aluminum oxide facial implants in primates

SCIENTIFIC ARTiCLES J Oral Maxillofac 40:771-

Surg

775. 1982

A Comparison of Porous Composite PTFEIGraphite and PTFEIAluminum Oxide Facial Implants in Primates RUSSELL

L. WESTFALL, DDS,* CHARLES A. HOMSY, ScD,t JOHN N. KENT, DDS$

AND

Comparison of tissue ingrowth density values for Proplast I and its aluminum oxide analog, Proplast II, when implanted on the primate infraorbital rim and inferior border of the mandible, showed no difference between the two test materials. A similar comparison of local cellular response ratings showed slightly less response to Proplast II. Microscopic and clinical examination did not otherwise reveal any significant differences in biologic reaction to these materials.

Clinical applications of microporous alloplasts for facial augmentation have been well documented.‘,* Because of fibrous ingrowth resulting in increased tissue stabilization, the microporous composite alloplast Proplast I has been shown to be more clinically useful than other nonporous po1ymers.3-5 This clinical advantage is gained from the intrinsic biocompatibility of the carbon and PTFE (polytetrafluoroethylene) components, a high surface energy and area characteristics of the carbon, and the careful matching of the alloplast’s elastic modulus to prevent shearing of the ingrown tissue buds under stress.6-” The implant porosity size, pore volume, and interpore connections allow active tissue metabolism and tissue maturation to the extent of intraimplant ossification. The thermal stability of the alloplast allows presurgical autoclaving to insure sterility at the time of surgical placement, and the spongelike character of the Proplast block lends itself to custom contouring by carving at the time of surgery. Although conventional Proplast I works well in

most applications, its usefulness may be limited in more superficial subperiosteal or supraperiosteal locations because of its dark color. A bluish surface discoloration has been observed when Proplast I has been used superficially in fair-skinned persons, especially in the paraorbital and paranasal regions. With this clinical limitation in mind, a porous Proplast I analog, Proplast II, in which alumina (A1203) is substituted for graphite to provide more neutral coloration, has been developed. The characteristics of the two materials are analogous except for a smaller alumina fiber diameter and the elastic modulus of Proplast II, which is three quarters that of Proplast I (indicating more deformation of the implant material with equal stresses). It was the purpose of this study to compare the aluminum oxide analog, Proplast II, with Proplast I for subperiosteal, soft tissue facial augmentation in primates. This model approximates the clinical conditions of facial augmentation in humans. The biocompatibility of the new analog was characterized according to tissue ingrowth-stabilization and local cellular response and was compared with control facial implants of Proplast I in the same animal.

* ClinicalAssistantProfessor, Oral and Maxillofacial Surgery, LSU Medical Center. Charity Hospital, New Orleans, Louisiana. t Director, Prosthesis Research Laboratory, Fondren Orthopedic Center, The Methodist Hospital: Research Associate Professor, Division of Orthopedic Surgery, Baylor College of Medicine. Houston, Texas. $ Professor and Chairman, Department of Oral and Maxillofacial Surgery, LSU Medical Center, Chief, Oral and Maxillofacial Surgery, Charity Hospital, New Orleans, LA, 70110. Address correspondence and reprint requests to Dr. Kent.

Materials and Methods Each of eight Papio cynocephalus baboons served as host for four graphite/PTFE (Proplast I) and four aluminum oxidelPTFE (Proplast II) implant blocks. The baboons were sedated with phencyclidine hy-

027%2391/82/1200/0771 $01.00 @ American Association

771

of Oral and Maxillofacial Surgeons

772

PTFFYGRAPHITE

A2

VS PTFE!AI.UMINIIM

A4

Al-

B4

of

Description

Category

1.

B3 Placement

and numbering

of infused

I

implants

= lnfraorbitat

area:

right, lateral

Proplast

I

A2 = Infraorbital

area:

right,

Proplast

II

A3 = lnfraorbitdl

area:

left, medial

Proplast

I

A4 = Infraorbital

area:

left. lateral

Proplast

II

Al

medial

right, posterior

Proplast

1

B? = Mandibular

border:

right, anterior

Proplast

II

B3 = Mandibular

border:

left, anterior

Proplast

I

B4 = Mandibular

border:

left. posterior

Proplast

II

B I = Mandibular

(From

Kent

plast: Primate

border:

JN,

Westfall

RL:

facial augmentation.

Presurgical

infusion

J Oral Surg 37:637.

Fibrin and erythrocytes interspaces:

deposited

no vascular

in

ingrowth

evident 7

Granulation

3

Complete

granulation

ri\sue

4

lngrowth

primarily

decreasing number 5

of Pro-

Mature

ingrowth

beginning

tissue ingrowth

collagenous

vascularity:

with

moderate

of fibroblasts

collagenous

tissue with marked

decrease

in vascularity:

tissue

ingrowth

perpendicular

to implant

laminations

evident

1979.)

drochloride (1 mgikg) supplemented with 65.0 mg of pentobarbital intravenously as needed. Incisions at the lateral extent of the infraorbital rims were made to the depth of the bone, and subperiosteal tunnels were developed along the rims to the nasal bridge. Similarly, subperiosteal tunnels were developed bilaterally at the inferior mandibular border through a single symphyseal incision. Two blocks of each material were implanted on the infraorbital rims and the inferior border of the mandible in each animal, one block in the medial extent of the area and the other at the lateral extent of the implantation area (Fig. 1). The sterile alloplast blocks measured 3 x 4 x 6 mm and were placed subperiosteally with lamination planes parallel with the cortical osseous surface. The implants were inserted under sterile conditions, and received no preplacement antibiotic infusion. Care was taken that there was no hematoma formation around the implants. After implantation intervals of one, two, four, eight, twelve. sixteen, twenty and twenty-four weeks, the alloplast blocks, as well as the surrounding con-

I‘S

tissues. were surgically removed and immediately fixed in 10%: formalin solution. The tixsues were subsequently decalcified. and each alloplast block was sampled by means of three representative tissue-implant interface sections made perpendicular to the alloplast’s lamination planes. I” The sections were stained with hematoxylin and eosin and Mallory’s trichrome stain. The sections were examined histologically for local cellular response and extent and type of tissue ingrowth. These characteristics were quantified according to a modification of the classification system used in the authors’ previous study of Proplast I (Tables 1 and 2). ‘I’ Linear regression analyses were performed on data for tissue ingrowth and local cellular response

Table 1. Classification Tissue lngrowth

FIGURE

IMPI.AN

nective

A3

B2

OXIDE

Table 2. Classification Cellular Response

of

LOCal

Description

Category I

No histiocytes

2

Slight chronic

or giant cells present histiocytic

and giant cells; fewer mononuclear millimeter 3

Chronic

cells per square

as counted

high power

response than 100 on five random

fields

histiocytic

response:

than 100 mononuclear

more

cells per

square millimeter 4

Mixed

histiocytic

mononuclear a significant

response:

cells predominant number

polymorphonuclear 5

Moderate

cells evident

acute inflammation:

polymorphonuclear

with

of acute. primarily

cells seen. but

fewer than 80 per square millimeter 6

Distinct diffuse marked

acute inflammation;

numerous

polymorphonuclear

cells or

focal accumulation

polymorphonuclear

80 per square millimeter 7

Frank

necrosis evident

of

cells: more than

773

WESTFALL

ET AL.

Table 3.

Tissue lngrowth

and Local Cellular

Response

Data

Proplast I Tissue lngrowth

Proplast II Tissue tngrowth

Proplast I Local Cellular Response

Proplast II Local Cellular Response

I week Pooled maxillary implants Pooled mandibular implants

1.50 2.25

1.75 2.00

2.25 3.00

2.00 2.25

2 weeks Pooled maxillary implants Pooled mandibular implants

2.00 2.75

2.00 2.00

3.50 4.00

3.25 3.75

4 weeks Pooled maxillary implants Pooled mandibular implants

1.50 2.00

2.25 7_.__ ‘5

5.00 4.25

3.75 3.25

8 weeks Pooled maxillary implants Pooled mandibular implants

3.00 2.75

2.75 2.75

3.75 3.50

3.50 3.25

I2 weeks Pooled maxillary implants Pooled mandibular implants

2.25 3.50

2.00 2.75

3.75 3.25

5.50 2.75

16 weeks Pooled maxillary implants Pooled mandibular implants

3.50 3.00

3.25 3.50

3.50 4.50

3.25 4.00

2.50 3.00

3.00 2.75

3.75 4.00

3.75 3.75

Interval and Placement

20 weeks Pooled Pooled

maxillary implants mandibular implants

24 weeks Pooled maxillary Pooled ” Specimens

mandibular avulsed

implants implants

3.00

_.i

3.75

-

3.75

3.25

3.50

3.25

prior to retrieval

with the variable of implantation duration. To evaluate differences in host response to the two implant types, paired t tests were applied to tissue ingrowth and local cellular response data for implants placed in the same animal for the same time interval. Results

Gross examination of the infraorbital rim and inferior mandibular border implantation sites revealed no remarkable clinical differences. Manipulation of the implants by the animals in this study was much more pronounced than in our previous studies. Of the 64 implants, two were clinically infected and two others were completely avulsed because of manipulation by the animals. Tissue ingrowth values for all recovered implants were determined according to the criteria described in Table 1 by examining sections from the end and middle of each implant. These sections, identified by code symbols only, were examined by the same observer on two different occasions. The two rat-

ings obtained for each implant location for each time period were arithmetically averaged. These results are tabulated in Table 3 and plotted in Figure 2. The ratings for local cellular response were similarly treated and are shown in Table 3 and Figure 3. The arithmetic average of the tissue ingrowth ratings for a given histologic section, and time of implantation, were used for a linear regression and correlation analysis. The linear regression parameters of slope and intercept, and the correlation coefficient, r, are tabulated in Table 4 for tissue ingrowth ratings in each location. The slope value, 0.06, and intercept value, 2.1, for both pooled Proplast I and Proplast II are the same and are shown by the line in Figure 2. This means that the characteristics of tissue ingrowth improved with time for both types of implant. Correlation coefficients between the cellular response ratings and corresponding time of implantation were r = 0.08 and r = 0.06, respectively, for the Proplast I data and the Proplast II data. These values were not statistically significant. indicating that

774

PTFE/GRAPHITE

TISSUE INGROWTH

MRSLIS IlhrL

A Maxillary Proplast I Blah 0 MIiIIary Proplast II Biaks 0 Mandibular Pmplast I Blats OMardibular Proplarl II Blocks - Linear Regression Both Proplast I & Proplast I I Nale: 24 *etk Maxillary Proplast I I Blocks nulse4 before examination

7,

LOCAL CELLULAR

RESPONSE

VERSUS

TIME

6II

0

0 A

&

A

A 0

A

0

0

KEY: AMaxillary

qMaxillary

Proplast

I Blocks

Proplast

II Blocks

OMandibular

Proplast

OMandibular

Proplast

Note: 24 week Maxillary avulsed

h

I Blocks I I Blocks Proplast

I I Blocks

before examination

20 Weeks of lmplantat~on

FIGURE 2. Above, Data cluster and linear regression analysis of tissue ingrowth vs time. FIGURE 3. Be/o~l, Data clusters: local cellular response vs time.

local cellular response ratings (Table 3) did not vary with duration of implantation. Paired 1 tests were used to compare tissue ingrowth and local cellular response in Proplast I vs Proplast II. The tests showed that for the two Proplasts the mean difference in tissue ingrowth equaled 0.07 and was not significant, and the mean difference in local cellular response equaled 0.32 and was significant (P < .Ol). The latter significant difference indicates that there was a slightly greater local cellular response to the Proplast I. Discussion

Stabilization of microporous alloplasts by ingrowth of surrounding connective tissue has been

VS PTFEIALLJMINIJM

OXIDE IMPLANTS

found desirable for long-term clinical stability.“,” !’ The rapidity of stabilization from such tissue ingrowth is related to the biocompatibility of the implanted material. Characteristics including bulk chemistry, implant surface area and geometry, dynamic mechanical characteristics, and surface chemistry are foremost in determining biocompatibility of the implanted material.Y.” Similarly, local cellular reaction is also determined by the preceding characteristics. The effects of implant surface area and geometry characteristics have been well demonstrated with studies showing implanted films inducing neoplasia in mice.” These characteristics influence local cellular reaction to an implanted material and may involve anaplastic tissue response, an acute inflammatory reaction, or a chronic giant cell infiltration characteristic of implants that are mobile. Careful matching of the implant characteristics with mechanical behavior of tissue has been attained in the development of the Proplast I implant material. Further refinement of the implant characteristics has been accomplished with the development of the aluminum oxide (Proplast II) implant analog. In the initial comparison of the PTFE/ aluminum oxide analog to Proplast I, implant blocks were placed intraosseously in dog femora and showed very similar tissue responses (Homsy and Anderson: Personal communication, 1979). However, there was some difference in the rate of intra-implant ossification; the aluminum oxide analog had slightly less rapid appearance of osteoid and bone, and these were peripheral in intra-implant distribution. Considerable implant manipulation by the host baboons was observed in this study. This may have caused the clinical infections that occurred in two of the study blocks. Such manipulation certainly results in greater motion and stresses at the implanttissue interface. This motion is known to exacerbate local cellular reaction to an implanted material and is significant in determining giant cell infiltration and population at the implantation site.“.’ These stresses also inhibit initial soft tissue penetration into the implanted material and, if prolonged, may result in poor integration of the implant material and poor tissue acceptance. This influence on tissue ingrowth integration may even be more pronounced in areas with more tissue mobility, as in the infraorbital rim implantation area. The rate of tissue ingrowth in this study was less for both materials than that observed in our earlier Proplast I study using similar protocols.” The increased manipulation by the animals may have had significant bearing on the findings. Statistical analyses of the data on progression of

775

WESTFALL

ET AL

Table 4.

Comparison

of Tissue lngrowth

Slope

Data Base PI~,~/h*ct I A. Mandible/mid B. Mandible/end A. K; B. pooled

vs Time for Proplast

I and Proplast II

Intercept

Correlation Coefficient.

0.05 0.05 0.05

2.3 2.4 2.5

0.6 I 0.53 0.60

0.04 0.06 0.05

I.Y 2.1 2.0

0.50 0.57 0.5s

0.06

2.1

0.x?;

0.05 0.06

2.1 2. I

0.05

2. I

0.67-i o.hY-i 0.7%

0.07 0.07

2.0 2.0

G. M H. pooled

0.07

I.9

0.73-I 0.70, 0.X6:

I- . F.. G.. & H. pooled

0.06

2.1

0.76,

(‘. Infmorbitalimid I). Infraorbital/end C‘. & D. pooled

section section

section section

A.. B.. C.. k D. pooled Pwpltrs I II I:. Mandible/mid F. Mandible/end

section section

I<. Kr F. pooled (i. lnfraorbitalimid H. Infraorbital/end

section section

P c 0.05 that this value equals +1-’ 5. 0.01 that this value equals

I

zero. zero.

tissue ingrowth with time revealed a positive correlation, but there was no statistical difference between the data for the two materials. This increase of tissue density with time was expected and was seen to progress at the same rate for both test materials. No significant change in local cellular response was seen during the study period. It seems that whatever prevented a decrease in local cellular reaction over time may have acted to reduce the rate of tissue ingrowth over that observed in our previous work.“’ Possible explanations for this discrepancy may be the different host animal species used (baboon vs monkey) or the increased manipulation of the implants by the animals. There was a slightly lower cellular response to Proplast 11 compared with Proplast I. This somewhat milder reaction may be a reflection of the lower modulus of elasticity of the aluminum oxide analog. Less relative motion at the tissue implant interface can moderate the cellular response to an implant.

The authors thank Roger Weinburg, PhD, Professor. Department of Biometry, LSU Medical Center. for his assistance with statistical analyses in this study.

References I. Kent JN, Homsy CA. Hinds EC: Proplast in dental facial reconstruction. Oral Surg 39:347, 1975 2. Kent JN, Homsy CA. Gross BD. Hinds EC: Pilot studies of a porous implant in dentistry and oral surgery. J Oral Surg 30:608. 1972 3. Homsy CA: Bio-compatibility in selection of materials foi implantation. J Biomed Mater Res 4:341. 1970 4. Arem AJ, Rasmussen D, Madden JW: Soft tissue response to Proplast: Quantitation of scar ingrowth. Plast Reconstr Surg 61:214. 1978 5. Homsy CA: Implant stabilization-chemical and biochemical considerations. Symposium on Interposition and Lmplant Arthroplasty. Orthop Clin North Am 4:295, 1973 6. Hinds EC, Homsy CA, Kent JN: Use of a biocompatible interface for combining tissue and prosthesis in oral surgery. Oral Surg 38:512, 1974 7. Homsy CA, Kent JN, Hinds EC: Materials for oral implantation-biological and functional criteria. J Am Dent Assoc 86:817. 1973 8. Homsy CA. Cain TE, Kessler FB. Anderson MS. King JW: Porous implant systems for prosthesis stabilization. Clin Orthop 89:220. 1972 9 Homsy CA: Bio-compatibility of perfluorinated polymers and composites of these polymers. In Williams DF (Ed.): Biocompatibility, Vol II. Boca Raton, CRC Press. 1981 IO. Kent JN. Westfall RL: Presurgical infusion of Proplast: Primate facial augmentation. J Oral Surg 37:637, 1979 I I. Homsy CA, Anderson MS: Functional stabilization of soft tissue and bone prosthesis with a porous low modulus material system. In Williams DF (Ed): Biocompatibility of Implanted Materials. Tumbridge Wells. Sector Publishing. Ltd. 1976 12. Brand KG et al: Foreign-body tumorigenesis induced by glass and smooth and rough plastic: Comparative study of preneoplastic events. J Natl Cancer lnst 5?:319. 1975