Received: 12 June 2020Revised: 20 September 2020Accepted: 29 September 2020

DOI: 10.1002/JPER.20-0458

ORIGIN AL AR TICLE

Impact of mucosal phenotype on marginal bone levels

around tissue level implants: A prospective controlled trial

Carlos Garaicoa-Pazmino1,2 Gustavo Alice Ou3

Mendonça3
Hsun-Liang Chan3 James Mailoa4 Fernando Suárez-López Del Amo5
Hom-Lay Wang3

1
Department of Periodontology, School of
Dentistry, Oregon Health & Science
University, Portland, OR, USA Abstract
2
School of Dentistry, Espiritu Santo Background: The aim of this 1-year prospective clinical trial was to com- pare
University, Samborondon, Ecuador clinical parameters and marginal bone levels (MBLs) around tissue level
3
Department of Periodontics and Oral implants with a partially smooth collar between patients with thin (≤2 mm) and thick
Medicine, University of Michigan School of
Dentistry, Ann Arbor, MI, USA (>2 mm) vertical mucosal phenotypes.
4
Private Practice, Sulawesi, Makassar, Methods: Thirty patients needing a single dental implant were recruited and
Indonesia allocated to thin (n = 14) or thick (n = 16) phenotype groups. Post-restoration,
5
Private Practice, Tacoma, WA, USA
clinical (probing depth, recession, width of keratinized mucosa, bleeding on
Correspondence probing, suppuration, implant mobility, plaque index, and gingival index) and
Hom-Lay Wang, Department of Peri- radiographic bone level measurements were recorded at different timepoints for 1
odontics and Oral Medicine, University of year.
Michigan School of Dentistry, 1011 North
University Avenue, Ann Arbor, MI 48109- Results: Twenty-six patients (13 per group) completed the 1-year examination.
1078, USA. No implants were lost (100% survival rate). There were no significant differences (P
Email: homlay@umich.edu >0.05) between thin and thick vertical mucosal phenotypes for any clinical
parameter or for the radiographic MBL.
Conclusions: Tissue level implants at 1 year of function placed in thin vertical
mucosa achieved similar clinical parameters and radiographic MBLs as those in thick
tissue. The formation of the peri-implant supracrestal tissue height plays a key role
in MBL than mucosal thickness in tissue level implant.

KEYW ORDS
phenotype, dental implant, soft tissue therapy, peri-implant endosseous healing, alveolar bone loss

1 INTRODUCTION by Avila-Ortiz et al., the peri-implant STH is composed of

the sulcular epithelium, junctional epithelium, and the
A recent literature review proposed that the peri-implant supracrestal connective tissue around an implant; the authors
mucosal phenotype (i.e., horizontal and/or vertical mucosal stated that STH affects bone remodeling independently from
thickness) may influence bone remodeling around dental implant level design or prosthetic features.3 In dogs, a
implants.1 An animal study has corre- lated the presence of surgically-induced thin (≤2 mm) phe- notype produced
angular bony defects with thin peri-implant supracrestal slightly more bone resorption, implying that a minimum
tissue height (STH).2 Defined mucosal thickness is required to allow

J Periodontol. 2021;92:771–783. © 2020 American Academy of Periodontology771

 GARAICOA-PAZMINO
77 ET AL.

the formation of a stable STH. 4 In a series of prospec- tive

trials on humans, Linkevicius and coworkers have shown 2 MATERIALS AND METHODS
that implant sites in subjects with a thin (≤2 mm) vertical
mucosal phenotype develop more radiographic bone loss than This prospective cohort study was reviewed and approved by
sites in subjects with a thick (>2 mm) phenotype.5–8 the University of Michigan Health Science Institu- tional
Several authors have suggested that marginal bone loss can Review Board (HUM00095933), registered at Clin-
be mitigated by platform switching, or the lateral positioning icalTrials.gov (ID:NCT02925078), and conducted in accor-
of the implant platform-abutment interface away from the dance with the Helsinki Declaration of 1964 as revised in
alveolar bone and toward the center of the implant.9–11 2013. Research subjects were recruited from new or active
Vanderweghe and DeBruyn concluded that platform patients receiving dental care at the University of Michigan
switching reduces marginal bone loss by up to 30% only in School of Dentistry from November 2016 through Decem-
sites where the peri-implant mucosa is thicker than 4.22 mm.12 ber 2019. Before enrollment, each subject received infor-
Linkevicius et al. found platform switch- ing does not mation about the study design and signed an informed
prevent radiographic bone loss in sites with a thin mucosal consent. A summary of this study timeline is depicted in
Figure 1A.
phenotype.6 A systematic review by Hsu et al. reported a
mean marginal bone loss of 0.36 mm within the first year of
function in platform-switched implants and a trend toward less 2.1 Patient selection
bone resorption at sites with a thick hor- izontal mucosal
phenotype.13
The vertical positioning of the implant platform with respect Patients who were eligible for the study fulfilled all seven of
to the alveolar crest (e.g., subcrestal, equicrestal, the following criteria: 1) aged >18 years, 2) partially
edentulous at a maxillary or mandibular premolar or first molar
region, 3) adjacent teeth present mesial and distal to the
edentulous
bone width site, 4) residual bone height >9 mm and
or supracrestal) at time of placement14 as well as pros- >5 mm, 5)>2 mm width of KM, 6) optimal
thetic factors that create vertical distance between bone 26
and restorative components (e.g., abutment height, crown oral hygiene (full-mouth plaque scores of <10%), and 7)
15 clinical gingival health on an intact or reduced periodon- tium.
contours) can also affect post-surgical bone remodel- ing.
Several researchers have argued that the marginal bone is Exclusion criteria included any of the following: 1) need for
preserved not by having thick mucosa but by using an bone augmentation, 2) current smoking or smok- ing cessation
abutment over 2 to 3 mm tall.15–17 Pico et al. of <1 year, 3) current or planned pregnancy,
demonstrated that marginal bone loss is twice as severe when 4) uncontrolled systemic disease, 5) conditions known to alter
short (1 mm) instead of tall (3 mm) abutments were used on bone metabolism (e.g., diabetes, osteopenia, osteo- porosis,
platform-switched implants placed equicre- stally, regardless of hyperparathyroidism), 6) current or historical use of oral or
mucosal phenotype.18 Over-contoured crowns (emergence intravenous bisphosphonates, 7) history of radi- ation therapy, 8)
angle >30◦) placed on bone level implants have four times need for active periodontal therapy, or
more radiographic bone loss than tissue level implants due to 9) poor oral hygiene. Figure 1B shows the experimental
patient’s reduced ability to clean these restorations during self- flowchart for this study.
perform mechani- cal plaque control.19 As most studies find
that thin ver- tical and horizontal mucosal phenotypes and a 2.2 Presurgical screening
lack of keratinized mucosa increase the risk of peri-implant
dis- eases, the current clinical dogma is to place implants in
sites with thick and adequate keratinized mucosa (KM), Patients were allocated to the thin (≤2 mm) or thick (>2
whether these conditions are natively present or surgi- cally mm) vertical mucosal phenotype group at a presur- gical
enhanced.20,21–24 Scarce material exists on the impact of screening appointment.8 Under local anesthesia, an endodontic
mucosal phenotype on the marginal bone level (MBL) file with a rubber stopper was used to mea- sure the vertical
around tissue level implants.25 The aim of this prospec- tive mucosal thickness of the edentulous site at the mid-crestal
clinical trial is to compare clinical parameters and MBL region. Standardized intraoral radio- graphs and cone-beam
around implants with a 1.8-mm supracrestal smooth collar computerized tomography (CBCT) were taken to confirm
between patients with a thin (≤2 mm) vertical mucosal adequate ridge dimensions that pre- cluded advanced grafting.
Customized putty bite blocks were fabricated for each patient
phenotype and those with a thick (>2 mm) presentation. to ensure reproducibility of standardized digital intraoral
radiographs. Preliminary alginate impressions were taken to
fabricate study models,
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FIGURE 1 Experiment timeline and flowchart.A)Study timeline.B) Flowchart of patient allocation, intervention and postoperative follow-ups

and a surgical guide was made based on ideal prosthetic

positioning, which was confirmed through CBCT analysis. with 1:50,000 epinephrine for hemostasis. Intrasulcular
incisions were made around the teeth adjacent to the eden-
tulous site, and a mid-crestal incision was made bisecting the
width of KM. A full-thickness flap was raised on the buccal
2.3 Surgical protocol and lingual/palatal aspects of the edentulous site to expose the
alveolar ridge. A dental caliper* and a peri-
Each implant placement (IP) was performed by an expe-
rienced periodontist (HLW) under local anesthesia with
2% lidocaine with 1:100,000 epinephrine and 2% lidocaine *
Backhaus dental implant caliper, ProDent USA, East Brunswick, NJ.
 GARAICOA-PAZMINO
77 ET AL.

F I G U R E 2 Illustration of clinical and radiographic measurements. A) A periodontal probe and (B) a dental caliper were used to measure mucosal
thickness and alveolar ridge width. C) Diagram to illustrate radiographic measurements included distance from first implant thread to bone-implant
contact (BIC) (first thread-BIC) and implant platform to BIC (platform-BIC)

odontal probe* were used to measure mucosal thickness at 3 were used to close each surgical site. A standardized peri-
mm apical to the incision line on the buccal flap (hor- apical radiograph was taken post-surgically.
izontal mucosal thickness) and vertical mucosa height in the
center of the ridge at the time of surgery (Figure 2A).
Osteotomies were performed following the manufac-
turer’s drilling sequence using a surgical guide. After site 2.4 Postoperative instructions
preparation was completed, a dental implant † was placed in the
premolar or first molar region; the smooth-rough junction along Subjects were instructed to rinse with warm salt water once a
the implant collar was surgically positioned at the crest such that day for 2 weeks. All subjects were prescribed amoxicillin
only the machined portion was supracrestal. Either 3.8-mm 500 mg three times a day for 10 days. If an allergy to amox-
diameter, 3.5-mm platform implants or 4.5-mm diameter, icillin was reported, the patient was prescribed a 5-day dose
4.6-mm platform fixtures were placed based upon available pack of azithromycin 250 mg. Additionally, ibupro- fen 600
ridge width. Fixture length ranged between 9 to 12 mm mg was prescribed for swelling and pain control. Sutures
based on anatomical variations. Following placement, a 4-mm were removed 2 weeks postoperatively; checks to ensure
tall healing abut- ment with a regular emergence profile proper healing were performed 1 and 4 months post-
implantation.
(<30◦) was seated, and interrupted dense
polytetrafluoroethylene‡ sutures
2.5 Prosthetic protocol
*
University of North Carolina manual probe with 1 mm markings, Hu-
Friedy, Chicago, IL. All restorative treatment was completed by Gustavo
†
Tapered Tissue Level implant, BioHorizons, Birmingham, AL. Mendonca. Final crown impressions were performed 3 to
‡
dPTFE, Osteogenics Biomedical, Lubbock, TX. 5 months after implant placement. Crown delivery
GARAICOA-PAZMINO
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77
occurred 2- to 4-weeks post-impression. Custom abut-
ments and screw-retained implant prostheses were used. TA B L E 1 Baseline demographic data
Proper occlusion, flat or slightly convex crown con- tours, Thin group (n=13)
Thick group (n=13)
and sealed crown margins were achieved and/or confirmed
at the final restorative visit. Post-delivery adjustments were Variables
made based on patient need.
Age (years) 56.54 (10.39) 56.54 (13.30)
Sex (%) Women 5 (38.46%) 5 (38.46%)
Men 8 (61.53%) 8 (61.53%)
2.6 Clinical assessment
Vertical mucosal Preoperative 1.77 (0.72) 2.42 (0.49)
Clinical measurements including probing depths (PD), thickness (mm) Intraoperative 1.9 (0.48) 2.42 (0.45)
recession (REC), bleeding on probing (BOP), suppura- tion, Horizontal mucosal Intraoperative 0.65 (0.24) 0.99 (0.43)
plaque index (PI), gingival index (GI) at six sites (mesio- thickness (mm)
buccal, mid-buccal, disto-buccal, mesio-lingual, mid-
lingual, and disto-lingual) were recorded using a University Implant location (%) Maxilla 2 (15.38%) 6 (46.15%)
of North Carolina manual probe,* and implant mobility. Mean Mandible 11 7 (53.84%)
values among the six sites were obtained at the time of (84.61%)
implant crown delivery (CD) as well as Replaced tooth (%) Molar 9 (69.23%) 5 (38.46%)
6 months (T6) and 12 months (T12) post-restoration. Premolar 4 (30.76%) 8 (61.53%)
Additionally, width of KM was recorded post-surgically at
mid-facial during IP from mid-buccal mucosal margin to the Preoperative CBCT 7.45 (1.11) 6.85 (1.27)
mucogingival margin. Supportive implant therapy using Ridge width (mm)
mechanical instrumentation was also performed at T6 and
T12.
design.† According to a previous study,8 mean bone loss
around an implant placed in a thin tissue biotype (μ1) is
2.7 Radiographic assessment 1.450 mm; an implant placed in a thick tissue biotype has
0.170 mm of mean bone loss (μ2). The difference in means
between the two groups (μ 1– μ2) is 1.280 mm with a
Standardized radiographs were taken at crown impres- sion, common standard deviation (σ) of 1.160 mm. Based on
CD, T6, and T12; a new CBCT scan was taken at T12. these figures, the sample (n) needed in each group in this
Radiographic measurements included distance from first present study was calculated to be 14 patients. A non-
implant thread to bone-implant contact (BIC) (first thread- parametric analysis for longitudinal data (Brunner-Langer model)
BIC) ‒ pathologic bone remodeling and implant platform to was performed for all clinical and radiographic measurements.
BIC (platform-BIC) – physiologic bone remod- eling; these ANOVA-type statistics were used to detect differences
were taken at the time of implant placement (IP) through between groups at a 95% confidence interval.
T12 (Figure 2C). Preoperative and postoper- ative bone
width (BW) of the buccal and palatal/lingual plates were
measured from CBCT images using computer software.* 3 RESULTS
All measurements were collected (by CGP and JM) after
intra- and inter-examiner calibration. Using the Kappa test, the
inter- and intra-examiner agreements were calculated to be A total of 30 patients were identified—16 were allocated to the
0.79 and 0.85, respectively. thick tissue group (>2 mm vertical mucosal height), and 14
were allocated to the thin tissue group (≤2 mm vertical
mucosal height). Three patients in the thick tis- sue group
2.8 Statistical analysis dropped out of the study (one reported finan- cial limitation,
one moved away, and one was lost for unknown reasons); one
A test significance level (α) of 5% was used, and the power patient from the thin tissue group was dismissed due to non-
analysis was 80%. Sample size for each group was compliance. Twenty-six patients (13 per group) completed
calculated using a computer program with two-sided the 1-year study. A summary of the baseline demographic
equivalence for difference of proportions in two group data is presented in Table 1. No statistical difference was
noted between groups at base- line demographic, clinical, and
radiographic parameters (P >0.05). Figure 3 documents the
treatment and follow- up of a patient with a thick vertical
mucosal phenotype (Figures 3A and 3B) and one with a
thin vertical mucosal phenotype (Figures 3C and 3D).

†
*
Blue Sky Bio, Libertyville, IL. nQuery Advisor, version 7.0; Statsols, Los Angeles, CA.
 GARAICOA-PAZMINO
77 ET AL.

F I G U R E 3 Clinical cases illustration in both treatment groups. A) Thick tissue phenotype group; baseline, intraoperative, 6 months, and 12 months
postoperative documentation of a dental implant with thick (>2 mm) mucosal phenotype. B) Preoperative and 12 months postoperative CBCT evaluation
of a dental implant with thick (>2 mm) mucosal phenotype. C) Thin tissue phenotype group; baseline, intraoperative, 6 months, and 12 months
postoperative documentation of a dental implant with thin (≤2 mm) mucosal phenotype. D) Preoperative and 12 months postoperative CBCT
evaluation of a dental implant with thin (≤2 mm) mucosal phenotype
GARAICOA-PAZMINO
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77

3.1 Clinical findings TA B L E 2 Mean differences in clinical and radiographic

measurements between vertical and horizontal mucosal phenotypes (Mean
In the thick vertical tissue group, the intraoperative mean mid- differences in clinical measurements between thin (≤2 mm) and thick
buccal and mid-lingual bone width immediately fol- lowing (>2 mm) vertical mucosal phenotypes)
implant placement was 1.65 ± 0.98 mm and 1.65 Thin-
± 0.82 mm, respectively. In the thin vertical tissue group, Thin Thick thick
the corresponding measurements were 1.04 ± 0.64 mm and Variable Timeline Mean (SD) Mean (SD) (mm)
1.69 ± 0.75 mm, respectively. There were no significant PD (mm) CD 2.47 (0.46) 2.12 (0.25) 0.35
dif- ferences noted in buccal (P = 0.072) or lingual (P =
T6 3.42 (0.37) 3.36 (0.42) 0.06
0.902) bone thickness between the two groups immediately
fol- lowing implant placement. T12 3.13 (0.45) 3.46 (0.53) 0.33
Normal healthy clinical parameters (e.g., PD <4 mm, CD-T6 0.96 (0.57)* 1.24 (0.43)* 0.28
≥2 mm KM, and <0.5 mm REC) were observed in T6-T12 −0.29 (0.26)* 0.10.(0.51) 0.36*
both thin (≤2 mm) and thick (>2 mm) vertical tissue height CD-T12 0.65 (0.62)* 1.35 0.70*
groups for all recorded measurements (Tables 2 through 5). (0.58)*
Between CD and T12, the mean PD in the thin tissue KM (mm) IP 3.96 (1.65) 3.92 (1.36) 0.04
group increased by 0.65 mm (CD = 2.47 mm, T12 = CD 2.77 (1.24) 2.92 (1.05) 0.15
3.13 mm, P <0.001); mean PD deepened by 1.35 mm T6 3.00 (1.35) 3.00 (0.93) 0.00
(CD = 2.12 mm, T12 = 3.46 mm, P <0.001) in the thick
T12 2.96 (1.13) 2.96 (1.12) 0.00
phenotype group (Figure 4A). Deeper PDs were found
around implants with thick mucosa compared with those with IP-CD −1.19 −1.00 (0.96) 0.11
thin phenotypes from CD-T6 and CD-T12 (P <0.05). (1.15)*
Mid-facial PD and REC values, however, did not differ IP-T6 −0.96 −0.92 (0.86) 0.26
between groups from CD- T12 (P = 0.195) (see (1.35)*
supplementary Figure 1 in online Jour- nal of IP-T12 −1.00 (1.47)* −0.96 (1.03) 0.26
Periodontology). Mean REC values remained ≤0.3 mm CD-T6 0.23 (0.73) 0.08 (0.28) 0.15
and did not differ between groups at any timepoint (P CD-T12 0.19 (0.63) 0.04 (0.14) 0.15
>0.05) (Table 2, Figure 4B).
T6-T12 −0.04 (0.59) −0.04 (0.32) 0.00
There was a trend toward higher PI (thin group = 0.26 ±
REC CD 0.03 (0.09) 0.00 (0.00) 0.02
0.23 mm, thick group = 0.13 ± 0.13 mm), BOP (thin (mm)
group T6 0.03 (0.06) 0.00 (0.00) 0.03
= 42.31%, thick group = 34.62%), and GI (thin group = T12 0.03 (0.16) 0.02 (0.05) 0.01
0.58, thick group = 0.35) in the thin phenotype compared CD-T6 0.00 (0.07) 0.00 (0.00) 0.00
with the thick at 1-year post-restoration, but none of these
differences were statistically significant (Table 2; Figures T6-T12 0.00 (0.00) 0.02 (0.05) 0.02
4C through 4E). The width of KM decreased by ≈ 1 mm CD-T12 −0.04 (0.59) 0.02 (0.05) 0.06
in both groups from implant placement to crown delivery (IP- BOP (%) CD 19.23 (24.39) 3.84 (9.99) 15.39
CD) (thin: P <0.05; thick: P <0.05) and remained sta- ble T6 33.33 29.48 (22.72) 3.85
from crown delivery to 1-year post-restoration (CD-T12) (P (24.62)
>0.05) (Figure 4F). No statistically significant difference in T12 42.31 (24.17) 34.62 (22.01) 7.69
mean KM width between the thin and thick mucosal groups CD-T6 15.28 25.64 10.36
were detected at all time points (P = 0.687). No mobility of (39.22) (25.11)*
any implant was detected at any timepoint. T6-T12 8.33 5.13 3.20
A subset analysis was performed to examine the influ- (18.12) (32.19)
ence of horizontal mucosal thickness (thin <1 mm and thick CD-T12 23.08 30.77 7.69
≥1 mm) on PD, KM, BOP, and GI (Table 3), no statis- tical (39.40)* (23.42)*
PI (Score) CD 0.20 (0.29) 0.10 (0.30) 0.10
significance difference (P >0.05) was found between
T6 0.10 (0.24) 0.10 (0.30) 0.00
groups.
T12 0.26 (0.23) 0.13 (0.33) 0.13
CD-T6 −0.10 (0.29) −0.01 (0.18) 0.09
3.2 Radiographic findings T6-T12 0.15 (0.36)* 0.03 (0.22) 0.12
CD-T12 0.06 (0.35) 0.02 (0.23) 0.04
At T12, the mean mid-buccal bone width obtained through a
CBCT evaluation was 1.73 ± 0.74 mm in the thick tissue GI (Score) CD 0.09 (0.13) 0.03 (0.06) 0.06
group and 1.37 ± 0.43 mm in the thin tissue group, and no T6 0.36 (0.32) 0.33 (0.25) 0.03
T12 0.58 (0.31) 0.35 (0.25) 0.23
CD-T6 0.29 (0.38)* 0.31 (0.26)* 0.02
T6-T12 0.22 (0.36)* 0.31 (0.26) 0.21
CD-T12 0.49 (0.34)* 0.31 (0.26)* 0.17
BOP, bleeding on probing; CD, crown delivery; GI, gingival index; IP, implant
placement; KM, keratinized mucosa (post-surgically); PD, probing depth; PI,
plaque index; REC, recession; T12, 12-month follow-up; T6, 6-month follow-
 GARAICOA-PAZMINO
77 ET AL.
up.
*P <0.05.
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F I G U R E 4 Clinical and radiographic outcomes between thin (≤2 mm) and thick (>2 mm) mucosal phenotypes. PD: Probing depths, REC:
Recession, Pl: Plaque Index, BOP: Bleeding on probing, GI: Gingival Index, KM: Keratinized mucosa, MBL: Marginal bone loss

statistically significant difference presented between phe-

A statistically significant apical positioning of the
notypes (P = 0.151) (Table 4). From implant marginal bone level from IP-CD was noted in both thin
placement through 1 year of function (IP-T12), there was no (0.52 ± 0.43 mm, P <0.001) and thick (0.33 ± 0.52
signifi- cant change in mid-buccal bone width between
groups (P mm,
P = 0.022) phenotype groups using this implant design
>0.05). (Table 4). Slightly less bone remodeling occurred in the
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TA B L E 3 Mean differences in clinical and radiographic placement; KM, keratinized mucosa (post-surgically); PD, probing depth; PI,
measurements between vertical and horizontal mucosal phenotypes (mean plaque index; REC, recession; T12, 12-month follow-up; T6, 6-month follow- up.
differences in clinical measurements between thin (<1 mm) and thick *P <0.05.
(≥1 mm) horizontal mucosal phenotypes)
Thin-
Thin Thick thick
Variable Timeline Mean (SD) Mean (SD) (mm)
PD (mm) CD 2.31 (0.47) 2.27 (0.29) 0.04
T6 3.43 (0.38) 3.31 (0.42) 0.12
T12 3.21 (0.54) 3.43 (0.46) 0.22
CD-T6 1.11 1.09 (0.43)* 0.08
(0.57)*
T6-T12 −0.22 (0.27)* 0.19 (0.58) 0.30
CD- 0.90 (0.71)* 1.17 0.26
T12 (0.63)*
KM (mm) IP 3.97 (1.61) 3.90 (1.35) 0.06
CD 2.91 (1.24) 2.75 (0.98) 0.15
T6 3.09 (1.32) 2.85 (0.82) 0.24
T12 3.09 (1.13) 2.75 (0.98) 0.34
IP-CD −1.06 (1.41)* −1.15 (0.97) 0.09
IP-T6 −0.88 (1.26)* −1.05 (0.86)* 0.18
IP-T12 −0.88 (1.41)* −1.15 0.28
(0.97)*
CD-T6 0.19 (0.66) 0.10 (0.32) 0.09
CD- 0.19 (0.57) 0.00 (0.00) 0.19
T12
T6-T12 0.00 (0.55) −0.10 (0.32) 0.10
REC CD 0.02 (0.08) 0.00 (0.00) 0.02
(mm)
T6 0.02 (0.06) 0.00 (0.00) 0.02
T12 0.02 (0.06) 0.03 (0.06) 0.00
CD-T6 0.00 (0.06) 0.00 (0.00) 0.00
T6-T12 0.00 (0.00) 0.03 (0.06) 0.02
CD- 0.00 (0.06) 0.03 (0.06) 0.02
T12
BOP (%) CD 15.63 5.00 (11.25) 0.10
(23.15)
T6 34.38 25.93 (23.73) 0.09
(23.15)
T12 40.63 (21.92) 35.00 (25.40) 0.06
CD-T6 18.75 24.07 0.01
(36.45)* (25.15)*
T6-T12 6.25 (17.08) 7.41 (38.29) 0.03
CD- 25.00 30.00 0.04
T12 (36.51)* (24.60)*
PI (Score) CD 0.21 (0.29) 0.06 (0.10) 0.17
T6 0.11 (0.24) 0.08 (0.21) 0.03
T12 0.21 (0.21) 0.17 (0.28) 0.04
CD-T6 −0.10 (0.26) 0.02 (0.19) 0.14
T6-T12 0.09 (0.29)* 0.08 (0.33) 0.03
CD- 0.00 (0.28) 0.11 (0.31) 0.13
T12
GI (Score) CD 0.05 (0.10) 0.07 (0.12) 0.01
T6 0.39 (0.29) 0.28 (0.28) 0.11
T12 0.52 (0.31) 0.37 (0.27) 0.16
CD-T6 0.33 (0.34)* 0.24 (0.28)* 0.12
T6-T12 0.14 (0.36) 0.07 (0.38) 0.05
CD- 0.47 (0.32)* 0.30 (0.28)* 0.17
T12
BOP, bleeding on probing; CD, crown delivery; GI, gingival index; IP, implant
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78
thick biotype group, but this tendency did not reach sta-
tistical significance under comparison (P = 0.277). From
CD-T12, there was a non-significant (P >0.05) MBL
change of 0.26 ± 0.44 mm in the thin vertical tissue group
and a non-significant change of 0.28 ± 0.57 mm for the thick
ver- tical tissue group. At 1 year (T12), the radiographic
MBL for the thin and thick vertical tissue phenotypes was
1.69
± 0.54 mm and 1.59 ± 0.83 mm, respectively; this differ-
ence between groups was not significant (Table 4, Fig- ure
4G). The mean MBL change from IP-T12 was statisti-
cally significant at 0.78 ± 0.66 mm (thin group) and 0.61
±
0.71 mm (thick group), but there was no significant differ-
ence between the groups (P = 0.591).
We compared results from quartile phenotypic extremes to
check for hidden trends. Four of the thinnest sites (mean
vertical tissue height: 1.33 ± 0.28 mm) were evalu- ated
against four of the thickest sites (mean vertical tissue height:
3.00 ± 0.40 mm). At T12, a slighter greater MBL
was noted in the thin group (1.92 ± 0.52 mm) compared
with the thick group (1.42 ± 0.97 mm), but neither this
dif- ference nor the ones for clinical parameters reached statis-
tical significance between the group extremes (P >0.05).
A subset analysis was performed to examine the influ-
ence of horizontal mucosal thickness (thin <1 mm and
thick ≥1 mm) on MBL (Table 5), no statistical
significance difference (P >0.05) was found between
groups although both groups showed significant MBL
changes from IP up to T12 were noted in both groups.

4 DISCUSSION

Although most clinical studies27–30 have previously evalu-

ated MBL changes occurring around tissue level implants, the
present prospective study did not find significant clini- cal or
MBL changes in tissue level implants when consider- ing thin
and thick mucosal phenotypes. These results dif- fer from
those reported by most clinical studies5,7,8,31–33 and systematic
reviews,21,34 which have indicated that thicker mucosa
moderates bone remodeling. The main differences between
other studies and this clinical trial are the type of implant
used and the implant platform depth rela- tive to the
alveolar crest. We used a tissue level implant placed
supracrestally (smooth collar placed above the crest)
whereas others followed bone level implants placed
equicrestally or subcrestally (roughened collar below the crest).
Linkevicius et al. compared the effects of rough-
surfaced implants when placed 1.5mm subcrestally and
epicrestally.32 The authors observed less reduction of MBL
when implants were placed subcrestally compared with
epicrestally placed implants.8,31 Soft tissue tenting over 2- mm
healing abutments and subcrestal implant placement
 GARAICOA-PAZMINO
78 ET AL.

TA B L E 4 Mean differences in clinical and radiographic measurements between vertical and horizontal mucosal phenotypes (mean differences
in radiographic measurements between thin (≤2 mm) and thick (>2 mm) vertical mucosal phenotypes)
Thin Thick Thin-thick
Variable Timeline Mean (SD) Mean (SD) (mm)
IP intraoperative bone width Buccal 1.04 (0.64) 1.65 (0.98) 0.61
Lingual 1.69 (0.75) 1.65 (0.82) 0.00
Average 1.37 (0.58) 1.65 (0.71) 0.28
MBL (mm) IP 0.90 (0.61) 0.98 (0.69) 0.08
CD 1.43 (0.56) 1.31 (0.68) 0.12
T6 1.50 (0.61) 1.51 (0.91) 0.01
T12 1.69 (0.54) 1.59 (0.83) 0.10
IP-CD 0.52 0.33 (0.52) 0.2
(0.43)*
IP-T6 0.60 (0.67)* 0.53 (0.75) 0.07
IP-T12 0.78 (0.66)* 0.61 (0.71) 0.18
CD-T6 0.07 (0.37) 0.20 (0.59) 0.13
CD-T12 0.26 (0.44) 0.28 (0.57) 0.02
T6-T12 0.19 (0.34) 0.08 (0.38) 0.61
T12 CBCT bone width (mm) Buccal 1.96 (0.63) 1.95 (0.74) 0.01
Lingual 2.52 (1.00) 1.80 (0.69) 0.57
Average 2.24 (0.79) 1.92 (0.60) 0.32
CBCT, cone-beam computerized tomography; CD, crown delivery; IP, implant placement; MBL, marginal bone level; T12, 12-month follow-up; T6, 6-month follow-
up.
*P <0.05.

TA B L E 5 Mean differences in clinical and radiographic measurements between vertical and horizontal mucosal phenotypes (mean differences
in radiographic measurements between thin (<1 mm) and thick (≥1 mm) horizontal mucosal phenotypes)
Thin Thick Thin-thick
Variable Timeline Mean (SD) Mean (SD) (mm)
IP intraoperative bone width Buccal 1.15 (0.88) 1.65 (0.81) 0.50
Lingual 1.75 (0.81) 1.55 (0.72) 0.20
Average 1.45 (0.70) 1.6 (0.60) 0.15
MBL (mm) IP 1.06 (0.67) 0.76 (0.58) 0.30
CD 1.46 (0.60) 1.21 (0.63) 0.25
T6 1.73 (0.74) 1.13 (0.67) 0.60
T12 1.87 (0.61) 1.26 (0.65) 0.82
IP-CD 0.41 (0.51)* 0.45 (0.45)* 0.05
IP-T6 0.68 (0.75)* 0.38 (0.60)* 0.30
IP-T12 0.82 (0.72)* 0.50 (0.58)* 0.32
CD-T6 0.27 (0.52) −0.08 (0.35) 0.35
CD-T12 0.41 (0.47) 0.05 (0.48) 0.37
T6-T12 0.14 (0.30) 0.12 (0.45) 0.02
T12 CBCT bone width (mm) Buccal 2.03 (0.71) 1.84 (0.64) 0.19
Lingual 2.32 (0.83) 2.01 (1.02) 0.31
Average 2.17 (0.72) 1.92 (0.71) 0.25
CBCT, cone-beam computerized tomography; CD, crown delivery; IP, implant placement; MBL, marginal bone level; T12, 12-month follow-up; T6, 6-month follow-
up.
*P <0.05.
GARAICOA-PAZMINO
ET AL.
78
can significantly reduce crestal bone loss, compared with
vertical soft tissue thickening by tenting of epicrestally placed those with a thin vertical mucosal phenotype (0.71 ±
implants. Ercoli et al. noted that subcrestal implant positioning of 1.53 mm).37 To prevent such biological complications, soft
a platform-switched implant generates less crestal bone loss than tissue augmentation is currently endorsed to correct thin
an equicrestally placed implant with a tenting healing phenotypes.23,38 Mucosal autografts or allografts can thicken soft
abutment.14,32 tissue7 and improve esthetics.38 Soft tissue augmentation
Formation of the peri-implant STH, along with implant around bone level implants with thin phe- notypes results in
design (polished collar, laser-microtexturing),35,36 fixture significantly less radiographic bone loss compared with non-
positioning (supracrestal), and prosthetic features (partic- ular grafted sites.7,24
abutment lengths, gently contoured crowns),15,16 has likely Implants lacking KM are associated with plaque accu-
influenced the outcomes of this study and dwarfed any effects mulation, tissue inflammation, recession, and attachment loss,
of the native mucosal thickness. Linkevicius et al. determined though not with radiographic bone loss. 39,40 In this trial, we
that platform switching did not maintain crestal bone loss in ensured that a sufficient band of KM (≥2 mm) was present
patients with thin tissue phenotypes.36 Conversely, Wallner and at the time of implantation. Irrespective of pheno- type or
coworkers reported that mucosal phenotype does not affect adequate initial KM, we noted an ≈1 mm reduction in KM
marginal bone loss.35 In the present study, minimal but width from implantation to CD, which may be due to
statistically significant MBL increases were noted in both coronally flap repositioning around the polish collars that triggers
groups from implant place- ment through timepoints up to 1 a slight loss of KM. Nonetheless, post-crown delivery, the peri-
year. The statistically relevant resorption occurred before CD, implant tissues remained stable for up to 1 year. One study
signifying that for- mation of the peri-implant STH causes the using the same implant type as in the present study
greatest alter- ations in MBL (Table 4). No implant in either determined that KM width is unchanged up to 3 years if
phenotypic group displayed radiographic bone loss beyond flap was positioned in the bone level.41
physiologi- cal bone remodeling after 1 year in function. These Scarce evidence is available related to influence of hori-
findings suggest that the peri-implant STH is re-established zontal mucosal thickness on the clinical and radiographic
regard- less of mucosal phenotype before the prosthetic parameters. Results from this study indicated there is no
phase and is maintained during function in tissue level difference between thin (<1 mm) and thick (≥1 mm) with
implants with a 1.8-mm tall, polished collar. The biological
response may differ for bone level implants, as evidenced by regards to MBL and clinical parameters recorded. More
studies from the Linkevicius and van Eekeren groups that study in this area is needed to further validate these find- ings.
Nonetheless, it has been demonstrated that hori- zontal
linked thin phenotypes to greater bone loss.5–8,25 mucosal thickness is inversely correlated with the integrity and
This study did not find differences in clinical or radio-
thickness of the buccal bone.42 The present data were in line
graphic measurements between thin and thick verti- cal with this observation which showed buc- cal thickness of 0.57
tissue phenotypes; this may imply that once peri- implant
STH is established with relative health, the influ- ence of mm and 1.21 mm in thin (<1 mm) and thick (≥1 mm)
mucosal phenotype may be neutralized. Although implants in horizontal tissue phenotypes, respectively. This study tracked
the thin tissue group trended toward greater BOP, PI, and GI implants for 12 months post-crown delivery; a longer follow-
score compared with those in the thick group, no up may reveal soft tissue and MBL changes that do not appear
statistical differences were found between groups in BOP, PI, until later. Although we assessed signs of inflammation, we
or GI, and no peri-implant disease was diagnosed for any did not directly eval- uate peri-implant diseases or the
fixture at any time. Additionally, correla- tions between influence of tissue phe- notype on them. These results apply
intraoperative and CBCT outcomes should be interpreted only to one type of tissue level implant; future studies should
carefully. A slight increase in buccal bone width was noted analyze various implant designs, placement depths, and
after 1 year of implant placement in CBCT evaluation when prosthetic features to clarify the effect of tissue phenotype in
compared with intraoperative measure- ments. The difference other scenarios.
may be caused by the CBCT scat- tering or beam hardening.
Furthermore, these differences address the limitations between
the chosen non-invasive (CBCT) and invasive (surgical re- 5 CONCLUSIONS
entry) techniques.
Thin peri-implant mucosa may raise the risk for peri- Within the limitations of this study, tissue level implants at 1 year
implant diseases. In a cross-sectional study, Mailoa et al. noted of function placed in thin vertical mucosa achieved similar
significantly greater mid-facial recession in sites with peri- clinical parameters and radiographic MBL as those in thick
implantitis (0.79 ± 2.22 mm) as well as in vertical tissue; the native soft tissue phe- notype does not
impact implant health possibly because peri-implant STH is
rapidly established in the implant design we used.
Longitudinal studies are required to
 GARAICOA-PAZMINO
78 ET AL.

confirm the impact of mucosal thickness in different implant

designs and surgical and prosthetic situations. 5. Puisys A, Linkevicius T. The influence of mucosal tissue thick-
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The authors would like to thank Dr. Debby Hwang (Ann 6. Linkevicius T, Puisys A, Steigmann M, Vindasiute E, Linkevi-
Arbor, Michigan) for critical review of this paper and Juan ciene L. Influence of vertical soft tissue thickness on crestal bone
Luis Gomez (stHalley Statistics, Valencia, Spain) for his changes around implants with platform switching: a compara- tive
support with statistical analysis. Additionally, Andrea Frantz and clinical study. Clin Implant Dent Relat Res. 2015;17:1228-1236.
7. Linkevicius T, Puisys A, Linkeviciene L, Peciuliene V, Schlee M.
Michelle Arnett are gratefully acknowledged for their Crestal bone stability around implants with horizontally match- ing
support as research coordinators. connection after soft tissue thickening: a prospective clinical trial. Clin
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Hsun-Liang Chan, James Mailoa, Fernando Suárez-López switched, laser-microtextured implant on marginal bone level: A 24-
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cid.12903 Online ahead of print
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