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Evaluation of Alveolar Bone Quality: Correlation Between Histomorphometric

Analysis and Lekholm and Zarb Classification

Article  in  Journal of Craniofacial Surgery · January 2021

DOI: 10.1097/SCS.0000000000007405

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CLINICAL STUDY
Evaluation of Alveolar Bone Quality: Correlation Between
Histomorphometric Analysis and Lekholm and
Zarb Classification
Marina Reis Oliveira, PhD, Andréa Gonçalves, PhD,
Marisa Aparecida Cabrini Gabrielli, PhD, Cleverton Roberto de Andrade, PhD,y
Eduardo Hochuli Vieira, PhD, and Valfrido Antonio Pereira-Filho, PhD
Downloaded from https://journals.lww.com/jcraniofacialsurgery by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdtwnfKZBYtws= on 02/03/2021
Objectives: This study evaluated the bone quality of the maxilla
and mandible by using the classification proposed by Lekholm and
Zarb (L & Z) and histomorphometry.
Methods: Sixty edentulous areas were evaluated. The classification
by L & Z was obtained through the evaluation of periapical and
panoramic radiographs associated with the surgeon’s tactile
perception during milling and implant installation. Before
implant installation, bone biopsies of standardized sizes were
performed for histological evaluation.
Results: Type III bone quality was more frequent in the posterior
(73.33%) and anterior (73.33%) maxilla, whereas type II bone
quality was more frequent in the posterior (53.33%) and anterior
(60.00%) mandible. Through histometry, statistical difference was
observed for the amount of bone tissue of the posterior region of the
maxilla in relation to the anterior and posterior regions of the
mandible (P  0.043). However, there was no difference in
osteocyte counts between alveolar regions (P ¼ 0.2946). In the
female gender, the age showed a low positive correlation with
the L & Z classification (rho ¼ 0.398; P ¼ 0.006) and in the male
gender, a moderate negative correlation was observed (rho ¼ –
0.650, P ¼ 0.016).
Conclusions: Both methods detected differences in the bone quality
of the alveolar regions of the maxilla/mandible and that the
classification by L & Z is a reliable method, since it was
consistent with histomorphometry, considered the ‘‘gold
standard’’ method for the evaluation of bone quality and greater
bone density was observed in older men.
From the Diagnosis and Surgery Department, Araraquara Dental School,
São Paulo State University (FOAr/UNESP); and yPathology and Physi-
ology Department, Araraquara Dental School, São Paulo State Univer-
sity (FOAr/UNESP), Araraquara, SP, Brazil.
Received August 5, 2020.
Accepted for publication November 18, 2020.
Address correspondence and reprint requests to Marina Reis Oliveira, PhD,
Rua Humaitá, 1680, Centro, Araraquara, 14903-385, SP, Brazil;
E-mail: marinareis89@hotmail.com
Funding was provided by the FAPESP (Foundation for Research Support of
the State of São Paulo) (Process number: 2014/25253-1).
The authors report no conflicts of interest.
Supplemental digital contents are available for this article. Direct URL
citations appear in the printed text and are provided in the HTML and
PDF versions of this article on the journal’s Web site (www.jcraniofa-
cialsurgery.com).
Copyright # 2020 by Mutaz B. Habal, MD
ISSN: 1049-2275
DOI: 10.1097/SCS.0000000000007405
The Journal of Craniofacial Surgery  Volume 00, Number 00, Month 2021
Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Key Words: Bone quality, classification by Lekholm and Zarb,
dental implants, histomorphometry
(J Craniofac Surg 2021;00: 00–00)
T here are currently several methods for evaluating bone quality.
However, computed tomography (CT) is the image examination
considered more adequate for such purpose, since it associates
information of quantity and morphology.1 – 2 Despite this, it is not
a resource applied in all cases of clinical practice.3 Leckholm and
Zarb (L & Z) classification is still the most used method to
evaluate bone quality because it has low cost and is easy to
apply.4 – 7
In this classification, the volume and structural characteristics of
the bone tissue are evaluated based on panoramic/periapical radio-
graphs and surgical evaluation of the bone hardness perceived by
the surgeon during the perforation to install the implant. The bone is
then classified based on a scale ranging from 1 to 4 according to the
amount of trabecular and cortical bone. Regarding the amount of
bone available, the classification varies from A to E, where: A
corresponds to most of the preserved alveolar bone and E indicates
that the basal bone is already extremely reabsorbed.8 The main
limitation of this classification is that it can be influenced by the
surgeon’s experience, resulting in a somewhat subjective bone
characterization and difficult reproducibility.1– 9 However, it has
been verified that tactile perception allows an acceptable classifi-
cation of bone types.10
The histomorphometry, in turn, includes small bone biopsies for
histological evaluation and quantification of the percentage of
trabeculae in the total area of the bone fragment, and remains
the gold standard method for the assessment of bone quality.7
However, it is not a viable resource in clinical practice. In this
context, although there is a great diversity of methods available for
preoperative assessment of bone quality, only a few are routinely
used.11 In addition, many factors of bone quality and their relation
to dental implants are misunderstood.12 This is because, with the
exception of a few studies,6 –7 most of the studies to date have
evaluated the initial stability of the implant using bone histomor-
phometry in cadavers, which hinders the extrapolation of results for
in vivo clinical practice. Therefore, it is important to perform in
vivo studies to understand the clinical situation, in which several
biological factors are interfering with the primary stability of
implants.13
In addition, Oliveira et al (2008)12 observed in their study that
different bone qualities can be found in different regions of the
maxilla and mandible. Therefore, site-specific assessment is impor-
tant and careful planning for rehabilitation with implants is always
necessary. In this context, studies like our study are necessary to
compare the bone quality assessed by the classic classification of L
& Z and histomorphometry, which is still considered the gold
standard method for the evaluation of bone quality.
1
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Oliveira et al The Journal of Craniofacial Surgery  Volume 00, Number 00, Month 2021

MATERIALS AND METHODS

Patient Selection and Sample Division

Thirty-six healthy patients of both genders were selected,
accounting for 60 alveolar regions that met the following inclusion
criteria: age between 20 and 75 years; patients with no serious
diseases or decompensations that could change bone density;
edentulous areas of maxilla and/or mandible, in which it was
possible to install an implant with a minimum of 3.75 mm in
diameter  9 mm in length (External Hexagon - HE, Titamax
TI, Neodent, Curitiba, PR, Brazil); and degree of atrophy B and C.8
Before any study procedure was initiated, the selected patients
signed the informed consent form. In addition, this study was only
initiated after approval by the Ethics Committee on Human
Research (Process number: 917.255/2014). The 60 edentulous areas
evaluated were divided into 4 groups of 15 areas each, according to
the site in the maxilla: posterior maxilla, posterior mandible,
anterior maxilla, and anterior mandible. FIGURE 1. (A) Trephine with 2.5 mm diameter positioned for bone biopsy; (B)
Bone fragment removed.
Preoperative Evaluation
All patients were submitted to anamnesis and were clinically model HM 325). The sections were stained with hematoxylin and
assessed for residual bone quantity. Scanned panoramic and peri- eosin and submitted to histometry and osteocyte count.
apical radiographs were obtained using VistaScanCombi Plus soft-
ware (Durr Dental AG, Bietigheim-Bissingen, Germany). In
addition, the panoramic and periapical radiographic examinations
Histomorphometric Analysis
were performed in a standardized way and always by the same For the histomorphometric analysis, 3 histological slides from
person. With the information obtained, we planned the surgical each biopsied area were selected by the stereometry (cervical,
procedure and determined the length of the implants. middle, and apical third of the bone fragment). Quantification of
the bone tissue was performed by an experienced examiner, without
knowledge of the alveolar region, in each group. Quantitative
Bone Classification by L & Z analysis was performed over the entire length extension of the 3
This classification was performed before the surgery by a single histological sections selected. The final value of bone tissue in mm
examiner, who was also the surgeon responsible for conducting the and the osteocyte count resulted from the sum of the values obtained
surgeries. Thus, it was possible to determine the classification of bone in the 3 histological sections evaluated. Optical Microscope (Dia-
quality of the edentulous areas based on the radiographic aspect and star – Leica Reichert Jung Products Germany) was used with 4.0/
surgeon’s tactile perception to the bone resistance during the perfo- 100X magnification lens and 5X and 10X magnification eyepieces
ration, as proposed in the original L & Z classification. The intraob- for histometry and osteocyte count, respectively. Figures 2 and 3
server calibration was performed and the Kappa index obtained was show histological images of the different alveolar regions with 5-
0.87 (almost a perfect match according to Landis and Koch, 197714). and 10-fold increase of the maxilla and mandible, respectively.
Thus, after the visual evaluation of these radiographs, the evaluator The images were selected and transferred to a PC (Pentium 4
classified the different areas according to L & Z as follows: bone type Intel) through a camera (Olimpus CAMEDIA C50/60 Wide Zoom)
1, bone type 2, bone type 3, and bone type 4.

Surgical Procedure
The technique to prepare the sites for the installation of the
implants was employed in a standard way and taking into account
the manufacturer’s recommendations. The same experienced sur-
geon performed all surgeries, in order to reduce the chances of
errors among operators. Surgical access was performed by a linear
incision on the ridge with subsequent complete displacement of the
flap to expose the bone tissue. Before starting the perforation, a
bone biopsy was performed with a trephine of 2.5 mm outside
diameter (Maximus, Contagem, MG, Brazil) at 30 rpm. The tre-
phine was always inserted until the same height (8 mm) (Fig. 1).
Shortly after its removal, the bone fragment was washed with
sterile saline and fixed in 4% buffered formaldehyde. The trephine
served as the initial mill for the preparation of the surgical alveolus.
At the time of perforation to install the implants the surgeon was
asked about the bone quality as proposed by L & Z.

Histological Processing
The bone fragments obtained were were submitted to routine
histological processing. Serial cuts were made in the axial direction
of the specimen with 6-mm thickness using a microtome (Micron,
FIGURE 2. Histological image of bone biopsy of the anterior region of the
maxilla [(A) 5-fold increase for histometry, (B) 10-fold increase for osteocyte
count]; histological image of bone biopsy of the posterior region of the maxilla
[(C) 5-fold increase for histometry, (D) 10-fold increase for osteocyte count].

2 # 2021 Mutaz B. Habal, MD

Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
CE: D.C.; SCS-20-01701; Total nos of Pages: 5;
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The Journal of Craniofacial Surgery  Volume 00, Number 00, Month 2021
FIGURE 3. Histological image of bone biopsy of the anterior region of the
mandible [(A) 5-fold increase for histometry, (B) 10-fold increase for osteocyte
count], histological image of bone biopsy of the posterior region of the
mandible [(C) 5-fold increase for histometry, (D) 10-fold increase for osteocyte
count].
coupled to the optical microscope. With the aid of Image J Launcher
software (National Institutes of Health, Bethesda, Maryland, USA
(http://rsb.info.nih.gov/ij/index.htm), the total area was delimited
and quantified as 100%. Subsequently, other structures, such as
empty spaces, cells, and blood vessels, were subtracted from the
narrowly defined bone areas. The final bone quantity of each
edentulous region was obtained by calculating the sum of the bone
area of the 3 quantified slides. Then, osteocyte count was carried out
on the selected slides throughout their length. The count was done in
duplicate for each slide and the arithmetic mean of the 2 counts
was calculated.
Statistical Analysis
The data underwent the Shapiro–Wilk test to evaluate normality.
When normality assumptions were met, analysis of variance was
used, followed by Tukey post-test; when the data did not respond to
normality, the Kruskal–Wallis nonparametric test was employed,
followed by the Dunn post-test to test the existence of differences in
the radiographic optical bone density between the alveolar regions
of maxilla and mandible. In addition, a correlation analysis was
performed through the Spearman correlation coefficient. The mag-
nitude of the correlations obtained in the present study was based on
Munro’s (2001)15 classification: low correlation (0.26  rho 
0.49); moderate correlation (0.50  rho  0.69); high correlation
(0.70  rho  0.89); and very high correlation (0.90  rho  1.00).
The level of significance adopted in all statistical tests was 5% of
significance. All statistical tests were calculated using SPSS soft-
ware (v.21, SPSS Inc., Chicago, IL).
RESULTS
Classification by L & Z
The final bone quality obtained by the radiological evaluation
and surgeon’s tactile perception as proposed in the original L & Z
classification is presented in Supplementary Digital Content,
Table 1, http://links.lww.com/SCS/C276. It was observed that
the most frequent bone quality in the posterior region of the maxilla
was the type III (73.33%), and type II (13.33%) and IV (13.33%)
bone qualities were observed in only 2 cases each. Type I bone
# 2021 Mutaz B. Habal, MD
Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Bone Quality in the Maxilla and Mandible
quality was not observed in the posterior maxillary region. On the
other hand, in the posterior mandibular region the most common
bone quality was type II (53.33%), followed by type III (26.67%),
and type I was observed in 2 cases (13.33%). Type IV bone quality
was observed in only 1 case in the posterior region of the mandible
(6.67%). In the anterior maxillary region, the most frequent bone
quality was type III (73.33%), followed by type II bone quality
(20.00%), and type IV was observed in 1 case only (6.67%). On the
other hand, in the anterior area of the mandible only the type I and II
bone qualities were observed, with higher frequency for type II
(60.00%) when compared to type I (40.00%).
Histometry and Osteocyte Count
The mean values of bone tissue (mm) evaluated by histometry
for each of the regions were as follows: 2243110.76 (1450895.64)
for the posterior region of the maxilla, 3992425.76 (2018654.67)
for the posterior region of the mandible, 2660685.75 (110304.20)
for the anterior region of the maxilla and 3745390.01
(1346277.67) for the anterior region of the mandible. After
submitting the data to the analysis of variance test a statistical
difference was observed among the groups (P ¼ 0.0062) (Supple-
mentary Digital Content, Table 2, http://links.lww.com/SCS/C278).
Tukey post-test showed that the mean bone tissue (mm) of the
posterior maxilla is statistically different from that of the posterior
(P ¼ 0.013) and anterior mandible (P ¼ 0.043). In contrast, no
statistically significant differences were observed between the
anterior and posterior maxillary area (P ¼ 0.875) and the anterior
and posterior mandibular area (P ¼ 0.970). Similarly, no statisti-
cally significant differences were observed between the anterior
mandibular region and the anterior maxillary region (P ¼ 0.217)
(Fig. 4).
In turn, the mean osteocyte count for each of the analyzed
regions was as follows: 542.73 (482.81) for the posterior region of
the maxilla, 778.60 (422.98) for the posterior region of the
mandible, 616.36 (444.12) for the anterior region of the maxilla,
and 678 (392.71) for the anterior region of the mandible. Since the
osteocyte count values did not respond to normality, it was neces-
sary to use nonparametric statistics. After the Kruskal–Wallis test,
the data revealed no statistical difference among the groups
(H(3) ¼ 3.7098; P ¼ 0.2946).
Correlation Analysis
As for the correlation analysis taking into account gender, in the
female gender, the age variable showed a low positive correlation
with the L & Z classification (rho ¼ 0.398) with high statistical
FIGURE 4. Mean and standard deviation of the variable bone tissue according
to the alveolar region. Different letters indicate statistically different means
according to the Tukey test (P  0.043).
3
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Oliveira et al The Journal of Craniofacial Surgery
significance (P ¼ 0.006). This means that the older the patient, the
higher the L & Z classification score, and the more medullary the
bone. On the other hand, regarding the histomorphometric (rho ¼ –
0.254, P ¼ 0.0085) and osteocytes count (rho ¼ –0.278, P ¼ 0.058),
no statistically significant correlations were observed for the
women’s age in the present study sample.
In the male gender, a moderate negative correlation was
observed (rho ¼ –0.650, P ¼ 0.016) in the analysis of the correla-
tion between age and the L & Z classification, which means the
older the patient, the lower the bone quality score and the more
cortical the bone. However, regarding the histomorphometric
(rho ¼ –0.02, P ¼ 0.949) and osteocytes count (rho ¼ –0.308,
P ¼ 0.306), no statistically significant correlations were observed
for the men’s age in the present study sample.
DISCUSSION
According to Oliveira et al (2008),12 alveolar bone quality can be
extremely variable in any of the maxilla and mandible regions.
Therefore, preoperative planning is extremely important in order to
achieve higher success rates in the long term.16 Much has been
discussed regarding the use of CT for implant planning, since this is
considered the gold standard imaging exam for the evaluation of
bone quality.4,5 However, because of the cost and dose of radiation
received by the patient, most professionals still use conventional
radiographs, especially panoramic radiography, and other subjec-
tive methods for the assessment of bone quality, such as the L & Z
classification.17,18 In addition, the literature lacks studies on such
matter, such as our study, in which the bone quality of the different
regions of the maxilla and mandible is evaluated by using the
classical L & Z classification and histomorphometry, which is still
considered the gold standard method for evaluation of bone quality.
Besides the maxillomandibular location, others factors can
interfering in the bone quality, such as: use of drugs, systemic
diseases, gender, and age.5 So much so, that the results obtained
show in the male gender, a moderate negative correlation was
observed (rho ¼ –0.650, P ¼ 0.016) in the analysis of the correla-
tion between age and the L & Z classification and a low positive
correlation between the female gender and the L & Z classification
(rho ¼ 0.398; P ¼ 0.006). This means that the older women, the
higher the L & Z classification score and the more medullary the
bone and in the men, which means the older the patient, the lower
the bone quality score and the more cortical the bone. However, in
the both genders there was no correlation of the age with histologi-
cal analysis (P > or ¼ 0.058).
The most traditional method for evaluation of bone quality is the
classification proposed by L & Z, in 1985,8 performed by using
radiographs associated with the surgeon’s tactile perception. In a
study by Lindh et al (2014),19 in which the knowledge on bone
quality of Swiss and Brazilian implant specialists was evaluated,
both groups attested to frequently use the aforementioned classifi-
cation. Despite the wide use, this method is subjective and difficult
to reproduce and therefore little investigated scientifically.1–9
Because of this, the evaluations in present study has been done
by a single evaluator. Therefore, the intraobserver calibration was
performed to evaluate the bone quality according to L & Z
classification based on the panoramic radiographs in order to reduce
the bias to the maximum. The analysis only started after calculating
kappa, which was 0.87, that is, excellent.14
According to Linck et al (2016),20 the lack of scientific evidence
on the use of the L & Z classification is due to the variety of ways
the method is used. Although some authors classify bone tissue
based on radiographic evaluation only, others associate the sur-
geon’s tactile perception. However, the 2 classifications (original
and modified) are strongly correlated and the surgeon’s tactile
4 #
Copyright © 2020 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
 Volume 00, Number 00, Month 2021
perception does not seem to have much interference with bone
classification.18 Nevertheless, in this study, the original L & Z
classification was used, considering the radiographic evaluation and
the surgeon’s tactile perception. This is because tactile intraoper-
ative perception can add important information about the charac-
teristics of bone tissue.19 In addition, the original L & Z
classification has been shown to be more correlated with the
micro-CT than the L & Z classification based only on radiographic
images.7 In addition, in 1999, Trisi and Rao10 verified that tactile
perception allows an acceptable differentiation of the type of
bone quality.
In this study, the highest bone quality in the posterior (73.33%)
and anterior (73.33%) areas of the maxilla was type III and in the
posterior (53.33%) and anterior areas (60.00%) of the mandible the
type II bone quality was the most observed. Linck et al (2016)20 also
reported that most of the implant insertion areas were of type II or
III. Another study evaluating bone quality and quantity only in the
anterior maxillary region showed that type III bone quality was the
most frequent in this region (69.7%).21 Similarly, Ribeiro-Rotta
et al (2014)7 also found higher prevalence of type II and III bone
quality (58.7%) according to the L & Z classification. However,
different bone qualities can be found in the anterior and posterior
regions of the maxilla and mandible, so individualized evaluation is
always very important.12
A pioneering study for the validation of L & Z classification was
done by Ribeiro-Rotta et al (2014),7 comparing the initial stability
of the implant, L & Z classification and bone biopsies evaluated by
micro-CT. However, the authors emphasized the importance of
other comparative studies of this classification, since it is widely
used. The comparison with bone histomorphometry is very impor-
tant, because although it is not feasible in all in vivo procedures, it is
still the gold standard for the evaluation of bone quality,7 since it
cannot be completely replaced with micro-CT.22,23
Regarding the histomorphometric analysis, bone fragments were
removed with the use of a trephine before implant installation.
However, although the bone biopsies were always obtained with the
same trephine, tailor made for this study, the length of bone
fragments was not always the same. It is believed that this occurred
due to the differences in bone microarchitecture of the different
alveolar regions of the maxilla and mandible, as previously empha-
sized by authors who used similar methodology.7 In order to avoid
compromising the histological analysis, each specimen was evalu-
ated in 3 regions (cervical, middle, and apical), so that the entire
extension (cortical and medullary bone) could be evaluated.
Although it is not an applicable feature in the routine clinic,
histometry is considered the gold standard to assess bone qual-
ity.24,25 Trisi and Rao (1999)10 found a positive correlation between
the clinical and histomorphometric evaluation of bone quality after
implant insertion in 56 patients, mainly in the differentiation of
bone types I and IV. In the identification between intermediate bone
types (II and III), nonsignificant correlation was observed. In
contrast, in this study it was possible to detect statistical differences
regarding the histometry between the posterior regions of the
maxilla and the anterior (P ¼ 0.043) and posterior (P ¼ 0.013)
regions of the mandible. These results suggest that it was possible
to detect differences in bone quality through histometry not only in
the extreme bone qualities but also in the intermediate ones. This is
because, in the posterior maxillary region, the most frequent bone
quality was type III (73.33%) although type IV was also observed
(13.33%), and in the anterior mandibular region, bone types II
(60.00%) and I (40.00%) were observed. However, no significant
statistical differences were observed in the histometry of the
anterior and posterior regions of the maxilla and mandible. It is
believed that this may have occurred because most of the bone
quality of the anterior and posterior maxillary area consists of type
2021 Mutaz B. Habal, MD
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The Journal of Craniofacial Surgery  Volume 00, Number 00, Month 2021
III bone. On the other hand, the bone quality most observed in the
anterior mandibular region was type II and it was the type III for the
posterior mandibular, followed by type II. Thus, it can be suggested
that in the sample studied between the posterior and anterior regions
of the same maxilla there is similarity in bone quality.
Regarding the osteocyte count, no statistical differences were
observed between the different regions evaluated (P ¼ 02946).
Hernández-Cortés et al (2014)24 also used osteocyte count as an
indicator to assess bone quality. However, the authors did not find
statistically significant differences in the amount of osteocytes in
the femoral head with osteoporosis and osteoarthritis. Thus, as in
this study, the authors concluded that osteocyte count is not a good
indicator to assess bone quality.
Thus, the methodology used allowed to conclude that both
methods allowed to detect differences in the bone quality of the
alveolar regions of the maxilla/mandible and that the classification
by L & Z is a reliable method to evaluate bone quality, since it was
consistent with histomorphometry, considered the gold standard
method for the evaluation of bone quality.
ACKNOWLEDGMENTS
The authors thank CAPES (Coordination for the Improvement of
Higher Education Personnel) and FAPESP (Foundation for
Research Support of the State of São Paulo) (Process number:
2014/25253-1).
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