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Characteristics of Corneal Xenograft Rejection in a Discordant Species Combination

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Characteristics of Corneal Xenograft Rejection in a Discordant Species Combination Characteristics of Corneal Xenograft Rejection in a Discordant Species Combination Joel R. Ross, David N. Howell, and Fred P. Sanfilippo Purpose. To characterize the fate of Lewis rat corneas transplanted to Hartley guinea pigs. Methods. Full-thickness Lewis rat corneal buttons were grafted orthotopically to Hartley guinea pigs (xenografts), ACI rats (allografts), or Lewis rats (isografts). Two panels of recipi- ents were presensitized with xenogeneic skin grafts or allogeneic skin grafts. Serum samples were collected pre- and post-transplant and analyzed by flow cytometry and indirect immuno- fluorescence. Results. Unlike vascularized xenografts that reject within 30 min, corneal xenografts had a mean survival time of 8 days. Presensitization with guinea pig skin grafts increased recipient IgM and IgG xenoantibody levels, as measured by flow cytometry on guinea pig hematopoietic cells, and significantly accelerated corneal xenograft rejection with a mean survival time of 5 days. Presensitization with allogeneic ACI skin grafts had no effect on xenoantibody levels or xenogeneic corneal graft survival. Guinea pig corneas stained by indirect immunofluorescence with normal rat serum exhibited low (1+) but significant binding of IgG and IgM, primarily on epithelium and stroma. Serum from Lewis rats that rejected a corneal xenograft had elevated IgG and IgM xenoantibodies that reacted strongly (4+) with guinea pig cornea and heart. Conclusions. In the discordant guinea pig-to-rat species combination, donor corneas express xenoantigens; rejection of corneal xenografts stimulates IgM and IgG xenoantibody produc- tion; sensitization to xenoantigens can accelerate corneal xenograft rejection; and discordant corneal xenografts, unlike vascularized organs, are not hyperacutely rejected. Invest Ophthal- mol Vis Sci. 1993:34:2469-2476. 1 he shortage of human organs has led to a renewed ents (limited in number) are considered unlikely interest in the possibility of using xenogeneic tissues candidates as donors of xenogeneic tissues for a vari- for transplantation. Potential xenogeneic donors can ety of practical and ethical reasons.3"6 The possibility be subdivided into "discordant" donors, against of using discordant tissue sources for xenotransplan- whose tissues the recipient possesses preformed xe- tation is, then, of considerable importance. noreactive natural antibodies (NAb), and "concor- The major obstacle to transplantation of vascular- dant" donors, against whose tissues such NAb are ab- ized xenogeneic organs in discordant species combina- sent.12 Primate species concordant with human recipi- tions is hyperacute rejection. This rapid form of rejec- tion, which typically occurs within minutes to a few hours of transplantation, is generally thought to be From the Departments of Pathology, Immunology, ami Surgery, Duke University and VA Medical Centers, Durham, North Carolina. mediated by NAb via activation of the classical com- Submitted for publication July 22, 1992; accepted December 21, 1992. plement (C) pathway, though direct activation of the Proprietary interest categoiy: N. Reprint requests: Fred Sanfilippo, M.D., Ph.D., Johns Hopkins Medical alternative C pathway appears to play a role in some Institutions, Department of Pathology, 600 N. Wolfe Street, Baltimore, MD 21205. species combinations.12'78 Because orthotopic cor- lnvestigative Ophthalmology & Visual Science, July 1993, Vol. 34, No. 8 Copyright © Association for Research in Vision and Ophthalmology 2469 Downloaded from iovs.arvojournals.org on 09/25/2021 2470 Investigative Ophthalmology & Visual Science, July 1993, Vol. 34, No. 8 neal transplants are placed in an avascular graft site, nized by corneal xenografts has elevated levels of IgM the role of these humoral rejection mechanisms may and IgG xenoantibody. be considerably diminished. Therefore, the transplan- tation of xenogeneic corneas may prove to be more successful than that of vascularized organs. METHODS Worldwide, the shortage of donor corneas has Animals been estimated to be as high as 10 million. The lack of corneas stems from many factors, including religious All animals involved in this study were cared for and or ethnic beliefs, lack of adequate eye banking facili- used in accordance with the ARVO Resolution on Use 1 ties, and poor quality of locally donated corneas. In of Animals in Research. Male Lewis (RT1 ) rats and the U.S., the need for corneas is not as acute, but Hartley guinea pigs were obtained from Charles availability varies from region to region. Potentially, as Rivers Laboratories (Wilmington, MA). ACI (RTla) with other tissues and organs, the use of xenogeneic rats were bred at the VA Medical Center Animal Re- donors may be a way to alleviate the shortage of donor source Facility. corneas. Many early studies of corneal xenografts exam- Orthotopic Corneal Transplantation ined the survival of heterotopic9 or intralamellar Full-thickness, 3.5-mm penetrating corneal grafts grafts,10"12 which have only limited clinical use and are were performed as previously described.23 Briefly, ani- not subjected to the same exposure to the host im- mals were anesthetized by intramuscular injection of mune system as are full-thickness grafts. Only a few with a combination of 100 mg/kg of a 100 mg/ml so- investigators have used a penetrating keratoplasty lution of ketamine (Parke-Davis, Morris Plains, NJ) technique to perform xenografts (Table 1). 13-21 Of and 2 mg/kg of a 100 mg/ml solution of xylazine (Mo- these, none have used animal species associated with bay, Shawnee, KS). Topical anesthesia, proparacaine well-established models of xenotransplantation. Con- (Alcon, Ft. Worth, TX) was applied to the eye. A sub- cordant models of corneal xenotransplantation have conjunctival injection of 0.05 ml of a solution contain- yielded promising results18"21 but, as mentioned, are ing 1 mg/ml atropine (Elkins-Sinn, Cherry Hill, NJ) of little practical usefulness for human corneal trans- and 1:1000 epinephrine (Parke-Davis) was used to di- plantation. late the iris. A 3.5-mm trephine was used to score the We have examined the survival of guinea pig cor- donor cornea, and the donor graft was removed using neas transplanted to Lewis rat recipients. This discor- curved corneal scissors. The recipient cornea was simi- dant species combination has been widely used to ex- larly scored with a 3.0-mm trephine, and the central amine the hyperacute rejection of vascularized xeno- 3-mm area was removed. The donor graft was then geneic transplants.1'28-22 Our findings indicate that, in sewn in place using 12 interrupted sutures of 11-0 contrast to cardiac xenografts, which fail in 17 ± 4 nylon (Alcon). The anterior chambers of recipients min,22 guinea pig corneal xenografts are not hyper- were re-formed with sodium hyaluronate (Healon, acutely rejected in Lewis rats, and that rejection is sig- Pharmacia, Piscataway, NJ). Six sutures were removed nificantly accelerated when the recipients are presen- on postgraft day 5 and the remaining six on postgraft sitized with xenogenic (but not allogeneic) skin grafts. day 8. Topical antibiotic, tobramycin (Alcon), was ap- Antibody labeling studies demonstrate that normal rat plied immediately after surgery and on postoperative serum contains NAb that binds to antigens expressed days 4 and 7. No immunosuppressant agents were ad- on guinea pig cornea and that serum from rats immu- ministered at any time during the study. TABLE l. Historical Development of Orthotopic Corneal Xenotransplantation Author Year Model Outcome Reference Kissam 1844 Pig to human Failed 13 D'Amico 1969 Cat to rabbit 33% successful 14 Haq 1972 Fish to human Failed 15 Durrani 1974 Bovine to human 21% improved vision 16 Bahn 1982 Bovine to cat Failed 17 Moore 1987 Cat to rabbit Failed 18 Insler 1991 Human to primate 67% successful 19 Li 1992 Human to primate 55% successful 20 She 1992 Mouse to rat Successful 21 Downloaded from iovs.arvojournals.org on 09/25/2021 Rejection of Corneal Xenografts 2471 Grafts were observed every other day for the first ACI rats (allografts), or Hartley guinea pigs (xeno- week and at least twice a week thereafter. Grafts were grafts). Two grafts from each donor category were graded for clarity, edema, and vascularization. When performed on the same day. Graft survival was ana- at least two of the three criteria were moderate to se- lyzed by a Mantel-Haenzel program, and differences vere, the grafts were considered to be rejected. between the groups were analyzed by Student's Mest. Skin Grafts RESULTS Recipients were grafted orthotopically with 1 cm2 do- nor skin on the thorax, as described.24 Grafts were Corneal Grafts in Naive Recipients inspected visually, and the percent of visible epithelial The results of corneal grafts into naive recipients are necrosis was recorded. shown in Figure 1. All 8 isografts survived throughout Measurement of Xenoreactive Antibody the 30-day observation period. Five of 6 ACI allografts were rejected in this high-responder strain combina- Guinea pig cervical lymph nodes were removed and tion, with a mean survival time of 11 days. All 10 Hart- teased apart in phosphate-buffered saline containing ley guinea pig xenografts were rejected between 6 and 0.5% bovine serum albumin (Sigma, St. Louis, MO) 9 days, with an average survival time of 8 days. Though and 0.02% NaN3 (PBA). Cells were then washed three the survival of xenografts was significantly shorter times in PBA and resuspended at a concentration of 3 6 than that of both isografts (P < .001) and allografts (P X 10 cells/ml. Cells were stained with serial dilutions = .016), it was strikingly longer than the brief survival of serum using PBA as the diluent for 30 min at 4°C. time of heart grafts in the same species combination, After washing twice with PBA, cells were stained with a which survived 17 ± 4 min.22 The histologic features of 1:100 dilution of goat anti-rat IgM-phycoerythrin the rejected corneal grafts included a massive diffuse conjugate and goat anti-rat IgG-fluorescein conjugate infiltration of mononuclear cells and polymorphonu- (Jackson Immunoresearch, West Grove, PA) for 30 clear cells, accompanied by severe edema throughout min at 4°C.
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