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Aus der Poliklinik für Zahnerhaltung, Parodontologie, Endodontologie,
Präventive Zahnmedizin und Kinderzahnheilkunde
(Leiter: Prof. Dr. Thomas Kocher)
im Zentrum für Zahn-, Mund- und Kieferheilkunde
(Geschäftsführender Direktor: Prof. Dr. Reiner Biffar)
der Universitätsmedizin Greifswald
Estimating effects of craniofacial morphology on gingival recession and
clinical attachment loss
Inaugural – Dissertation
zur
Erlangung des akademischen
Grades
Doktor der Zahnmedizin
(Dr. med. dent.)
der
Universitätsmedizin
der
Ernst-Moritz-Arndt-Universität Greifswald
2017
vorgelegt von: Loutfi Salti
geb. am: 26.11.1957
in: Damaskus, Syrien
2
Dekan: Prof. Dr. rer. nat. Max P. Baur
1. Gutachter: Prof. Dr. Ralf Radlanski
2. Gutachter: Prof. Dr. Thomas Kocher
Ort, Raum: Universität Greifswald, Hoersaal-Zahnklinik
Tag der Disputation: 23.01.2018
3
List of contents
List of abbreviations………………………………………………………………………………..4
Chapter 1 Introduction……………………………………………………………………………..5
Chapter 2: Background and literature review……………………………………………………...6
2.1 Craniofacial morphology...…………………………………………………………. 6
2.1.1 Classification of craniofacial morphology………………………………………....6
2.1.2 Craniofacial morphology, aging and gender……………………………………….7
2.2 Gingival biotype...........................................................................................................7
2.3 Gingival recession……………………………………………………………………8
2.4 Long face (leptoprosopic) vs. short face (euriprosopic)...............................................8
2.5 Face morphology, gingival biotype and gingival recession………………………… 9
2.6 MRI and craniofacial landmarks……………………………………………………...9
Chapter 3: Aims and Objectives…………………………………………………………………….. 10
Chapter 4: Materials and Methods……………………………………………………………………11
4.1 Subjects and Study of Health in Pomerania.................................................................... 11
4.2 Periodontal assessmen......................................................................................................11
4.3 MRI data and landmark identification........................................................................... 12
4.4 Exclusion criteria……………………………………………………………………… 14
4.5 Covariates……………………………………………………………………………….15
4.6 Statistical analyses…………………………………………………………………….. 16
Chapter 5: Results…………………………………………………………………………………… 17
Chapter 6: Discussion……………………………………………………………………………….. 21
Financial support and permission license…………………………………………………………… 23
References…………………………………………………………………………………………… 24
Abstract ……………………………………………………………………………………………... 33
License copyright transfer agreement ………………………………………………………………..34
Eidesstattliche Erklärung …………………………………………………………………………….35
Acknowledgment ...…………………………………………………………………………………. 36
4
List of abbreviations
CAL Clinical Attachment Loss
CI Confidence Interval
DICOM Digital Imaging and Communication in Medicine Format
GR Gingival Recession
GEDAS Greifswald Digital Analyzing System
ICC Intraclass Correlation Coefficient
MRI Magnetic Resonance Imaging
SHIP Study of Health in Pomerania
SD Standard Deviation
5
Relationship between Craniofacial Morphology and Gingival Recession and Clinical
Attachment Loss
Chapter 1: Introduction
Biomedical research has started to relate craniofacial morphology with hormonal environments,
sexual dimorphism and with various other phenotypes in the context of dentistry. The study of
craniofacial morphology is valuable in reconstructive plastic surgery of the face, because face
morphology plays an important role in diagnostic comprehension between patient and normal
populations. Consideration of facial type also plays a key role in the formulation of an orthodontic
treatment plan and prognosis of treatment. Many studies revealed significant correlations between
facial morphology and dental characteristics and maxillofacial structures. Of particular importance is
the vertical relationship, that is, whether an individual is long-faced (leptoprosopic), or short-faced
(europrosopic). The vertical facial type provides a clue regarding the growth direction of the facial
complex. Several factors are associated with gingival recession, whose etiology is complicated.
Amongst others the gingival biotype is a significant risk factor for developing recession, particularly
the thin gingival type (Baker et al., 2002). In this study, we investigated the relationship between
craniofacial morphology and gingival recession and clinical loss attachment. The results obtained will
help to analyze which face type is more prone to gingival recession.
6
Chapter 2: Background and literature review
2.1 Craniofacial morphology
The craniofacial morphology is a complex non-linear system with inter-individual morphological
phenotypic variations. It is determined both by genetic and environmental factors. Facial height is
considered more heritable than other craniofacial traits (Carson, 2006). During development, growth
and shape of the human craniofacial structures are determined by cartilaginous, sutural, and periosteal
and endosteal growth processes in many locations in the craniofacial region. Growth of the
craniofacial structures, including oral soft and hard tissues must take place in proper coordination. It
is generally considered that the various growth processes do not proceed autonomously but mutually
influence each other (Weijs & Hillen, 1986). Recent study refered the high heritability of the facial
phenotype to a large number of DNA variants with relatively small individual effect size (Fan Liu,
2012). Historically, several studies of craniofacial morphology types were performed in the context
of dentistry. It was suggested that, the vertical dimension of the craniofacial morphology was
affected by bite force (Ringqvist, 1973). Christie et al. (1977) concluded that subjects with normal
occlusion tend to have shorter face types than long face patterns. Study of the relationship between
masseter muscle size and craniofacial morphology showed variation in muscle size and facial types
(Raadsheer et al., 1996). The correlation between craniofacial morphology and dentoalveolar bone
heights was confirmed (Beckmann et al.,1998). Variations in alveolar bone thickness were confirmed
between facial phenotypes (Tsunori et al., 1998 and Gracco et al.2009). Furthermore, variations in
buccolingual molar inclination were reported between craniofacial morphology types (Masumoto et
al.2001). Relationship between craniofacial morphology and upper and lower arches was documented
(Forster et al., 2008). The effect of face growth pattern on clincal crown length was reported (Öncag
et al., 2011). Recently, TMJ morphology and facial types revealed significant relations (Sleiman et
al., 2015).
2.1.1 Classification of craniofacial morphology
According to anthropometric measurements, facial morphology can be classified as
hypereuriprosopic (very short broad face), euriprosopic (short broad face), mesoprosopic (medium or
intermediate face), leptoprosopic (long face) and hyperleptoprosopic (very long narrow face)
(Williams et al., 1995). From an orthodontic view of point, in the light of cephalometric
radiographical results, the face morphology classifications only take the facial profile for
7
classification. Hence, face width is not included in most classifications. The terms brachyfacial,
dolichofacial and mesofacial are commonly used by orthodontists (Bishara et al., 1985).
2.1.2 Craniofacial morphology, aging and gender
Several studies postulated, that the craniofacial complex size was larger in adult males than in
females (Wellens et al., 2013). This difference is influenced by hormons, longer development and
larger body size (Wood et al., 1991). The aging process affects the craniofacial skeletal, or more
specifically, bony remodeling which occurs throughout life. This is reflected in the continuous
increase in certain facial anthropometric measurements with age such as the nasion-to-anterior nasal
spine and the facial width (Bartlett et al., 1992). The increase in the total anterior facial height is
attributed to an increase in the lower face height (Schendel et al., 1985). However, most of these
changes range in the magnitude from 1.1 to 1.60 mm (Albert et al., 2007). The difference in the
amount of anterior face height growth between the sexes was confirmed (Fudalej et al., 2007 ). The
increase in the anterior face height between ages 12-50 years was greater in males than in females,
however, the difference decreased siginificantly after the second decade. Another study indicated,
that males and females express similar proportional trends in the increase of total anterior face height
in the late adulthood (West et et al., 1999), whereas recent studies reported sexual dimorphism in
facial width-to-length ratio, with males showing higher ratio than females (Weston et al., 2007). This
difference can be explained by testosterone hormone influence on the facial bone size, particularly
facial width within men (Lefevre et al., 2013). It was reported that about 1 mm of the increase in the
anterior face height mihgt be due to to continued eruption of the maxillary incisors (Forsberg et al.,
1991). ). The continuous eruption occurs between the 25th and the 45th year (Levers et al., 1983).
Study of individuals with no attrition or moderate attrition revealed slow continuous deposition of
bone at the lower border of the mandible which accounts for the increased face length of older
individuals (Levers et al., 1983). Behrents (1985) documented that the increase in facial height is
attributed to combination of the continued eruption of the teeth along with downward movement of
the maxilla and thus the anterior nasal spine. We reviewed the literature and we identified an absence
of reliable evidence describing effects of craniofacial morphology on gingival recession and clinical
attachment loss.
8
2.2 Gingival biotype
Gingival biotype describes varying gingival thickness in the faciopalatal / faciolingual dimension.
According to Siebert gingival biotype can be classified into thick / flat and thin / scalloped biotypes
(Seibert & Lindhe, 1989). Thick gingival biotype usually depicts flat gingiva contour, dense and
fibrotic tissue , whereas the thin gingival biotype is delicate with highly scalloped soft tissue (Claffey
& Shanley, 1986). The structure of the thick biotype indicates thick underlying bony architecture and
is more resistant to gingival recession. However, non-inflamed sites with a thin biotype are moreover
associated with more recession than those sites with a thick biotype (Claffey & Shanley, 1986). A
thick gingival biotype was found more prevalent in majority of the population (Olsson et al., 1991).
Claffey et al. proposed thickness not more than 1.5 mm as a thin biotype while more than 2 mm as a
thick biotype (Claffey & Shanley, 1986). The thinner biotype is more prevalent in females (Müller et
al., 2000). Studies on humans revealed that the gingival thickness varies according to the dental arch,
gender, and age (Vandana et al., 2005). Various studies documented associations between gingival
biotype, bone morphology and teeth dimensions (Zweers et al., 2014). Cook et al. concluded that a
significant correlation existed between labial plate thickness and gingival biotype (Cook et al., 2011).
It has been reported that the thick gingival biotype was associated with square tooth shape while thin
gingival biotype was associated with triangular tooth shape (Ochsenbein et al., 1969). Moreover,
thick gingival biotype was associated with short-wide tooth form (Müller & Eger,1997).
2.3 Gingival recession
Gingival recession (GR) is described as the migration of the gingival margin apically from the
cemento-enamel junction (CEJ), which may be observed on all surfaces of the tooth (Glickman and
Carranza 1979). However, heretofore, the mechanism of GR is not completely understood. Over the
last decades, several causative factors were identified. There is evidence that recession increased both
in prevalence and severity with increasing age (Kassab & Cohen, 2003) and with male gender
(Albandar, 2002). Some authors suggested tooth malposition (Wennstrom et al., 1987, Stoner &
Mazdyasna, 1980) and tooth position in the arch as risk factors for recession (Gorman, 1967). Studies
have shown that the cervical convexity of the crown affects the gingival margin, a tooth with
pronounced cervical convexity results in a gingival margin located more apically (Morris. 1958).
Others proposed that the mechanism of recession is of inflammatory nature (Kassab & Cohen, 2003).
The thin gingival biotype with a delicate marginal tissue has been postulated to play a role in
9
recession. Gingival recession is seen both in populations with high and poor standards of oral hygiene
(Wennström et al., 2003). Other etiologic factors include tooth brushing trauma (Kassab & Cohen,
2003), mechanical trauma, local irritants, iatrogenic restorative treatment and aberrant frenum
attachments.
2.4. Long face (leptoprosopic) vs. short face (euriprosopic)
From an orthodontic point of view, the long and short anterior face differentiates in many aspects.
The long face type is characterized by greater maxillary and mandibular anterior alveolar and basal
height with greater lingual inclination of the lower incisors than the short face type (Arruda et al.,
2012, Bhishek et al., 2012). This suggests a compensatory mechanism for increased facial vertical
dimensions with reduced labiolingual dimensions of the basal and alveolar bone in the anterior part of
both jaws. Moreover, long face subjects have a longer dentoalveolar height in the molar region
(Martina et al., 2005). In contrast to long face types the short face individuals have a smaller
mandibular alveolar height (Adam et al., 2011). An individual with a short broad face type has
stronger or thicker mandibular elevator muscles than inviduals with a long face type and hence can
have an increased mechanical loading of the jaws (Kiliaridis, 1995). Hence, individuals with long
face pattern have thin alveolar bone thickness (Horner et al., 2012, Sato et al., 2005). Evaluation of
the relationship between morphological characterstics of the mandible and face type revealed, that
the buccal cortical bone was thicker in short-faced subjects than in the average and long-faced
individuals (Tsunori et al., 1998). Furthermore, inclination of teeth in the short-faced group was
likely more lingually than in the average- and long-faced groups. Another study reported, that buccal
and lingual cortical plate thickness was thicker in the sections of the first molar and second molar in
short face individuals than in the average and long face subjects (Masumoto et al., 2001). Long face
type individuals have more vertical facial growth, whereas short face types have reduced vertical
growth (Field et al., 1984). In the context of arch width, upper and lower arch widths in long face
group are smaller (Apivatanagul et al., 2004), therefore, the dental arches often exhibit crowding of
the teeth.
2.5 Face morphology, gingival biotype and gingival recession
Few studies have been conducted to study the relationship between facial morphology and
periodontal structures. So far, there is one anthropological study evaluating the relationship between
facial morphology and GR based on Australian aboriginal skulls (Danenberg et al., 1991), but further
10
studies from population-based studies are lacking. Anthropological studies documented that severe
attrition which has an association with age, often resulted in almost complete destruction of
anatomical crowns. However, continous tooth eruption provided a partial explanation for the
mechanism for maintenance of face height. This process resulted in loss of periodontal attachment as
less root surface is embedded within the bone (Danenberg et al. , 1991). Masahiro et al. (1998)
reported that the buccal cortical bone plate of the mandibular molars was thicker in the short facial
type than average or long facial types. Many studies found no correlation between facial morphology,
respective Angle’s classification of malocclusion and periodontal structures (Alzoubi et al. 2008 and
Zawawi et al., 2012).
2.6 Magnetic Resonance Imaging (MRI) and craniofacial landmarks
MRI is a noninvasive, nonradioactive technique of evaluating the human body. MRI technology
depends on release of pulses of radio waves through the body, causing “excitement” in hydrogen
atoms in the body cells. When the radio waves stop, the hydrogen atoms relax and release energy.
Different parts of the body have characteristic patterns of how they are affected by the radio waves;
these patterns are displayed on a computer monitor as pictures of the anatomy of the body. MRI
provides very detailed images of soft tissues like the brain. However, air and hard bone do not give
an MRI signal so these areas appear black. Bone marrow, blood and soft tissues vary in intensity
from black to white, depending on the amount of fat and water present in each tissue. The face is
considered a 3D structure. Therefore, the three-dimensional image reformation in three planes of
space (x, y and z) provides a more accurate representation of the craniofacial morphology than the
two-dimensional cephalometric methods. MRI offers a new method of cephalometry with potential to
carry out landmark identification and planes on three-dimensional (3D) reconstructed images (Eley
et al., 2013).The ability of conventional MRI to distinguish hitherto used cranial anthropometric
landmarks was confirmed by Cotton et al., 2005, who studied MRI images sequences and concluded
that these sequences permitted visualization of the cephalometric landmarks. The high contrast
between bone and soft tissue on MRI provides accurate 3D craniofacial measurements (Goto et al.,
2007). The study of reproducibility of craniofacial landmarks on MRI showed high inter- and intra-
examiner reproducibility (Daboul et al., 2012).
11
Chapter 3: Aims and Objectives
The present study aimed to investigate the relationship between certain craniofacial parameters and
gingival recession as well as clinical attachment loss in a general population sample. We hypothesize,
that the facial morphology is related to gingival recession and to clinical attachment loss. We
evaluated the following hypothesis:
A broad face is associated with less gingival recession (GR) and clinical attachment loss (CAL) than
a long face.
12
Chapter 4: Materials and Methods
4.1 Subjects and Study of Health in Pomerania
The Study of Health in Pomerania (SHIP) is a population-based longitudinal survey conducted in the
northeast of Germany (West Pomerania) (Hensel et al., 2003, John et al., 2001). The subject selection
is illustrated in figure 1. The final sample consisted of 556 subjects with: i. readable MRI head
scans, ii. periodontal data and iii. covariates data from SHIP2 (Figure 1). The SHIP study protocol
including the MRI and dental examinations was approved by the local ethics committee of University
of Greifswald and written informed consent was obtained from all the subjects who agreed to
participate.
4308
• Participants (SHIP-0) aged 20-81 years . The study was conducted between 1997 - 2001
3300
• participated in the 5-year follow-up (SHIP-1) aged 25 – 85 years. The study was conducted between 2002 - 2006
2333
• Particiantants SHIP 2 follow up 11 year aged 26 – 78 years.The study was conducted between 2008 - 2012
1115• whole body MRI
719
• After excluding 396 with unreadable MRIs and excluding 40 double entries
556
• -No linking with MRI data: N=38
• -No information on gingival recession: N=83
• -No information on confounders: N=1
• -No information on posterior support: N=1
Figure 1: Flow chart: inclusion and exclusion criteria for participants
from the Study of Health in Pomerania (SHIP-0, SHIP-1 and SHIP-2)
4.2 Periodontal assessment
The periodontal parameters PD, GR and CAL were assessed according to the half-mouth technique
(excluding third molars) at four sites per tooth (mesiobuccal, distobuccal, midbuccal, and
midlingual/midpalatal), using a periodontal probe (Hu-Friedy, Chicago, IL, USA). The diameter for
PCP11 was 0.48 mm and the probing force was about 0.3 to 0.5 N. PD was measured from the
gingival margin to the base of the periodontal pocket. GR was measured from the CEJ to the gingival
margin. CAL represents the distance from the CEJ to the periodontal pocket base. According to the
positional relation of gingival margin and CEJ, GR could have a positive or a negative value. When
13
the CEJ was visible, CAL and PD were measured directly and GR (positive value) was obtained as
CAL-PD. Otherwise, GR (negative value) and PD were measured directly and then CAL was
calculated as PD+GR. If the determination of the CEJ was indistinct because of wedge-shaped
defects, fillings or crown margins, CAL was not recorded. Mean GR values were calculated on a
subject-level. The percentage of sites with recession ≥2 mm or ≥ 3 mm was considered as alternative
outcome. All examiners were initially trained and calibrated prior to the study. Further calibration
exercises on an independent test group were performed every 6 - 12 months during the course of the
study. For CAL assessments, intra-class correlations of 0.76 - 0.88 per examiner and an inter-class
correlation of 0.74 were achieved.
4.3 MRI data and landmark identification
4.3.1 MRI data
The MRI head studies were performed using the same system (Magnetom Avanto; Siemens Medical
Solutions, Erlangen, Germany - 1.5 Tesla) as a part of a whole-body MRI protocol in the SHIP center
for magnetic resonance research at the University of Greifswald. The complete whole body MRI
protocol was previously described in Hegenscheid et al., 2009. The analyzed MRI sequence was an
axial T1-weighted head scans (ultra-fast gradient echo sequence) using following imaging
parameters: repetition time, 1900 ms; echo time 3.37 ms; flip angle 15o; matrix, 176 x 256 x 176
acquisition matrix; voxel size 1 x 1 x 1 mm. The postprocessing of the axial T1-weighted head scan
resulted in a multi-planar reconstruction (MPR) with 3 mm slice thickness for further interpretation.
4.3.2 Landmarks
Three-dimensional (3D) analyses of the craniofacial area were performed through selecting a set of
predefined landmarks (Figure 2) and subsequently defined distances were calculated (Table 1and 2).
Table 1: craniofacial landmarks
Landmark Definition
Anterior nasal spine
(ANS)
The tip of the bony anterior nasal spine at the inferior margin of the piriform
aperture, in the midsagittal plane.
Nasion (N) The intersection of the internasal and frontonasal sutures, in the midsagittal
plane.
Zygion (Zy) The most lateral point on the zygomatic arch.
Eurion (Eu) The most lateral point of the parieto-temporal region of the skull.
Menton (Me) The most inferior point of the mandibular symphysis, in the midsagittal plane.
14
Table 2: calculated distances between craniofacial landmarks
Distance Description
Eu-Eu Maximal cranial width
Zy-Zy Facial width
N-ANS upper facial height
ANS-Me Lower facial height
N-Me Total facial height
A B C Nasion Eurion-Eurion Zygion-Zygion
Anterior nasal spine Zygion-Zygion
Menton
Figure 2: MRI scans of the head show the craniofacial landmarks.
According to Williams et al. the prosopic facial index was categorized in five categories, ranging
from broad to long faces (Figure 3).
Classification of facial morphology
hypereuriprosopic
very short broad
euriprosopic
short broad
mesoprosopic
mediumleptoprosopic
long
hyperleptoprosopic
very long narrow
Prosopic index * (facial index) =Face length
Face widthX 100
Hypothesis: a long narrow face is associated with
more recession and attachment loss than a broad square
face.
Ba
ckg
rou
nd
3* Williams et al (1995) Skeletal system. In: Gray’s anatomy, 38th edition, pp. 607-612. London: Elbs with Churchill Livingston.
Hypereuriprosopic euriprosopic mesoprosopic leptoprosopic Hyperleptoprosopic
< 79.9 80 – 84.9 90 – 94.9 90 – 94.9 > 95
very short broad short broad medium long very long narrow
Figure 3: Prosopic facial index (Prosopic facial index = (total facial height / face width)*100).
15
In order to analyze MRI data, an open source DICOM viewer Osirix software (version 3.8.1, 64 bit,
Pixmeo Sarl, Bernex, Switzerland) was used on two workstations with 27 inch monitors (iMac Quad
core i7; Apple Corp. Cupertino, CA, USA). Three dimensional coordinates for each image were
calculated from the DICOM headers which were based on the MRI scanner coordinates. The
coordinates (x, y, z) for each voxel were defined by Osirix and the actual calculated size of voxels
was converted to millimetres. In each MRI head scan, the X-axis represented the right-left direction,
the y-axis and z-axis corresponded to the posterior-anterior and superior-inferior directions
respectively. This predetermined system of three axes is always the same when the same set of
images is uploaded to the software. Since a selected point will give the same (x, y, z) value in any
new rendered slice view, T1-weighted MPR were used to accurately identify the predefined
landmarks included in this analysis. Sagittal, axial, and coronal rendered slices, as well as the 3D
image reconstruction were used to determine the 3D positional coordinates of each landmark based
on its anatomical position. Distances between landmarks were later calculated by activating a script
with the formula:
Landmark detection and identification was performed by 3 examiners over a period of 6 months. All
examiners were well trained dentists in the use of Osirix software and craniofacial landmark
identification. For investigator blinding, the images were identified by code and analyzed
anonymously in random order. Inter-examiner reproducibility was assessed by using intraclass
correlation coefficients (ICC) (Table 4). Following the recommendation by Shrout & Fleiss (Shrout
& Fleiss, 1979), ICC Shrout & Fleiss model (2.1) (Shrout & Fleiss, 1979) was used to assess if the
standardized reading procedure can be effectively used by a variety of readers. Intra -examiner
reproducibility of all landmarks identification in respect to the three coordinates (x, y and z )
showed excellent agreement with ICC values ranging from 0.94 to 0.999.
Table 4: Intra-Examiner Reproducibility- Intra-class Correlation
Landmark X coordinate Y coordinate Z coordinate
Nasion 0,95 (0,90-0,98) 0,96 (0,77-0,99) 0,97 (0,86-0,99)
ANS 0,99 (0,98-0,99) 0,94 (0,88-0,97) 0,96 (0,71-0,98)
Eurion R 0,94 (0,86-0,97) 0,95 (0,83-0,98) 0,97 (0,85-0,99)
Eurion L 0,97 (0,94-0,98) 0,96 (0,81-0,99) 0,97 (0,86-0,99)
Zygion R 0,98 (0,91-0,99) 0,98 (0,96-0,99) 0,99 (0,99-0,99)
Zygion L 0,98 (0,93-0,99) 0,99 (0,98-0,99) 0,99 (0,99-0,99)
Menton 0,99 (0,97-0,99) 0,99 (0,96-0,99) 0,98 (0,93-0,99)
16
4.4 Assessment of exclusion criteria
Subjects with full arches were selected to ensure the posterior support and to exclude the impact of
occlusal collapse on face morphology. We used GEDAS bites which displayed the extent and
localization of occlusal contact in intercuspation position based on digitized silicone registrations.
GEDAS has been successfully used within the scope of SHIP (Hützen et al., 2006). A mush bite of
extra-hard silicone (Greenbite apple, Detax, Ettlingen, Germany) was taken in habitual occlusion and
first scanned with transmitted light to visualize the occlusal contacts, and thereafter, with incident
light to record the tooth contours. The two resulting images were then edited and superimposed using
the software Adobe Photoshop (V7.0, Adobe Systems, San Jose, USA) (Figure 4). We used GEDAS
bites which displayed the extent and localization of occlusal contact in intercuspation position based
on digitized silicone registrations. A complete arch was defined as presence of natural teeth
(including natural teeth, crowned teeth and crowned implants) or fixed dentures in the region
extending from first premolar- to second molar in each quadrant. Participants with removable
prosthodontic appliances were excluded from this study. Three subjects without posterior support
were excluded from the study. The occlusal contact bites were scored according to the following
findings:
1 = presence of at least one premolar and at least one molar with occlusal contact in the
region of tooth 4 to 8 on the left and right side.
0 = no contact.
9 = missing tooth with no gap.
8 = missing tooth with gap > 3 mm.
7 = missing tooth with gap ˂ 3 mm.
(.) = deformed tooth.
Furthermore, the scoring system presence of prosthesis / crown / implant was as the following:
1 = presence of prosthesis / crown / implant .
0 = no prosthesis / crown / implant.
17
Upper dentiation Lower dentition
Figure 4: Greifswald Digital Analyzing System bites (GEDAS ) show the occlusal contacts.
4.5 Covariates
Education: Socio-demographic and behavioral risk factors were assessed by computer assisted
interviews. The socio-economic status was defined as <10, 10 and >10 years of school education.
Smoking status: Participants were categorized into never smokers, former smokers and current
smokers.
Oral care: Oral health behavior was assessed via dental visits during the last 12 months (yes/no) and
tooth brushing frequency (3 times/day, 2 times/day, < 2 times/day).
Waist circumference: Waist circumference was measured in cm using an inelastic tape.
Diabetes mellitus: Diabetes was defined as self-reported physician's diagnosis or antidiabetic
treatment (Anatomical Therapeutic Chemical Classification System (ATC) code A10) or non-fasting
glucose levels ≥11.1 mmol/l or glycated hemoglobin (HbA1c) concentrations of ≥48 mmol/mol.
Orthodontic treatment: Subjects were asked, if they had orthodontic treatment in adolescence.
4.6 Statistical analyses
Descriptive statistics was used to evaluate means and standard deviations (SD) for continuous data
and assessment of frequency distributions for categorical data. Associations between MRI distances
and periodontal variables were analyzed using linear regression models adjusting for age and gender.
To calculate mean GR and mean CAL on subject level, either all teeth or incisors and canines or
premolars and molars were considered. In addition to models including exposures as continuous
variables, the facial indexes were categorized into five categories (Williams et al., 1995). Regression
coefficients (B) with 95% confidence intervals (CI) were reported. Model assumptions were checked
analytically and graphically. As sensitivity analysis, the main analyses were repeated including age,
18
gender, education, smoking status, diabetes, waist circumference, tooth brushing frequency and any
dental visit within the last 12 months. Further sensitivity analyses were performed restricting analyses
to subjects without orthodontic treatment, or to subjects with posterior support but without
bridgework. All analyses were performed using STATA/SE 13.0 (Stata Corp, 2013) and two-sided
P-values < 0.05 were considered statistically significant.
19
Chapter 5: Results
5.1 SHIP sample characteristics
The results obtained following statistical analyses are depicted in Table 5. The mean age was about
56 years and did not vary across the groups. Results indicate that, the higher the facial index, the
more pronounced were mean GR and mean CAL, irrespective of the type of teeth considered.
Subjects belonging to the long narrow facial type had about 0.3 mm more GR and 0.5 mm more CAL
as compared to subjects with broad square faces (considering all teeth).
Table 5: Characteristics of study subjects according to their facial index.
Facial index
<80 (broad) 80-84.9 85-89.9 90-94.9 ≥95 (long)
N=41 N=107 N=192 N=145 N=71
General properties
Age, years 57.5±11.5 54.6±12.7 55.5±11.1 55.1±12.3 56.8±11.7
Male gender 41.5%* 45.8%* 48.4%* 53.8% 64.8%
Education
<10 years 31.7% 14.0% 15.1% 18.6% 14.1%
10 years 36.6% 54.2% 57.3% 60.7% 64.8%
>10 years 31.7%* 31.8% 27.6% 20.7% 21.1%
Smoking status
Never 53.7% 44.9% 41.7% 35.9% 35.2%
Former 31.7% 41.1% 41.2% 44.8% 46.5%
Current 14.6% 14.0% 17.2% 19.3% 18.3%
BMI, kg/m2 27.9±4.7 27.6±4.3 27.6±4.1 28.1±4.3 27.3±4.1
Waist circumference, cm 91.6±12.7 89.0±11.5 89.7±12.8 91.5±12.2 91.1±13.0
Diabetes 7.3% 6.5% 6.8% 6.2% 4.2%
Oral care
Tooth brushing
3 times/day 9.8% 6.5% 7.8% 11.0% 7.0%
2 times/day 85.4% 85.1% 78.1% 75.9% 78.9%
<2 times/day 4.9% 8.4% 14.1% 13.1% 14.1%
Dental visit within the last 12 months 92.7% 94.4% 94.3% 93.8% 94.4%
Control-oriented oral health behaviour 92.3% 94.4% 91.7% 93.1% 90.1%
Oral health
Number of teeth 22.5±5.9* 22.7±4.7* 21.6±6.0 21.7±5.5 20.0±6.6
Mean GR, mm 0.32±1.2 0.13±1.0* 0.30±1.1 0.30±1.1 0.66±1.5
Mean GR, incisors and canines, mm 0.07±1.1 0.04±1.1* 0.19±1.2 0.27±1.2 0.52±1.4
Mean GR, premolars and molars , mm 0.41±1.2 0.20±1.1 0.38±1.2 0.18±1.0 0.65±1.5
Mean CAL, mm 2.8±1.6 2.6±1.2* 2.9±1.6 2.9±1.3 3.3±1.8
Mean CAL, incisors and canines, mm 2.3±1.3* 2.4±1.3* 2.6±1.6 2.7±1.4 3.0±1.8
Mean CAL, premolars and molars , mm 3.0±1.6 2.8±1.2* 3.0±1.6 2.9±1.3* 3.6±1.9
MRI distances
Eurion-Eurion, mm 157.0±7.5* 154.6±7.7 154.4±8.5 153.5±8.4 153.0±7.4
Zygion-Zygion, mm 130.8±5.6* 129.3±5.9* 127.8±6.0 127.4±6.5 126.7±6.1
Nasion-ANS, mm 45.3±4.0* 47.4±5.6* 48.7±4.6* 49.8±4.4 51.1±5.2
Nasion-Menton, mm 100.9±4.6* 107.1±5.3* 112.1±5.5* 117.5±6.3* 124.3±7.0
ANS-Menton, mm 56.1±5.5* 60.3±5.4* 63.9±5.1* 68.3±5.9* 73.9±6.7
Subject’s characteristics are presented as mean ± standard deviation or percentages. P values were retrieved from Mann-
Whitney U tests or Chi squared tests. *p<0.05 for comparison with the highest facial index group (≥95).
20
5.2 MRI distances
Distances were found to increase across increasing quartiles of distances (Table 6). MRI distances
did not materially differ between the complete cohort and subjects without orthodontic treatment, and
between subjects with posterior support but no fixed prostheses or subjects with a complete arch
respectively (Table 7).
Table 6: Summary of MRI distances and the facial index in study subjects for all subjects (N=556)
Range within quartiles
MRI distances Q1 Q2 Q3 Q4
Width measures (mm)
Eurion-Eurion 133.7-147.8 147.9-153.9 154.0-159.7 159.9-175.4
Zygion-Zygion 111.1-123.2 123.2-128.0 128.0-132.1 132.2-148.0
Height measures (mm)
Nasion-ANS 36.1-45.2 45.2-49.0 49.0-52.0 52.1-67.4
Nasion-Menton 91.0-107.1 107.2-112.9 113.0-119.0 119.1-140.2
ANS-Menton 41.5-60.2 60.2-64.8 64.8-69.6 69.6-89.0
Data are presented as mean ± standard deviation or numbers (percentages). Also, for continuous measures, the range
(min-max) is given for quartiles (Q1-Q4).
Table 7: Summary of MRI distances and the facial index within specific subsamples applying
different restrictions regarding the dental status.
MRI distances I. Without orthodontic
treatment (N=443)
II. With posterior support
and no prosthesis (N=279)
III. with posterior support
as complete arch (N=97)
Width measures(mm)
Eurion-Eurion 154.7±8.2 155.2±8.2 154.2±8.0
Zygion-Zygion 128.3±6.1 128.4±6.4 127.5±6.5
Height measures(mm)
Nasion-Menton 113.5±8.5 112.9±8.2 111.8±7.8
ANS-Menton 65.1±7.5 65.0±7.0 63.7±6.8
Nasion-ANS 48.9±5.0 48.5±4.7 48.7±4.5
Indices
Facial index
<80 (broad) 35 (7.9%) 22 (7.9%) 8 (8.3%)
80-84.9 83 (18.7%) 60 (21.5%) 21 (21.7%)
85-89.9 155 (35.0%) 104 (37.3%) 34 (35.0%)
90-94.9 116 (26.2%) 67 (24.0%) 29 (29.9%)
≥95 (long) 54 (12.2%) 26 (9.3%) 5 (5.1%)
Facial index 88.5±5.9 88.0±3.6 87.8±5.1
5.3 Association between MRI distances and periodontal variables
A significant trend in GR and CAL was found for categories of the facial index, the higher the facial
type category (longer face) the more pronounced were GR and CAL whereby the extent of the
observed association varied across the different types of teeth (Table 8). Considering MRI measures
21
as quartiles led to similar results (Table 9). Restriction to subjects without orthodontic treatment
(N=443) or to subjects with posterior support but without bridgework (N=279) did not materially
change the presented results (data not shown).
Table 8: Regression coefficients from linear models of mean gingival recession and mean clinical
attachment loss on MRI distances. Models include all teeth or specific subgroups.
Mean gingival recession Mean clinical attachment loss
MRI
distances
All teeth
N=556
Incisors and
canines
N=547
Premolars and
molars
N=487
All teeth
N=556
Incisors and
canines
N=547
Premolars and
molars
N=487
Width measures (mm)
Eurion-
Eurion
-0.016 (-0.030;-
0.003)*
-0.016 (-0.030;-
0.002)*
-0.018 (-0.033;-
0.003)*
-0.023 (-0.040;-
0.005)*
-0.021 (-0.039; -
0.003)*
-0.026 (-0.045; -
0.006)*
Zygion-
Zygion
-0.009 (-
0.027;0.010) -0.013 (-0.032;0.005) -0.0003 (-0.022;0.021)
-0.016 (-
0.040;0.008) -0.017 (-0.042;0.007) -0.011 (-0.038;0.016)
Height measures (mm)
Nasion-ANS 0.014 (-0.004;0.032) 0.019 (0.0002;0.037)* 0.004 (-0.018;0.026) 0.017 (-0.007;0.041) 0.021 (-0.003;0.045) 0.012 (-0.015;0.040)
Nasion-
Menton 0.008 (-0.003;0.020) 0.011 (-0.001;0.023) 0.005 (-0.008;0.019) 0.009 (-0.006;0.024) 0.014 (-0.001;0.030) 0.010 (-0.007;0.027)
ANS-Menton 0.003 (-0.009;0.015) 0.004 (-0.008;0.017) 0.003 (-0.011;0.017) 0.002 (-0.013;0.018) 0.006 (-0.010;0.023) 0.005 (-0.013;0.022)
Prosopic face index
<80 (broad) 0.00 (ref.) 0.00 (ref.) 0.00 (ref.) 0.00 (ref.) 0.00 (ref.) 0.00 (ref.)
80-84.9 0.049 (-0.402;0.303) 0.092 (-0.281;0.464) -0.036 (-0.430;0.358) -0.085 (-
0.554;0.384) 0.186 (-0.300;0.672) -0.088 (-0.586;0.409)
85-89.9 0.067 (-0.263;0.397) 0.202 (-0.148;0.552) 0.095 (-0.273;0.462) 0.134 (-0.305;0.574) 0.384 (-0.072;0.841) 0.162 (-0.302;0.626)
90-94.9 0.087 (-0.253;0.427) 0.285(-0.075;0.645) -0.079 (-0.460;0.302) 0.144 (-0.309;0.596) 0.432 (-0.038;0.901) 0.040 (-0.440;0.521)
≥95 (long) 0.353 (-0.024;0.731) 0.456 (0.057;0.855)* 0.312 (-0.121;0.745) 0.472 (-0.031;0.974) 0.638 (0.118;1.158)* 0.556 (0.010;1.103)*
P trend 0.02 0.01 0.31 0.01 0.01 0.04
Regression coefficients are presented as B (95% confidence interval). Models were adjusted for age and gender; ANS,
anterior nasal spine; *p<0.05.
22
Table 9: Regression coefficients from linear models of mean gingival recession and mean clinical
attachment loss on quartiles of MRI distances (N=556).
Mean gingival recession
Quartiles of MRI
distances
1st 2nd 3rd 4th P
trend
Width measures
(mm)
Eurion-Eurion 0.00 (ref) -0.272 (-0.505;-0.038)* -0.250 (-0.517;0.016) -0.470 (-0.766;-0.174)* 0.004
Zygion-Zygion 0.00 (ref.) 0.075 (-0.160;0.309) -0.133 (-0.406;0.139) -0.036 (-0.338;0.266) 0.64
Height measures
(mm)
Nasion-ANS 0.00 (ref.) -0.066 (-0.302;0.169) 0.014 (-0.230;0.258) 0.126 (-0.129;0.381) 0.26
Nasion-Menton 0.00 (ref.) -0.070 (-0.300;0.159) -0.031 (-0.276;0.214) 0.328 (0.061;0.595)* 0.03
ANS-Menton 0.00 (ref.) -0.250 (-0.479;-0.020)* -0.085 (-0.319;0.149) 0.127 (-0.115;0.369) 0.18
Indices
Prosopic face index 0.00 (ref.) 0.070 (-0.159;0.299) 0.073 (-0.156;0.302) 0.361 (0.130;0.594)* 0.004
Mean clinical attachment loss
Quartiles of MRI
distances
1st 2nd 3rd 4th P
trend
Width measures
(mm)
Eurion-Eurion 0.00 (ref) -0.462 (-0.773;-0.152)* -0.295 (-0.649;0.059) -0.657 (-1.050;-0.264)* 0.004
Zygion-Zygion 0.00 (ref.) 0.040 (-0.273;0.352) -0.222 (-0.585;0.140) -0.201 (-0.603;0.201) 0.24
Height measures
(mm)
Nasion-ANS 0.00 (ref.) 0.100 (-0.214;0.414) 0.022 (-0.303;0.347) 0.154 (-0.186;0.495) 0.49
Nasion-Menton 0.00 (ref.) -0.052 (-0.354;0.251) -0.123 (-0.446;0.200) 0.303 (-0.050;0.657) 0.10
ANS-Menton 0.00 (ref.) -0.305 (-0.612;0.002) -0.070 (-0.382;0.242) 0.092 (-0.231;0.415) 0.35
Indices
Prosopic face index 0.00 (ref.) 0.191 (-0.114;0.496) 0.159 (-0.147;0.464) 0.491 (0.184;0.799)* 0.004
Regression coefficients are presented as B (95% confidence interval). Models were adjusted for age and gender; ANS,
anterior nasal spine; *p<0.05.
23
Chapter 6: Discussion
Results from this study suggest a significant relationship between craniofacial morphology,
specifically the facial index, and GR and CAL. The study confirms that, when including all teeth,
subjects belonging to the long narrow face type had more GR and CAL as compared to subjects with
the broad square facial type. Similar differences of GR and CAL were found after stratifying
according to incisors and canines or premolars and molars. It has been reported that subjects with a
larger than average cranial width usually have a broad, square and short face, whereas individuals
with narrower cranial width usually exhibit a narrow shaped head and a long narrow face (Musa et
al., 2014). Importantly, it is neither the facial length nor width that affects periodontal destruction, but
the ratio between height and width measurements. It was not expected that all height and most width
measurements were not associated with periodontal destruction. We could not explain at this point
why there was a significant inverse association between mean GR and CAL and maximum cranial
width (Eurion-Eurion) but not with facial width (Zygion-Zygion). We presumed that an underlying
biological process or growth relationship would cause this inverse association between cranial width
and GR and CAL, whereas facial width is indirectly associated with the periodontal markers through
its function as the denominator in the calculation of the facial index. After analyzing results of the
study, we can affirm that GR and CAL are more pronounced in long narrow faces. One possible
interpretation is subjects with a short face pattern are characterized by thicker alveolar ridge than
those with long face patterns (Tsunori et al., 1998, Garib et al., 2010) possibly due to the common
influence from the strong masticatory muscles (Kiliaridis et al., 1991, Satiroglu et al., 2005, Jonasson
et al., 2005, Denes et al., 2013). Furthermore, bone thickness and alveolar crest positions are related
to the gingival biotype (Cook et al., 2011, Fu et al., 2010) and the gingival biotype is, in turn,
associated with tooth shape. Müller concluded that subjects with a long narrow form of the maxillary
central incisors had a thinner scalloped biotype while subjects who had a thicker gingival biotype
were associated with a shorter and wider form (Müller and Eger, 1997). Another possible explanation
is the inverse relationship between the maxillary arch width and the face type. It has been
documented that as the face length increases, the maxillary arch width tends to decrease (Forster et
al., 2008). Chang stated that tooth size and maxillary arch width were determining factors in the
formation of dental crowding (Chang et al., 1986). Since tooth malposition causes difficulties in oral
hygiene and bacterial plaque retention and accumulation, this results in pathological periodontal
changes (Gusmao et al., 2011). Third explication is the facial growth and continuous eruption of the
24
teeth. It has been concluded by Forsberg that the total anterior face height increases by 1.60 mm in
both genders between 25-45 years on average of which 1 mm was related to a continuous eruption of
maxillary incisors (Forsberg et al., 1991). Barker in 1975 studied the relation between tooth attrition
and height of the alveolar crest in 36 aboriginal skulls. He found with attrition, there was significant
eruption of the tooth in response. Therefore, as a result of continuous eruption of teeth from their
sockets with aging, GR occurs in the absence of periodontitis (Barker, 1975). On the hand, teeth with
bigger amount of eruption bring with them thinner alveolar bone than those with less eruption
movement. Additionally, a possible inflammation may react differentially on erupted teeth with thick
alveolar bone and gingiva as compared to those with thin alveolar bone and gingiva. Thin inflamed
gingival tissue might render a site more susceptible to recession and loss of attachment (Wennstrom
et al., 1987, Ericsson and Lindhe, 1984).
This study has a few limitations. First, loss to follow-up between SHIP-0 and SHIP-2, mainly due to
death, constitutes a major aspect. Second, the study sample again represents a subset of participants
of SHIP-2 mainly due to (not-at-random) missing participation in full body MRI scan and dental
examinations. Third, edentulous subjects were also excluded because of missing periodontal data.
Thus, the study population cannot be considered as being representative for the general population
and possible source of bias was present in this study. Although we only had cross-sectional MRI data,
continuous eruption of teeth should be reflected in increasing facial height. In fact, we found a small,
albeit significant correlation of age with Nasion-ANS (0.12 p=0.004) and with Nasion-Menton (0.10
p=0.02). Since we have no longitudinal MRI data, we do not know whether this eruption accounts for
the greater facial height. Finally, our conclusions and explanations are based on cross-sectional
measurements, thus longitudinal data as well as information about gingival and alveolar bone
thickness will be necessary to either confirm or refute these assumptions.
In view of the foregoing discussion, the current study provides the first empirical evidence for an
association between maximum cranial width and the facial index reflecting craniofacial morphology
and periodontal variables, namely GR and CAL.
25
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Estimating effects of craniofacial morphology on gingival recession and clinical attachment loss
Loutfi Salti
Abstract
Objectives: Currently, evidence for the association between face morphology, attachment loss and
recession is lacking. Face type can be described by the ratio of facial width and facial length. We
hypothesize, that the facial type might be related to gingival recession (REC) and clinical attachment
loss (CAL) and that a broad face is associated with less recession and attachment loss than a long
face.
Materials and methods: Data from the 10 year follow-up of the Study of Health in Pomerania
(SHIP-2; 2008-2012; 2333 participants) were used. Periodontitis was assessed by probing depth (PD)
and clinical attachment loss (CAL). Generalized regression models were used to assess associations
between specific landmark distances extracted from magnetic resonance images (MRI) head scans
and clinically assessed gingival recession adjusting(REC) or clinical attachment loss(CAL) adjusting
for relevant confounders.
Results: Maximum cranial width was negatively associated with mean REC and mean CAL
(p<0.05). Also, higher mean REC and higher mean CAL correlate positively with long face
(B=0.361 with 95% CI), upper anterior facial height.
Conclusion: According to the results of the present study, gingival recession and clinical attachment
loss were associated with higher Prosopic face and facial length indices results.
34
Financial support
This research was supported by an educational grant from the Deutsche Gesellschaft für Zahn-,
Mund- und Kieferheilkunde (DGZMK).
Permission licence
This research is part of article "Estimating effects of craniofacial morphology on gingival recession
and clinical attachment loss". Journal of Clinical Periodontology. 2017; (4): 364-371.
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Goldweber, Paulette - Hoboken [email protected]
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35
Eidesstattliche Erklärung
Hiermit erkläre ich, dass ich die vorliegende Dissertation selbständig verfasst und keine anderen als
die angegebenen Hilfsmittel benutzt habe.
Die Dissertation ist bisher keiner anderen Fakultät, keiner anderen wissenschaftlichen Einrichtung
vorgelegt worden.
Ich erkläre, dass ich bisher kein Promotionsverfahren erfolglos beendet habe und dass eine
Aberkennung eines bereits erworbenen Doktorgrades nicht vorliegt.
Datum Unterschrift
36
Acknowledgment
It is with great honor and pride that I convey my sincere and deep gratitude to my guide Prof.
Thomas Kocher, for his guidance, suggestions, constant support and constructive criticism. I would
like to express much appreciation to Dr. Birte Holtfreter and Mrs. Christiane Pink for their sincere
efforts exerted during the course of this study. Finally, very special thanks to my wife, for her
patience and positive attitude.