International Journal of Oral & Maxillofacial Surgery
Volume 39, Issue 6 , Pages 593-598, June 2010

The influence of masticatory hypofunction on developing rat craniofacial structure☆

  • C.Y. Tsai

      Affiliations

    • Graduate Institute of Dentistry, College of Oral Medicine, Taipei Medical University and Hospital, Taipei, Taiwan, ROC
    • Corresponding Author InformationAddress: Chi Yang Tsai, No. 250 Wu-Hsing Street, Taipei 11042, Taiwan, ROC. Tel.: +886 2 27361661x5139; fax: +886 2 27362295/87739467.
    • ,
  • L.Y. Yang

      Affiliations

    • Department of Physiology, College of Medicine, Taipei Medical University, Taipei, Taiwan, ROC
    • ,
  • K.T. Chen

      Affiliations

    • Craniofacial Center, Chang-Gung Memorial Hospital, Taipei, Taiwan, ROC
    • Chang-Gung University, College of Medicine, Linkou, Taiwan, ROC
    • ,
  • W.C. Chiu

      Affiliations

    • Graduate Institute of Dentistry, College of Oral Medicine, Taipei Medical University and Hospital, Taipei, Taiwan, ROC
    • Department of Orthodontics, Cardinal Tien Hospital Yung Ho Branch, Taiwan, ROC

Accepted 5 February 2010. published online 11 March 2010.

Article Outline

Abstract 

The purpose of this study was to use botulinum neurotoxin type A (BoNT/A) selectively to evaluate the influence of localized masticatory atrophy and paresis on craniofacial growth and development. 60 growing rats, 4 weeks old, weighing approximately 120g, were randomly divided according as follows (Long-Evans, N=15 per group): I (Mb+Tns); II (Mns+Tb); III (Mb+Tb); IV (Mns+Tns), where Mb or Tb is the BoNT/A-injected masseter or temporalis muscles (1.0U/muscle, 2.5ml) and Mns or Tns is the saline-injected muscles (2.5ml). After 7 weeks, the mature rats were killed, the muscles dissected and mean muscle mass recorded. Anthropometric cranial, maxillary and mandibular measurements were taken from the dried skulls. Changes in animal weight during the growth period were not statistically significant. The mean masticatory muscle mass was smaller for the BoNT/A-injected muscles of Mb and Tb. Anthropometric measurements of bony structures inserted by masseter and temporalis muscles revealed a significant treatment effect. The measurements showed a facial morphology typical of a dolichofacial profile: short upper face accompanied by a long lower face with an extended mandibular length and ramus height and constricted bicoronoidal and bigonial widths. The results suggest that induction of localized masticatory muscle atrophy with BoNT/A alters craniofacial growth and development.

Key words: botulinum neurotoxin, masseter muscle, temporalis muscle, masticatory muscle atrophy, craniofacial growth and development

 

Moss's functional matrix theory states that facial muscles play a central role in bone growth19. The surrounding muscular environment directs the cells concerned with the morphology, orientation and spatial relationship of bone growth, while other tissues (embryonic functional matrices) guide differentiation at appropriate times and locations15, 16, 17, 18, 19, 25. Hypothetically, therefore, induction of muscle dysfunction and hypoactivity would alter craniofacial growth and local development around muscle attachment and insertion sites.

Optimal dental treatment involves understanding the effects of masticatory muscle function on craniofacial bone growth to achieve a desirable outcome. In addition to appropriate application of biomechanical principles, optimal treatment planning requires an understanding of the craniofacial muscular environment of each patient. The facial muscles play an important role in the etiology and treatment of malocclusions and jaw deformities and are crucial for the stability of dental treatment22.

Previous investigations of the effect of muscle function on facial bone growth have been limited by major shortcomings in the experimental models. For example, changes in diet consistency2, 8, 28 such as eating a soft or comminuted diet, can indirectly induce masticatory hypofunction, but do not reflect the actual influences of muscle activity on function. Myotomy13 or myoectomy21, 26 decrease the blood supply, change the loading of the entire skeleton, and often introduce biomechanical force. Denervation1, 3, 23 is likely to cause a loss of sensation or damage to the motor nucleus5, 7, which could interfere with normal growth of bone5, 30.

Botulinum neurotoxins (BoNTs) have been used widely in medical applications due to their rapid and safe effects. BoNTs are fermentation products of the spore-forming bacterium Clostridium botulinum24. Seven neurotoxins have been identified (type A–G)6, which inhibit the release of acetylcholine from the presynaptic nerve terminal of cholinergic nerve endings and induce muscle paralysis14. The onset and duration of muscle paralysis are influenced by the origin of presynaptic nerve terminal and the type of toxin used. At the neuromuscular junction in humans, toxin recovery takes 2–4 months while recovery of the autonomic nervous system is more prolonged20. Among the neurotoxins, the action of botulinum neurotoxin type A (BoNT/A) has the longest recovery time in animal studies with a reversible, temporary inhibition of acetylcholine release14.

Clinical evaluation of the effects of masseter muscle function following BoNT/A injections have mainly been focused on enhancing cosmetics (volumetric reduction) or diminishing excessive muscle activity (bruxism decrease). Basic scientific research with BoNT/A is limited27, and its full anatomical effects are not known, particularly with regard to the mandible and relevant anthropometric measurements. The purpose of this study was to evaluate the influence of the musculature on the craniofacial skeleton in a growing animal model by inducing localized masticatory atrophy and paresis.

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Materials and Methods 

This was an open-label study over 7 weeks. Prior to the start of the study, full protocol and ethics approval were obtained from the animal centre of Taipei Medical University. 60 male growing Long-Evans rats, weighing approximately 120g, were enrolled in the study. All study animals were male to limit sexual dimorphism. Study animals were housed in separate cages in the same room under light and climate-controlled conditions, and were fed a standard diet of hard pellets and water ad libitum. Mean weights (accuracy to nearest 0.01g) were measured during the 7-week experimental period (T1–T7) with an electronic digital scale.

At age 4 weeks (T0), weaned study animals were injected with BoNT/A (Botox®, Allergan Pharmaceuticals, Irvine, CA, USA). BoNT/A was diluted with 4.0ml sterile, non-preserved 0.9% saline to yield 25U/ml preparation. Study animals received a 2.5-ml intramuscular injection of BoNT/A (1.0U/muscle mass) as follows. Group I (Mb+Tns): injection into bilateral masseter muscles (bilateral temporalis muscles received equivalent amounts of 0.9% sterile, non-preserved saline). Group II (Mns+Tb): injection into bilateral temporalis muscles (bilateral masseter muscles received equivalent amounts of 0.9% sterile, non-preserved saline). Group III (Mb+Tb): injection into bilateral masseter and temporalis muscles. Group IV (control, Mns+Tns): injection of 0.9% sterile, non-preserved saline into bilateral masseter and temporalis muscles.

A single dose of 50mg/kg ketamine (Zoletil®, Virbac Inc., CA, USA) and 10mg/kg xylazine (Rompum®, Bayer Inc., Toronto, Canada) were administered intraperitoneally to achieve initial anaesthesia for injections of BoNT/A and saline. The bilateral injection sites for the temporalis muscles were located one-third and two-thirds along the line connecting the orbitale and outer meatus. Masseter muscles received superficial and deep muscle layer injections. The superficial muscle site was located halfway along the line connecting the orbitale and outer meatus, perpendicular to the line adjoining the mandibular plane angle and outer oral commisure. The deep muscle site was posterior to the orbitale on the line connecting the outer meatus and orbitale. Every temporalis injection site received 1.0U and every masseter injection site received 0.5U of BoNT/A or the equivalent amount of saline. At the end of the 7-week experimental period, the rats were perfused and killed.

The masseter and temporalis muscles were dissected carefully and harvested by the same operator (W.C.C.). The mean muscle mass was recorded with a precision balance (model ZSA80, Scientech, Denver, USA) and differences were compared among Groups I, II, III and the control. Dried skulls were prepared for direct cranial, maxillary and mandibular anthropometric measurements. 40 anthropometric parameters were analyzed (Fig. 1a and b) as described by Levrini et al.11, Yamamoto29, Ulgen et al.28, Tsai and Liao27, and Matic et al.12.

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  • Fig. 1. 

    (a) Landmarks of anthropometric points. Cranial anthropometric points: 1, Internasal point; 2, Nasofrontal point; 3, Lateral nasal point; 4, Orbita point; 5, Zygion point; 6, Frontoparietal point; 7, Squama temporalis point; 8, Occipital point; 9, Tympanic point; 10, Nasomaxillary point. Maxillary anthropometric points: 11, Key ridge point; 12, Zygomatic arc, inferior point; 13, Zygomatic arc, anterior point; 14, Incisive foramen, lateral point; 15, Posterior nasal spine; 16, Prosthion point; 17, Incisive superior alveolar point; 18, U1, incisal point; 19, U1, cervicolabial point; 20, U1, cervicopalatal point; 21, U1, mesial point; 22, U1, distal point; 23, U6, mesial point; 24, U6, mesiobuccal cusp point; 25, U8, distal point; 26, U8, mesiobuccal cusp point. Mandibular anthropometric points: 27, Coronoid point; 28, Coronoid notch point; 29, Condylion point; 30, Gonion point; 31, Gnathion; 32, Mn point; 33, Antegonial incisure; 34, Anterior masseteric line; 35, Menthon point; 36, Mandibular alveolar point; 37, Infradental point; 38, Incisive inferior alveolar point; 39, L1, incisal point; 40, L1, cervicolabial point; 41, L1, cervicolingual point; 42, L1, mesial point; 43, L1, distal point; 44, L6, mesial point; 45, L6, mesiobuccal cusp point; 46, L8, distal point; 47, L8, mesiobuccal cusp point. (b) Anthropometric measurements. Cranial Measurements: 1, Total skull length; 2, Nasal length; 3, Nasal width; 4, Interorbital width; 5, Interzygomatic width; 6, Maximum skull width; 7, Maximum skull height; 8, Upper anterior facial height; 9, Lower anterior facial height; 10, Total anterior facial height. Maxillary measurements: 11, Total maxillary length; 12, Incisive foramen width; 13, Maxillary width; 14, U6 intermolar width; 15, U8 intermolar width; 16, U1 incisor crown height; 17, U6 height; 18, Maxillary posterior arch length; 19, U1, labiolingual distance; 20, U1, mesiodistal distance. Mandibular measurements: 21, Mandibular length I; 22, Mandibular length II; 23, Mandibular length III; 24, Corpus length; 25, Ramus height I; 26, Ramus height II; 27, Ramus height III; 28, Ramus height IV; 29, Corpus height; 30, Mandibular plane angle; 31, Bicoronoidal width; 32, Bicondylar width; 33, Bigonial width; 34, L6 intermolar width; 35, L8 intermolar width; 36, L1, incisor crown height; 37, L6 height; 38, Mandibular posterior arch length; 39, L1, labiolingual distance; 40, L1, mesiodistal distance.

Animal weight data were compared using repeated measures of analysis of variance (ANOVA) followed by post hoc tests using least square deviation. For description of data, mean values and standard deviations were calculated and presented as mean±SD. Changes in muscle mass and anthropometric measurements were analyzed using one-way ANOVA followed by the Mann–Whitney U-test for comparison between experimental groups and control. Statistical significance was defined at the 5% level. All statistical analyses were performed using SPSS version 13.0 software (SPSS Inc., Chicago, IL, USA).

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Results 

Changes in animal weight 

Rats were enrolled 4 weeks after weaning (T0) with a mean weight of 123.6±29.7g for the experimental groups (Groups I, II, III) and 119.0±17.4g for the control group. At age 8 weeks (T4), rats reached maturity and had a mean weight of 323.3±43.8g in the experimental groups and 327.5±37.9g in the control group. Thereafter, weight increased at a slower rate. At the end of the study (T7), rats were age 11 weeks and had a mean weight of 391.3±46.1g in the experimental groups and 388.2±29.7g in the control group. No statistically significant differences were found in animal weights as shown in Fig. 2. Weight gain remained stable throughout the study. Neither disturbances in growth nor clinically evident differences in size or shape of the animals were seen.

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  • Fig. 2. 

    Changes in weight over time. Weight gain remained stable throughout the study. Neither disturbances in growth nor clinically evident differences in animal size or shape were seen. No statistically significant differences were found in animal weights.

Changes in muscle mass 

Data showed that BoNT/A-treated masseter muscles were smaller than saline-injected masseter muscles with a significant difference between Group III and the control (Fig. 3). BoNT/A-treated temporalis muscles showed a similar result with a significance difference between Groups II and III (p<0.001).

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  • Fig. 3. 

    Changes in muscle mass. Masseter muscles were smaller in BoNT/A-treated groups (I and III). Temporalis muscles were smaller in BoNT/A-treated groups (II and III). **p<0.001.

Comparisons of direct anthropometric measurements 

Only statistically significant parameters compared with control are listed and displayed in Table 1 and discussed.

Table 1. Statistically significant anthropometric measurements.
Group/parametersGroup IGroup IIGroup IIIGroup IV
MeanSDMeanSDMeanSDMeanSD
Sagittal cranial measurements
1. Maximum skull height (7)15.880.6015.590.3814.90*1.4115.920.43
2. Upper anterior facial height (8)7.100.326.6*0.716.53*0.737.430.86
3. Lower anterior facial height (9)12.51*0.7512.210.7713.09*0.9712.070.58
4. Total anterior facial height (10)17.840.6316.73*0.7918.010.7917.730.63

Maxillary dental measurements
5. U8 intermolar distance (15)9.13*0.198.980.189.19*0.168.910.21

Sagittal Mandibular measurements
6. Mandibular length I (21)9.690.519.470.8410.21*0.769.410.52
7. Mandibular length II (22)10.16*0.559.70*0.8610.970.5510.100.58
8. Mandibular length III (23)15.850.5615.271.2516.54*0.4115.251.18
9. Corpus length (24)25.160.7525.001.8524.75*1.0126.010.73

Vertical mandibular measurements
10. Ramus height I (25)11.670.5711.040.2911.34*0.3010.490.68
11. Ramus height II (26)11.790.3111.440.3211.66*0.2810.910.62
12. Ramus height III (27)12.060.4811.39*0.2911.95*0.5811.240.77
13. Ramus height IV (28)14.410.3513.930.4514.32*0.4913.660.74
14. Mandibular plane angle (30)22.67*3.1623.41*3.5125.01*1.9219.662.24

Transverse mandibular measurements
15. Bicoronoidal width (31)17.221.1617.350.8116.37*0.8017.630.77
16. Bigonial width (33)17.100.5717.881.3616.16*0.8717.881.32

Data are presented as mean±SD. Least square deviation was used to compare differences between group IV (the control) with groups I, II and III.

Numbers in parentheses refer to the reference lines in Fig. 1b.

*p<0.05.**p<0.001.

Statistically significant parameters for cranial measurements (p<0.05) compared with the control included maximum skull height, upper anterior facial height, lower anterior facial height, and total anterior facial height. Maximum skull height and upper anterior facial height were shorter in BoNT/A-injected temporalis muscles. Maximum skull height was significantly shorter in Group III while upper anterior facial height was significantly shorter in Groups II and III. Lower anterior facial height was significantly longer in BoNT/A-injected masseter muscles. Total anterior facial height (upper anterior facial height plus lower anterior facial height) was statistically significantly smaller in BoNT/A-injected temporalis muscles in Group II only.

Only one maxillary parameter (p<0.05) showed statistical significance. Upper intermolar width showed wider posterior arch form in BoNT/A-injected masseter muscles.

Data for mandibular measurements were significant (p<0.05) in sagittal, vertical and transverse dimensions, but no significant results were observed for dental measurements (Table 1).

Group III had the longest mandibular length with the steepest mandibular plane angle. Mandibular lengths I and III were significant in Group III while mandibular length II was significant in Groups I and II. Mandibular plane angle showed significance in all groups. The corpus length was the shortest and significant in Group III.

Ramus lengths I–IV were longest in Group I, followed by Groups III and II. Group III showed statistically significant results in all ramus lengths. Ramus length III was also statistically significant in Group II. Bicoronoidal and bigonial widths were wider in Groups I and III where BoNT/A was directly injected into the masseter muscle. Both measurements were significant in Group III.

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Discussion 

The dose of BoNT/A expected to cause muscle paralysis is 20–30U for rodents12, therefore 25U/ml was used in this experiment. There is considerable uncertainty regarding the minimal dose of BoNT required to cause paralysis in different animal species and different muscle types. In the current study, local injections of BoNT-A did not interfere with the normal growth and development of study animals. Weights of animals in the experimental and control groups were similar at the start and the end of the study with no statistically significant difference. No clinical evidence of differences in size or shape was seen.

The growth curve of rodents is characterized by weaning on day 21, puberty on day 35, and maturity on day 60. In the current study, BoNT/A injections were performed in 4-week-old (pre-pubertal) rats to allow time for masseter and temporalis muscle growth and to investigate the effects of muscle influence on bone during growth. The duration of BoNT action in humans is 2–4 months. Animal studies have shown that 4 weeks is sufficient to induce morphological bone changes9, thus a 45-day period was chosen to ensure effective BoNT activity.

There was no significant difference in masseter mass due to the fact that masseter mass is heavier than temporalis muscle mass and, therefore, relatively greater effects are observed in temporalis muscles. Since the same dose of BoNT was used in masseter (Group I), temporalis (Group II), and both masseter and temporalis (Group III) muscles, there were more changes in Groups II and III than in Group I. When the dose is given to both the muscles in the same rat, the effects are more evident than when it is given to a single muscle mass.

Physiologically, muscles exert a contraction force on the periosteum. Bone deposition occurs when a pulling force is applied to the periosteum4. Injections of BoNT/A decrease the force of masseter and/or temporalis muscle contractions and decrease tension on the periosteum. As a result, bone deposition decreases and a morphological change is induced9.

Alterations in craniofacial bone morphology occurred primarily at attachment sites overlying the muscle groups. Insertion points of the temporalis muscles lie at the medial surface and the rostral edge of the coronoid process; therefore, the area around this region (maximum skull height and upper anterior facial height) was most affected by BoNT/A injection into temporalis muscles. This implies that the main influence on the upper face is primarily from temporalis muscles. The superficial masseter muscles are attached to the lateral surface and the lower margins of the mandible. Accordingly, the results for lower anterior facial height, and bicoronoidal and bigonial widths were most pronounced due to the effects of BoNT/A injection on masseter muscles. These findings further confirm site-specific influences on the upper face and lower face.

Following BoNT/A injections, the increase in facial height (long, lower face accompanied by short skull height and upper anterior height in BoNT/A-injected temporalis groups; long lower and total anterior facial heights in BoNT/A-injected masseter muscles) is due to the paralysis of the masseter and temporalis muscles. The consequent relaxation of the jaws of the rats resulted in greater growth of the upper incisors with less grinding. A dolichofacial, open-bite, or clockwise-rotation of the mandible was observed. As a result, the anterior facial height was increased.

In contrast to previous studies1, 10, 12, 23, 27, 28, this study showed long mandibular length and ramus height, which is consistent with a dolichofacial pattern. The discrepant findings in earlier studies can probably be attributed to different media used to induce muscle dysfunction. Soft diet, myoectomy or denervation cause some degree of injury to experimental animals. In this study, botulinum neurotoxin was employed and produced reversible, temporary inhibition of nerve endings.

Changes in craniofacial morphology are influenced by the extent of muscle atrophy and changes in bone remodeling rate are affected by the duration of the study. Results on the temporalis muscles are more obvious; therefore, modification of dose on masseter muscles in subsequent studies should be explored. Since the lateral pterygoid muscles act on the condyle and condylar neck, the authors are investigating injections of BoNT on these muscles. Lateral pterygoids and suprahyoid muscles are difficult to locate for clinical injections in rat models so a larger animal model should be used. Investigations of minimal lethal dose, time of action, and time of recovery on muscle function from BoNT injection should be investigated further. Complete observations of muscle function following BoNT injection should also be verified by electromyography.

Botulinum neurotoxin represents a potential addition to the armamentarium of the dental professional. It may be possible to refine the use of botulinum neurotoxin in the treatment of bruxism or clenching to decrease dental wear, improve smile aesthetics, or treat deep overbite with short lower anterior facial height as an adjunct to orthodontic treatment. Use of botulinum neurotoxin can decrease the tension and activity of masticatory muscles that interfere with the achievement of ideal treatment goals.

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Funding 

None.

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Competing interests 

None declared.

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Ethical approval 

Full protocol and ethics approval was obtained through the Council of Animal Center at Taipei Medical University (Ref no: M204093007).

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References 

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☆ This research is based on a thesis submitted to the graduate faculty of College of Oral Medicine, Taipei Medical University, in fulfillment of the requirements for the M.S. degree by Wan Chi Chiu.

PII: S0901-5027(10)00054-8

doi:10.1016/j.ijom.2010.02.011

International Journal of Oral & Maxillofacial Surgery
Volume 39, Issue 6 , Pages 593-598, June 2010

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