~~
~
Development of a new percutaneous access device for implantation in soft tissues J. A. Jamen,* J. P.C. M. van der Waerden, and K. de Groot Biornaterials Research Group, Department of Biomaterials, School of Medicine, University of Leiden, Rijnsburgerweg 10, 2333 AA Leiden, The Netherlands The objective of this study was to evaluate a new type of percutaneous device (PD) designed to be implanted in soft tissues. The new PD consisted out of: (1) a flange-shaped subcutaneous component, made from sintered titanium fiber-web, and (2) a percutaneous component, made from dense sintered hydroxyapatite. The PDs were inserted in the back of 15 rabbits. The surgical procedure was performed in two steps. In the first session the subcutaneous component was placed. In the second session, after 3-4 months the percutaneous component was fixed in the subcutaneous component. The implants were left ilz situ for 1 and 4 months
after the second implantation session. Clinical and histological investigations were performed. It is found, that there was only a l i m i t e d epidermal d o w n growth in the percutaneous area. No inflammatory reaction was observed in the dermal connective tissue. Histological analysis also demonstrated that titanium fiber mesh evokes minor adverse effects of the surrounding tissues. In conclusion, these experiments have shown that stabilization of the PD in the hypodermal area by using a sintered titanium fiber-web structure favors the longevity of PDs implanted in soft tissues.
INTRODUCTION
Considerable research activities have already been undertaken to develop methods for the successful implantation of percutaneous implants in man or animal. However, up to now the results of clinical experiments with percutaneous implants that must be able to function for a longer period of time have not been very promising. The experiments mostly failed after a period of approximately 3 months, infer d i n owing to infection or marsupialization of the implants. In earlier reports'-3 we describe the results of our investigations with percutaneous implants in rabbits. The outcomes of these experiments demonstrated that direct attachment of the percutaneous device to bony skeletal tissues is effective in the maintenance of a long-term failure free percutaneous passage. The stably anchoring of the implant to bone minimizes the mechanical stresses at the interface between the implant and the skin and benefits the percutaneous longevity. Although these skeleton-anchored devices are successful, in many situations where percutaneous conduits are indicated, solely soft-tissue anchored *To whom correspondence should be addressed. Journal of Biomedical Materials Research, Vol. 25, 1535-1545 (1991) CCC 0021-9304/91/121535-11$4.00 0 1991 John Wiley & Sons, Inc.
1536
JANSEN, VAN DER WAERDEN, A N D DE GROOT
systems have to be used. Peritoneal dialysis, for example, demands insertion of the percutaneous implant in the highly mobile tissue of the abdominal wall. It is therefore the purpose of this study to evaluate a new type of percutaneous conduit capable of functioning in soft tissues for a longer period of time, also if no bony tissue is present to stabilize the percutaneous device.
MATERIAL A N D METHODS
Implants The percutaneous devices (Fig. 1) consisted of two elements: (1) a flangeshaped subcutaneous component which provides a firm base in the soft tissue and stabilizes the interface between the tissue and the implant, and (2) a percutaneous component which penetrates the skin and interfaces with its tissues. The subcutaneous part was fabricated from sintered titanium fiber mesh sheet. The subcutaneous part measured about 3 X 4 cm. The fiber diameter was 50 pm. The porosity of the fiber structure was 80%. In the middle of the subcutaneous part a rigid pure titanium disk was fixed. Centrally, the titanium disk was provided with a threaded hole for the firm and stable attachment of the skin-penetrating part. The percutaneous part was made from dense hydroxyapatite prepared from commercially available hydroxyapatite powders. The basic shape of this component was a cylinder. Three versions, with varying diameters (0.5-1.5 cm), were constructed. The percutaneous part was fixed in the central hole of the subcutaneous part by means of a screw.
Animals and surgical procedures Fifteen adult New Zealand White rabbits were used in this experiment. Percutaneous devices were implanted in the dorsum of the experimental ani-
Figure 1. Percutaneous device used in the experiments
A N E W SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1537
mals. The surgical procedure was performed in two steps. The first stage of the implantation procedure comprises applying the subcutaneous part of the implant. In a second stage of the implantation procedure the percutaneous part is fixed to the subcutaneous component. During surgery the animals were sedated by intramuscular injections of Hypnorm (Duphar, Amsterdam). After sedation of the rabbits the back is, on both sides of the spinal column, shaved, depilated, washed, and disinfected with iodine. In the first session a longitudinal incision is made through the full thickness of the skin, parallel to the spinal column. The incision is about 3-4 cm in length. Then, laterally to the incision a subcutaneous pocket is created by undermining the skin with a pair of scissors. The subcutaneous part of the implant is placed in this pocket and the wound is carefully closed by means of sutures. In the second session, after 3-4 months, the skin is incised over the central fixed disk of the subcutaneous component. After exposing the threaded hole, the percutaneous component of the implant is fixed in the subcutaneous part. Finally, the skin is sutured. All animals were inspected once every week and the percutaneous implantation sites were carefully cleaned. During these inspections, the animal's reaction to the implant, its health, and the condition of the local tissues around the implant were evaluated. The rabbits were sacrificed 1 and 4 months after the second implantation session by injecting Nembutal peritoneally. Five rabbits were killed after 1 month and 10 rabbits 4 months after surgery. Histological procedures After killing the animals, the implants with their surrounding tissues were excised immediately and fixed in 10% buffered formalin solution for histological processing. All tissue specimens were embedded in methylmetacrylate. After polymerization thin (10 pm) sections were cut, containing the implants as well as the surrounding tissues attached to them. The sections were made using a standard diamond blade sawing t e c h n i q ~ eThis . ~ simple method provides sections which can be used directly for light microscopy without the need of extending grinding and polishing procedures. The sections were stained with methylene blue and basic fuchsin and investigated by light microscopy.
RESULTS
Clinical findings The results of the percutaneous implants in the rabbits are summarized in Table I. The experimental animals appeared to be in good general health throughout the test periods. Of the 15 implants, 4 were lost. One implant failed because of fracture of the percutaneous hydroxyapatite part of the implant. The
JANSEN, VAN DER WAERDEN, AND DE GROOT
1538
TABLE I Clinical Results Percutaneous Implants Implants 1 month ( n = 5) 4 months (n = 10)
Infection
Undisturbed Wound Healing
Failure
5 6
4
other three implants failed because the fiber web tore at the junction of the fiber mesh/percutaneous holding plate (Fig. 2). These failures occurred after an implantation time of 1-2 months. The rest of the implants showed an uneventful healing without any macroscopical evidence of an inflammatory reaction (Fig. 3). No signs of redness or swelling were found in the tissues surrounding the percutaneous part and covering the subcutaneous part of the implant. There was also no appearance of exudate at the skinhmplant interface.
Figure 2. Clincial appearance of a failed implant. The tear in the fiber web has developed at the change fiber web/holding plate (arrow).
Figure 3. Clinical appearance of a successful implant 4 months after the second surgical session. There are no signs of an inflammatory reaction. The skin is closely adapted to the percutaneous part.
A N E W SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1539
Histological findings
Light microscopic evaluation of the 1-month implants demonstrated a limited downgrowth of the epiderms with the formation of a sinus tract. The sinus was filled with keratin. In the sections two types of epidermal response to the percutaneous implant surface could be observed. The first type was characterized by the formation of a direct epithelial tissue-implant contact (Fig. 4), while in the second type the epidermis failed to form a direct connection with the implant surface (Fig. 5). Epidermal downgrowth without attachment was associated with a mild inflammatory response of the surrounding dermal connective tissue. Histological analysis of the successful 4-month implants showed that the epidermal downgrowth had proceeded. However, the epidermal downgrowth did not progress any further than the holding plate for the fixation of the percutaneous component of the implant. Similar to the 1-month implants in most specimens the epidermis formed a close junction with the percutaneous part of the implant (Fig. 6). In these specimens no inflammatory reaction was observed in the dermal connective tissue. Occasionally, it was observed, that the superficial epidermis did not reach to the neck part of the implants (Fig. 7). The connective tissue surrounding these nonadherent implants displayed a mild inflammatory response.
Figure 4. Histological section of a successful percutaneous implant 1 month after the second surgical session. A small sinus has developed. The sinus is filled with keratin (K). The epithelium (E) is attached to the implant surface (I). (A) original magnification X42, bar = 238 pm, (8)origi, = 82 pm. nal magnification ~ 1 2 2bar
1540
JANSEN, VAN DER WAERDEN, AND DE GROOT
Figure 5. Micrograph showing the second type of epithelial reaction, 1 month after insertion of the percutaneous part. The sinus is filled with keratin (K). Note the mild inflammatory reaction in the surrounding connective tissue. (A) original magnification ~ 3 0 bar , = 330 pm, ( 8 ) original , = 82 pm. magnification ~ 1 2 2bar
Examination of the failed percutaneous implants revealed, that at the side where the tear of the fiber mesh sheet had occurred the epidermis had grown under the titanium holding plate [Fig. 8(A)]. The epithelium appeared to be in intimate contact with the holding plate. No inflammatory cells were seen. At the other side, the epidermis had grown downward along the neck of the implant. This downgrowth was seemingly arrested at the borderline between percutaneous component and titanium holding plate and the epithelium was seen attached to the neck of the implant at this location [Fig. 8(B)]. Histological assessment of the subcutaneous tissue response to the titaniun fiber sheets showed that this portion of the implants was surrounded by a thin fibrous capsule (Fig. 9). The material caused remarkably little tissue reaction. The pores of the fiber web structure were infiltrated by blood vessels, connective tissue cells, and find collagen fibrils (Fig. 10). Only occasionally macrophages were seen inside the implants. These macrophages were always concentrated at one side of the titanium fibers.
DISCUSSION A N D CONCLUSION
The results of this study demonstrate that stabilization of the percutaneous device in the hypodermal area by using a sintered titanium fiber structure favors the longevity of percutaneous devices implanted in soft tissue. It is
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1541
Figure 6. Percutaneous passage of-an implant 4 months after placement of the percutaneous part. A limited downgrowth of the epidermis is observed. The epithelium (E) at the bottom of the sinus terminates in direct apposition with the implant surface (I). The sinus tract (S) is filled with keratin. The connective tissue (C) is free of inflammation. (A) original , = magnification X42, bar = 238 pm, (B) original magnification ~ 1 2 2 bar 82 pm.
also shown that titanium fiber mesh evokes minor adverse effects of the surrounding tissues. The successful healing event was associated with the ingrowth into the mesh apertures of connective tissue, specifically fibroblasts, collagen fibrils, and blood vessels. The observations in this study are supported by earlier findings of Winter? Squier,6Lundgren; Campbell: von Recum," and Yan." Winter studied the reactions of porcine epidermis surrounding various solid and porous implants. Epidermal migration was, in contrast to the other implants, not observed alongside the implants of hydron sponge with pores of 40 pm in diameter and porous PTFE with pores of 10 pm. The pores of these materials were invaded by fibrous tissue collagen and collagen fibers were formed across the interface between the implant and the surrounding epidermis. He concluded that the presence of healthy fibrous tissue around implants benefits the epithelial downgrowth. Squier inserted Millipore filters of different pore sizes into the backskin of pigs. Histological observations revealed a relationship between the extent of connective tissue infiltration and the rate of epithelial migration. It was found that 3 pm is the minimum pore size, that allows connective tissue infiltration which forms a barrier against epidermal migration. Lundgren coated monofilament polyester fabrics with titanium. These fabrics were implanted percutaneously in the back of rabbits. Ingrowth of connective tissue into the mesh apertures were observed, especially in fabrics with
1542
JANSEN,V A N DER WAERDEN, A N D D E G R O O T
Figure 7. A specimen of 4-month percutaneous device, showing that the epithelium is separated from the implant surface by a sinus tract (S) filled with keratin. The connective tissue surrounding this implant displayed a mild inflammatory response, original magnification X76, bar = 130 pm.
large mesh apertures ( 2 80 pm). Campbell and von Recum demonstrated that the connective tissue response to the implant is influenced by the porosity of the implant material. They implanted Versapore filters with five different pore sizes into the subcutaneous space in the back of dogs. It was concluded that pores of 1-2 pm diameter allow the direct attachment of fibroblasts to the implants and the production of a normal connective tissue. Yan tested Dacron velour implants vacuum coated with titanium. The results in this study indicated that titanium coating affects the quality of the interfacing tissue and may improve long-term histocompatibility. However, as we demonstrated in previous experiments3with different types of percutaneous implants inserted in rabbits, formation of a thin fibrous capsule and connective tissue ingrowth is not enough to obtain a good and durable percutaneous passage. When no other provisions are met to minimize the mechanical stresses at the interface between the implant and the skin the epidermal downgrowth will proceed, which finally will lead to implant failure. As already mentioned in the introduction, one of the most clinically successful methods to reduce these mechanical stresses around percutaneous devices is the direct anchoring of the implant to the skeletal b~ne.’-~,’’,’~ A long-term failure free percutaneous passage, however, remains a problem for applications where no underlying skeletal bone is available for the stabilization of the implant. In such cases other techniques are required to alleviate the mechanical stresses. For example, subcutaneous anchors can be
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1543
Figure 8. Histological section of a failed percutaneous implant. (A) At the side were the tear has developed in the fiber-web mesh, the skin had grown under the titanium holding plate (H). The epithelium (E) appeared to form a junction with the holding plate. The connective tissue (C) below the epithelium is free of inflammation, original magnification ~ 1 2 2 , bar = 82 pm, (B) At the other side, the epithelium has migrated downward until it reached the holding plate (H). The epithelium appears to form a stable junction with the holding plate, original magnification ~ 3 0 bar , = 130 p m .
ap~1ied.I~ The purpose of a subcutaneous anchor is to transfer the mechanical forces from the percutaneous area to the deeper subdermal tissues. Various designs for the configuration of the subcutaneous anchors have been proposed, ranging from simple to more complex structures. Although, it is speculated that flexible anchors distribute stresses into the deeper laying tissues more evenly,I4the criteria for the optimal implant design are still not known. The success with our subcutaneous anchor configuration, now, is probably a result of the unique properties of metal fiber mesh sheet. The fact is, that a mesh sheet made of metallic fibers is firm and porous at the same time, while it is also elastic permitting bending of the sheet to allow for movement of the skin.
1544
JANSEN, VAN DER WAERDEN, AND DE GROOT
Figure 9. The titanium fiber-web structure is surrounded by a thin fibrous capsule (between black arrows), original magnification ~ 1 6 0bar , = 62 pm.
Figure 10. Light micrographs showing the ingrowth of connective tissue, collagen fibers and capillaries into the fiber-web structure. There is remarkably little adverse tissue reaction. (A) Original magnification ~ 1 6 0 , bar = 62 pm, (B) Detail showing more clearly the tissue reaction, original , = 20 ym. magnification ~ 4 9 0 bar
In conclusion, these experiments have demonstrated that percutaneous devices can be maintained when stabilized by sintered titanium fiber sheet structures. On the basis of the described results and all the above mentioned studies, it may also be hypothesized that the reason for success with this new type of percutaneous conduit lies in the combination of the excellent tissue
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1545
characteristics of titanium with the typical characteristics of fiber products as flexibility and stiffness. In this light, further investigations have to be performed to study the long-term behavior of this fiber mesh percutaneous implants. In addition, to improve the design of the implant, comparative studies have to be conducted to determine the optimal fiber mesh configuration in porosity, flexibility, and metallic fiber in relation to tissue response. These investigations are supported by the Netherlands Technology Foundation (STW). The authors also would like to thank Mr. J. Grimbergen for this technical assistance in the experimental animal experiments.
References 1. J. A. Jansen, J. P.C. M. van der Waerden, and K. de Groot, "Epithelial re-
2. 3. 4.
8.
9. 10. 11. 12.
13. 14.
action to percutaneous implant materials: in vitro and in vivo experiments," J. Invest. Surg., 2, 29-49 (1989). J. A. Jansen, J. P.C. M. van der Waerden, H. B. M. van der Lubbe, and K. de Groot, "Tissue response to percutaneous implants in rabbits," J. Biomed. Mater. Res., 24, 295-307 (1990). J. A. Jansen, J. P.C. M. van der Waerden, and K. de Groot, "Wound healing phenomena around percutaneous devices implanted in rabbits," Materials in Medicine, 1, 192-197 (1990). H. 8. M. van der Lubbe, C. P. A.T. Klein, and K. de Groot, "A simple method for preparing thin (10 pm) histological sections of undecalcified plastic embedded bone with implants," Stain Technol., 63, 171-177 (1988). G. D. Winter, "Transcutaneous implants: reactions of the skin-implant interface," J. Biorned. Muter. Res., 5, 99-113 (1974). C. A. Squier and P. Collins, "The relationship between soft tissue attachment, epithelial downgrowth and surface porosity," ]. Periodontal Res., 16, 434-440 (1981). D. Lundgren, J. P. Hakansson, and P. Bodo, "Morphometric analysis of tissue components adjacent to percutaneous implants," in Tissue Integration in Oral and Maxillo-Facial Reconstruction, Excerpta Medica, Elsevier Science Publishers B. V., Amsterdam, 1986, pp. 173-180. C. E. Campbell and A. F. von Recum, "Microtopography and soft tissue response," 1.Invest. Surg., 2, 51-74 (1989). A. F. von Recum, "New aspects of biocompatibility: motion at the interface," in Advances in Biomaterials Vol. 9, Elsevier Science Publishers B. V., Amsterdam, 1990, pp. 297-302. J.Y. J. Yan, F. W. Cooke, P. S. Vaskelis, and A. F. von Recum, "Titaniumcoated Dacron velour: A study of interfacial connective tissue formation," J. Biomed. Mater. Res., 23, 171-189 (1989). T. Albrektsson, P.-I. Branemark, M. Jacobsson, and A. Tjellstrom, "Present clinical application of osseointegrated percutaneous implants," Plast. Reconstr. Surg., 79, 721-732 (1986). K. M. Holgers, A. Tjellstrom, L. M. Bjursten, and B. E. Erlandsson, "Soft tissue reaction around percutaneous implants: a clinical study on skin-penetrating titanium implants used for bone-anchored auricular prosthesis," Int. J. Oral Maxillofac. Irnpl. 2, 35-39 (1987). C. G. Grosse-Siestrup and K. Affeld, "Design criteria for percutaneous devices," 1. Biomed. Mater. Res., 18, 357-382 (1984). A. F. von Recum and J. B. Park, "Permanent percutaneous devices," CXC Crit. Rev. Bioeng., 5, 37-77 (1981).
Received November 6,1990 Accepted June 12,1991
~
Development of a new percutaneous access device for implantation in soft tissues J. A. Jamen,* J. P.C. M. van der Waerden, and K. de Groot Biornaterials Research Group, Department of Biomaterials, School of Medicine, University of Leiden, Rijnsburgerweg 10, 2333 AA Leiden, The Netherlands The objective of this study was to evaluate a new type of percutaneous device (PD) designed to be implanted in soft tissues. The new PD consisted out of: (1) a flange-shaped subcutaneous component, made from sintered titanium fiber-web, and (2) a percutaneous component, made from dense sintered hydroxyapatite. The PDs were inserted in the back of 15 rabbits. The surgical procedure was performed in two steps. In the first session the subcutaneous component was placed. In the second session, after 3-4 months the percutaneous component was fixed in the subcutaneous component. The implants were left ilz situ for 1 and 4 months
after the second implantation session. Clinical and histological investigations were performed. It is found, that there was only a l i m i t e d epidermal d o w n growth in the percutaneous area. No inflammatory reaction was observed in the dermal connective tissue. Histological analysis also demonstrated that titanium fiber mesh evokes minor adverse effects of the surrounding tissues. In conclusion, these experiments have shown that stabilization of the PD in the hypodermal area by using a sintered titanium fiber-web structure favors the longevity of PDs implanted in soft tissues.
INTRODUCTION
Considerable research activities have already been undertaken to develop methods for the successful implantation of percutaneous implants in man or animal. However, up to now the results of clinical experiments with percutaneous implants that must be able to function for a longer period of time have not been very promising. The experiments mostly failed after a period of approximately 3 months, infer d i n owing to infection or marsupialization of the implants. In earlier reports'-3 we describe the results of our investigations with percutaneous implants in rabbits. The outcomes of these experiments demonstrated that direct attachment of the percutaneous device to bony skeletal tissues is effective in the maintenance of a long-term failure free percutaneous passage. The stably anchoring of the implant to bone minimizes the mechanical stresses at the interface between the implant and the skin and benefits the percutaneous longevity. Although these skeleton-anchored devices are successful, in many situations where percutaneous conduits are indicated, solely soft-tissue anchored *To whom correspondence should be addressed. Journal of Biomedical Materials Research, Vol. 25, 1535-1545 (1991) CCC 0021-9304/91/121535-11$4.00 0 1991 John Wiley & Sons, Inc.
1536
JANSEN, VAN DER WAERDEN, A N D DE GROOT
systems have to be used. Peritoneal dialysis, for example, demands insertion of the percutaneous implant in the highly mobile tissue of the abdominal wall. It is therefore the purpose of this study to evaluate a new type of percutaneous conduit capable of functioning in soft tissues for a longer period of time, also if no bony tissue is present to stabilize the percutaneous device.
MATERIAL A N D METHODS
Implants The percutaneous devices (Fig. 1) consisted of two elements: (1) a flangeshaped subcutaneous component which provides a firm base in the soft tissue and stabilizes the interface between the tissue and the implant, and (2) a percutaneous component which penetrates the skin and interfaces with its tissues. The subcutaneous part was fabricated from sintered titanium fiber mesh sheet. The subcutaneous part measured about 3 X 4 cm. The fiber diameter was 50 pm. The porosity of the fiber structure was 80%. In the middle of the subcutaneous part a rigid pure titanium disk was fixed. Centrally, the titanium disk was provided with a threaded hole for the firm and stable attachment of the skin-penetrating part. The percutaneous part was made from dense hydroxyapatite prepared from commercially available hydroxyapatite powders. The basic shape of this component was a cylinder. Three versions, with varying diameters (0.5-1.5 cm), were constructed. The percutaneous part was fixed in the central hole of the subcutaneous part by means of a screw.
Animals and surgical procedures Fifteen adult New Zealand White rabbits were used in this experiment. Percutaneous devices were implanted in the dorsum of the experimental ani-
Figure 1. Percutaneous device used in the experiments
A N E W SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1537
mals. The surgical procedure was performed in two steps. The first stage of the implantation procedure comprises applying the subcutaneous part of the implant. In a second stage of the implantation procedure the percutaneous part is fixed to the subcutaneous component. During surgery the animals were sedated by intramuscular injections of Hypnorm (Duphar, Amsterdam). After sedation of the rabbits the back is, on both sides of the spinal column, shaved, depilated, washed, and disinfected with iodine. In the first session a longitudinal incision is made through the full thickness of the skin, parallel to the spinal column. The incision is about 3-4 cm in length. Then, laterally to the incision a subcutaneous pocket is created by undermining the skin with a pair of scissors. The subcutaneous part of the implant is placed in this pocket and the wound is carefully closed by means of sutures. In the second session, after 3-4 months, the skin is incised over the central fixed disk of the subcutaneous component. After exposing the threaded hole, the percutaneous component of the implant is fixed in the subcutaneous part. Finally, the skin is sutured. All animals were inspected once every week and the percutaneous implantation sites were carefully cleaned. During these inspections, the animal's reaction to the implant, its health, and the condition of the local tissues around the implant were evaluated. The rabbits were sacrificed 1 and 4 months after the second implantation session by injecting Nembutal peritoneally. Five rabbits were killed after 1 month and 10 rabbits 4 months after surgery. Histological procedures After killing the animals, the implants with their surrounding tissues were excised immediately and fixed in 10% buffered formalin solution for histological processing. All tissue specimens were embedded in methylmetacrylate. After polymerization thin (10 pm) sections were cut, containing the implants as well as the surrounding tissues attached to them. The sections were made using a standard diamond blade sawing t e c h n i q ~ eThis . ~ simple method provides sections which can be used directly for light microscopy without the need of extending grinding and polishing procedures. The sections were stained with methylene blue and basic fuchsin and investigated by light microscopy.
RESULTS
Clinical findings The results of the percutaneous implants in the rabbits are summarized in Table I. The experimental animals appeared to be in good general health throughout the test periods. Of the 15 implants, 4 were lost. One implant failed because of fracture of the percutaneous hydroxyapatite part of the implant. The
JANSEN, VAN DER WAERDEN, AND DE GROOT
1538
TABLE I Clinical Results Percutaneous Implants Implants 1 month ( n = 5) 4 months (n = 10)
Infection
Undisturbed Wound Healing
Failure
5 6
4
other three implants failed because the fiber web tore at the junction of the fiber mesh/percutaneous holding plate (Fig. 2). These failures occurred after an implantation time of 1-2 months. The rest of the implants showed an uneventful healing without any macroscopical evidence of an inflammatory reaction (Fig. 3). No signs of redness or swelling were found in the tissues surrounding the percutaneous part and covering the subcutaneous part of the implant. There was also no appearance of exudate at the skinhmplant interface.
Figure 2. Clincial appearance of a failed implant. The tear in the fiber web has developed at the change fiber web/holding plate (arrow).
Figure 3. Clinical appearance of a successful implant 4 months after the second surgical session. There are no signs of an inflammatory reaction. The skin is closely adapted to the percutaneous part.
A N E W SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1539
Histological findings
Light microscopic evaluation of the 1-month implants demonstrated a limited downgrowth of the epiderms with the formation of a sinus tract. The sinus was filled with keratin. In the sections two types of epidermal response to the percutaneous implant surface could be observed. The first type was characterized by the formation of a direct epithelial tissue-implant contact (Fig. 4), while in the second type the epidermis failed to form a direct connection with the implant surface (Fig. 5). Epidermal downgrowth without attachment was associated with a mild inflammatory response of the surrounding dermal connective tissue. Histological analysis of the successful 4-month implants showed that the epidermal downgrowth had proceeded. However, the epidermal downgrowth did not progress any further than the holding plate for the fixation of the percutaneous component of the implant. Similar to the 1-month implants in most specimens the epidermis formed a close junction with the percutaneous part of the implant (Fig. 6). In these specimens no inflammatory reaction was observed in the dermal connective tissue. Occasionally, it was observed, that the superficial epidermis did not reach to the neck part of the implants (Fig. 7). The connective tissue surrounding these nonadherent implants displayed a mild inflammatory response.
Figure 4. Histological section of a successful percutaneous implant 1 month after the second surgical session. A small sinus has developed. The sinus is filled with keratin (K). The epithelium (E) is attached to the implant surface (I). (A) original magnification X42, bar = 238 pm, (8)origi, = 82 pm. nal magnification ~ 1 2 2bar
1540
JANSEN, VAN DER WAERDEN, AND DE GROOT
Figure 5. Micrograph showing the second type of epithelial reaction, 1 month after insertion of the percutaneous part. The sinus is filled with keratin (K). Note the mild inflammatory reaction in the surrounding connective tissue. (A) original magnification ~ 3 0 bar , = 330 pm, ( 8 ) original , = 82 pm. magnification ~ 1 2 2bar
Examination of the failed percutaneous implants revealed, that at the side where the tear of the fiber mesh sheet had occurred the epidermis had grown under the titanium holding plate [Fig. 8(A)]. The epithelium appeared to be in intimate contact with the holding plate. No inflammatory cells were seen. At the other side, the epidermis had grown downward along the neck of the implant. This downgrowth was seemingly arrested at the borderline between percutaneous component and titanium holding plate and the epithelium was seen attached to the neck of the implant at this location [Fig. 8(B)]. Histological assessment of the subcutaneous tissue response to the titaniun fiber sheets showed that this portion of the implants was surrounded by a thin fibrous capsule (Fig. 9). The material caused remarkably little tissue reaction. The pores of the fiber web structure were infiltrated by blood vessels, connective tissue cells, and find collagen fibrils (Fig. 10). Only occasionally macrophages were seen inside the implants. These macrophages were always concentrated at one side of the titanium fibers.
DISCUSSION A N D CONCLUSION
The results of this study demonstrate that stabilization of the percutaneous device in the hypodermal area by using a sintered titanium fiber structure favors the longevity of percutaneous devices implanted in soft tissue. It is
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1541
Figure 6. Percutaneous passage of-an implant 4 months after placement of the percutaneous part. A limited downgrowth of the epidermis is observed. The epithelium (E) at the bottom of the sinus terminates in direct apposition with the implant surface (I). The sinus tract (S) is filled with keratin. The connective tissue (C) is free of inflammation. (A) original , = magnification X42, bar = 238 pm, (B) original magnification ~ 1 2 2 bar 82 pm.
also shown that titanium fiber mesh evokes minor adverse effects of the surrounding tissues. The successful healing event was associated with the ingrowth into the mesh apertures of connective tissue, specifically fibroblasts, collagen fibrils, and blood vessels. The observations in this study are supported by earlier findings of Winter? Squier,6Lundgren; Campbell: von Recum," and Yan." Winter studied the reactions of porcine epidermis surrounding various solid and porous implants. Epidermal migration was, in contrast to the other implants, not observed alongside the implants of hydron sponge with pores of 40 pm in diameter and porous PTFE with pores of 10 pm. The pores of these materials were invaded by fibrous tissue collagen and collagen fibers were formed across the interface between the implant and the surrounding epidermis. He concluded that the presence of healthy fibrous tissue around implants benefits the epithelial downgrowth. Squier inserted Millipore filters of different pore sizes into the backskin of pigs. Histological observations revealed a relationship between the extent of connective tissue infiltration and the rate of epithelial migration. It was found that 3 pm is the minimum pore size, that allows connective tissue infiltration which forms a barrier against epidermal migration. Lundgren coated monofilament polyester fabrics with titanium. These fabrics were implanted percutaneously in the back of rabbits. Ingrowth of connective tissue into the mesh apertures were observed, especially in fabrics with
1542
JANSEN,V A N DER WAERDEN, A N D D E G R O O T
Figure 7. A specimen of 4-month percutaneous device, showing that the epithelium is separated from the implant surface by a sinus tract (S) filled with keratin. The connective tissue surrounding this implant displayed a mild inflammatory response, original magnification X76, bar = 130 pm.
large mesh apertures ( 2 80 pm). Campbell and von Recum demonstrated that the connective tissue response to the implant is influenced by the porosity of the implant material. They implanted Versapore filters with five different pore sizes into the subcutaneous space in the back of dogs. It was concluded that pores of 1-2 pm diameter allow the direct attachment of fibroblasts to the implants and the production of a normal connective tissue. Yan tested Dacron velour implants vacuum coated with titanium. The results in this study indicated that titanium coating affects the quality of the interfacing tissue and may improve long-term histocompatibility. However, as we demonstrated in previous experiments3with different types of percutaneous implants inserted in rabbits, formation of a thin fibrous capsule and connective tissue ingrowth is not enough to obtain a good and durable percutaneous passage. When no other provisions are met to minimize the mechanical stresses at the interface between the implant and the skin the epidermal downgrowth will proceed, which finally will lead to implant failure. As already mentioned in the introduction, one of the most clinically successful methods to reduce these mechanical stresses around percutaneous devices is the direct anchoring of the implant to the skeletal b~ne.’-~,’’,’~ A long-term failure free percutaneous passage, however, remains a problem for applications where no underlying skeletal bone is available for the stabilization of the implant. In such cases other techniques are required to alleviate the mechanical stresses. For example, subcutaneous anchors can be
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1543
Figure 8. Histological section of a failed percutaneous implant. (A) At the side were the tear has developed in the fiber-web mesh, the skin had grown under the titanium holding plate (H). The epithelium (E) appeared to form a junction with the holding plate. The connective tissue (C) below the epithelium is free of inflammation, original magnification ~ 1 2 2 , bar = 82 pm, (B) At the other side, the epithelium has migrated downward until it reached the holding plate (H). The epithelium appears to form a stable junction with the holding plate, original magnification ~ 3 0 bar , = 130 p m .
ap~1ied.I~ The purpose of a subcutaneous anchor is to transfer the mechanical forces from the percutaneous area to the deeper subdermal tissues. Various designs for the configuration of the subcutaneous anchors have been proposed, ranging from simple to more complex structures. Although, it is speculated that flexible anchors distribute stresses into the deeper laying tissues more evenly,I4the criteria for the optimal implant design are still not known. The success with our subcutaneous anchor configuration, now, is probably a result of the unique properties of metal fiber mesh sheet. The fact is, that a mesh sheet made of metallic fibers is firm and porous at the same time, while it is also elastic permitting bending of the sheet to allow for movement of the skin.
1544
JANSEN, VAN DER WAERDEN, AND DE GROOT
Figure 9. The titanium fiber-web structure is surrounded by a thin fibrous capsule (between black arrows), original magnification ~ 1 6 0bar , = 62 pm.
Figure 10. Light micrographs showing the ingrowth of connective tissue, collagen fibers and capillaries into the fiber-web structure. There is remarkably little adverse tissue reaction. (A) Original magnification ~ 1 6 0 , bar = 62 pm, (B) Detail showing more clearly the tissue reaction, original , = 20 ym. magnification ~ 4 9 0 bar
In conclusion, these experiments have demonstrated that percutaneous devices can be maintained when stabilized by sintered titanium fiber sheet structures. On the basis of the described results and all the above mentioned studies, it may also be hypothesized that the reason for success with this new type of percutaneous conduit lies in the combination of the excellent tissue
A NEW SOFT TISSUE ANCHORED PERCUTANEOUS DEVICE
1545
characteristics of titanium with the typical characteristics of fiber products as flexibility and stiffness. In this light, further investigations have to be performed to study the long-term behavior of this fiber mesh percutaneous implants. In addition, to improve the design of the implant, comparative studies have to be conducted to determine the optimal fiber mesh configuration in porosity, flexibility, and metallic fiber in relation to tissue response. These investigations are supported by the Netherlands Technology Foundation (STW). The authors also would like to thank Mr. J. Grimbergen for this technical assistance in the experimental animal experiments.
References 1. J. A. Jansen, J. P.C. M. van der Waerden, and K. de Groot, "Epithelial re-
2. 3. 4.
8.
9. 10. 11. 12.
13. 14.
action to percutaneous implant materials: in vitro and in vivo experiments," J. Invest. Surg., 2, 29-49 (1989). J. A. Jansen, J. P.C. M. van der Waerden, H. B. M. van der Lubbe, and K. de Groot, "Tissue response to percutaneous implants in rabbits," J. Biomed. Mater. Res., 24, 295-307 (1990). J. A. Jansen, J. P.C. M. van der Waerden, and K. de Groot, "Wound healing phenomena around percutaneous devices implanted in rabbits," Materials in Medicine, 1, 192-197 (1990). H. 8. M. van der Lubbe, C. P. A.T. Klein, and K. de Groot, "A simple method for preparing thin (10 pm) histological sections of undecalcified plastic embedded bone with implants," Stain Technol., 63, 171-177 (1988). G. D. Winter, "Transcutaneous implants: reactions of the skin-implant interface," J. Biorned. Muter. Res., 5, 99-113 (1974). C. A. Squier and P. Collins, "The relationship between soft tissue attachment, epithelial downgrowth and surface porosity," ]. Periodontal Res., 16, 434-440 (1981). D. Lundgren, J. P. Hakansson, and P. Bodo, "Morphometric analysis of tissue components adjacent to percutaneous implants," in Tissue Integration in Oral and Maxillo-Facial Reconstruction, Excerpta Medica, Elsevier Science Publishers B. V., Amsterdam, 1986, pp. 173-180. C. E. Campbell and A. F. von Recum, "Microtopography and soft tissue response," 1.Invest. Surg., 2, 51-74 (1989). A. F. von Recum, "New aspects of biocompatibility: motion at the interface," in Advances in Biomaterials Vol. 9, Elsevier Science Publishers B. V., Amsterdam, 1990, pp. 297-302. J.Y. J. Yan, F. W. Cooke, P. S. Vaskelis, and A. F. von Recum, "Titaniumcoated Dacron velour: A study of interfacial connective tissue formation," J. Biomed. Mater. Res., 23, 171-189 (1989). T. Albrektsson, P.-I. Branemark, M. Jacobsson, and A. Tjellstrom, "Present clinical application of osseointegrated percutaneous implants," Plast. Reconstr. Surg., 79, 721-732 (1986). K. M. Holgers, A. Tjellstrom, L. M. Bjursten, and B. E. Erlandsson, "Soft tissue reaction around percutaneous implants: a clinical study on skin-penetrating titanium implants used for bone-anchored auricular prosthesis," Int. J. Oral Maxillofac. Irnpl. 2, 35-39 (1987). C. G. Grosse-Siestrup and K. Affeld, "Design criteria for percutaneous devices," 1. Biomed. Mater. Res., 18, 357-382 (1984). A. F. von Recum and J. B. Park, "Permanent percutaneous devices," CXC Crit. Rev. Bioeng., 5, 37-77 (1981).
Received November 6,1990 Accepted June 12,1991
