Effect of cigarette smoking on alveolar bone thickness and density in patients undergoing leveling and alignment of crowded lower anterior teeth: a controlled clinical trial

Abstract

Objective

To evaluate the effect of cigarette smoking on the alveolar bone thickness and density in patients undergoing leveling and alignment of crowded lower anterior teeth.

Methods

This controlled clinical trial involved 17 smokers and 17 nonsmokers with mild to moderate crowding of the anterior mandibular teeth. Two cone-beam computed tomography images of the mandible were taken before and after treatment. The length of each tooth root was calculated in each T0 image, and the root was divided into three equal regions. Three lines were drawn parallel to the line of the cementoenamel junction at these three regions of the root, and the previously drawn lines were used to measure bone thickness and bone density.

Results

The mean changes in cortical bone thickness and bone density were significantly smaller in smokers than nonsmokers. Cortical bone thickness and bone density were significantly lower after than before treatment in both smokers and nonsmokers.

Conclusion

In addition to all of its known dangers, cigarette smoking may also harm the alveolar bone by decreasing the bone thickness and density during orthodontic treatment in heavy smokers.

Introduction

The alveolar bone undergoes changes in thickness due to orthodontic treatment. It has been suggested that such movements can lead to alveolar bone defects or perforations through the buccal or lingual cortical lamina depending on the pattern of the dental movement.^1,2 The application of orthodontic forces triggers a series of biological reactions in the dental tissues that lead to remodeling of the alveolar bone, allowing tooth movement to occur.³ The mineralization of the newly formed bone is low; this low mineralization combined with the short-term decrease in the mineral density of the alveolar bone weakens the structural resistance of the bone and facilitates the process of dental movement.⁴

Bone loss alters the position of the center of resistance of the teeth,⁵ and traditional orthodontic treatment may thus be associated with a high risk of complications such as intrusion and tipping. Before starting orthodontic treatment, the alveolar bone status should be observed in patients who are more likely to develop periodontal disease, and existing disease should be controlled.

Bone mineral density is the amount of calcium and mineral salts present in one unit of area or volume of the bone,⁶ and it represents the level of mineralization of the organic bone template. The proportion of organic template mineralization varies among different parts of the bone. Therefore, the density of the bone is the average density of all its parts.⁷ Bone density can be affected by many factors, including age; sex; genetic factors; lack of calcium absorption; vitamin D deficiency; chronic diseases such as endocrine, digestive, and rheumatic diseases; and smoking.^8–11

Computed tomography (CT) has been considered the most beneficial method to assess bone density in many previous studies.^12,13 However, it is not a recommended diagnostic method in patients undergoing orthodontic treatment because of its high radiation dosage.¹⁴ Therefore, many studies used cone-beam CT (CBCT) instead of CT because its radiation dosage is lower than that of CT (3.00 mGy for CT¹⁵ and 0.62 mGy for CBCT¹⁶). Aranyarachkul et al.¹⁷ indicated that CBCT can be a proper alternative method to assess bone density because it has a much lower radiation dosage than does CT. Chang et al.¹⁴ showed that CBCT is a valuable method to evaluate the changes in bone density after orthodontic treatment.

The relationship between smoking and bone density has been indicated in several studies. However, the results were not consistent. Studies have also shown that smoking has a detrimental effect on bone mass.^18–20 A cross-sectional study on same-sex twins showed a clear association between smoking and bone density regardless of age, sex, and gene expression.²¹ A systematic review showed that heavy smoking (represented by the smoking duration in years and the number of cigarettes smoked daily) is associated with decreased bone density in multiple skeletal sites.²² Moreover, studies have shown that smoking is directly linked with decreased bone density regardless of age, sex, and daily activities in people older than 60 years.^20,23 Smoking has also been shown to reduce bone density in young people when comparing smokers with nonsmokers of the same age.^24,25 Overall, epidemiological studies have shown that smoking impacts bone density changes independently of other factors affecting bone density.^23,25,26

In addition to all the known harms of smoking, many studies have shown that smoking affects orthodontic treatment in many ways, such as promoting adhesion and biofilm formation on orthodontic materials,²⁷ decreasing the shear bond strength,²⁸ and increasing pain caused by elastomeric separators.²⁹ Smoking may also affect the changes in alveolar bone after orthodontic treatment. However, no study to date has evaluated the relationship between smoking and alveolar bone changes after orthodontic treatment. Therefore, the present study was performed to assess the effect of cigarette smoking on the alveolar bone thickness and density in patients undergoing leveling and alignment of crowded lower anterior teeth.

Materials and Methods

Study design

This controlled clinical trial was performed to evaluate the effects of cigarette smoking on root and alveolar bone resorption in patients undergoing leveling and alignment of crowded lower anterior teeth. The reporting of this study conforms to the CONSORT statements.³⁰ The study was conducted at the Department of Orthodontics at the Faculty of Dental Medicine, Damascus University, Damascus, Syria. Ethical approval was obtained from the ethics committee at The Ministry of Higher Education, Damascus, Syria (UDDS-479-20112017/SRC-4118). This study was registered in the German Clinical Trials database (DRKS00027884) (https://www.drks.de/drks_web/navigate.do?navigationId=resultsExt).

Participants

The study population comprised patients who had visited the Department of Orthodontics at the Faculty of Dentistry, Damascus University; who were registered in its archive records; and whose treatment involved leveling and alignment of the lower anterior teeth. Data were collected from February 2018 to January 2021.

Inclusion and exclusion criteria

The inclusion criteria were an age of 19 to 30 years, simple or mild crowding (Little’s irregularity index of <6 mm), good oral hygiene, the presence of all mandibular teeth (besides the third molars), no previous orthodontic treatment, and a heavy smoking habit (>20 cigarettes a day³¹ (with each cigarette containing at least 0.2 mg nicotine and 0.2 mg tar or their equivalent. The patients were divided into a smoker group and nonsmoker group according to the World Health Organization classification, in which a nonsmoker is a patient who has not consumed any form of tobacco during his or her life.³² The exclusion criteria were generalized or localized clinical conditions that affect tooth movement, treatment with medication that affects orthodontic tooth movement, periodontal diseases that occurred during treatment, and lack of patient commitment to follow-up. The research objectives and methods were explained to the patients, and written informed consent was obtained from those who agreed to participate in the study.

Interventions

All diagnostic and treatment procedures were performed by one of the researchers (G.S.). Diagnostic study casts were used to precisely measure the amount of crowding and Little’s irregularity index³³ before orthodontic treatment. High-resolution CBCT images of the lower teeth were taken before starting the orthodontic treatment (T0) using an PaX-i3D Green device (Vatech Co., Ltd., Gyeonggi-do, Korea) with the following settings: 50 to 90 KVp, 4 to 16 mA, voxel size of 0.2 mm, exposure time of 5.9 s, field of view of 16 × 10 cm. Once the diagnostic procedures were completed, an elastic separator was applied for 7 days, and orthodontic bands and brackets were then attached (American Orthodontics, Sheboygan, WI, USA). The starter wire (nickel–titanium (NiTi 0.012-inch) was immediately fitted for the patients in both groups, followed by fitting of a second wire (NiTi 0.014-inch) 3 weeks later. The third wire was NiTi 0.016-inch, the fourth was NiTi 0.016- × 0.022-inch, and the fifth was NiTi 0.017- × 0.025-inch. The end of the leveling and alignment stage was reached when it became possible to insert the base wire (stainless steel 0.019- × 0.025-inch; American Orthodontics) neutrally within the slots of the brackets while Little’s irregularity index was <1 mm.³³ This point was considered the end of the leveling and alignment stage, and the second CBCT image (T1) was taken.

Outcome measures

Radiographic study

The radiological study was performed using Ez3D Plus Program (Vatech Co., Ltd.) and involved acquisition of a longitudinal section (buccal–lingual) at each of the six lower front teeth at T0 with repeating of the same section at T1. The line passing through the cementoenamel junction was used as a reference line for making all measurements. The axes of each tooth were positioned separately in the three sections (axial, coronal, and sagittal) to achieve the best image with which to determine the reference line as follows.

• Axial section: The intersection point of the two axes was positioned in the center of the pulp canal in the coronal part of the tooth so that the first axis passed through the middle of the vestibular and lingual surfaces while the second axis passed through the distal and mesial surfaces (Figure 1(a)).

• Coronal section: The intersection point of the two axes was positioned in the center of the pulp canal so that the first axis passed from the middle of the incisal to the apical foramen (the longitudinal axis of the tooth) while the second axis passed from the distal and mesial surfaces (Figure 1(b)).

• Sagittal section: The intersection point of the two axes was positioned in the center of the pulp canal so that the first axis passed from the middle of the incisal to the apical foramen (the longitudinal axis of the tooth) while the second axis passed from the vestibular and lingual surfaces (Figure 1(c)).

Figure 1.

Positioning of axes. (a) Positioning the axis of a lower central incisor on the axial view. (b) Positioning the axis of a lower central incisor on the coronal view and (c) Positioning the axis of a lower central incisor on the sagittal view.

After positioning the axes in the three sections, the largest distal–mesial width of the studied tooth was demonstrated in the coronal section, and the largest buccal–lingual width of the studied tooth was demonstrated in the sagittal section. The line passing through the buccal cementoenamel junction point and the lingual cementoenamel junction point was drawn and defined as a reference line for making all radial measurements in the sagittal section.

Bone thickness measurements

The bone thickness was measured in the sagittal plane according to the method described by Garlock et al.³⁴ The linear measurement tool in the Tools menu in Ez3D Plus Program was used to perform the following steps. The longitudinal axis of the tooth root (the line extending from the cementoenamel junction line to the tooth’s apex) was drawn. Next, the length of each tooth root was calculated in each T0 image, and the root was divided into three equal regions: the cervical region, the middle region, and the apical region.

Three lines were drawn parallel to the line of the cementoenamel junction at these three regions of the root (Figure 2). The first line represented the cervical region and was located on the longitudinal axis of the tooth in the middle of the previously defined cervical region. The second line represented the middle region and was located on the longitudinal axis of the tooth in the center of the middle region of the root. The third line represented the apical region and was located on the longitudinal axis of the tooth in the middle of the apical region. The intersection of these lines with the cortical bone resulted in three buccal and three lingual regions.

Figure 2.

Bone thickness of the buccal and lingual surfaces of the lower left central incisor in the sagittal view.

CEJ, cementoenamel junction.

The thickness of the alveolar bone was measured on the buccal and lingual sides for each studied tooth by calculating the distance between the inner and outer edges of the cortical bone at each of the previously created lines. The distance of each of the previously drawn lines from the cementoenamel junction was measured to repeat the measurements in the T1 images.

Bone density measurements

The previously drawn lines were used to measure bone density as follows. The tool for measuring bone density in the list of tools was used to calculate the bone density for each of the buccal and lingual surfaces of each lower incisor separately, thus giving the average bone density between the inner and outer edges of the cortical bone at each of the previously created lines (Figure 3). The radiographic study for all CBCT images was performed by one of the researchers (G.S.).

Figure 3.

Bone densities of the buccal and lingual sides of the lower right canine in the sagittal view.

CEJ, cementoenamel junction.

Sample size estimation

The sample size was estimated using G*Power version 3.1.6 software as described in the report by Lund et al.³⁵ The effect size was calculated according to the mean and standard deviation of the bone changes in the control group before and after orthodontic treatment in the previous study, which was 0.1 mm around the lateral incisor. A further 0.5 mm was added to consider smoking as a risk factor for alveolar bone. By dividing the two means on the standard deviation of the same variable in the mentioned article, the effect size was 1. The statistical power was 80% with a significance level of 0.05. We found that the appropriate sample size for the current study was 17 patients in each group, and the total sample size was 34 patients.

Statistical analysis

IBM SPSS version 23 (IBM Corp., Armonk, NY, USA) was used to perform all statistical analyses at a confidence level of 95% and significance level of 5%. The normality of the data distribution was determined by the Shapiro–Wilk test. Evaluations of the differences between before and after treatment in both groups were performed using the Wilcoxon test, and the Mann–Whitney test was applied to evaluate the differences between the two groups.

Error of method

The paired t-test was conducted to study the significance of differences in the mean of each of the studied variables between the first and second reading measurement groups using 10 images randomly selected from the research sample. There were no statistically significant differences (P > 0.05) in the mean of each of the measured variables between the first and second readings. Intraclass correlation coefficients were calculated to study the reliability of the measurements. The intraclass correlation coefficients were relatively high and close to 1, meaning that the values of the studied variables were consistent in the first and second readings; therefore, one reading was sufficient to determine the values of each of the studied variables in the research sample (Table 1).

Table 1.

Differences between the first and second readings to determine interexaminer and intraexaminer errors.

Studied variable	Patient number	ICC	P-value*	t-value	P-value**
Cortical bone thickness	10	0.925	<0.001	−0.673	0.518
Bone density	10	0.977	<0.001	−1.04	0.324

ICC, intraclass correlation coefficient.

*P-value of ICC, **P-value of paired t-test.

Results

Patient follow-up during the study stages

At the beginning of the study, the clinical examination was conducted on 35 smoking patients and 40 nonsmoking patients with crowded lower anterior teeth among all patients from the Department of Orthodontics at the Faculty of Dentistry of Damascus University. Fifteen smoking patients and 13 nonsmoking patients were excluded either because they did not meet the inclusion criteria (or met the exclusion criteria) or because they refused to participate in the study. Therefore, the number of patients who fulfilled the enrollment requirements became 20 smokers and 27 nonsmokers. A number was given to each patient, and the smoking patients were logged into the website www.randomizer.org to select 17 patients from the sample. The same procedure was repeated for the patients from the control group. No patient withdrew, and the data analysis was therefore conducted for 34 patients included in the study sample.

Main findings

The descriptive statistics of the study sample in terms of treatment period, age, sex, and amount of crowding before treatment are shown in Table 2.

Table 2.

Descriptive statistics of the sample.

Group	n	Age (years)				Sex		Amount of crowding (mm)
		Mean	SD	Min	Max	Male	Female	Mean	SD	Min	Max
Smoker	17	24	2.37	20	30	9	8	4.08	0.79	2	5
Nonsmoker	17	24.35	2.34	19	29	6	11	3.75	0.6	3	5
Total sample	34	24.17	2.32	19	30	15	19	3.92	0.71	2.5	5.5

SD, standard deviation; Min, minimum; Max, maximum.

Table 2 shows the descriptive statistics of cortical bone thickness and bone density in the two groups before and after orthodontic treatment. The cortical bone thickness significantly decreased from before to after treatment in both groups (Wilcoxon test: P = 0.007 in nonsmoker group and P < 0.001 in smoker group). Likewise, the bone density significantly decreased from before to after treatment in both groups (P < 0.001 for both).

The Mann–Whitney test showed that P = 0.007 for cortical bone thickness and P = 0.048 for bone density, meaning that at a confidence level of 95%, there were statistically significant decreases in the mean changes of cortical bone thickness and bone density in the smoker group compared with the nonsmoker group (Table 3).

Table 3.

Descriptive statistics and mean changes in cortical bone thickness and bone density before and after treatment within each group and between the two groups.

	Cortical bone thickness (mm)				Bone density (Hounsfield units)
	Smoker		Nonsmoker		Smoker		Nonsmoker
	Mean	SD	Mean	SD	Mean	SD	Mean	SD
Pretreatment	1.26	0.20	1.18	0.25	2094.5	177.6	2128.6	271
Post-treatment	1.01	0.20	1.06	0.25	1601.8	181.5	1760.8	299
P-value (Wilcoxon test)	<0.001*		0.007*		<0.001*		<0.001*
P-value (Mann–Whitney test)	0.007*				0.048*

SD, standard deviation.

*Statistically significant difference.

Discussion

Several studies have shown a high prevalence of the proportion of smokers who are treated with fixed orthodontics.³⁶ Smoking is considered one of the most important direct causes of death worldwide, and the number of such deaths may approach 5.4 million annually.³⁷ The relationship between smoking and bone density has been indicated in many studies, but the results were not consistent; however, these studies showed that smoking has a detrimental effect on bone mass.^18–20,38 The effect of smoking on bone is significantly correlated with the duration and dose of smoking and the patient’s body weight.^20,39,40 A systematic review showed that heavy smoking (expressed as the smoking duration in years and number of cigarettes smoked daily) is associated with decreased bone density in multiple skeletal sites.²² Epidemiological studies showed that smoking affects bone density changes independently of other factors affecting bone density.^23,25,26,40 However, no studies to date have evaluated the effect of cigarette smoking on both cortical bone thickness and density during orthodontic movement.

Dental malocclusions of moderate severity (4–6 mm) that did not require extraction were selected in the present study. Interproximal enamel reduction was performed using diamond-coated abrasive strips to avoid alignment with excessive tilting movements that might compromise the treatment plan and the accuracy of evaluating of the changes in the bone. This was especially important considering the admission of high values of dental crowding in this study as a criterion for evaluating the effect of smoking on changes in the structure of the alveolar bone during orthodontic tooth movement.

The wire sequence in this study was chosen to ensure an easy transition between each wire and the next while facilitating the alignment and straightening process. Our decision took into account the results of previous studies and systematic reviews that showed no effect of the wire material or wire sequence on the time required to complete the alignment and straightening.⁴¹

Cigarette smoking was also chosen because it is the most common form of nicotine delivery to the body according to the World Health Organization. Furthermore, there is no difference in the effect of nicotine according to the way it is delivered into the body.³²

The smoking dose was set at ≥20 cigarettes to avoid the effect of the smoking dose on the accuracy of the assessment of root resorption and changes in the alveolar bone structure that occurred during orthodontic movement. Many studies have considered those who smoke ≥20 cigarettes to be heavy smokers.³¹

Finally, the CBCT imaging method was chosen because according to previous studies, CT is one of the most accurate methods for evaluating bone resorption compared with traditional methods.⁴² Additionally, a study by Timock et al.⁴³ indicated that CBCT images could be used to accurately assess the thickness and height of the alveolar ridge.

Effect of smoking on cortical bone thickness

The results of this study showed that smoking had a detrimental effect on cortical bone thickness as shown by the 19.8% decrease in cortical bone thickness in smokers compared with the 10.1% decrease in nonsmokers.

These findings may be explained by the ability of nicotine to influence bone metabolism. Several laboratory studies have shown that nicotine stimulates the formation and differentiation of osteoclasts, while it suppresses the activity of osteoblasts and thus reduces the amount of osteogenesis.^44,45 These findings are in agreement with the results of a study by Ghadimi et al.,⁴⁶ which showed a correlation of smoking with decreases in bone mass and osteoporosis in the lumbar vertebrae and femur. They are also in agreement with the results of a review conducted by Yoon et al.,⁴⁷ which showed that tobacco consumption is a risk factor for bone fractures regardless of body mass and bone density. However, the results of the present study differ from the results of a study by Lee et al.,⁴⁸ which was conducted on experimental animals and showed no effect of nicotine on bone remodeling during orthodontic tooth movement. The reason for the difference in the study findings may be because their study was conducted on experimental animals.

Effect of smoking on cortical bone density

The results of this study showed that smoking had a detrimental effect on cortical bone density. A 23.5% decrease in cortical bone density occurred in smokers, whereas only a 17.2% decrease occurred in nonsmokers.

These results can be explained by the fact that nicotine upregulates osteolytic mediators such as interleukins 1 and 8 as well as the receptor activator of nuclear factor-κB (RANK) and its ligand (RANKL), which in turn stimulates the differentiation and activity of osteoclasts. Nicotine also downregulates osteoprotegerin, which affects the differentiation and activity of osteoblasts.^49–51 These results are similar to the results reported by Rosa et al.,⁵² who showed that smoking had a detrimental effect on both alveolar bone height and density when comparing smoking students and nonsmokers. Additionally, our findings are similar to the results of the above-mentioned review conducted by Yoon et al.,⁴⁷ which showed that smoking is associated with decreased bone density depending on the duration and dose of smoking, whereas they differ from the results of the study by Lee et al.,⁴⁸ which showed no effect of nicotine on alveolar bone density during orthodontic movement. As noted above, the reason for this discrepancy can be because this study was conducted on experimental animals.

Limitations

This study had several limitations. First, the number of cigarettes smoked per day was not accurate because the patients answered this question only approximately. Second, there was a slight distortion in some of the images taken after treatment because of the presence of braces. Third, the bone changes were evaluated only by CBCT images; no histological analysis was performed. Fourth, only the six lower anterior teeth were evaluated; multiple-root teeth should be evaluated in future studies. Finally, the sample size may be too small to generalize the results of this study. Future studies with larger sample sizes will be needed to confirm these results.

Clinical implications

Smokers undergoing orthodontic treatment should discontinue smoking because of its dangers to periodontal tissues. Furthermore, the orthodontist should pay particular attention to the forces and moments of orthodontic treatment in smoking patients.

Conclusions

In addition to all the known dangers of cigarette smoking, heavy smoking may also harm the alveolar bone by decreasing the bone thickness and density during orthodontic treatment.

ORCID iD

Ghaith F Sahtout https://orcid.org/0000-0001-7236-2850