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Jornal Vascular Brasileiro

versão impressa ISSN 1677-5449versão On-line ISSN 1677-7301

J. vasc. bras. v.6 n.2 Porto Alegre jun. 2007 



Latex-derived vascular prosthesis



Marcelo Luiz BrandãoI; Joaquim Coutinho NettoII; Jose Antonio ThomaziniIII; João José LachatIII; Valdair Francisco MugliaIV; Carlos Eli PiccinatoV

IPhD, Department of Surgery and Anatomy, Faculdade de Medicina de Ribeirão Preto — Universidade de São Paulo (FMRP-USP), Ribeirão Preto, SP, Brazil
IIAssociate professor, Department of Biochemistry and Immunology, FMRP-USP, Ribeirão Preto, SP, Brazil
IIIPhD, Division of Anatomy, Department of Surgery and Anatomy, FMRP-USP, Ribeirão Preto, SP, Brazil
IVPhD, Division of Image Sciences, Department of Medical Clinic, FMRP-USP, Ribeirão Preto, SP, Brazil
VProfessor, Division of Vascular Surgery, Department of Surgery and Anatomy, FMRP-USP, Ribeirão Preto, SP, Brazil





BACKGROUND: The development of vascular grafts has been crucial for advances and achievements in reconstructive vascular surgery over the past 5 decades.
OBJECTIVES: To develop a new model of microperforated vascular graft using fabric covered with a natural latex-derived polymer taken from Hevea brasiliensis and assess its patency, thrombogenicity, biocompatibility and healing process, besides some mechanical properties (adaptability, elasticity, impermeability and possibility of suture), using expanded polytetrafluoroethylene graft as control.
METHODS: Fifteen dogs were divided into three groups of five animals. The microperforated latex graft was implanted in all dogs and the expanded polytetrafluoroethylene graft was implanted in the contralateral pelvic limb. Postoperative follow-up was 4, 8 and 12 weeks. Analysis of results was performed according to clinical evaluation of pulses, complications (fluid collection, dehiscence, granuloma and infection), arteriography, macroscopic analysis and scanning electron micrography.
RESULTS: Statistical tests revealed no significant differences (p > 0.05) concerning post-operative complications and graft patency. Both grafts were properly integrated to surrounding tissues, with connective tissue formed by collagen fibers. A neointimal layer covering all extension of the luminal surface was observed in the microperforated latex graft. Conversely, the endothelial development over the neointimal surface was limited to regions adjacent to the anastomoses in the expanded polytetrafluoroethylene graft.
CONCLUSIONS: The microperforated latex graft showed satisfactory structural qualities (adaptability, elasticity, impermeability and possibility of suture) as a vascular substitute. It stimulated endothelial growth beyond contact regions with the artery in anastomoses and was biocompatible in the dog's arterial system, presenting adequate tissue integration.

Keywords: Vascular graft, latex, polytetrafluoroethylene, endothelium, porosity, femoral artery.




After Mrué1 described the first model of a biosynthetic esophageal graft built from a membrane originated from a polymerized natural latex extracted from rubber trees (Hevea brasiliensis), Freitas2 developed a biocompatible vascular patch made of the same material, implanting it in femoral arteries of dogs. A latex biomembrane has been recently used for the treatment of ulcers of the lower limbs of varied etiology3,4 and in myringoplasties5 in humans.

Grisotto6 used tubular grafts developed from a 'stocking-type' tissue patch covered with natural latex. Four weeks after implantation in femoral arteries of dogs, those grafts had 75% patency, excellent integration to neighboring tissues and young endothelial cells covering the whole internal surface. The outcome concerning this endothelial growth was the reason to maintain the development of this new vascular substitute, increasing postoperative observation time and adding microporosity in its wall, in the sense of bringing it closer to the models used in clinical practice.

Therefore, this study aimed at evaluating patency, thrombogenicity, biocompatibility, healing process stimulated by that material and certain mechanical properties (adaptability, elasticity, impermeability and possibility of suture), using expanded polytetrafluoroethylene graft (ePTFE) as control.



Fifteen adult mongrel dogs (Canis familiaris) were used, with weight ranging between 15 and 20 kg. Surgical planning was based on and performed according to the Ethical Principles of Animal Experimentation of Colégio Brasileiro de Experimentação Animal (Brazilian College of Animal Experimentation - COBEA).7 The research protocol was previously submitted to and approved by the Research Ethics Committee of Faculdade de Medicina de Ribeirão Preto at Universidade de São Paulo (FMRP-USP).

The animals were randomly distributed into three experimental groups of five dogs. Each animal, individually, was its own control, and a new nylon microperforated vascular graft was implanted in one of the pelvic limbs embedded in a compound derived from the natural latex of rubber trees (Hevea brasiliensis) and, in the contralateral pelvic limb, a traditional ePTFE graft was implanted, both with 3.5 cm in length and 0.4 cm in diameter to replace a 3.0-cm segment in the common femoral artery. The only difference between groups was postoperative clinical observation time until arteriography and euthanasia for graft removal (Figure 1).



Description of the technique for graft development

The new graft was developed as a joint work by the Department of Biochemistry and Immunology (Laboratory of Neurochemistry) and the Department of Surgery and Anatomy at FMRP-USP in association with the Group of Photonics at Instituto de Física de São Carlos da Universidade de São Paulo (IFSC-USP). Manufacturing of the microperforated latex and tissue (MLT) graft was performed according to the following sequence:

-wrapping of a glass mold with a tissue patch made of 85% polyamide and 15% elastane;

-immersion of the mold wrapped by the tissue in a Becker containing 500 mL of a compound derivate from natural latex at room temperature of 15-25 ºC, for 20-30 seconds;

-emersion of the mold and heating in a greenhouse at 70 ºC;

-removal of the graft from the glass rod by cooling in running water;

-graft reheating in a greenhouse at 70 ºC, completing the process of latex drying and polymerization;

-new removal from the greenhouse and spontaneous cooling, reaching room temperature (15-25 ºC).

The grafts had their whole extension microperforated. Microperforations had a diameter of 50 µm and spacing between them was 0.44 mm. For that procedure, we used the frequency-doubled Q-Switched Nd:YAG laser (wavelength of 532 nm) focused on the graft, with pulse duration of 70 ps (70 x 10-12 s), exposure time of 150 ms/hole and potency of 200 mW.

Graft implantation

Approach to femoral arteries was performed by longitudinal inguinotomies. The grafts (Figure 2) were anastomosed to the arteries using simple, continuous, 7-0 polypropylene suture with cardiovascular needle 3/8 — 1 cm (Prolene®, Ethicon). The extremity to be anastomosed first was also randomly chosen.



After flow release, hemostasis in the suture line was expected by the animal's blood coagulation or circumstantially, with additional simple hemostatic suture (Figure 3).



During the first postoperative week, the animals were submitted to daily clinical examinations to evaluate graft patency (palpation of pulses) and to detect occurrence of complications at surgical site. After the first 7 postoperative days, clinical examination was performed weekly until euthanasia for graft removal. Recorded complications were fluid collection (hematoma or seroma), suture dehiscence, granuloma and infection. After clinical observation time was over in each group, pulse was qualified as normal, reduced or absent, and complications as present or absent.

At the end of 4, 8 and 12 weeks, the dogs were anesthetized again and submitted to arteriography to evaluate and register graft patency conditions. The following qualitative and quantitative information was analyzed: patency (absence of stenosis or graft occlusion), non-significant stenosis (when stenosis affected less than 70% of the femoral artery diameter), significant stenosis (when stenosis was equal or higher than 70% of the femoral artery diameter) and thrombosis (graft occlusion).

After arteriographies, inguinotomies were performed for graft removal. During the procedures, the following local characteristics determined by presence of implanted material were evaluated: graft incorporation or adherence to neighboring tissues, graft dilatation, formation of anastomotic pseudoaneurysms, fluid collection, fibrosis and/or granuloma.

Next, grafts were removed and femoral arteries were sectioned approximately 1 cm proximally and distally to anastomoses. The tissues were immersed in 10% formol solution at room temperature and sent to microscopic analysis.

Finally, the dogs were submitted to euthanasia using an intravenous injection of 5% sodium thiopental at 50 mg/kg.

Scanning electron microscopy (SEM)

A scanning electron microscope Jeol — JSM 5200 (Japan) and Kodak® 120 mm films (ISO 400) were used to evaluate and register samples of external and internal surfaces of all implanted grafts. Collection points of samples were transitory regions between the artery and the graft (proximal and distal anastomoses) and the middle region of the grafts.

The following parameters were analyzed: formation of fibrous tissue and perigraft vascular neoformation, neointimal hyperplasia in anastomosed areas, migration (infiltration) of collagen tissue and of vascular neoformation through graft porosities, organization of fibrinous layer (neointima) in the luminal surface and endothelial proliferation in the graft flow surface. Each of those items were catalogued as absent or present.

Statistical analysis

Critical level from which differences were considered significant was 5% (p < 0.05). Clinical and arteriographic parameters of each group were analyzed individually and between themselves. For that, we used the software Statistic Package Science Social (SPSS) version 8.0, using the following statistical tests:8,9 (1) median test, for comparisons between groups, relating each variable to a single type of graft (ePTFE x ePTFE or MLT x MLT). In cases in which values did not allow their use (constant values), Kruskal-Wallis test was used; (2) McNemar's test, for comparisons within each group, relating each variable to both types of grafts (ePTFE x MLT).

Analyses of macroscopy and scanning electron microscopy results were performed descriptively.



Global analysis showed rate of infection with dehiscence of 3.3% (1/30 inguinotomies). Non-infectious complications (formation of granuloma and seroma) were 6.6% (2/30 inguinotomies), representing 10% of general complication rate (3/30 inguinotomies), which is acceptable due to difficulties in antiseptic cares for these animals when maintained free in kennels.

When complications for each type of graft were individually analyzed, they were 13.3% for MLT graft (2/15 implants), which presented one inguinotomy with infection and dehiscence (6.6%) and another with granuloma and seroma (6.6%). The ePTFE graft had low complication rate (6.6%, 1/15 implants), due to development of granuloma with seroma in one inguinotomy.

There was loss of femoral pulse (graft thrombosis) in 13 pelvic limbs, with impairment of nine MLT grafts and four ePTFE grafts (Figure 4).



In clinical evaluations, no dogs showed reduced pulse, and only one was normal or absent. The animals that presented absence of pulse (graft thrombosis) initially evolved with reduction in temperature of the ipsilateral pelvic limb and some difficulty in walking. However, 10 to 15 days after the surgery, the animals recovered normal limb temperature and walking ability, independent of type of graft, maintaining absence of pulse.

General analysis of all 30 arteriographies showed patency in 17 grafts (11 ePTFE and 6 MLT grafts), and two ePTFE grafts presented images with non-significant stenoses (20 and 30%). There was occurrence of thrombosis in 13 grafts (four ePTFE and nine MLT grafts) (Figure 5).



Statistical tests did not show significant changes (p > 0.05) concerning postoperative complications, presence of pulse and results of arteriographies when compared with both types of grafts in each group of dogs (ePTFE x MLT). Similarly, there were no significant differences when each graft model was compared between the three groups of animals (ePTFE x ePTFE or MLT x MLT).

MLT graft showed adequate elasticity, adaptability and easy handling, especially when suturing it with the receiving artery. The needle penetrated easily in the graft wall, which molded well to the arterial stroma.

During the procedure of surgical dissection for graft removal, there was a tissue of bright and transparent incorporation completely covering both graft models. Such tissue, around MLT grafts, showed a more delicate consistency. On the contrary, ePTFE grafts presented a thicker incorporation tissue, with a more marked fibrous reaction.

Another macroscopic characteristic in common, verified in those 27 grafts (13 MLT and 14 ePTFE) that did not have clinical complications, was presence of a thick, rugged and bright external covering, completely involving the grafts in anastomosed regions and extending to the adventitia of both arterial extremities (Figure 6).



As to internal covering tissue growth, it completely expanded through the whole luminal surface of ePTFE and MLT grafts in all groups of dogs, i.e., in both types of grafts the internal covering tissue was uninterrupted with the intima of both arterial extremities. However, when comparing both types of grafts, it was also possible to notice that the internal covering tissue of MLT graft presented a more consistent (thicker) development than the ePTFE graft in all groups of animals (Figure 7).



Scanning electron microscopic analysis of external and internal surface coverings of ePTFE and MLT grafts also demonstrated identical results in the three groups of animals. In both grafts, there was growth of a supporting connective tissue (neoadventitia), composed of collagen fibers similar to those found in the artery adventitia. It is worth stressing that the same characteristics seen in neoadventitias of grafts 4 weeks after the surgery remained unaltered at 8 and 12 weeks (Figure 8).



Four weeks after the surgery, it was possible to note the formation of fibrin connective tissue entirely covering luminal surfaces of both types of grafts. This tissue was uninterrupted with the artery intima in both anastomoses, which characterizes a neointimal development in both grafts. In the ePTFE graft, there was continuity of the transmural fibrin connective tissue with the internal surface neointima. Similarly, in the MLT graft, the neointima went deep inside the cavities formed by the laser in the luminal surface. There were no differences between the neointima formed by proximal anastomosis with that originated from distal anastomosis. The same characteristics observed in graft neointimas 4 weeks after the surgery remained unaltered after 8 and 12 weeks.

Specifically concerning endothelial development, there were differences between ePTFE and MLT grafts. There was presence of young endothelial cells in both grafts 4 weeks after the surgery. However, in the ePTFE graft, that growth was restricted to regions close to anastomoses, without progression to the central region of this graft, which remained covered only by the neointimal tissue. On the other hand, the endothelium developed itself through the whole neointima in the MLT graft, also occupying the middle region of this graft, but at a lower proportion, which presupposes centripetal growth from anastomoses. Endothelial covering of both grafts completely covered the suture areas (arterial-graft transition) and was continuous with the endothelium of adjacent arterial extremities. The endothelium formed by grafts was similar to a typical arterial endothelium.

Endothelial covering in the middle region of the MLT graft had better development of endothelial cells, almost identical to the anastomosed regions, 4 and 12 weeks after the surgery. There was no endothelial development in the middle region of the ePTFE graft. There were no differences in endothelium characteristics in the extremities of proximal and distal anastomoses in the three groups (Figure 9).



Although arterial or venous autogenous grafts are close to the ideal vascular substitute and provide the best results in vascular reconstructions, it is evident that they are not always available nor are adequate, often because they have already been used or due to complication risks associated with vein stripping. For that and many other reasons, a synthetic substitute is required, which supports the interest in researching this field of vascular surgery.10,11

Selection of patients and indication for surgery are important to determine long-term clinical success of revascularizations using grafts and may explain some of the variations found in results described in the literature. Since many grafts are initially tested in several experimental animal models, it should be considered that there is a large interspecies variation concerning response to implanted vascular graft. These models aim at examining the blood-graft interaction in terms of effect of the material on platelet function, blood coagulation, fibrinolysis and cell infiltration, besides many other biological and mechanical characteristics.

In general, healing of vascular substitutes has been primarily studied in three species: pigs, dogs and humans.12 Some authors describe that graft behavior in dogs is the most similar to that in humans, which explain its preference as favorite animal model to evaluate vascular grafts,13-15 an opinion that is corroborated by Sauvage,16 who believes that human healing is never better than that observed in dogs. Therefore, a graft that presents poor healing in those animals will not have better results in human beings.

However, such opinion is not consensual in the literature, and the porcine model is pointed as the closest to the human model concerning characteristics of the cardiovascular system and to analyze healing, coagulation, fibrinolysis and platelets.17 Nevertheless, there might be complete neoendothelization of the graft flow surface in pigs, different from what occurs in humans and in dogs.15,18 These discrepancies should be considered when reviewing and comparing published results.

Therefore, in this study we selected the canine model because its healing characteristics (as to endothelization process of the graft internal surface) are similar to those seen in humans. In those two species, graft healing beyond a limited area adjacent to anastomoses is much less complete, being restricted to proliferation of vascularized fibrous tissue inside the interstices until about half the thickness of its wall, in most cases with low expected progression after that.16

Wu et al.,19 in a study of vascular graft implants in different anatomical regions of the same dog, define the period of 8 weeks as ideal to evaluate arterial grafts, since their findings over that period of time were comparable to those found 3 years after implantation in the same experiment.

In our study, there were three different periods in observation time: 4, 8 and 12 weeks. By using those intervals, it was possible to properly and sequentially evaluate maintenance of patency and graft healing characteristics (encapsulation reaction, endothelization and neointimal hyperplasia).

Clinical results ratify the previously described biocompatibility of the natural latex compound used to develop the MLT graft.1-3,5,6,20-25

The MLT graft also has the characteristic of biomaterial, i.e., it is a synthetic material used to replace part of a living system or to function in close contact with a living tissue.

The combination between polyamide and elastane tissue and the compound originated from natural latex was adequate to the development of a tubular graft, proving to be physically resistant until the 12th week of observation, since there was no case of dimensional instability (dilatation).

Since the early stages of textile synthetic graft development, porosity has been considered as an important characteristic for the success of a vascular substitute, besides being considered essential for functionality of small-caliber synthetic vascular grafts. Theoretically, porosity is required for fluid and ion transference through graft matrix. In addition, porous material provides a frame or structure for internal growth of perivascular tissues.12 The results observed in ePTFE and MLT grafts in this study corroborate that concept.

Both grafts show presence of fibrin connective tissue and blood-borne elements through their microporosities. Better development of fibrin network in ePTFE may be due to the characteristics of microporosity of this material, which only has nodes interconnected by thin fibrils, opposed to the MLT graft, in which there is presence of holes with varied contours and sizes (diameters of 54-441 µm), irregularly distributed. Such holes are probably the openings of microtunnels formed in the body of the graft wall when passing (transfixation) through the laser beam (Figure 10).



The synthetic vascular grafts that presented the best clinical results are composed of a porous supporting structure and a material used to close frame interstices, in case it is sufficiently wide to allow blood release. Supporting structure is classified as microporous if the interstices are so small that heparinized blood viscosity and superficial tension avoid hemorrhage, or as macroporous if these factors cannot avoid blood loss. A microporous structure does not require any additional material to close its microscopic interstices and can be used without precoagulation, including in heparinized patients. ePTFE is an example of this type of structure. Although it has about 85% open space in its frame, it is impermeable to blood, probably due to a more significant length of its interstitial channels (around 800 µm) compared with its small caliber of around 15-30µm.16

Despite not being clearly demonstrated by scanning electron microscopy, the technique used to microperforate the MLT graft was efficient in producing microporosity in its wall. This property was empirically confirmed by a water leakage test and by observing mild bleeding ('transudation') after blood flow release during surgeries for graft implantation.

Transmural growth of the healing tissue was continuous in the ePTFE graft. In the MLT graft, such continuity was impaired by irregularity of microtunnels and possibly by the presence of tissue monofilaments inside the holes, even if this may represent a supporting structure to organize the fibrin network. There were no differences in neoadventitias formed in both types of grafts, which were continuous with the arterial adventitia, adequately integrating to perivascular tissues.

There was endothelial growth in both grafts 4 weeks after the surgery. In the ePTFE graft such growth was restricted to perianastomotic areas, being absent in the graft central area, which remained internally covered only by neointimal tissue. Such characteristic remained in all groups 8 and 12 weeks after the surgery, corroborating previously described results in the literature using this type of vascular substitute.26,27

On the contrary, in the MLT graft there was growth of an endothelial covering through the whole neointima, including in the middle region of this graft. Because higher development of the endothelial layer is closer to anastomoses, it can be assumed that progression of these cells has a centripetal character. Endothelial covering entirely involved suture areas (arterial-graft transition) and was continuous and similar to the endothelium of adjacent arterial extremities.

In the animals of groups with 8 and 12 weeks after the surgery, the endothelial layer of the MLT graft central area had better development, similar to that observed in anastomoses.

These results are very significant because, similar to what occurs in humans, endothelial development in dogs usually remains in perianastomotic areas, as demonstrated in the ePTFE. There has been no description of a material able to stimulate endothelial growth through its whole extension in this implantation anatomical region.18,26,28-30

Results concerning endothelial growth in the MLT graft are of great importance due to the peculiar characteristics of its development in synthetic vascular grafts in humans (similar to dogs). So far, any vascular substitute has been entirely covered by endothelium in these two genders of animals. For that reason, development of this graft open a great perspective, using a material that can finally stimulate endothelial growth much beyond the proximities of arterial grafts.



The MLT graft showed mechanical properties (adaptability, elasticity, impermeability and possibility of suture) favoring its use as vascular substitute. As to biological properties, it proved to be biocompatible in the dog's arterial system, presenting adequate tissue integration and endothelial growth beyond regions in contact with the artery in anastomoses, and neointima was entirely covered by endothelium.



To Professor Dr. Sérgio Carlos Zílio and to Dr. Lino Misoguti, at Group of Photonics of Instituto de Física de São Carlos at Universidade de São Paulo (IFSC — USP), for performing laser perforations in latex vascular grafts; to Silvia Helena Epifânio, for her invaluable help in surgeries and graft development; to João Sérgio Epifânio, for caring the animals, and to the employees at Laboratory of Surgical Technique and Experimental Surgery and Electronic Microscopy at FMRP-USP.



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Carlos Eli Piccinato
Depto. de Cirurgia e Anatomia da Faculdade de Medicina de Ribeirão Preto
Av. Bandeirantes, 3.900
CEP 14049-900 — Ribeirão Preto, SP, Brazil
Tel.:(16) 3602.2407
Fax:(16) 3633.0836

Partial financial support: CAPES and CNPq.
Manuscript received January 18, 2007, accepted April 5, 2007.



This study was carried out at Laboratory of Surgical Technique and Experimental Surgery, Department of Surgery and Anatomy, FMRP-USP, Ribeirão Preto, SP, Brazil.

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