showed a faster initial tooth movement in juvenile than in adult animals. However, once tooth movement had reached the linear phase, the rate of tooth movement was the same in both groups. The results indicate that, besides a delay in the onset of tooth movement in adult animals, tooth movement could be equally efficient in adults once it had started.

KEY WORDS: orthodontics • tooth movement • velocity • age-effect • rats


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although a tremendous increase in the demand for adult orthodontic therapy was seen in the past decades, our knowledge on the efficiency of adult tooth movement is still rather incomplete. Clinical experience has shown that tooth movement through the alveolar bone in adults is indeed possible by means of treatment modalities based on experiences in adolescents. However, certain treatments seem to be more time-consuming in adult than in juvenile patients. This led Goz (1990) to the conclusion that, in adults, the biological possibilities for tooth movement are decreased to about one-third of those found in children.

This might be due to the biological limitations of the adult bone, since it is well-known that, during aging, the bone composition changes, its cells become less reactive, and its metabolism slows (Klingsberg and Butcher, 1960; Baumhammers et al., 1965). Another possible cause might be the use of inappropriate stimuli, because the biological requirements for inducing optimal tissue responses in young and adult individuals may be different (Melsen, 1991).

In contrast, Bond (1972) and Melsen (1991) suggested that, in the clinical situation, adults and juveniles are equally responsive to mechanical stimuli once tooth movement has started, and that the longer treatment duration in adults might be caused by a delay in the initial response. However, these ideas are only experience-based and not evidence-based. Until now, no attempt has been made to conduct a clinical or experimental study on the age-related changes in bone reactivity during orthodontic treatment by standardized and reproducible methods of force application over a longer period of time.

The few experimental studies on age effects on orthodontic tooth movement have been performed in rodents. Some of them indicate that tooth movement occurs at higher rates and over a greater distance in young than in adult rats (Bridges et al., 1988; Takano-Yamamoto et al., 1992; Kyomen and Tanne, 1997), while others (Jager and Radlanski, 1991; Kabasawa et al., 1996) found similar osteoblastic and osteoclastic activity during orthodontic tooth movement in young and adult rats.

There are, however, some common drawbacks in these studies. The forces are either not defined, since separation elastics were used (Jager and Radlanski, 1991; Kabasawa et al., 1996), or were rather large. Bridges et al. (1988) used 60 cN, Kyomen and Tanne (1997) used 10 and 40 cN, and Takano-Yamamoto et al. (1992) used forces ranging from 5 to 20 cN to move a first molar. Since a rat molar is about 1/60th the size of a human molar, even a force of 5 cN has to be considered to be a heavy one. A second problem is that the definition of "adult" differed from study to study. It ranged from 14 wks (Kyomen and Tanne, 1997) to 71 wks (Jager and Radlanski, 1991). Finally, the observation periods in these studies were relatively short: 1 or 2 wks in most cases. Previous research has shown that tooth movement can be divided into several phases, and it takes quite some time before the linear phase is attained and "real" orthodontic tooth movement occurs (Pilon et al., 1996). So, research focusing only on early phases of tooth movement may elicit misleading results. Furthermore, in many cases, some features specific to rodents—such as continuous eruption of incisors and physiological distal drift of molars—were not taken into account. Continuous eruption of the incisors may affect the direction of the applied force, since incisors are often used as anchorage, and distal drift might camouflage the amount of real experimental tooth movement.

The present study was meant to investigate the effect of age on experimental tooth movement in rats using a standardized appliance, in which magnitude and direction of force were kept constant. The longest observation time was 12 wks, which has been proven to cover all phases of tooth movement. The null hypothesis tested is that there is no difference in rate of tooth movement between adult and young rats in both initial and linear phases.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Design
Two groups of 30 male Wistar rats were used as experimental animals. Young rats were 6 wks old (body weight, 150–250 g) and adult rats were 9–12 mos old (body weight, 400–550 g). The animals were acclimatized for at least 1 wk before the experiment started. The animals were housed under normal laboratory conditions and were fed powdered laboratory rat chow (Sniff, Soest, The Netherlands) and water ad libitum. A standard 12-hour light-dark cycle was maintained. Ethical permission for the study was obtained according to the guidelines for animal experiments of the University of Nijmegen.

A split-mouth design was used, with the experimental side randomly chosen and the contralateral as control. For each experimental side, an orthodontic appliance was made. Stainless steel ligature wires with a diameter of 0.008'' (Dentaurum, Pforzheim, Germany) were bent to enclose all three maxillary molars as one unit, with a dry rat skull as a model. To this ligature wire, a Sentalloy® closed-coil spring (10 cN, wire diameter 0.009'', eyelet diameter 0.022'', GAC, New York, NY, USA) was attached. At one side of the spring, the eyelet was removed. The remaining length was about 6 mm. A schematic drawing of the appliance system is shown in Fig. 1Go. The super-elastic properties of the springs and the delivered force were tested in a laboratory set-up at 38°C. Five springs were randomly chosen from a package of 80. Over 150 measurements were collected for the testing of each spring. The springs proved to deliver a reproducible force of 10 cN ± 2 cN over a range of 3–15 mm activation (Fig. 2Go).



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  		Figure 1. Schematic view of the orthodontic appliance design. Two incisors are pinned together by a ligature wire going through the snout. Three molars are circled by a ligature wire and bonded together by a light-cure material. A force of 10 cN is applied by a super-elastic spring.

 


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  		Figure 2. Force-deflection curve of 10 cN coil springs used in this study.

 
Placement of Appliance
Before the orthodontic appliance was placed, general anesthesia was induced with an intraperitoneal injection of FFM-mix containing fentanyl citrate 0.079 mg/mL, fluanisone 2.5 mg/mL (Jansen Animal Health, Beerse, Belgium), and midazolam 2.5 mg/mL (Roche, Mijdrecht, The Netherlands) in a dosage of 2.7 mL/kg body weight. Oxygen was supplied during operation to facilitate the animals’ breathing, which may become temporarily difficult due to bleeding inside the nasal cavity.

Before the orthodontic appliance was placed, a transverse hole was drilled through the alveolar bone and both maxillary incisors at the mid-root level by means of a drilling bur (D0205, Dentsply, Mortigny le Bretonneux, France). Cooling was achieved with a syringe and physiologic saline. A stainless steel ligature wire (diameter 0.012'') (Dentaurum, Pforzheim, Germany) was put through the hole.

The pre-formed orthodontic appliance was bonded onto the experimental maxillary molar unit with light-curing bonding material (Clearfil SE BOND, Kuraray Europe GmbH, Düsseldorf, Germany). Bonding was applied until the buccal and palatal wires were completely embedded in the bonding material, after which it was light-cured. The Sentalloy® spring was kept free of bonding material at the mesial side of the pre-formed wire. It was activated and subsequently attached to the ligature wire through the snout and the incisors.

Measurements with a digital caliper (Mitutoyo Co., Kawasaki, Japan) were performed while the animals were under general inhalation anesthesia (isofluorane and N2O, Abbott B.V., Hoofddorp, The Netherlands) at 0, 1, 2, 3, 4, 8, and 12 wks after appliance activation. The distance between the most mesial point of the maxillary molar unit and the enamel-cementum border of the ipsilateral maxillary incisor at the gingival level was measured (I–M distance) at the experimental and the control sides. A split-mouth design was indicated because of the confounding effects of the physiological distal drift of the molars, the physiological growth of the snout and the concomitant forward movement of the incisors, and the possible bilateral distal tipping of the incisors that were used as anchorage. Calculation of the differences between the I–M distances at the experimental and the control sides achieved compensation for these effects. The changes in these differences were considered to represent the actual experimental tooth movement caused by the orthodontic appliance. They were expressed as positive values.

The same investigator (YR) performed all measurements, and every measurement was repeated 3 times. The mean value of each triplet was used as the final measurement. Appliance condition, oral hygiene, and body weights were checked once a week. Bonding material was added if necessary. Five rats from each group were killed after 1, 2, 4, 8, and 12 wks for future histological and immunohistochemical studies.

Statistics
The intra-observer measurement error appeared to be 0.07 mm in young rats and 0.05 mm in old rats. The reliability coefficient was 0.99 in both. Previous studies on orthodontic tooth movement have shown that time-displacement curves can be divided roughly into a non-linear and a linear phase. Therefore, the time-displacement curves in the present study were divided into two phases, a non-linear phase (0 to 3 wks) and a linear phase (4 to 12 wks). Statistical analysis was performed on the data over the total period and on the data for the two phases.

All data were normally distributed, and paired t tests could be performed for analysis of the differences between experimental and control sides within each rat. t tests for independent measurements were applied for the comparison of young and adult animals. Significant differences were indicated if p < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
As a result of decreased eruption and abrasion, the crowns of maxillary incisors shortened to some degree during the experimental period, and the mandibular incisors overerupted to compensate for this. A slight palatal tipping of the incisors was observed, but no visible rotation of incisors to the experimental side was present. The activation of the spring remained parallel to the maxilla throughout the experimental period. The amount of experimental tooth movement was defined as the difference of the I–M distance (Incisor - Molar distance) at the experimental and the control sides, expressed as a positive value.

The TableGo shows the changes in I–M distances at experimental sides as compared with the changes at control sides for each time interval in young and old rats. All comparisons between the two sides showed a significant difference for each time interval (p < 0.001).


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  		Table. Changes in the I–M Distance in mm (mean ± SD) for Young Rats over Different Time Intervals
 
Fig. 3Go shows the experimental movement of the molar unit produced by orthodontic force over time for young and adult animals. The total amount of experimental tooth movement for young animals was larger than for adults for each measuring point (p < 0.001). The initial period (0 to 3 wks) showed a faster movement for the young than for the adult animals (p < 0.001). For the linear phase (4 to 12 wks), however, no difference in the rates of tooth movement for the two age groups was found (p = 0.32).



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  		Figure 3. Experimental tooth movement in mm (mean and standard deviation) during the experimental period in young and adult rats. N’s for both young and adult rats at 1, 2, 3, 4, 8, and 12 weeks were 30, 25, 25, 20, 15, and 10, respectively.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Most of the animal experiments on orthodontic tooth movement have been performed in rats. Forces are mostly derived from separation elastics or from coil springs delivering forces such as 40 cN, 60 cN or even 120 cN and 200 cN to move a first molar (King and Fischlschweiger, 1982; King and Keeling, 1994). Considering the tiny size of rat first molars, this kind of force can be detrimental. Few authors describe the use of lower forces such as 15 or 10 cN, but the way the forces have been measured and controlled remains unclear (Takano-Yamamoto et al., 1992; Kagayama et al., 1996; Karsten and Hellsing, 1997).

The present study used a Sentalloy® super-elastic coil spring delivering a constant force of 10 cN on the 3 molars together as one unit. A split-mouth design, as chosen for this study, overcomes three important problems: the physiological distal drift of the molars (Kraw and Enlow, 1967); the undesired movement of the anchorage unit; and the growth of the snout, especially in young animals (Baer et al., 1983).

The continuous eruption of the maxillary incisors was blocked, and the incisors were shortened and abrased to some degree during the experiment, but overeruption of mandibular incisors compensated for that. Slight tipping movement of incisors may have affected the stability of the anchorage. But since this was the same for experimental and control sides, because both incisors were anchored to each other and to the bone, and since no obvious rotation was found, this was considered to be overcome by the split-mouth design. Based on these assumptions, the amount of experimental tooth movement was defined as the difference between the I–M distance (Incisor - Molar distance) at the experimental and control sides. These results then included the correction of the experimental data for all three types of bias concerning tooth movement mentioned above, which most other studies failed to overcome.

The difference in control measurements between young and adult rats might be explained by growth cessation in the adults. This means that the growth of the snout, which compensated for the decrease of I–M distance in young rats, played no role in adult rats. Thus, the decrease in I–M distance was more in young than in adult rats. But, since the effect of growth was compensated for by calculation of the difference between experimental and control measurements, it had no influence on the estimation of experimental tooth movement.

The results from this study only partly supported our hypothesis that there was no difference in rate of tooth movement between young and adult rats. It appeared that, in the initial phase, experimental tooth movement in the adult animals was slower than in the young animals; however, such a difference between the age groups was not found in the linear phase. The fact that young and adult rats showed comparable rates of tooth movement in the linear phase indicates that the bone turnover capacity itself is not age-dependent, and that the slower initial tooth movement in adult animals might be caused by a delay in the initial biological response.

One possible explanation for this delay in initial response in adult animals might be related to the structure of aged periodontal ligament and to reduced bone activity. An overall reduction in organic matrix production in the periodontal ligament, a decrease in the mitotic activity of cells, and also a decrease in the amount of soluble collagen have been described in the literature (van der Velden, 1984). Significant differences in the proliferative activity of PDL cells between young and adult rats were also found during the early stage of tooth movement (Kyomen and Tanne, 1997). Concerning the age effect on bone activity, there is evidence that bone-formative activity of osteoblasts and bone-resorptive activity of osteoclasts decrease with age (Nishimoto et al., 1985; King and Keeling, 1995), but also, in adults, these cells may recover a highly activated state under orthodontic stimuli (Kabasawa et al., 1996). This re-activation in adults, however, may take more time than in juveniles.

In contrast, the periodontal ligament in rats becomes narrower with age (Abiko et al., 1998). This might explain why, if an orthodontic force is applied to the tooth of an adult, hyalinized tissue at the pressure side is more easily formed than in young individuals (Kabasawa et al., 1996). Such hyalinizations are always followed by a prolonged period without tooth movement, which might provide another explanation for the delay in initial tooth movement.

Further histological and immunohistochemical studies will help to elaborate the mechanism of this delay.


   ACKNOWLEDGMENTS
 
This study was supported by the Department of Orthodontics and Oral Biology, University Medical Centre Nijmegen, and by a grant from the Dutch Royal Academy of Sciences (99CDP004). The custom-made Sentalloy springs were kindly provided by GAC (Lomberg BV, Soest, The Netherlands). We thank G. Poelen and D. Smale for their skillful assistance in the animal laboratory.

Received December 27, 2001; Last revision July 10, 2002; Accepted October 18, 2002


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Abiko Y, Shimizu N, Yamaguchi M, Suzuki H, Takiguchi H (1998). Effect of aging on functional changes of periodontal tissue cells. Ann Periodontol 3:350–369.[Medline]

Baer MJ, Bosma JF, Ackerman JL (1983). The postnatal development of the rat skull. Ann Arbor: The University of Michigan Press.

Baumhammers A, Stallard RE, Zander HA (1965). Remodeling of alveolar bone. J Periodontol 36:439–442.[ISI][Medline]

Bond JA (1972). The child versus the adult. Dent Clin North Am 16:401–412.[ISI][Medline]

Bridges T, King G, Mohammed A (1988). The effect of age on tooth movement and mineral density in the alveolar tissues of the rat. Am J Orthod Dentofac Orthop 93:245–250.[ISI][Medline]

Goz G (1990). The age dependence of the tissue reaction in tooth movements. Fortschr Kieferorthop 51:4–7.[Medline]

Jager A, Radlanski RJ (1991). Alveolar bone remodelling following orthodontic tooth movement in aged rats. An animal experimental study. Dtsch Stomatol 41:399–406.

Kabasawa M, Ejiri S, Hanada K, Ozawa H (1996). Effect of age on physiologic and mechanically stressed rat alveolar bone: a cytologic and histochemical study. Int J Adult Orthodon Orthognath Surg 11:313–327.[Medline]

Kagayama M, Sasano Y, Mizoguchi I, Kamo N, Takahashi I, Mitani H (1996). Localization of glycosaminoglycans in periodontal ligament during physiological and experimental tooth movement. J Periodontal Res 31:229–234.[ISI][Medline]

Karsten J, Hellsing E (1997). Effect of phenytoin on periodontal tissues exposed to orthodontic force—an experimental study in rats. Br J Orthod 24:209–215.[Abstract]

King GJ, Fischlschweiger W (1982). The effect of force magnitude on extractable bone resorptive activity and cemental cratering in orthodontic tooth movement. J Dent Res 61:775–779.[Abstract/Free Full Text]

King GJ, Keeling SD (1994). The effect of age on orthodontic tooth movement in the rats. In: The biological mechanisms of tooth eruption, resorption and replacement. Davidovitch Z, editor. Boston: Harvard Society for the Advancement of Orthodontics, pp. 761–768.

King GJ, Keeling SD (1995). Orthodontic bone remodeling in relation to appliance decay. Angle Orthod 65:129–140.[ISI][Medline]

Klingsberg J, Butcher E (1960). Comparative histology of age changes in oral tissues of rat, hamster, and monkey. J Dent Res 39:158–169.[Abstract/Free Full Text]

Kraw AG, Enlow DM (1967). Continuous attachment of the periodontal membrane. Am J Anat 120:133–148.

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Melsen B (1991). Limitations in adult orthodontics. In: Current controversies in orthodontics. Melsen B, editor. Chicago: Quintessence, pp. 147–180.

Nishimoto SK, Chang CH, Gendler E, Stryker WF, Nimni ME (1985). The effect of aging on bone formation in rats: biochemical and histological evidence for decreased bone formation capacity. Calcif Tissue Int 37:617–624.[ISI][Medline]

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Van der Velden U (1984). Effect of age on the periodontium. J Clin Periodontol 11:281–294.[ISI][Medline]




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