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 535

Comparison of Bone-Level and Tissue-Level Implants:

A Pilot Study with a Histologic Analysis and a 4-Year Follow-up

Maria Menini, PhD, DDS1 One of the potential variables iden-

Elena Dellepiane, DDS, PhD1 tified as playing a major role in the
Talita Deiana, DDS1 preservation of peri-implant tissues
Ezio Fulcheri, MD2 is the implant collar design.1,2 Al-
Paolo Pera, MD, DDS, PhD1/Paolo Pesce, DDS, PhD1 though there is a large variety of im-
plant configurations available on the
This study clinically and histologically evaluated the performance of implants with market, implant systems can gener-
different crestal morphologies: tissue-level implants and bone-level implants. Nine ally be divided into bone-level and
patients received at least two adjacent implants in an edentulous area: one bone- tissue-level. In a tissue-level implant,
level implant (EO) and one tissue-level implant (TG) (total: 23 implants), placed
the transmucosal component fac-
beside each other using a single-stage delayed loading protocol. The implants
were rehabilitated with screw-retained fixed partial dentures. Plaque Index (PI), ing peri-implant soft tissues is part
bleeding on probing (BOP), probing depth (PD), and peri-implant bone level were of the implant body. These implants
recorded at various postsurgical follow-ups, including 2 and 6 months as well as are placed with a one-stage surgery
1 and 4 years. At 3 months postsurgery, soft tissue biopsy samples were taken and they immediately pierce the
from all implant sites and histologically analyzed. Longitudinal assessment of the soft tissue barrier (nonsubmerged
results (TG vs EO implants) was performed using a linear mixed model with random
approach). In a bone-level implant
intercept and by using Spearman correlation or chi-square after visual inspection
of the probability distribution. Student t test was used to compare means, and chi- system, the transmucosal compo-
square test was used for dichotomic variables. P < .05 was considered statistically nent is a separate device from the
significant. All implants were functional at 4 years. Peri-implant bone resorption endosseous implant body. These
was limited, with means of 1.20 ± 0.71 mm and 1.24 ± 0.82 mm for TG and EO implants can either be submerged
implants, respectively. No significant differences in clinical parameters were under soft tissue during the healing
identified between EO and TG implants. Histologic analysis revealed normal peri-
period (two-stage surgery), or they
implant soft tissue healing with poor inflammatory infiltrate. Differences in the
histologic appearance of soft tissues were more related to patients than implant can be placed following a one-stage
type. Both implants appeared to be suitable for partial rehabilitation of edentulous surgery using healing abutments.
arches without differences in the investigated clinical and histologic parameters. The bone-level implant systems
However, TG implants showed a greater risk of implant collar exposure. Int J present a microgap between the
Periodontics Restorative Dent 2022;42:535–543. doi: 10.11607/prd.4990 endosseous implant and the trans-
mucosal component. The microgap
is generally located in proximity to
the alveolar bone crest and might
present an issue of microbial coloni-
Division of Implant Prosthodontics, Department of Surgical Sciences, University of Genoa,
1
zation; still, several studies reported
Genoa, Italy. no adverse effect on peri-implant
2
Department of Surgical Sciences, University of Genoa, Genoa, Italy.
bone loss3 if a supracrestal connec-
Correspondence to: Dr Elena Dellepiane, Department of Fixed and Implant Prosthodontics, tive tissue barrier is established after
University of Genoa, Largo R. Benzi 10, 16132 Genoa, Italy. Email: [email protected] implant placement.4 In contrast, the
evaluation of four different implant-
Submitted March 29, 2020; accepted August 15, 2020.
©2022 by Quintessence Publishing Co Inc. abutment interfaces showed that

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536

all of the analyzed connections pre- titanium healing abutments in the tional bone-level implants, recording
sented contamination after 5 years short term. Other studies16 agree clinical parameters and histologically
of functional loading.5 It also ap- that abutment design may influ- analyzing soft peri-implant tissues.
peared that the connection design ence marginal bone loss but do not
might have qualitatively and quan- impact soft tissues. However, the
titatively influenced bacterial count existing evidence is moderate, as Materials and Methods
levels, especially inside the implant few randomized controlled trials
connections, showing better results were conducted and the follow-up Between February and October
for the conical connection.6 Similar- periods were short.16 2015, a sample of nine patients (three
ly, different abutment types showed Some studies compared the women, six men) with a mean age of
significant variations in mean micro- performance of implants with dif- 61 years (range: 52 to 78 years) was
gap size within the first 5 hours of ferent crestal morphologies.17–19 recruited for the present study. The
loading.7 However, no significant in- Thoma et al20 compared clinical and patients referred to the Division of
fluence of micro-leakage was found radiographic outcomes of implants Implant Prosthodontics of the De-
in bacterial count at 24 hours, 48 and implant-supported reconstruc- partment of Surgical Sciences at the
hours, and 14 days postplacement. tions using bone-level and tissue- University of Genoa and needed
It has been suggested that peri- level implants. Within the first year fixed partial dentures supported by
implant soft tissue can create a bio- of functional loading, high survival at least two adjacent implants in the
logic seal, protecting peri-implant rates and minimal changes in mar- same dental quadrant.
bone from the highly contaminated ginal bone levels were found for Inclusion criteria for the study
oral environment8 and reducing the both implant systems. were as follows: good systemic
risk of bone resorption.9 Cell adhe- Although several authors have health without contraindications
sion to the abutment surface is me- provided evidence of successful os- for oral surgery; partial edentulism;
diated by the formation of hemides- seointegration with bone- or tissue- teeth in treated areas were extract-
mosomes, similar to that found at level implants, as well as with either ed at least 1 year before; no need
natural teeth.10,11 Limited data from nonsubmerged or submerged inser- for bone regenerative procedures;
animal studies suggest that some tion protocols, most studies report no unbalanced diabetes or meta-
characteristics of the transmuco- soft tissue parameters and interprox- bolic osseous diseases; no heavy
sal implant components may affect imal bone level measurements,21,22 smokers (≥ 20 cigarettes/day) nor
peri-implant soft-tissue adhesion neglecting the histologic aspect. The habitual alcohol consumers.
and stabilization but do not allow results of several studies23–25 seem All patients were informed
definitive conclusions.12 to indicate that the dimensions and about the study protocol and pro-
Thus, it can be assumed that composition of the biologic width vided written informed consent
titanium surface treatment could are not significantly influenced by im- prior to the start of the study. All
influence the quality/quantity of plant type (bone- or tissue-level) or treatments were performed in
cell attachment as well as the heal- surgical protocol (one- or two-stage). agreement with the World Medical
ing process and host response.10,11,13 However, limited evidence suggests Association Helsinki Declaration.
However, a recent systematic re- that implants placed more deeply The study was approved by the lo-
view14,15 analyzing peri-implant tis- lead to a longer biologic width. cal ethical committee of the Univer-
sue behavior around titanium abut- Moreover, randomized clinical sity of Genoa (protocol no. 527).
ment surface modifications did not trials comparing bone- and tissue- Each patient received at least
reveal any variations in terms of level implants are scarce in the lit- two adjacent implants in an eden-
Plaque Index (PI), bleeding on prob- erature. Therefore, the aim of this tulous quadrant, with at least one
ing (BOP), or probing depth (PD) split-mouth study was to evaluate the Premium Straight implant (bone lev-
between machined and modified outcomes of tissue-level and tradi- el; EO) and one adjacent Premium

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 537

a b c
Fig 1  Each patient received two adjacent implants into an edentulous quadrant: (a) one Premium Transgingival implant (TG, test site) and
(b) one endosseous Premium Straight implant (EO, control site). (c) Example clinical view from a study patient. A machined surgical screw
was placed on the TG implant (left), and a standard machined healing abutment was placed on the EO implant (right).

Transgingival implant (tissue level; implants, the interface between the Radiographic Analysis of
TG) (Sweden & Martina) per edentu- ZirTi surface and the machined collar Interproximal Bone Levels
lous area (Figs 1a and 1b), with the was placed at the bone crest level.
most distal implant chosen on the During surgery, cortical and Standardized periapical radiographs
basis of a draw. cancellous bone quality were sub- were taken to investigate interproxi-
Both EO and TG implants were jectively evaluated by the surgeon mal bone levels at baseline (immedi-
made of commercially pure tita- and classified as 1 (dense), 2 (me- ately after implant insertion) and at
nium (grade IV) with a ZirTi (zirco- dium), or 3 (soft).26 2, 4, and 6 months and 1 and 4 years
nium airborne particle–abraded Implants were placed according after implant placement (Fig 2). The
and acid-etched titanium) surface to a single-stage surgical protocol radiographs were taken using a
(Sa = 1.3 µm) and were cylinder- and were assigned specific codes long-cone parallel technique with
shaped with a conical progression for blinding, as described in a pre- an individualized film holder (Rinn
only in the apical portion. EO im- vious study.26 Due to the different bite film holder, Dentsply Sirona).
plants had a machined collar (Sa = morphologies of the coronal portion The implant-abutment inter-
0.6 µm) that was 0.80 mm high and of the implants, blinding was not face (the microgap) was used as the
an internal hexagon connection. possible during clinical procedures. reference point for interproximal
TG implants differ from EO ones Only the statistician was blinded. bone-level measurements. Bone re-
only for the machined transgingival EO implants received standard ma- sorption (BR) over the study period
portion, which was 2.2 mm high (re- chined healing abutments, while TG was assessed from these reference
gardless of the endosseous implant implants received machined surgical points to the most coronal bone
length). The prosthetic connection screws (Fig 1c). at the mesial and distal aspects of
makes use of both the conical fric- The healing abutments and each implant. The measurements
tion concept and internal hexagon screws remained in situ up to the were performed with a diapha-
connection. All implants had a diam- 4-month follow-up, when implant noscope and magnifying lens. To
eter of 3.8 mm, with lengths ranging impressions were taken to fabricate calculate BR, overcoming possible
between 10 and 13 mm (depending the fixed prostheses. Screw-retained radiographic deformations, the fol-
on bone availability). EO implants fixed partial dentures were delivered lowing equation was used:
were placed completely endosse- 2 weeks later. They were provided BR = (Li x BRrx) / Lirx
ously, with their coronal platform with a metal framework and compos- Where Li = implant length;
at the bone crest level, while for TG ite resin veneering material. Lirx = implant length as measured in

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538

a b c
Fig 2  Peri-implant soft tissue biopsy samples that contained both epithelium and connective tissue were collected from each implant site
and stained with hematoxylin and eosin. (a) Section of a biopsy sample taken from the peri-implant mucosa surrounding an EO implant.
Reactive and reparative characteristics of the epithelium can be seen. (b) A magnified view of Fig 6a shows inflammatory aggregates.
(c) Section of a biopsy sample taken from the peri-implant mucosa surrounding a TG implant. Hyperkeratotic epithelium (with a thickened,
cornified layer) and acanthotic epithelium (with prominent epithelial ridges and reduced connective tissue papillae) can be seen.

the radiograph; BRrx = bone resorp- categories according to periodontal were marked with the clinical chart
tion as measured in the radiograph. biotype (thin or thick). To evaluate number to preserve anonymity.
the biotype, a periodontal probe
was placed into the facial aspect of
Soft Tissue Health Parameters the peri-implant mucosa. The peri- Histologic Analysis
implant biotype was categorized as
PI (according to O’Leary et al27) thin if the outline of the underlying Three months after surgery, palatal
was used with the help of a plaque periodontal probe could be seen or lingual minimally invasive peri-
detector based on eritrosin (But- through the gingiva and thick if the implant soft tissue biopsy samples
ler GUM Red-Cote Liquid, Sunstar probe could not be seen.28 (diameter: < 3 mm) containing both
Americas). BOP (yes/no) and PD The patient satisfaction ques- epithelium and connective tissue
were recorded with the nonmetal- tionnaire included six questions were collected from each implant
lic periodontal probe at four points related to the following: possible site using a surgical blade.
for each implant. PI was recorded presence of pain (question 1); satis- The samples were fixed in for-
at 1, 2, 3, and 6 months and at 1 faction regarding masticatory abil- malin 10% and analyzed at the Divi-
and 4 years after implant place- ity (question 2); satisfaction regard- sion of Pathological Anatomy (De-
ment; BOP and PD were recorded ing the esthetic appearance of the partment of Surgical Sciences) of the
at 2, 3, and 6 months and at 1 and rehabilitation (question 3); global University of Genoa. The samples
4 years after implant placement. At satisfaction regarding the implant were embedded in resin because of
the 4-year follow-up, the health of prosthodontic rehabilitation (ques- their small size. Then, they were fixed
peri-implant tissues (suppuration, tion 4); and satisfaction regarding and left for 3 days in alcohol and
spontaneous bleeding, presence/ instructions and care provided by later in a solution of 50% absolute
absence of keratinized gingiva, the dental team regarding oral hy- alcohol + 50% ether + grains of silica
presence/absence of a frenulum giene (questions 5 and 6). Each item gel (or 80% absolute alcohol + 20%
next to the implant, periodontal was rated on a scale of 1 to 5, with ether) at room temperature for at
biotype, and covered/not covered 1 being the worst score and 5 being least 24 hours. The samples were
implant collar) and patient satisfac- the best score. An additional space dehydrated with absolute alcohol
tion after implant therapy were also was left for free comments. Patients and infiltrated with a Sulphur solution
investigated using specific ques- completed the questionnaire alone for 72 hours in solution A (100 mL of
tionnaires realized for this study. but were able to call a clinician for resin [Technovit 8100, Kulzer] + 0.6 g
Implant sites were divided into two help if needed. The questionnaires of hardener 1). The samples were then

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 539

embedded in a cold PTFE (polytet- was the outcome and the indepen- other clinical parameters recorded
rafluroethylene) plate with 15 mL of dent variables were time indices, (PI, PD, BOP), and no statistically
solution A + 0.5 mL hardener 2. The the treatment group (TG or EO), and significant correlation was found
plate was cooled for 5 to 10 minutes their interaction. P < .05 was con- between bone resorption over time
with ice and put in the fridge for 24 sidered statistically significant, and and bone quality and implant stabil-
hours. Technovit 3400 resin (Kul- SPSS (version 21, IBM) was used for ity at implant insertion.
zer) was drained into the wells of the computation. The histologic analysis revealed
plate to create the blocks. The blocks that soft tissues were healthy, with a
were cut by a microtome, creating normal epithelium and chorion, with-
sections 2 to 3 µm thick. The sec- Results out signs of impaired repair in a ma-
tions were stained with hematoxylin jority of samples. None of the sam-
and eosin and analyzed by optical A total of 23 implants (11 EO, 12 TG) ples showed atrophy. The histologic
microscope. A form was completed were inserted in nine patients: one appearance was more favorable for
for each sample that indicated char- woman received 3 implants in an EO implants than TG implants. In
acteristics of the epithelium (normal, edentulous area, and two patients fact, three TG samples showed a re-
acanthotic, hyperkeratotic, atrophic, were each rehabilitated with two active and reparative epithelium, one
with reactive and reparative changes), fixed partial dentures each support- TG sample had a very vascularized
chorion (normal, with hyalinosis, with ed by 2 implants. All other patients chorion, and five TG samples were
fibrosis, very vascularized, poorly vas- received 2 adjacent implants. characterized by aggregated inflam-
cularized), and inflammation (absent, No patient was lost to recall mation in the basal membrane with
small near vessels, scattered, aggre- during the 4-year follow-up. Be- initial intraepithelial involvement;
gated, aggregated with connection tween the 1-year and 4-year follow- those characteristics were present in
to the basal membrane with initial in- ups, patients were recalled at least three, none, and three EO samples,
traepithelial involvement). The type of once a year for professional oral hy- respectively. However, the differenc-
phlogistic reaction was also classified giene and control, and all patients es between the samples appeared to
as a lympho-plasmo or a lympho- attended the scheduled follow-up be more related to the patients than
granular predominant type. appointments. Four years after im- to the implant type; ie, there were
plant placement, all implants were differences between the patients but
functional and stable, with implant not between implants inserted in the
Statistical Analysis survival and prosthodontic survival same patient.
rates of 100%. All patients showed Some histologic patterns were
Quantitative characteristics and de- limited crestal bone resorption at 4 repeated in the samples: Repara-
scriptive analyses were reported as years, with a mean of 1.20 ± 0.71 mm tive epithelium was present in six
mean ± SD. Longitudinal assess- for TG and 1.24 ± 0.82 mm for EO cases, and small inflammation near
ment of the implant results (TG vs implants (Table 1, Fig 3). Student the vessels was seen in four of those
EO) throughout the study was per- t test showed a nonsignificant dif- six cases.
formed using a linear mixed model ference between TG and EO for Considering TG and EO, chi-
with random intercept and by using bone resorption after 4 years square test showed a nonsignificant
Spearman correlation or chi-square (P = .592). The linear mixed model difference for the following variables
test after visual inspection of the showed a significant difference (P = at 4 years: suppuration, spontane-
probability distribution. Student t .001) over time when treatment was ous bleeding, presence/absence
test was used to compare means. considered as grouping variable of keratinized gingiva, presence/
Chi-square test was used for dichot- (time*treatment interaction). No absence of frenulum, and periodon-
omous variables. In all regression significant differences were present tal biotype (Table 2). Four months
models, the dependent variable between the two implants for the after surgery, two women presented

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540

1.24
1.20

1.00
1.20
0.84
Bone resorption (mm)

0.80
0.81
0.62
0.49
0.60
0.60
0.43
0.40
0.30

TG
0.29
0.20
EO

0.00
T0

2 mo

4 mo

6 mo

1y

4y
Time

Fig 3  Mean bone resorption (in millimeters) over time for endosseous (EO; bone-level) and transgingival (TG; tissue-level) implants.
T0 = baseline.

Table 1  Health Parameters of Peri-implant Tissues: Assessments Over Time

Treatment Implants, n Baseline 6 mo 1y 4y
Bone resorption, mm
EO 11 0.00 ± 0.00 0.60 ± 0.68 0.81 ± 0.81 1.24 ± 0.82
TG 12 0.00 ± 0.00 0.43 ± 0.77 0.84 ± 0.77 1.20 ± 0.71
EO + TG 23 0.00 ± 0.00 0.51 ± 0.72 0.82 ± 0.77 1.22 ± 0.74
Plaque Index
EO 11 – 0.45 ± 1.04 1.64 ± 1.91 0.73 ± 1.62
TG 12 – 0.62 ± 0.35 1.38 ± 1.26 1.81 ± 0.87
EO + TG 23 – 0.35 ± 0.83 1.26 ± 1.66 0.87 ± 1.69
Bleeding on probing (no. of surfaces presenting BOP per implant)
EO 11 – 0.36 ± 0.50 0.73 ± 0.90 0.45 ± 0.82
TG 12 – 0.50 ± 0.67 0.67 ± 0.78 0.50 ± 0.80
EO + TG 23 – 0.43 ± 0.59 0.70 ± 0.82 0.48 ± 0.79
Probing depth, mm
EO 11 – 1.83 ± 0.97 2.12 ± 1.11 2.37 ± 0.78
TG 12 – 1.43 ± 0.99 1.79 ± 1.02 2.49 ± 0.70
EO + TG 23 – 1.62 ± 0.98 1.95 ± 1.05 2.44 ± 0.72
EO = endosseous (bone-level) implants; TG = transgingival (tissue-level) implants; Baseline = immediately after implant placement.
Values are presented as mean ± SD.
Longitudinal assessment of the implant results throughout the study period was performed using a linear mixed model with random inter-
cept and by using Spearman correlation or chi-square tests. No significant differences were present between the two implants (EO vs TG)
for the clinical parameters recorded. The linear mixed model showed a significant difference in bone resorption over time when considering
treatment as grouping variable (time*treatment interaction) (P = .001).

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 541

Table 2  Descriptive Results for EO vs TG Implants at the 4-Year Follow-up

4-y outcomesa
No. of cases/total
Clinical parameter Implant % group no. Pb
EO 27 3/11
Presence of spontaneous
TG 8 1/12 .231
bleeding
EO+TG 17 4/23
EO 0 0/11
Presence of suppuration TG 0 0/12 –
EO+TG 0 0/23
EO 27 3/11
Thick periodontal biotype TG 25 3/12 .901
EO+TG 26 6/23
EO 2.18 mm 1.40 mm
Keratinized gingivaa,
TG 2.58 mm 1.62 mm .844
mean ± SD
EO+TG 2.39 mm 1.50 mm
EO 9 1/11
Frenulum presence TG 8 1/12 .949
EO+TG 9 2/23
EO 9 1/11
Exposed implant collar TG 25 3/12 .315
EO+TG 17 4/23
TG = transgingival (tissue-level) implants; EO = endosseous (bone-level) implants.
None of the evaluated parameters showed a statistically significant difference between EO and TG implants.
aAll data are presented as percentages (first outcome column) and numbers of cases/total sites per group (second outcome column) except

for keratinized gingiva, which is presented as means (first outcome column) and SDs (second outcome column).
bDifference between TG and EO.

an exposed TG implant collar (Fig was partially disappointed by the remodeling in the postsurgical pe-
4). At the 4-year follow-up, one man esthetic aspect of the rehabilitation, riod. At 4 years, the bone level was
showed one exposed collar of each and the other two patients declared within normal limits without statisti-
implant type. complete esthetic satisfaction. cally significant differences between
All patients completed the satis- the two implant types. However,
faction questionnaire and declared the main limit of the present study
to be globally satisfied after 4 years Discussion is the small number of evaluated
of treatment. None of the patients implants, which caused very large
reported the presence of pain. The Both implant systems appeared standard deviations and may pre-
satisfaction was particularly high re- to be suitable and reliable for re- vent one from drawing sound con-
garding the masticatory ability and habilitation of partially edentulous clusions from this data.
the instructions and care provided arches without differences in the Moreover, at implant insertion,
by the dental team for their oral hy- analyzed clinical parameters. The the TG implant with the 2.2-mm
giene. Despite the exposed implant small BR observed during the first machined collar had a rough sur-
collars in three patients, only one year corresponded to normal bone face at the crest. Meanwhile, the EO

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542

tissue-level implants with a diver- regarding tissue thickness, crown

gent collar. A gingival recession may height, and facial volume for both
be easier to manage using bone- implant types.
level implants that are more versa- The present study includes a re-
tile, whereas tissue-level systems duced number of patients, preclud-
are simpler and suitable for virtually ing robust conclusions. Nonethe-
any application in zones that are not less, there was no loss to follow-up,
esthetically sensitive. However, their and the randomization approach en-
positioning is problematic in areas sured identical assessments of both
where a display of grayish metal col- EO and TG implants. Moreover, the
or at the restoration margin should risk of bias was further minimized, as
be avoided. Recently, tissue-level the implants were identical except
Fig 4  Four months after implant place- implants with a convergent collar for their coronal portions.
ment, an exposed implant collar occurred
next to a TG implant due to gingival have been introduced to the market
recession (arrow). Although no statistically with the aim of avoiding such incon-
significant differences were found between
veniences.30 Unlike a divergent de- Conclusions
EO and TG implants in the investigated
clinical parameters (PI, BOP, PD, and BR), 3 sign, the convergent design of the
of 12 TG implants have an exposed metal transmucosal components increases Both implants appeared to be suit-
collar.
the available space for the connec- able and reliable for rehabilitation
tive compartment of the supra- of edentulous arches, without differ-
crestal tissue attachment, aiming to ences in the investigated clinical and
implant with the 0.8-mm machined increase tissue thickness.30 Further histologic parameters. However, tis-
collar was endosseous and had a research is needed to validate the sue-level implants showed a greater
microgap at the crest, meaning that advantages of this implant design. risk of implant collar exposure, sug-
the surface roughness was 0.8 mm An original aspect of the pres- gesting that their positioning should
below the bone crest. This could ent study is the method applied for be avoided in esthetic areas.
have impacted the peri-implant BR. the histologic analysis, which was
The present results agree with conducted on very small, minimally
those of other studies17–19,29 investi- invasive peri-implant soft tissue Acknowledgments
gating the marginal bone remodel- samples (< 3 mm). Due to their small
ing and soft tissue health surround- size, the samples were embedded The present research was partly funded by
ing bone- and tissue-level implants: in resin instead of paraffin. Sweden & Martina (Due Carrare, PD, Italy).
The authors declare no conflicts of interest.
Excellent clinical and radiographic Although a histologic compari-
conditions were reported for both son between the peri-implant soft
implant types. However, the tradi- tissue surrounding bone- vs tissue-
tional evaluated parameters (that level implants is not present in the References
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In fact, three patients showed an ated volumetric changes in hard and
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gingival recession, jeopardizing the sis insertion to the 1-year follow-up level changes at dental implants after 5
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the main drawback of traditional loading, minimal changes occurred

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 543

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Volume 42, Number 4, 2022

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