Factors Influencing the Presence of Papilla between Adjacent Implants and between a Tooth and an Implant.

AIM: The aim this study was to evaluate the factors that influence the presence or absence of the interproximal papilla between implants adjacent to the teeth or other implants, through clinical and radiographic evaluation.
MATERIAL AND METHODS: The non-probabilistic sample comprised 44 patients of both genders aged between 21 and 68 years, rehabilitated with 114 osseointegrated implants. Through a retrospective clinical study, the patients were divided according to the presence or absence of the interproximal papilla: Group 1 - Absence of Papilla, Group 2 - Partial Presence of Papilla and Group 3 - Total Presence of Papilla. The success of the implants, the periodontal biotype, and the vertical and horizontal distances of the interproximal regions included in the study were evaluated.
RESULTS: Of the 114 implants, 46.5% were considered unsuccessful, and bleeding was present in 29.8%. The periodontal biotype presented as thin and scalloped was found in 85.1% of the regions. The evaluation of the groups according to the confirmation of the interproximal space showed a statistically significant difference (p = 0.007), with 61.9% of the wide and long interproximal spaces classified as Group 1, while 31% of the narrow and short interproximal spaces were classified as Group 3.
CONCLUSION: It was concluded that the morphology of the interproximal space was the factor that was most strongly associated with the presence or absence of the interproximal papilla.

Introduction

In dentistry, increased esthetic demands require a soft-tissue contour with an intact papilla and a symmetric gingival outline (). Ideally, successful implant-supported restorations have an appearance as close as possible to natural teeth (). Color, texture, and peri-implant soft tissue height and thickness play a fundamental role in the implant restorations outcome ().

A successful bony integration of an implant does not ensure full patient satisfaction. Soft tissue health is critical to the patient’s perception of a successful restoration (). Currently, there is an increasing concern about the smile esthetics from patients seeking dental treatment. The presence or absence of the interproximal papilla between adjacent teeth, between a tooth and an implant, or between implants strongly influence the esthetic outcome, which demands a high level of skill and technical knowledge of the professionals to preserve the papilla in implant treatments ().

The papilla is characterized as an interproximal extension of the gingiva and its architecture is related to the condition of the contact point between the teeth as well as to the course of the cementum-enamel junction (). Furthermore, understanding the factors that are most strongly associated with the formation of the interdental papilla will decrease the peri-implantitis risk ratio and will be important for treatment planning and prognosis ().

The appearance and presence of the papilla may be influenced by a number of factors such as underlying bone structure, adjacent soft tissue quality, the shape of the restoration, the contact point between the crowns, dental positioning in the arch, and periodontal / peri-implant phenotype (-).

Since soft-tissues have become an important factor in the overall success of a large number of implant-supported restorations, the loss of the peri-implant papilla leads to an esthetic disadvantage known as the black triangle. Currently, one of the most challenging aspects of periodontal reconstructive surgery is to obtain a suitable peri-implant papilla in the esthetic area (). The existence of space below the contact area can lead not only to compromised esthetics but also to phonetic problems, periodontal diseases, and food impaction (, ). The peri-implant soft tissue condition appears to be a critical determinant for the occurrence of this undesirable space ().

In natural teeth, the height of the interproximal papilla is influenced by the position of the contact point between teeth and the level of the proximal bone crest. For single implants, similar findings were observed. A completely filled papilla is expected when the distance from the contact point to the proximal bone crest is less than 5 mm (, , ).

Some studies correlating the importance of the distance from the bone crest to the contact point of adjacent tooth crowns and implants were performed, as well as the studies correlating the distance between an implant and tooth and between implants in the presence of papilla. From these parameters, greater predictability can be obtained in the formation of the interproximal papilla in the rehabilitations. In addition to the vertical distance, the horizontal distance between adjacent implants when smaller than 3 mm determined the absence of interproximal papilla, independent of the vertical distance. When this distance is greater than or equal to 3 mm there is an interaction between the vertical and horizontal distances. In the interproximal areas with implant adjacent to the tooth, this horizontal distance can reach 1.5 mm, considering that the presence of dental structures exerts a greater influence on the formation of the papilla. In relation to prognosis in the peri-implant papilla formation, it was evident that it is related to the peri-implant bone height and the contact point (, , ).

The interproximal papilla morphology and the bone architecture that houses the tooth can be categorized into two periodontal biotypes (-). The first periodontal biotype is the scalloped periodontium, characterized by thin gingival tissue and long interproximal papilla. The second periodontal biotype is the flat periodontium, which is characterized by a flat morphology, bone structure and thick gingival tissue and short and wide papilla. Individuals with the thin periodontal biotype may have more soft tissue recession than those with the flat and thick periodontal biotype ().

The present study aimed to assess the factors that influence the presence or absence of the interproximal papilla between adjacent implants, and between tooth and implant, through clinical and radiographic evaluation.

Material and Methods

This study was approved by the Research Ethics Committee of the Health Sciences Center of the Federal University of Pernambuco (CCS-UFPE) under the CAAE 03534012.0.0000.5208, Opinion 84041. All individuals consented to the data collection by signing an Informed Consent.

A retrospective clinical study was performed with patients rehabilitated with osseointegrated implants in the Specialization Course in Implantology at the Federal University of Pernambuco (UFPE) from 2011 to 2015. The non-probabilistic sample comprised 44 patients, rehabilitated with 114 implants. Each patient was evaluated only once during this study.

Inclusion criteria were: the presence of at least one dental implant with a prosthetic crown in function for more than one year and those over 18 years of age. Exclusion criteria were: use of medications that act on bone remodeling (i.e., bisphosphonates) or interfere with the gingival condition (i.e., calcium channel blockers), history of periodontitis, pregnancy or lactation, immunosuppression, history of soft tissue graft surgery at the implant site, and the absence of the contact point between the crowns of the implant regions evaluated.

Clinical and radiographic evaluation

All the patients’ health histories were reviewed and submitted to the extra-oral and the intra-oral examination. In the course of intra-oral examination, the periodontal condition was recorded in a periogram previously calibrated using the North Carolina periodontal probe (Trinity®, São Paulo, Brazil), by a single examiner and the following parameters were evaluated and recorded: Plaque Index (PI), (), Bleeding Index (BI), (), Gingival Recession (GR), Probing Depth (PD), and Periodontal Attachment Level (PAL).

To evaluate the integration success of the implants placed, the criteria described by Ong et al. () which grouped several authors’ definitions, were used: the absence of mobility, the absence of persistent subjective complaints (pain, foreign body sensation and / or dysesthesia, the absence of recurrent peri-implant infection with suppuration, the absence of continuous radiolucency around the implant, the absence of probing depth greater than or equal to 5 mm, and the absence of bleeding on probing) (-). The annual vertical bone loss, mesial or distal, was not evaluated in this study due to the absence of annual radiographic records of all patients ().

The periodontal biotype classification was determined by Olsson & Lindhe, who categorized the gingiva into two tissue biotypes (flat or scalloped) with punctual and marked differences between them ().

After recording the clinical parameters, the papilla between adjacent implants or between implant and tooth were classified according to two authors:

Jemt (): this index evaluated the height of the papilla between tooth and implant, adapted for this study to classify the areas between adjacent implants as well.

Nordland & Tarnow (): this index evaluated the presence of papilla between adjacent teeth, being adapted for this study to classify the papillae between tooth and implant and between adjacent implants.

Then, the papilla between implants adjacent to tooth or another implant were categorized into 3 groups: G1 - Absence of Papilla [indexes 0 and 1 of Jemt () and Classes II and III of Nordland and Tarnow ()]; G2 - Partial Papilla Presence [Jemt index 2 () and Class I of Nordland and Tarnow ()]; G3 - Total Papilla Presence [indexes 3 and 4 of Jemt () and Normal classification of Nordland and Tarnow ()].

With the clinical data obtained, the prognosis was determined in relation to the presence of the papilla, considering the height of the interproximal bone crest up to the contact point and it was divided into three classes, according to Salama et al. (): Class 1: Favorable Prognosis; Class 2: Less Favorable Prognosis; Class 3: Unfavorable Prognosis.

To determine the vertical distance (distance from the peak of the alveolar crest to the base of the contact point), the methodology proposed by Tarnow et al. () was used. The procedure was the same for the areas between implants adjacent to the tooth or implant.

After the clinical examination and the classification of the interproximal papillae, the patient underwent a radiographic examination, standardized in a ratio of 1:1, periapicaly in the region of each implant, using the parallelism technique through positioners for periapical radiographs. The radiographic analysis was performed using a magnifying glass on a radiographic light to obtain the following data: presence or absence of radiolucency around the implant; horizontal distance between adjacent implants, measured from one implant platform to the other, or between tooth and implant; measurement of the implant platform at the root of the adjacent tooth at the location of cementum-enamel junction; distance from cement-enamel junction to bone crest; and distance from the apical end of the contact point to the bone crest.

Associating the already established measurement of the bone crest to the contact point and the horizontal distance between adjacent implants or between tooth and implant, the association of the morphology of the interproximal space with the presence of recession of the interproximal papilla was evaluated. Thus, the interproximal space was classified according to Table 1, (1).

Table 1

Classification of interproximal space according to Chang, 2007.

	Height ≤ 4mm	Height > 4 mm
Wide ≤ 2mm	Narrow ans Short	Narrow and Long
Wide > 2mm	Wide and Short	Wide and Long≤

Statistical analysis

After data collection, data were expressed as mean, standard deviation, and absolute and relative frequency distributions. Continuous variables were compared by the Mann Whitney non-parametric test, since the results did not follow normal distribution, and, when it was not possible to perform the Chi-square test because the assumption of expected values below 20%, in most cases the proportions were violated and a comparison was performed by the Likelihood Ratio test. The level of significance was set at P 0.05, and the confidence level at 95%. The software used was the Statistical Package of Social Science (SPSS) version 20.0 and the data were entered in Microsoft Excel.

Results

Forty-four patients were involved in the study. They were rehabilitated with 114 implants and presented 176 interproximal areas for papilla formation. Age ranged from 21 to 68 years, averaging 49 years, and 63.6% of the patients were female. The mean loading time of the implants evaluated was 32.4 months.

The periodontal biotype was classified as thin and scalloped in 85.1% of the evaluated regions. Among the criteria of Ong et al. (), 46.5% of implants were considered unsuccessful. Bleeding on probing showed the highest percentage with 29.8%, followed by the probing depth > 5 mm, with 28.9% (Table 2).

Table 2

– Implants success classification according to Ong et. al. (2008) criteria.

Implants	N	%
Mobility
Yes	1	0.9
No	113	99.1
Subjective complaints
Yes	2	1.8
No	112	98.2
Inffection with supuration
Yes	2	1.8
No	112	98.2
Radiolucency
Yes	1	0.9
No	113	99.1
Probing Depth > 5mm
Yes	33	28.9
No	81	71.1
Bleeding on Probing
Yes	34	29.8
No	80	702
Total	114	100.0

Of the total number of papilla evaluated, 86 belonged to Group 1 (48.9%), 68 to Group 2 (38.6%) and 22 to Group 3 (12.5%). The evaluation of the presence of bone graft prior to implant installation was performed on 171 papillae taking into account the fact that information was not obtained for 5 papillae.

The differences between the groups were statistically significant for the position of the papilla and for the region of the papilla in the arch (Table 3).

Table 3

- Group distribution according to the variables of interest.

Variables		Presence of Papilla
		G1		G2		G3		Total
		N	%	N	%	N	%	N	%
Prior to bone graft	Yes	25	47.2	20	37.7	8	15.1	53	100.0
	No	60	50.8	45	38.1	13	11.0	118	100.0
	total	85	49.7	65	38.0	21	12.3	171	100.0
Vertical distance	< 5mm	37	48.7	29	38.2	10	13.2	76	100.0
	> 5mm	49	49.0	39	39.0	12	12.0	100	100.0
	total	86	48.9	68	38.6	22	12.5	176	100.0
Horizontal distance	< 3mm	27	40.3	27	40.3	13	19.4	67	100.0
	> 3mm	59	54.1	41	37.6	9	8.3	109	100.0
	total	86	48.9	68	38.6	22	12.5	176	100.0
Papilla position	Tooth-implant	51	37.5	63	46.3	22	16.2	136	100.0
	Implant-tooth	35	87.5	5	12,5	-	-	40	100.0
	total	86	48.9	68	38.6	22	12.5	176	100.0
Region in the arch	Anterior	24	46.2	15	28.8	13	25.0	52	100.0
	Posterior	62	50.0	53	42.7	9	7.3	124	100.0
	total	86	48.9	68	38.6	22	12.5	176	100.0
Crown of adjacent implant	Cemented	64	50.4	51	40.2	12	9.4	127	100.0
	Screw-retained	22	44.9	17	34.7	10	20.4	49	100.0
	total	86	48.9	68	38.6	22	12.5	176	100.0

1- Pearson Chi-square test

The evaluation of the groups showed a statistically significant difference for the conformation of the interproximal space, revealing that 61.9% of spaces classified as wide and long belonged to Group 1, while 31% of the narrow and short spaces had papilla of Group 3. The p-value was also statistically significant for the position of the papilla, noting that papilla was not completely formed in the interproximal regions between adjacent implant. Considering the position in the arch, 50% of posterior interproximal regions with total absence of papilla were found (Table 4).

Table 4

- Distribution of the papilla presence according to variables of interest.

Variables		Presence of papilla
		G1		G2		G3		Total
N	%	N	%	N	%	N	%
Prognosis	Favorable	50	42.7	50	42.7	17	14.5	117	100.0
	Less favorable	26	56.5	15	32.6	5	10.9	46	100.0
	Unfavorable	10	76.9	3	23.1	-	-	13	100.0
	Total	86	48.9	68	38.6	22	12.5	176	100.0
Interproximalspace	Narrow and long	14	46.7	12	40.0	4	13.3	30	100.0
	Narrow and short	8	27.6	12	41.4	9	31.0	29	100.0
	Wide and long	39	61.9	22	34.9	2	3.2	63	100.0
	Wide and short	25	46.3	22	40.7	7	13.0	54	100.0
	Total	86	48.9	68	38.6	22	12.5	176	100.0
Papilla position	Tooth-implant	51	37.5	63	46.3	22	16.2	136	100.0
	Implant-implant	35	87.5	5	12.5	-	-	40	100.0
	Total	86	48.9	68	38.6	22	12.5	176	100.0
Position in the arch	Anterior	24	46.2	15	28.8	13	25.0	52	100.0
	Posterior	62	50.0	53	42.7	9	7.3	124	100.0
	Total	86	48.9	68	38.6	22	12.5	176	100.0

1- Pearson Chi-square test

Evaluating the interproximal regions between the tooth and the implant, we observed a statistically significant difference between the groups for prognosis, interproximal space and position in the arch. For regions between adjacent implants, these differences were not significant between the groups (Tables 5 and 6).

Table 5

Distribution of the groups of papilla between implant and tooth according to variables of interest.

Variables		Papilla between implant and tooth
		G1		G2		G3		Total
N	%	N	%	N	%	N	%
Prognosis	Favorable	25	28.4	46	52.3	17	19.3	88	100.0
	Less favorable	21	52.5	14	35.0	5	12.5	40	100.0
	Unfavorable	5	62.5	3	37.5	-	-	8	100.0
	total	51	37.5	63	46.3	22	16.2	136	100.0
Interproximal space	Narrow and long	13	44.8	12	41.4	4	13.8	29	100.0
	Narrow and short	7	25.0	12	42.9	9	32.1	28	100.0
	Wide and long	22	48.9	21	46.7	2	4.4	45	100.0
	Wide and short	9	26.5	18	52.9	7	20.6	34	100.0
	total	51	37.5	63	46.3	22	16.2	136	100.0
Position in the arch	Anterior	19	42.2	13	28.9	13	28.9	45	100.0
	Posterior	32	35.2	50	54.9	9	9.9	91	100.0
	total	51	37.5	63	46.3	22	16.2	136	100.0

1-Likelihood Ratio test; 2-Pearson Chi-square test

Table 6

Distribution of the groups of papilla between adjacent implants according to variables of interest.

Variables		Papilla between adjacent implants
		G1		G2		G3		Total
N	%	N	%	N	%	N	%
Prognosis	Favorable	25	86.2	4	13.8	-	-	29	100.0
	Less favorable	5	83.3	1	16.7	-	-	6	100.0
	Unfavorable	5	100.0	-	-	-	-	5	100.0
	total	35	87.5	5	12.5	-	-	40	100.0
Interproximal space	Narrow and long	1	100.0	-	-	-	-	1	100.0
	Narrow and short	1	100.0	-	-	-	-	1	100.0
	Wide and long	17	94.4	1	56	-	-	18	100.0
	Wide and short	16	80.0	4	20.0	-	-	20	100.0
	total	35	87.5	5	1.25	-	-	40	100.0
Position in the arch	Anterior	5	71.4	2	28.6	-	-	7	100.0
	Posterior	30	90.9	3	9.1	-	-	33	100.0
	total	35	87.5	5	12.5	-	-	40	100.0

1-Likelihood Ratio test

Discussion

The maintenance of soft tissue harmony after rehabilitation with dental implants constitutes a major challenge for modern dentistry. The focus of several studies is the interproximal papilla which is responsible for filling the space between dental crowns and should be present from the base of the contact point to the bone crest, which is considered to be a true papilla (, ).

Several studies demonstrate the difficulty in achieving the formation of a true papilla after a tooth loss and the rehabilitation of this space through osseointegrated implants. Moreover, in regions between adjacent implants, this difficulty is increased by the absence of important dental anatomical structures, such as the cement-enamel junction, which guides the papilla formation (). This can be observed in the results of this study, in which, although respecting the horizontal and vertical distances recommended in the literature, all regions between adjacent implants did not present completely formed papilla. Furthermore, when some researchers compared the presence of the interproximal papilla between different regions, the regions between adjacent implants obtained the less satisfactory results ().

The implants evaluated in this study obtained 46.5% of failure, according to the criteria grouped by Ong et al. () and bleeding was the most present factor of failure (29.8%). These results may demonstrate transitory conditions associated with other factors, such as poor oral hygiene.

Restoring the interproximal papilla is difficult when there is no natural tooth involved. In this scenario, a short papilla should be expected and implant-supported restorations demonstrate poorer results (). In this study, it was observed that almost half (48.9%) of the evaluated regions did not have interproximal papilla.

The presence of a thin and scalloped periodontal biotype contributes to a higher rate of papilla loss, due to the fact that this periodontal biotype is more susceptible to recessions (, ). It was observed in this study that 85.1% of the periodontal biotype in the regions of the implants evaluated was classified as thin, which may contribute to the absence of the papilla.

The prognosis for the presence of papilla proposed by Salama et al. () was not compatible with the presence of interproximal papilla in this study. This may be associated to the fact that this prognosis uses only the vertical distance as criteria, whereas, for the sample used in this study, the association of this distance with the horizontal distance was the determinant because both the anterior region and the posterior region were evaluated such as implants adjacent to teeth or to another implant.

The studies by Tarnow et al. () and Cho et al. () showed that when the distance from the contact point to the bone crest was ≤ 5 mm, the interproximal papilla was always present. In this study, it was observed that this did not apply to the regions between adjacent implants and between the tooth and the implant, since 48.7% of the regions that had vertical distance < 5mm did not present papilla formation. Thus, the importance of dental structures for the formation of the interproximal papilla is evident and the periodontal biotype may play an important role in those findings as well.

Evaluating the presence of the papilla between healthy teeth, Cho et al. () observed the correlation between the distance from the base of the contact point to the bone crest and the distance between the roots (horizontal distance) for the formation of the papilla. This association determines the interproximal space morphology. In the present study, the interproximal space morphology determined a 31% of papilla presence in narrow and short spaces, while the papilla was absent in 61.9% of the wide and long interproximal spaces.

The interproximal space morphology presented statistical significance among the groups evaluated in this study, demonstrating that the association between vertical and horizontal distances was an influencing factor for the presence or absence of the interproximal papilla. This fact demonstrates that for the planning of rehabilitations with osseointegrated implants, the association of vertical and horizontal distances may lead to a more satisfactory result for soft tissue esthetics in the interproximal regions.

Choquet et al. () described the presence of complete papilla in 58% of the interproximal regions between a tooth and an implant in the anterior region. In this study, 28.9% of the anterior tooth and implant regions had fully formed papilla. However, in the regions between the tooth and the posterior implant, a complete interproximal papilla was present only in 9.9% of them.

Conclusion

It was concluded that, in view of the investigated variables, the morphology of the interproximal space was the criterion that was most strongly associated with the presence or absence of the interproximal papilla. All other factors were observed and acted on the sample, but the morphology of the interproximal space that associates the vertical and horizontal distances was of great relevance.

From this observation, particular attention should be given to the planning phase of treatment with osseointegrated implants in order to observe all possible factors that may be associated with the formation of soft tissue between adjacent implants or between the implant adjacent to the tooth. In this way, the treatment process can be more easily performed and a more predictable prognosis can be given to the patient.