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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 15  |  Issue : 4  |  Page : 300-306

A comparative analysis of live-related ABO-incompatible and ABO-compatible renal transplantation: Effect of Vitamin D deficiency on antibody-mediated rejection - A retrospective observational study


Department of Nephrology, Sanjay Gandhi Post Graduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India

Date of Submission01-Aug-2020
Date of Decision15-Aug-2020
Date of Acceptance09-Jun-2021
Date of Web Publication30-Dec-2021

Correspondence Address:
Prof. Raj Kumar Sharma
Department of Nephrology, Sanjay Gandhi Post Graduate Institute of Medical Sciences, Rae Bareli Road, Lucknow, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijot.ijot_90_20

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  Abstract 

Background: ABO incompatible (ABOi) transplantation is a relatively newer option for renal transplant. Despite the encouraging results and the presence of organ shortage, it is still not routine in many developing countries. This can be attributed to the lack of experience, lack of technical infrastructure, and financial limitations. Objectives: Our study aimed to compare the outcomes of living-donor ABOi renal transplantation with matched recipients of ABO-compatible (ABOc) transplantation. We also assessed the impact of Vitamin D deficiency on posttransplant outcomes in terms of graft function and rejections in these groups. Methods: We retrospectively analyzed the results of 33 ABOi living-donor kidney transplants performed between January 2013 and June 2016 at our center. We compared patient and graft survival, acute rejection episodes, Vitamin D status, and graft function of the ABOi group with an equal number of matched live-related ABOc KTs done during the same time period. Results: The patient survival in both the groups was 97%; however, death-censored graft survival was 94% in the ABOi recipients versus 100% in ABOc group over a mean follow-up of 14–15 months, respectively. Graft function was overall better in the ABOc recipients, with statistical significance seen at 6 and 12 months posttransplant. We also observed a significantly higher incidence of acute antibody-mediated rejections (ABMRs) in the ABOi cohort, with 11 episodes of ABMR versus just 2 in the ABOc recipients (P = 0.005). Vitamin D deficiency was associated with higher levels of anti-ABO antibody and increased development of ABMR due to anti-ABO antibodies (P = 0.01). Conclusions: ABO incompatible transplantation is an option with excellent patient and graft survival; results almost comparable to the ABO compatible grafts. However, in our study, ABOi transplants were associated with higher risk of acute ABMR. These episodes were amenable to treatment, and thus, the overall graft survival had similar outcomes. Vitamin D deficiency was associated with increased ABMR in ABOi cohort of renal transplantation.

Keywords: ABO-incompatible kidney transplantation, antibody-mediated rejection, plasmapheresis, Vitamin D deficiency


How to cite this article:
Yachha M, Sharma RK, Mehrotra S, Prasad N, Gupta A, Bhadauria DS, Kaul A. A comparative analysis of live-related ABO-incompatible and ABO-compatible renal transplantation: Effect of Vitamin D deficiency on antibody-mediated rejection - A retrospective observational study. Indian J Transplant 2021;15:300-6

How to cite this URL:
Yachha M, Sharma RK, Mehrotra S, Prasad N, Gupta A, Bhadauria DS, Kaul A. A comparative analysis of live-related ABO-incompatible and ABO-compatible renal transplantation: Effect of Vitamin D deficiency on antibody-mediated rejection - A retrospective observational study. Indian J Transplant [serial online] 2021 [cited 2022 Jan 18];15:300-6. Available from: https://www.ijtonline.in/text.asp?2021/15/4/300/334437




  Introduction Top


Despite tremendous advances in dialysis, renal transplant remains the treatment of choice for end-stage kidney disease (ESKD). This is because dialysis and adjuvant medications cannot replace the various functions of a normal kidney. Furthermore, the available dialysis modalities are associated with several adverse effects.[1] Despite the need to transplant majority of ESKD patients, the goals are not met due to a huge mismatch between the patient numbers and the available kidney donors. ABO incompatibility between available donors and prospective recipients also functions as an add-on to this problem.

ABO blood group incompatibility (ABOi) was earlier considered a contraindication to kidney transplantation, due to theoretically significant risk of early antibody-mediated rejection (ABMR) of the ABO-incompatible donor grafts.[2],[3],[4],[5] Alexandre et al. in 1987 reported the first success story of 26 ABOi live donor kidney transplant patients with the use of an effective desensitization protocol that included preoperative plasmapheresis (PP), splenectomy, and triple drug maintenance immunosuppression with cyclosporine, azathioprine, and corticosteroids. They reported 1-year patient and graft survival rates of 88% and 75%, respectively.[6]

ABO-incompatible donor grafts have been widely adopted across the globe due to the shortage of kidney donors.[7] Despite the encouraging results and presence of organ shortage, ABO-incompatible transplantation is still not routine in many developing countries including India. This can be attributed to the lack of experience, lack of technical infrastructure, and financial limitations. The aim of this study was to evaluate the outcomes of ABOi KT and compare with ABO-compatible (ABOc) KT in Indian patients.

The anti-microbial and immunomodulatory functions of Vitamin D appear to be playing an important role in improving the outcomes in many diseases. Vitamin D can reduce the risk of transplant rejection by controlling adaptive immune responses and down-regulating dendritic cell proliferation, maturation and antigen presentation capacity. Adorini et al. suggested that the prevention of chronic allograft rejection by Vitamin D receptor agonists involves various mechanisms; including regulation of chemokines responsible for leukocyte infiltration and down-regulation of renal transforming growth factorbeta-1 production which has pro-fibrotic activity.[8] This may also inhibit the development of rejection in renal transplant patients. Animal model experiments show that survival of allografts of all type of transplants such as bone marrow, heart, kidney, liver, pancreatic islets, skin, and small intestine are significantly prolonged by administration of Vitamin D and its analogues. This is also associated with increased resistance to infections.[9],[10] Evidence from animal experimental studies suggests that administration of 1,25-dihydroxyvitamin D can prevent acute allograft rejection in liver, kidney, and heart transplantation. However, there is limited data from human studies. In kidney transplant recipients, calcitriol supplementation has been reported to be associated with fewer episodes of acute cellular rejection.[11],[12] There is evidence supporting that Vitamin D has immuno-modulatory effects and can improve overall allograft outcomes. There are also reports that provide evidence of the immunomodulatory properties of Vitamin-D receptor agonists in transplantation. In a small prospective study, treatment of 24 transplant recipients with calcitriol showed decreased co-stimulatory molecule expression of human leukocyte antigen (HLA)-DR, CD28, CD86, and CD40 on white blood cells.[13] Prospective study of nine transplant recipients, in which donors received calcitriol therapy, which was then continued in the recipients, showed an expansion of CD4+, CD25+ Tregs in the calcitriol-treated group.[14]

Objectives

To compare the outcomes of Living-Donor ABO-incompatible renal transplantation (ABO-i) with Living-Donor ABO-incompatible renal transplantation (ABOc) in relation to their vitamin D status levels with rejection in these groups.


  Methods Top


Patients and study design

This is a retrospective observational study conducted over a period of 40 months from January 2013 to June 2016. A total of 33 ABOi live-related renal transplants were done in our institute during the study period and were included in the study. Those unwilling to consent were excluded. The parameters analyzed were as follows: Donor/recipient age, gender, blood type, HLA mismatches, primary cause of renal failure, mean time on dialysis, past medical illnesses, previous transplants, anti-ABO titers, immunosuppressive regimen, patient survival, graft survival outcome, incidence of rejections, 25-OH Vitamin-D levels, complications, and the histological findings of the performed renal biopsies. We compared the clinical and laboratory findings of the ABOi kidney transplant recipients with those of a matched control group, consisting of ABOc recipients with their 25-OH Vitamin D levels. All the transplants in the study group were living-donor transplants. The control group comprising of 33 ABOc transplant patients was transplanted at approximately the same time during the study period and was randomly selected on the basis of similar baseline demographic and clinical characteristics of donors and recipients. 25-OH Vitamin D levels were assayed in serum by chemiluminescence micro-particle immunoassay (CMIA) (Architect i-1000 STAT Abbott).

ABOi kidney transplantation protocol for recipient

The preconditioning protocol for ABO incompatible transplant in our center is based on the use of preoperative rituximab with PP and intravenous immunoglobulin (IVIG). Single infusion of 375 mg/m2 body surface area (usually 500 mg) of Rituximab is administered, 10–12 days prior to KT. PP sessions are given starting from Day 10. Depending on the titres, we have given two to 10 sessions of PP with IVIG infusions pre-operatively, with the target isoagglutinin titer of 1:8 or less. We usually reach anti-blood group immunoglobulin G (IgG) titre of 1:4 or less, however in 1 patient transplant was done at titer of 1:16. Postoperative PP is performed only when the isoagglutinin titer is above a level of 1:8 within first two weeks of transplant. During PP, replacement is given with 5% Albumin and “AB” blood group plasma. For induction, usually Basiliximab 20 mg iv is given on the day of transplant and postopERATIVE day 4. However, in immunologically high-risk patients with either HLA-DSA positivity or those receiving second/third transplant, rabbit Anti-thymocyte globulin (r-ATG) is given (total dose 3–4.5 mg/kg body weight) starting on day 0 and then on alternate days posttransplant. Immunosuppressants (Tacrolimus and MMF) are started 10 days prior to surgery. During the transplant surgery, 500 mg of iv methyl prednisolone is given. Titers of anti-A and/or Anti-B are monitored by serial tube dilution method on daily basis, with target titers kept ≤1:8 on the day of transplant.

ABO-c KT recipients are given either no induction (in immunologically low-risk), Basiliximab (Day 0 and 4), or in high-risk group r-ATG is given. Immunosuppressants (tacrolimus, MMF) are started 3 days prior to surgery. IVIG or Rituximab is not routinely administered in ABO-c transplants.

Posttransplantation protocol

Titers of IgG anti-A and/or anti-B are monitored daily by tube dilution method. The targeted titer level is ≤1:8 till14 days posttransplantation.

Oral prednisolone 20 mg is started from Day 2, and tapered to 10 mg by 3 months. Mycophenolate mofetil (MMF) and Tacrolimus are continued. Tacrolimus nadir levels (C0) are regularly monitored to achieve target blood levels. Prophylaxis with valganciclovir for 100–200 days and cotrimoxazole for 1 year is given to all patients with ABOi transplant.

Statistical analysis

Statistical analysis was performed using the SPSS 20.0 software. Normally distributed data were expressed in terms of mean ± standard deviation, while skewed data were represented by median ± interquartile range. Comparisons were made with the Chi-square or Fisher's exact test for qualitative data; while for quantitative data independent sample ttest was used. P < 0.05 was considered statistically significant.

Patient consent

The patient consent has been taken for participation in the study and for the publication of clinical details and images. Patients understand that the names and initials would not be published, and all standard protocols will be followed to conceal their identity.

Ethics statement

The research followed the tenets of the declaration of Helsinki. This work was approved by the Research Committee of Sanjay Gandhi Post Graduate Institute of Medical Sciences and supported by grants from Intramural Research funds were obtained from Sanjay Gandhi Post Graduate Institute of Medical Sciences, Lucknow, India (Grant # PGI/DIR/RC/303/2013).


  Results Top


Patient characteristics

Donor and recipient baseline characteristics were similar in both groups [Table 1] and [Table 2]. Mean recipient age in both the groups was around 35 years which is similar to that reported in previous study on ABOi outcomes.[15] The mean donor age was also comparable, 43 and 47 years in the ABOi and ABOc group. There was no significant difference in recipient and donor gender, second transplant recipients, HLA mismatches, duration of dialysis, donor kidney GFR, native kidney diseases and past medical illnesses between the ABOi and ABOc groups. Median follow up of both the groups was comparable, ranging between 1 and 40 months. Majority of the patients in both groups received Basiliximab induction, with just 2 in ABOc who received no induction due to low-immunological risk profile.
Table 1: Baseline patient characteristics

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Table 2: Patient characteristics in ABO incompatible group

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In the ABOi group, more than one-third of the recipients (42%) were of 'O' blood group [Table 1]. The highest initial baseline titres of IgG anti A/anti B antibodies was 1:1024 with median of 1:64, the highest pretransplant titre was 1:16 in one patient while the median titres were 1:2. Median number of PP sessions required pretransplant were 5, ranging between 2 and 10 sessions, posttransplant a median of zero PP sessions were required, ranging between zero to five.

Patient survival

There was single patient mortality in both the groups. In the ABOi transplant group, the death occurred within 2 days posttransplant, while in the ABOc group, the patient died after 5 days of transplantation. Both the deaths occurred due to severe septic shock and had received r-ATG for induction. In the remaining 64 patients, patient survival was 100% in the follow-up period.

Graft survival

The death-censored graft survival was 94% in ABOi and 100% in ABOc groups at 1 year.

Graft function

Serial serum creatinine estimated at 2 weeks and 2 months was comparable between the two groups. Subsequent serum creatinine levels were significantly higher in the ABOi group at 6 and 12 months. Although this trend of a higher serum creatinine in the ABOi group persisted at 18, 24, 30, 36, and 40 months posttransplant, it did not reach significance [Table 3].
Table 3: Posttransplant graft function and rejection episodes

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Rejections

All rejections were biopsy-proven. Although statistically insignificant, the overall incidence of rejections was higher in the ABOi recipients (14 episodes [42.4%]) versus the ABOc group (8 episodes [24.2%], [P = 0.117]). This difference was mainly attributable to the significantly higher rate of acute ABMRs in the ABOi group (11/33 patients [33%]), than in the ABOc group (2/33 [6%]) (P = 0.005). Similar rates of ABMR (17.9%–30%) have been reported in the literature.[16],[17],[18]

The incidence of acute cellular rejection although higher in the ABOc group, accounting for 4 episodes (12.1%) versus just 1 (3%) in ABOi group, was not of statistical significance (P = 0.355) [Table 2]. Borderline rejections were similar in both the groups.

Most of these rejections occurred in the first 2 months of transplantation, 50% (7/14) in the ABOi recipients and nearly two-third (5/8) in the ABOc group.

No significant difference in patient or graft survival was seen among the two groups. The same has been reported by studies previously.[19],[20]

Vitamin D status

25(OH) Vitamin D levels were deficient or insufficient in all our patients at the time of transplant, in the ABOi group (18.2 ± 7.6 ng/ml) and in ABOc patients (23.67 ± 10.8 ng/ml). ABOi transplant patients had more ABMR (due to anti-ABO antibodies) as compared to ABOc patients who had ABMR due to anti-HLA DSA. ABMR in the ABOi transplant recipients was significantly associated with Vitamin D deficiency (P < 0.05). Anti-ABO antibody titers (both IgG and IgM) were higher in Vitamin D deficient group [Table 4].
Table 4: Patient demographics and vitamin D levels

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  Discussion Top


This study was designed to compare the outcomes of ABOi Live-related KT (LRKT) with ABOc LRKT in the North Indian population. Although such studies have been carried out across the globe, there is a paucity of data from the Indian subcontinent. Majority of studies worldwide have reported comparable patient survival in both the groups.[21],[22]

In our study, there was one death in each of the two groups. Both the patients succumbed to severe septic shock in the immediate postoperative period. The resultant overall patient-survival was 96% in the ABOi transplant recipients, similar to that reported in various other studies.[16],[17],[18] Similarly, the death-censored graft survival of 94% in our ABOi cohort was comparable to that reported by Tydén et al. (97%), Flint et al. (100%), and Lipshutz et al. (94.4%).[23],[24],[25] Our biopsy-proven acute rejection (BPAR) rate of 42.4% was comparable to the 40% rate reported by Wilpert et al. in their study of ABOi recipients with a similar immunosuppression protocol.[21] This overall trend of higher rejections in the ABOi group (14 [42.4%] versus 8 [24.2%] with a P = 0.117), was due to the significantly higher ABMR rates in ABOi group in this observational study (11 [33.3%] in ABOi, 2 [6%] in ABOc, P = 0.005). Two recent meta-analysis have shown a clearly higher risk of ABMR (RR, 3.86; P = 0.001) in ABOi transplant recipients compared to the ABOc.[26],[27]Ushigome et al. also published a significantly higher incidence of ABMR in their ABOi recipients compared with ABOc KT (18% vs. 1%) at 3 months.[28] Setoguchi et al. also showed that ABOi allografts had a higher overall incidence of ABMR compared with ABOc allografts (27% vs. 5.3%).[29]

Though few studies using rituximab have reported improved outcomes, with acute ABMR rates similar between ABOi KT and ABOc KT, 4.0% and 2.5%, respectively, during the first 5 years, we could not replicate these results and found a significant difference in incidence of ABMR between the two groups.[29],[30] The ABMR episodes in ABOi renal transplants in our study were not associated with significant rebound of ABO antibodies, except in one out of the 11 ABMR episodes. Other studies also did not find an association between the baseline pretransplant or elevation in posttransplant anti-AB titers, predictive of ABMR. Most of these ABMR episodes (81.8%)[31],[32] responded to anti-rejection treatment with PP and IVIG.

At the time of transplant, low Vitamin D levels were seen in all ABOi (18.2 ± 7.6 ng/ml) and ABOc patients (23.67 ± 10.8 ng/ml). ABMR in ABOi transplant was significantly associated with Vitamin D deficiency (P value = 0.01). Anti-ABO antibody titers (both IgG and IgM) were also higher in Vitamin D deficient group. High rates of ABMR in ABOi group in our study may be explained due to differences in genetic predisposing factors, high incidence of Vitamin D deficiency, and risk of infection-related immune triggers among the developing world populations.

There is an important relationship between Vitamin D and the innate and adaptive immune system. In some reports, Vitamin D metabolizing enzymes provide a biological mechanism for restricted auto-and paracrine exchange of the circulating forms of Vitamin D, to the active form of Vitamin D (calcitriol) in various immune cells. This process seems to be important for normal immune function. Impaired or insufficient Vitamin D levels may lead to dysregulation of immune response.

Expression of Vitamin D receptor VDR on B cells has been reported by many researchers.[33] Vitamin D could have a role in B-cell-related autoimmune disorders and its deficiency could trigger accelerated antibody response modulated by 1,25(OH) 2D. B-cell responses to Vitamin D may extend beyond its effects on B-cell proliferation and Ig synthesis. Active Vitamin D 1,25(OH) 2Dhas been reported to suppress B-cell proliferation and immunoglobulin (Ig) production. This was considered to be an indirect effect of Vitamin D mediated via Th cells.[34] Recent studies have also shown direct effects of 1,25(OH) 2D on B-cell proliferation including plasma cell inhibition and class switch differentiation of memory cells.[35],[36]


  Conclusions Top


There are various reports of ABOi transplantation experience from developing countries which show relatively good short-term outcomes. In the current study, although the short-term graft and patient survival has been excellent, a longer follow-up with a larger number of patient cohort is required for definite results. Our patients with ABOi transplant had a higher incidence of acute ABMR. Furthermore, Vitamin D deficiency was significantly associated with this higher incidence of ABMR. This phenomenon may be explained due to a different genetic constitution, high incidence of Vitamin D deficiency, and a higher risk and incidence of infection-related immune triggers amongst the developing world populations. Thus to conclude, a successful ABO incompatible transplantation is an appropriate option for an expanding donor pool with no other donor possibilities, providing a reasonable graft and patient survival. Vitamin D deficiency should be actively evaluated for and corrected prior to transplantation in all patients, both ABOi and ABOc cohorts, till further studies reach conclusive results of its beneficial role in preventing ABMR.

Study limitations

The study does not involve the supplementation of Vitamin D. This study was conducted on a limited number of patients with ABOi transplants. The association of Vitamin D deficiency with ABMR in the ABOc cohort was difficult to assess due to very few ABMRs in that group. Follow-up of these patients was also relatively short, and hence, long-term outcome cannot be completely commented upon. Larger studies are suggested. Using an almost similar long-term immunosuppression protocol in both the groups is the strength of our study.

Financial support and sponsorship

This work was financially supported by grants from Intramural Research funds from our institute “Sanjay Gandhi Post Graduate Institute of Medical Sciences”, Lucknow, India.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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