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Are Intraoral Radiographs Accurate in Determining the

Peri-implant Marginal Bone Level?


Michele Cassetta, DDS, PhD1/Roberto Di Giorgio, MD2/Ersilia Barbato, DDS, MS3

Purpose: The primary objective of this study was to assess the accuracy of periapical radiographs in
determining the peri-implant marginal bone level. The accuracy of the linear measurements on radiographs
was considered as the absolute difference between the true, intraoperative or surgical marginal bone level
measurements (direct bone measurements during surgical procedures) and the radiographic measured
distances. The secondary aims were to identify the variables influencing the radiographic evaluation
(arch: mandible/maxilla; implant location: anterior/posterior; timing of implant placement: “early delayed”
and “prolonged delayed”). The influence of vestibular and palatal/lingual crestal bone levels was also
investigated. Materials and Methods: STROBE guidelines were followed. As soon as the implant was
inserted, the marginal bone levels were recorded using a straight periodontal probe (intraoperative or surgical
measurements). At the same time, periapical radiographs were taken. To standardize the radiographic
images, periapical radiographs were acquired using the long-cone parallel technique and film holding system.
All radiographs were analyzed by two examiners blinded to the surgical measurements. Intraclass correlation
coefficient (ICC) was employed to assess the intraobserver and interobserver variability. The descriptive
statistics, t test, and multivariate statistics were used; the threshold for statistical significance was P ≤ .05.
Results: Two hundred sixty-eight implants were inserted in 142 patients. The interobserver agreement was
0.980; the intraobserver variability was 0.990 and 0.993. The mean difference between the radiographic
and surgical measurements was 0.45 mm (range: 0 to 8 mm; SD: 1.76). Comparing the radiographic and
surgical measurements, a statistically significant difference (P = .000) was detected. None of the variables
considered (arch, implant location, and timing of implant placement) significantly influenced the accuracy.
Neither the vestibular alveolar edge (P = .908) nor the lingual/palatal (P = .485) significantly influenced the
accuracy. Conclusion: The periapical radiograph statistically significantly overestimates the level of peri-
implant marginal bone compared with surgical measurements. The arch, implant location, timing of implant
placement, and level of vestibular or lingual/palatal alveolar edge do not influence deviation between the
intraoperative peri-implant marginal bone level measurements and the radiographically determined marginal
bone levels. Int J Oral Maxillofac Implants 2018;33:847–852. doi: 10.11607/jomi.5352

Keywords: alveolar bone loss, computer-assisted, dental implant, dental radiography, radiographic image
interpretation

S tability of bone support is an important criterion


1 Assistant Professor, Department of Oral and Maxillofacial
Sciences, School of Dentistry, “Sapienza” University of Rome, for the long-term success of osseointegrated im-
Rome, Italy.
2 Associate Professor, Department of Oral and Maxillofacial
plants.1–8 From the clinical practice point of view, it
Sciences, School of Dentistry, “Sapienza” University of Rome, is still very difficult to acquire the same exposure ge-
Rome, Italy. ometry that is required for peri-implant bone level
3Full Professor, Department of Oral and Maxillofacial Sciences,
follow-up,9 and to date, it has not been determined if
School of Dentistry, “Sapienza” University of Rome, the measurements of the marginal bone levels, per-
Rome, Italy.
formed using periapical radiographs, coincide with the
Correspondence to: Dr Michele Cassetta, Department of Oral bone levels measured at the time of surgery. The accu-
and Maxillofacial Sciences, “Sapienza” University of Rome, racy of the linear measurements on the radiographs is
School of Dentistry, Via Caserta, 6, 00161, Rome, Italy. the absolute difference between the true (intraopera-
Fax: +39.06.5016612. tive) and the radiographic measured distances.9
Email: michele.cassetta@uniroma1.it
The primary objective of the study was to assess
©2018 by Quintessence Publishing Co Inc. whether the intraoperative or surgical marginal bone

The International Journal of Oral & Maxillofacial Implants 847

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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Cassetta et al

level measurements (direct bone measurements dur- positive number (coronal to implant shoulder), zero (at
ing surgical procedures) and the marginal bone lev- the implant shoulder), or negative number (apical to
els measured by means of periapical radiographs are the implant shoulder). The marginal bone level value
statistically significantly different. Given that the sur- was rounded to the nearest millimeter. The distance
gical measurement is the reference, the smaller the between the same reference point (implant shoul-
difference is between the surgical and radiographic der) and the edge of peri-implant marginal bone at
measurements, the greater the accuracy of the radio- four sides around the implant was measured (in the
graphic measurements. middle of the distal and mesial implant surface and
The secondary objectives were: in the middle of the vestibular and lingual/palatal im-
plant surface) (Fig 1). All clinical measurements were
• to identify the variables that affect the peri-implant performed by one examiner, an expert prosthodontist
marginal bone level radiographic evaluation (arch: and oral surgeon (M.C.). At the same time, the marginal
mandible/maxilla; implant location: anterior/ bone level was also registered by means of periapical
posterior; timing of implant placement: “early radiographs (Fig 2). To standardize the periapical radio-
delayed” and “prolonged delayed”) graphic images, the long-cone parallel technique and
• to assess the influence of vestibular and palatal/ the Super-Bite (Kerr Corporation) film holding system
lingual crestal bone levels on the radiographic were used. The x-ray film was aligned in parallel to the
measurements: as the periapical radiography is long axis of the implants. Exposures were made with
bi-dimensional, the overlap between buccal and an intraoral radiation unit (Oralix AC, Gendex) using
palatal/lingual bone levels could prevent the a cylindrical tube head, 2.5-mm aluminum filtration,
correct determination of the peri-implant marginal and a focal spot distance of 200 mm. The exposure set-
bone levels tings were 70 kV ± 1.12 mAs. Digital radiographs were
saved via a digital intraoral imaging system (DenOp-
An assumption was made that statistically the intra- tix QST Digital X-ray Phosphor Plate System, Gendex),
operative (surgical) measurements and the marginal and direct measurements were performed using den-
bone levels measured using periapical radiographs are tal imaging software (VixWinPRO, Gendex). The mesial
significantly different. and distal marginal bone level measurements (ie, the
Moreover, it was assumed that at least one variable linear measurements between the implant shoulder
could influence the accuracy of periapical radiographs. and the marginal bone level) could be either a posi-
tive number, zero, or a negative number as previously
outlined. Contrast and brightness of the digital images
MATERIALS AND METHODS were adjusted using the same software. To reduce the
symmetric imaging error in the vertical plane, the dis-
The study was executed at the Department of Oral tortion of each individual radiograph was determined,
and Maxillofacial Sciences of “Sapienza” University and the radiographic measurements were adjusted
of Rome between February 2014 and February 2016. according to this distortion for each individual radio-
A prospective cohort study design was used, in ac- graph. The measurements were calibrated by means of
cordance with the Strengthening the Reporting of an object of known dimension— the known implant
Observational Studies in Epidemiology guidelines length or width. As well as during the intraopera-
(STROBE). The approval of the local ethics committee tive measurements, the radiographic marginal bone
was obtained (#304/07). The inclusion and exclusion level values were rounded to the nearest millimeter.
criteria as well as the preoperative radiographic exami- All radiographs were analyzed independently by two
nations used are the same as those already described examiners blinded to the surgical measurements.
in previous publications.2,3,5 A two-piece, tapered im- The intraobserver and interobserver variability was
plant was used (SM Torx Implant System, DioImplant). assessed using the intraclass correlation coefficient
The implant shoulder was machined, and the coronal (ICC). An estimated ICC close to 1 states that the cor-
part of the implant body was characterized by micro- relation is strong. A P value ≤ .05 was set as the sig-
threads. The implant lengths were 10, 12, and 14 mm; nificance level. The accuracy of peri-implant marginal
the diameters were 3.8 and 4.1 (narrow), 4.5 and 5.0 bone level radiographic measurements was assessed
(regular), and 5.3 mm (wide). The implants were in- by comparing the values measured on radiographs to
serted by raising a mucoperiosteal flap. When implants the intraoperative values. For the comparison with the
were inserted, the marginal bone levels were recorded radiographic measurements, the mesial and distal in-
with a straight periodontal probe (Williams Probe, Hu traoperative values were used. The predictor variables,
Friedy). Depending on the positioning of the mar- ie, the clinical factors that may affect the radiographic
ginal bone level, the following values were recorded: measurements, resulting in a difference between the

848 Volume 33, Number 4, 2018

© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
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Cassetta et al

Fig 1   Surgical, intraoperative peri-implant marginal bone level measurements of a prolonged delayed implant inserted in the pre-
molar area of the maxilla. The values were recorded in the middle of the distal and mesial implant surface and in the middle of the
vestibular and palatal implant surface.

intraoperative measurements and the radiographic


measurements, were classified as follows2,3,5:

• Arch: maxilla or mandible


• Implant position: anterior or posterior
• Timing of implant placement: distinguished
between “early delayed” and “prolonged delayed”

The influence of vestibular or lingual/palatal alveo-


lar bone edge (ie, the height of the alveolar ridge mea-
sured in correspondence to the implant in the middle
of the vestibular and lingual/palatal implant surface)
on the radiographic assessment of marginal bone lev-
els was evaluated as well.
Fig 2  Periapical radiograph obtained at the time of implant
placement with the long-cone parallel technique and the Super-
Statistical Analysis Bite (Kerr Corporation) film holding system.
The statistical analysis was performed at implant level.
Descriptive statistics and t test were used to detect

The International Journal of Oral & Maxillofacial Implants 849

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Cassetta et al

Table 1   Crestal Bone Levels Measured The intraobserver variability evaluated using ICC was
Radiographically and Surgically 0.990 and 0.993. Given the excellent interobserver
(n = 268) and intraobserver agreement, the radiographic mea-
surements were considered. The values of surgical
Mean Min Max SD and radiographic measurements are shown in Table 1.
rx.T0 m. 1.29 –3.70 8.20 1.49 Comparing the radiographic values to surgical mea-
rx.T0 d. 0.77 –6.80 6.50 1.56 surements, a mean difference of 0.45 mm was deter-
s.m.T0 m. 0.80 –7.00 7.00 2.09 mined (range: 0 to 8 mm; SD: 1.76). The radiographic
s.m.T0 d. 0.36 –5.00 7.00 1.97 analysis significantly overestimated (P = .000) the level
s.m.T0 v. –0.69 –8.00 3.00 1.89 of peri-implant marginal bone. The variables arch, im-
plant location, and timing of implant placement did
s.m.T0 p/l. –0.06 –10.00 5.00 1.84
not significantly influence the accuracy of radiographic
Marginal bone levels measured at the time of implant insertion.
rx.T0 m. = mesial marginal bone level measured radiographically; measurements. Regarding the influence of vestibular
rx.T0 d. = distal marginal bone level measured radiographically; and palatal/lingual crestal bone levels on the accuracy
s.m.T0 m. = intraoperative (surgical) mesial marginal bone
level measurement; s.m.T0 d. = intraoperative (surgical) distal
of the periapical radiograph, neither the vestibular al-
marginal bone level measurement; s.m.T0 v. = intraoperative veolar edge (P = .908) nor the lingual/palatal alveolar
(surgical) vestibular marginal bone level measurement; s.m.T0 edge (P = .485) significantly influenced the accuracy.
p/l. = intraoperative (surgical) palatal/lingual marginal bone level
measurement.

DISCUSSION
whether the intraoperative and the radiographic mar-
ginal bone level measurements were statistically sig- In the present study, the difference between the in-
nificantly different. Multivariate statistics were used traoperative measurements of peri-implant marginal
to evaluate if arch, implant location, and timing of bone levels and the marginal bone levels evaluated
implant placement statistically significantly affect the using periapical radiographs was determined. The
accuracy of radiographic measurements (difference hypothesis that a difference would be present was
between the radiographic and intraoperative margin- confirmed by the results: the radiographic analysis sig-
al bone measurements). To evaluate the influence of nificantly overestimated the marginal bone compared
vestibular or palatal/lingual marginal bone height on with the surgical measurements.
the difference between the surgical and radiographic The secondary objectives were to determine if vari-
measurements, multivariate statistics were also used. ables such as arch, implant location, timing of implant
Data were evaluated using statistical analysis software placement, and vestibular and palatal/lingual crestal
(SPSS v. 17.0, IBM Corporation). The statistical signifi- bone levels influenced the accuracy of peri-implant
cance was set at the level of P ≤ .05 for all evaluations. marginal bone level radiographic evaluation. The hy-
pothesis about the existence of at least one variable
associated with greater inaccuracy of periapical radio-
RESULTS graphs was not confirmed by the results.
In terms of study limitations, the evaluation of mar-
Two hundred fifty patients were examined for inclu- ginal bone level took place by means of standardized
sion in the study. Of the 250 patients, 85 were declared digital periapical radiographs without any custom-
as not in compliance with the requirements. Twenty- ization of the radiographic jig. To compare bone lev-
three patients did not assent to the study. A total of els over time, the radiographic film position has to
142 patients were in succession included in this study be similar.1 Individualizing standard film holders can
and given treatment (n = 85 women [59.9%]; n = 57 resolve the problems that originate from a different
men [40.1%]; age range at time of implant placement, projection in a research environment, but this is not
21 to 78 years; mean, 55.08 years [SD: 12.43]). A total easy to achieve in daily practice.1 Over the years, many
of 268 implants were placed. Considering the implant efforts have been made to standardize periapical ra-
location, 38 implants were anterior (14.2%) and 230 diographs.10 The paralleling technique is currently
posterior (85.8%). When the variable arch is consid- the most commonly used method to visualize minute
ered, 146 implants were inserted in the maxilla (54.5%) bone changes. If the paralleling technique is applied
and 122 in the mandible (45.5%). One hundred eighty- without additional devices to ensure true parallelism
two implants were “early delayed” (67.9%) and 86 “pro- (when the film and implant are not in parallel and the
longed delayed” (32.1%). focus-object distance is below 380 mm), radiographic
Considering the radiographic measurement reli- measurement of marginal bone level reaches only a
ability, the interobserver agreement (ICC) was 0.980. precision of 0.5 mm.11 Considering the determined

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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Cassetta et al

precision of 0.5 mm,11 in this study, the values were the present clinical study: comparing the radiographic
rounded to the nearest millimeter. analysis with surgical measurements, the radiograph-
In order to make the analysis as objective as pos- ic analysis significantly overestimates the level of
sible, all the surgeries, the intraoperative measure- peri-implant marginal bone compared with surgical
ments, and the intraoral periapical radiographs were measurements.
performed by an experienced operator (M.C.), and Considering all the limits of periapical radiography,
two researchers, experts in implantology and den- cone beam computed tomography (CBCT) has been
tal radiology, evaluated the periapical radiographs proposed in the evaluation of marginal bone levels.
independently. Raes et al16 carried out a comparison between mar-
Considering the detection threshold for marginal ginal bone level measurements on periapical radio-
bone loss using periapical radiographs, if the real clini- graphs and CBCT around a sample of implants. A mean
cal conditions were considered, Ahlqvist et al12 stated difference of 0.47 mm (range: –0.47 to 3.13 mm), with
that the recognition limit for marginal bone loss was a very good significance level (P < .001), was detected
above 0.47 mm. These considerations support the between periapical radiographs and CBCT, the latter
choice of rounding the radiographic measurements systematically underrating the bone level. According
to the nearest millimeter. In this way, the radiographic to De Bruyn et al,1 although the periapical radiograph-
and clinical measurements have been rounded us- ic technique is a two-dimensional technique and may
ing the same criterion. This makes the measurements underestimate the presence of vestibular and lingual/
comparable in the current analysis. palatal defects, it remains the most reliable method for
In the past, using analog x-ray machines, the same measuring the peri-implant marginal bone level.
kind of film and the same radiation parameters were Considering the possible sources of error, Brägger
employed.1 Nowadays, the availability of digital radio- et al17 stated the presence of a learning curve when
graphs has enabled standard and, henceforth easier, the peri-implant bone levels were assessed. In order
image contrast management.1,13 Considering the use to reduce the risk of error, in the present study, peri-
of a photostimulable phosphor system, the system apical radiographs were evaluated by experienced
used in the present study, the image contrast may be operators who had previously participated in similar
modified using dedicated software, making it easier to studies.2,3 Brägger et al 17 also pointed out that mea-
compare the images of the different follow-ups.13 An- surement errors may be related to variation in projec-
other aspect that must be considered is represented tion. A symmetric imaging error in the vertical plane
by the lower resolution of phosphor plate radiography. occurs frequently in patients with atrophic mandibles
Although the phosphor plate resolution performance when there is a limited mouth opening or when the
is inferior to that of film, it is sufficiently adequate for implant-supported prosthetic restoration is high and
the needs of oral radiology.4 the x-ray film is too short to reach the area of inter-
Evaluating the possible difference between the in- est.18 In these cases, it is difficult to obtain a parallelism
traoperative measurements of peri-implant marginal between the implant and the periapical radiograph,
bone levels and the bone levels determined using maintaining an orthogonal x-ray beam. The symmetric
periapical radiographs, Caulier et al14 stated that the imaging error in the vertical plane can be easily cor-
periapical radiographs underrate the real peri-implant rected by referring the thread pitch or implant length
bone loss, as evaluated histomorphometrically in an for calibration.1 In the present study, as already de-
experimental animal study. In a study aimed at eval- scribed,2,3 the distortion of each individual radiograph
uating the accuracy and reliability of radiographic was determined, and the radiographic measurements
techniques for measurement of the marginal bone were adjusted according to this distortion for each in-
level around oral implants in human corpses, the ra- dividual radiograph.
diographic measurements were found to be higher Sewerin, in a study conducted in 1990,10 analyzed
(overestimated) than the real measurements.9 The how the buccolingual bone size, along with angula-
difference, however, was not statistically significant tions of the implant axis to the central x-ray beam, and
(P > .05).9 Isidor, in a study aimed to evaluate the clini- position of the implant (buccal, central, lingual) affect
cal probe level, radiographic bone level, and histologic the peri-implant marginal bone level measurements.
bone level around implants in monkeys,15 demonstrat- The risk of overestimating bone height was greater
ed that radiographic assessment estimated the loss when the width of the alveolar ridge was higher, when
in marginal bone level around implants better than the angulation between the implant axis and central
clinical probing with or without a standardized prob- x-ray beam/film plane was higher than 1 degree, and
ing force, also concluding that radiographic evalua- when the position of the implant was lingual.10 In the
tion tends to underestimate the marginal bone loss. present study, variables such as arch, implant location,
These findings have been confirmed by the results of and timing of implant placement did not influence

The International Journal of Oral & Maxillofacial Implants 851

© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Cassetta et al

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The authors reported no conflicts of interest related to this study.

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© 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
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