© Borgis - Postępy Nauk Medycznych s1/2011, s. 23-28
Paweł Lampe, Beata Jabłońska*
Krótka historia sztucznego przełyku
A brief history of the artificial oesophagus
Katedra i Klinika Chirurgii Przewodu Pokarmowego SUM w Katowicach
Kierownik: prof. dr hab. med. Paweł Lampe
Pomimo postępów w diagnostyce rak przełyku jest często rozpoznawany w późnym stadium. Ze względu na zaawansowane stadium, w którym zazwyczaj się znajduje, leczenie raka przełyku jest tylko paliatywne u ponad 70% pacjentów. Chorzy po resekcji przełyku wymagają rekonstrukcji. Zabiegi chirurgiczne składające się z przeniesienia lub wszczepienia nieuszypułowanego odcinka przewodu pokarmowego są bardzo inwazyjne. W piśmiennictwie istnieje wiele doniesień na temat ulepszeń sztucznego przełyku przy użyciu różnych materiałów biologicznych i syntetycznych. Celem niniejszej pracy było przedstawienie krótkiej historii sztucznego przełyku powołując się na najważniejsze publikacje na ten temat.
Despite the progress in diagnostics procedures, oesophageal cancer is often diagnosed in its late stages. Because of the advanced stage at which it usually presents, treatment of carcinoma of the oesophagus is just palliative in over 70% of patients The surgical treatment of the esophageal cancer is associated in the esophagectomy. Patients following esophagectomy require the esophageal reconstruction. Procedures consisting of translocation or implantation of a pedunculated segment of the alimentary canal are extremely invasive. There are numerous reports regarding improvements of the artificial esophageal using different synthetic and biological materials in the literature. The aim of this paper was to present a short history of the artificial esophagus by citing the most important publications on this topic.
Despite the progress in diagnostics procedures, oesophageal cancer is often diagnosed in its late stages. The disease is characterized by a malignant course: early infiltration of the muscular coat, and metastases to the regional lymph nodes. Because of the advanced stage at which it usually presents, treatment of carcinoma of the oesophagus is just palliative in over 70% of patients (1-4).
Nutritional gastric and enteral fistulas and oesophageal tubes have multiple disadvantages. Different sophisticated methods, i.e. cutting through the neoplasm using laser followed by irradiation and chemotherapy, cause discomfort to the patient, and do not seem to improve the quality of survival (5-7).
However, palliative procedures consisting of translocation or implantation of a pedunculated segment of the alimentary canal are extremely invasive. Besides, the intended purpose, which is enabling the patient to eat naturally and to prevent the bronchial tree from being flooded with saliva and food, is not always achieved. In the 1940s, numerous studies were carried out in order to develop alloplastic oesophageal prostheses. The tubes were easily available and convenient to use for a surgeon. The duration of the operatio was cut down, and intra- and perioperative mortality rates lowered. However, despite numerous improvements of the tube structure over the years as well as various materials and methods of anastomosing the prosthesis to the oesophagus being used, fusion between the tissues and the implant was not achieved. The attempts to use biological, usually cell-rich, implants were unsuccessful.
Non-preserved connective tissue fibrous membranes were later considered as potential material for the development of an oesophageal prosthesis. The results of those investigations were not encouranging, and thus the prostheses were not widely used.
In search of an effective palliation, which would additionally maximize the quality of survival experimental and clinical studies were launched aimed at the development of an artificial oesophageal prosthesis. In 1922, Neuhoff and Ziegler (8) used rubber tubes as experimental oesophageal prostheses in dogs. In 1947, Grindlay (9) suggested that polyethylene tubes could be used as bilairy, tracheal and colonic prostheses. In 1952, Berman (10) selected metacrylic and polyethylene tubes. Out of 20 dogs operated on with the use of the above mentioned tubes. 6 died for various reasons. However, the condition of the surviving 14 dogs was satisfactory. In the same year, Berman reported his results on 28 operations in humans. He used polyethylene tubes for thr formation of an artificial oesophagus. In 1954, Berman (11) operated on 60 patients using the same prosthetic material; mortality rate was below 10%. According to Berman, the success of the procedure might be accounted for by the elimination of the trauma resulting from the mobilized stomach being advanced upwards.
In 1952, Ruffo (12) published the results of his investigations concerning the use of plastic tubes as oesophageal prostheses. However, out of 15 dogs that were operated on, 11 died (74%) in the perioperative period. Chalnot at al. (13) replaced the thoracic segment of the oesophagus in 16 dogs. Having excised a 2-4 cm segment of the thoracic oesophagus, they implanted much longer polyvinyl tubes; the results were encouraging.
In 1953, Roth et al. (14) used metacrylic and PVC tubes as the prostheses of the thoracic oesophagus in 5 dogs, and cervical oesophagus in 15 dogs. Following the procedures they found prosthesis displacement, stomach wall perforation by a PVC prosthesis, and anastomotic leakage. Similar observations were made by Razemon at al. (15).
Shackelford and Sparkuhl (16) reported on a patient who survived 183 day with a plastic prosthesis following a plalliative surgical treatment fo oesopahgeal cancer. In 1954, More et al (17) published the results of their studies which had carried out on 36 rabbits since 1949. Like Berman, they used plastic prostheses; the results, however, were unsatisfactory. The rabbits were dying, most frequently, of suppurative inflammation within the thoracic cavity.
Although, in 1954, Battersby and King (18) submitted a paper describing advantageous features of the prosthetic tube proposed by Berman, they als pointed out some of its shortcoming, i.e. the standard size and the fact that the prosthesis could not be anastomosed to the oesophagus using standard suture technique. They developed a multi-layer prosthesis which consisted of polyethylene sheeting and nylon mesh fused together in an autoclave. The prosthesis was anastomosed to the oesophagus; various anastomoses were used for the purpose. Out of 22 dogs which were operated on using this method, 14 died. During endoscopic procedures performed 3-4 months following the operation, Battersby and King found that the prosthesis and tissues were separated. The high risk was, however, attributed to the oesophageal surgery rather to the above mentioned technique of prosthesis implantation.
In 1956, Maynard et al. (19) reported on the use of a plastic tube as and endoprosthesis for palliative treatment of oesophageal cancer, and for the replacement of an oesophageal segment in a group consisting of 5 patients (Group I) and 9 patients (group II) respectively. The endoprosthesis functioned satisfactorily in 4 patients from Group I. In 8 patients from Group II, the results were poor p the prosthesis and the oesophagel tissues did not fuse together.
In 1956, Ebner (20) described the use of Berman’s prosthesis for palliative treatment of cancer of the oesophagu.
In 1963, bearing in mind that organ pullup was too risky in the case of patients presenting with cancer cachexia, Fryfogle et al. (2) used an alloplastic oesophageal prosthesis. The prosthesis was made of rubber with silicone lining. The outer surface was covered with Dacron. In order for anastomosis not to cause ischaemia of the margins of the oesophasus, the authors suggested a complex technique. The function of the prosthesis and possible methods of anastomosing the tube to the oesophagus were first studied in experiments on dogs; afterwards the prosthesis was used in1 patient with a good result. After 6 weeks, however, the patient started complaining of dry hacking cough, most probably caused by tracheal compression by the prosthesis.
In 1968, La Guerre et al. (21) used tubed made of new material, hydron (Hadron Laboratories New Brunswick, N.J.), in a teflon or Dacron cuff, as oesophageal prostheses in 24 dogs. In the first 7 dogs died due to leakage from the upper anastomosis; two others died after about 3 weeks. The survival period of the remaining 13 dogs ranged between 1.5 and 9 months. The authors warned surgeons not to divide the vagus nerve while excising oesophageal segments. Three dogs, in which the nerve was damaged during the operative procedure, developed considerable weight loss. One dog vomited the prosthesis, and very soon stricture developed within the prosthesis canal. Microscopic examination did not reveal any ingrowth of the oesophageal wall tissuses into the prosthesis. Epithelial growth was not found either.
Stuart (22, 23) reported on 5 patients with a plastic tube as a prosthesis of a rubber segment of the oesophagus. He considered the immediate result satisfactory, and the method accepatable for palliative treatment of cancer of the oesophagus.
In 1973, Goldsmith et al. (24) described a marlex mesh prosthesis. The mesh pores were sealed up with collodion, and the whole prosthesis wrapped up in pedunculated omentum. Out od 12 dogs, 7 survived for a long period of time. The remaining 5 died of complications.
Parallel to the trials with synthetic material, were the attempts to use auto-, allo-, and xenografts for oesophageal repair procedures. Allografts were used by Skinner (25) in an experiment on 20 dogs. Nine dogs died in the early postoperative period; 11 animals which survived the first week developed strictures. In 1952, in an experiment on dogs, Fiacavento (26) transplanted oesophageal prostheses which had been first preserved in Gross solution containing penicillin. The transplants were wrapped up in the pleura. Despite numerous early complications, the long-term results were encouraging – he observed slight strictures, oesophageal strump approximation, and epithelial growth in the prosthesis canal. In 1952, allografts, fresh and formalin-preserved, were transplanted by Ruffo (27), who observed marked shortening and stricture of the transplants in dogs. Lyophilized allografts were transplanted in 1953 by Pate and Sawyer (28), who found progressive graft atrophy due to retrograde changes. The results were confirmed in 1958 by Pataky, Molnari and Jakab (29), who found cicatrical strictures within lyophilized oesophageal segments which they had transplanted.
Then, the attention of researchers was frawn to the tube-shaped blood vessels and the trachea. Some of them believed that these structures could be used as oesophageal prostheses. In 1956, Giudice and Tawano (30) published the results of their experiment on 6 dogs, in which a short oesophageal segment was excised and replaced with autogenic trachea. In 1958, Galente et al. (31) noted poor results after the transplantation of allogenic trachea. Allogenic aorta, fresh and preserved, was used by Kuntz in 1952. His experiments on dogs were unsuccessful. He found strictures resulting in cachexia.
In 1953, Roux et al. (32) published the results of their experiments with homo- and heterografts prepared of blood vessels as oesophageal peostheses in dogs and goats. They used fresh and Hanks solution-preserved segments of the aorta and vena cava inferior. In the first part of the experiment, they evaluated aortic grafts; a segment of goat aorta was implanted to the intestine. The next part of the experiment was designed to assess the usefulness of the aorta to replace the cervical oesophagus. Aortic segments were preserved in Hank solution for between 1 and 59 days. Out of 10 goats with aortic interposition in the intestine, 2 died after the operation, 4 developed ileus, and 4 were sacrificed for the purpose of evaluation. In 3 of the latter, the results were poor. In the following part of the experiment, allogenic canine aorta and bovine vena cava inferior were used as oesophageal prostheses in dogs. The latter was preserved in Hank solution or in the serum with the addition of 20% alcohol. The results obtained revealed decrease dimensions of the prostheses shortening. According to the authors, stricture development begins early and is the stabilized.
In 1960, Sadlinski (33) assessed the value of heterogeneous aortic lyophilized grafts for plastic operations on canine oesophagus. Segment of bovine aorta were used for the replacement of the resected thoracic oesophagus. The results, however, were not satisfactory. Like other authors, Sadlinski emphasized the difficulties of oesophageal replacement in dogs – as in all animals, the prostheses ran horizontally and numerous problems were faced concerning the maintenance of postoperative diet.
In 1957, Smith and Raison (34) used formalin-preserved aorta as oesopgageal prosthesis in 5 patients. They empghasised the simplicity and short duratiosn of the procedure.
In 1958, Rogers et al. (35) presented an allogenic aortic prosthesis for carcinoma of the middle part of the oesophagus. However, the effects of the operation were dramatically diminished by an infiltration, which developed over the site of implantation.
In 1981, Fredrikson et al. (36) compared the results in a grous of patients with gastric advancement to the neck with those in patients in whom the alimentary canal was reconstructed with rhe use of a cutaneous-muscular flap. Mean hospital stay the former operation amounted to 12 days, and after the latter to 90 days.
In 1951, Klopp (37) used cutaneous flaps and a polyethylene film prosthesis. Complication rate in animals with cutaneous flaps used in addition to the polyethylene prosthesis was significantly lower.
Also in 1951, Edgerton (38) suggested the use of free cutaneous grafts spread on tantalum gauze for the repair of defects within the cervical oesophagus and the trachea. The immediate effects of the opereation were satisfactory in 4 patients.
In 1955, Dumm et al. (39) used the skin to wrap up a plastic prosthesis in one of the 4 patients he operated on (in 2 other patients the prosthesis was wrapped up in pleural flaps, and in 1 in fascia); the patient was able to swallow food normally for 9 months. In the same year, Foster and Campo (40) used free cutaneous flaps as oesophageal prostheses. For three weeks plastic tubes as shields for the prostheses, and were removed. However, a check-up disclosed plastic tube occlusion. Later, They used the method to bypass thoracic oesophagus infiltrations.
In 1956, Corner et al. (41) used autogeneous cutaneous flaps for oesophageal replacement in 14 dogs. Prosthesis shortening was observed; the circumference, however, remained unchanged. No fistulas were found; in one dog the oesophagus was punctrured by a foreign body. Epithelial ingrowth was observed inside the graft. In 5 dogs graft-internal plastic prosthesis was additionally applied, however, did not prevent stricture development. In 1956, Cenna (42) used free cutaneous flaps with similar results.
In 1963, Kaplan and Markowicz (43) used penile skin as clinical oesophageal prosthesis. The penis was then covered with thigh autogenic transplant.
Early on in the history the attention of surgeons was drawn to the fascia. In 1917, Neuhoff (44) used the fascia fo the repair of the oesophageal defects. In 1949, Rob and Bateman (45) used tantalum-gauze-lined broad fascia as an oesophageal prosthesis in 3 patients and for the repair of a tracheal defect in 1 patient. Postoperative condition of the patients was satisfactory. Later on, however, separation of necrotic fascia and tantalum mesh was observed.
In 1951, Baronofsky (46) used tantalum mesh lined and covered with autogenic broad fascia to repair defects after pharyngectomy and upper oesophagectomy. One month following the procedure, the mesh was excreted with faeces. The patient died after a few montsh due to cancer progress.
In 1955, Dumm et al. (39) used polyethylene prostheses wrapped up in autogenic broad fascia. The prostheses were implanted in 18 dogs. Perioperative mortality rate was 50%. Out of 9 dogs which died, 7 had developed fascia necrosis and anastomotis fistulas. In the group of surviving animals, malnutrition was found in 6 and mechanical occlusion in 4 dogs. On postoperative day 75, one dog vomited the prosthesis, and was sacrificed 32 days later. Autopsy revealed oesophageal stricture; fascia degeneration was attributed to the harmful effects of substances present in the alimentary tracy.
In 1956, Henry eta al. (47) attempted to form an intrathoracic oesophageal prosthesis using pleural and pericardium flaps. The former were implanted in 16, and the latter in 30 dogs. Survival rates were 62.5% and 63.4%, respectively.
In 1983, Kawamura et al. (48) developer and used (In dog experiments) collage-silicone polimer prostheses, chich were implanted into the intestine and thoracic oesophagus. Despite anastomostic leaks and strictures, their results seem to encourage further attemps.
In 1989, Lampe (49) described the results of his experiments with a biostatic oesophageal prosthesis of preserved bovine fascia. Following trypsin digestion, the outside of the prosthesis was preserved with ethyl alcohol, and the inside with glutaraldehyde. The prosthesis was the kept at temperature of 91 C about 180 days. It was used I 17 dogs for the replacement of the thoracic oesophagus with good results.
In 1998, Takimoto et al described artificial esophagus which was a two-layered tube consisting of a collagen sponge matrix and an inner silicone stent. Authors used it to replace 5 cm esophageal segmental defects in 43 dogs, and the inner silicone stent was removed endoscopically at weekly intervals from 2 to 4 weeks. In the 27 dogs from which the silicone stent was removed at 2 or 3 weeks, constriction of the regenerated esophagus progressed and the dogs became unable to swallow within 6 months. In the 16 dogs from which the silicone stent was removed at 4 weeks, highly regenerated esophageal tissue successfully replaced the defect, leaving no foreign body in the host. The regenerated esophagi had stratified flattened epithelia, striated muscle tissue composed of an inner circular and an outer longitudinal muscle layer, and esophageal glands (50).
In 1999, Yamamoto et al reported replacement of the intrathoracic esophagus with an artificial esophagus composed of a collagen sponge with a double-layered silicone tube and examined the state of host tissue regeneration. A 5-cm long gap was created in the intrathoracic esophagus in 9 dogs and repaired by interposition of their prosthesis. The dogs were fed only by intravenous hyperalimentation for 28 days. The silicone tube was removed at 29 days after the operation, and oral feeding was reintroduced. One dog was put to death at each of the following times: 1, 2, 3, 3, 6, 12, and 24 months after the operation. One dog was surviving without problems after more than 26 months. One dog died of malnutrition at 10 months. In all dogs, the host regenerated tissue had replaced the resulting gap at the time of silicone tube removal. The mucosa had fully regenerated within 3 months and the glands within 12 months. The process of stenosis and shrinkage was complete within 3 months and did not advance thereafter (51).
In 2003, Qin et al designed an oesophageal prosthesis made of composite materials. The inner stent were made with polyurethane of medical grade, and the outer surface of the prosthesis was coated with collagen-chitosan sponge. The silicone tube was used as a control. Authors reported that the esophageal prosthesis made of composite biomaterials had high biocompatibility and potential for long-segment esophageal reconstruction (52).
In 2005, Watanabe et al described an artificial esophagus simulating peristaltic movement with the use of a nickel-titanium shape memory alloy (NiTi-SMA) actuator. On the experimental animal model, they noted that the contraction of the artificial esophagus was similar to the esophageal peristaltic movement observed by x-ray examination in humans (53).
In 2006, Marzaro et al proposed an artificial esophagus composed of homologous esophageal acellular matrix and autologous smooth muscle cells (SMCs). Authors suggested to use the study results for the repair of esophageal injuries (54).
In 2006, Liang et al described replacement of a segment thoracic esophagus by using a nitinol alloy composite artificial esophagus on the pig model. A nitinol alloy composite artificial esophagus was made of a nitinol tube coated with a silicone membrane with a dacron flange 1 cm proximal to each end. All ten pigs had no leakage at the site of anastomosis and survived over 6 months. The longest survival was 20 months. The study results were satisfactory (55). In 2009, they noted improvement of their results by using of polyester connecting ring in the nitinol composite artificial esophagus. They noted the significant lower incidence of postoperative complications (anastomostic leakage and stenosis) and the increased long-term survival rate in the new type of oesophageal type with polyester connecting ring (56).
In 2008, Juhasz et al described esophageal replacement using cryopreserved tracheal graft on 12 dogs. Results revealed that the cryopreserved trachea could be suitable for the replacement of a 5-6-cm-long esophageal segment (57).
Until now, the artificial oesophagus is not applied in routine treatment of patients with esophageal cancer. It is still in the experimental phase. The aim of all studies is to develop an ideal model of an artificial prosthesis, which could in the best way to replace a natural organ without posing danger to the patient.
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