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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2011  |  Volume : 22  |  Issue : 5  |  Page : 901-910
Study on the role of humoral immunity in renal transplant rejections and its correlation with histopathological findings


1 UGC Advanced Immunodiagnostic Training & Research Centre, Division of Immunopathology, Department of Pathology, Banaras Hindu University, Varanasi, India
2 Department of Nephrology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, India

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Date of Web Publication6-Sep-2011
 

   Abstract 

Immunoglobulins (Ig) and complement, which are components of humoral immunity, are supposed to play a role in renal transplant rejection. The present study was undertaken to study the level of complement C3, C4 and IgG, A and M in patients with chronic renal failure (CRF) and in those with renal transplant rejection (Tx Rej) as well as stable transplant recipients (Tx Stb) and normal healthy controls (NHC) in order to assess their role in transplant rejection and to correlate them with histopathological findings. The mean level of C3 and C4 in the CRF, Tx Rej and Tx Stb groups was not significantly different from the NHC group (P > 0.05). The mean level of C3 in the Tx Rej group was not different from that in the Tx Stb group. However, the C4 level was significantly reduced in the Tx Rej group when compared with the Tx Stb group (P < 0.05). There was no histopathological correlation between C3 levels and acute cellular rejection (ACR) or chronic allograft nephropathy (CAN); however, C4 levels were reduced in about 50% of the cases with CAN. The mean serum IgG level was significantly reduced in patients with CRF and transplant recipients as compared with NHC. The serum IgA level was also significantly reduced in Tx Rej cases. Correlation of serum IgA with histopathology in cases with rejection showed that in ACR, a lower mean level of IgA was seen as compared with that seen in cases with CAN. The serum IgM level was significantly higher in the Tx Rej group as compared with the Tx Stb group. There was no significant correlation between serum IgM levels and renal histopathology in patients with ACR and CAN. The C3 level showed a significant positive correlation with IgG (r = +0.50, P < 0.05) in the Tx Stb group. This study shows that cell-mediated immunity is the main cause of rejection in both ACR and CAN while humoral immunity is also involved along with cellular immunity in some cases with CAN.

How to cite this article:
Sonkar GK, Usha, Singh R G. Study on the role of humoral immunity in renal transplant rejections and its correlation with histopathological findings. Saudi J Kidney Dis Transpl 2011;22:901-10

How to cite this URL:
Sonkar GK, Usha, Singh R G. Study on the role of humoral immunity in renal transplant rejections and its correlation with histopathological findings. Saudi J Kidney Dis Transpl [serial online] 2011 [cited 2022 May 23];22:901-10. Available from: https://www.sjkdt.org/text.asp?2011/22/5/901/84317

   Introduction Top


Immunoglobulins (Ig) and complement, which are components of humoral immunity, are supposed to play a role in renal transplant rejection. Post-transplant production of circulating antibodies to allo-antigens on the endothelium, including HLA class I, [1] class II [2] or non-major histo-compatibility complex antigens such as ABO antigens, [3] leads to acute humoral rejection. Earlier studies [4] on Ig and complement components C3 and C4 were conducted in the serum of patients who underwent cadaveric renal transplantation. They had reported that post-transplant serum IgG and IgM levels were significantly lower in recipients with stable graft than in the pre-transplant period. In post-transplant patients, the serum IgM level is increased during rejection episodes. However, there was no significant change in IgG levels. The mean C3 and C4 levels were significantly lower during the rejection episodes.

Bouts et al, [5] in their study on children with CRF, those on dialysis and in normal controls, found that total IgG, IgA and IgM levels were lower in the peritoneal dialysis group compared with normal controls. Children on dialysis and those with CRF had lower serum IgM and albumin levels compared with normal controls.

In a study from Iran, [6] the authors concluded that the IgG, IgM, IgA and IgE levels decreased post-transplantation due to the use of anti-rejection drugs. They concluded that a pre-transplant increase in IgE level is predictive of acute rejection. They also added that high levels of pre-transplant IgA were associated with better graft function.

Histological studies have been carried out by several workers to look for the role of humoral components in transplant rejection. The histological findings show mild infiltration of mononuclear cells (MNCs) and neutrophils in the renal interstitium. [1] The glomeruli show necrosis and thrombosis. [7] Acute tubular necrosis (ATN), in many cases, has been shown to be the first manifestation of acute humoral rejection (AHR). About 30-70% of the cases with AHR have been reported to have patchy infarction. [8],[9] They have further reported in their study that fibrinoid arterial necrosis is more characteristic of humoral than cellular rejection.

The present study was undertaken to study the levels of complement C3, C4 and IgG, A and M in patients with chronic renal failure (CRF), renal transplant rejection (Tx Rej), stable transplant recipients (Tx Stb) and normal healthy controls (NHC), and to assess their role in cases with transplant rejection and to correlate them with histo-pathological findings.


   Materials and Methods Top


A total of 103 subjects were enrolled in the study, and included the following:

  1. 35 cases with CRF not yet on dialysis,
  2. 32 post-renal transplant cases, which included 21 Tx Stb and 11 Tx Rej [cases were considered as stable when the serum creatinine (SCr) was <2 mg/dL with no adverse events, while SCr >2 mg/dL for more than 3 months was considered as cases undergoing rejection] and
  3. 36 cases of age- and sex-matched NHC. These cases were chosen from both the inpatient and the outpatient patients in the Department of Nephrology.


All renal transplant patients were given triple immunosuppressive therapy, i.e. cyclosporine + azathioprine + steroids. Patients with rejection episodes were given methylprednisolone in combination with cyclosporine and steroids. In the 11 cases with Tx Rej, three responded to therapy (grouped as acute rejection cases) while the other eight cases developed chronic allograft nephropathy (CAN). Biopsy-proven rejections were classified according to the Banff '97 criteria. [10] The serum complement components C3 and C4 were measured by single radial immunodiffusion method, kit of Bioscientifica S.A, Argentina, supplied by Priman Instruments Pvt. Ltd., Delhi, India. The serum IgG, IgA and IgM were measured by the immunoturbidometric method, using a Quantia kit and turbidometer of Tulip Diagnostics, Goa, India.

Informed consent was taken from all patients enrolled in this study and this work was cleared by the ethical committee of our institution.


   Statistical Analysis Top


Statistical analysis of the data was performed using Statistical Package for Social Sciences (SPSS, Chicago, IL, USA), version 15. Student's "t" test was carried out to compare the mean values of different groups to look for its significance. Pearson's correlation between the markers was done in the Tx Stb and Tx Rej groups. A P-value less than 0.05 was considered significant.


   Results Top


Histopathology of the kidney in patients with rejection showed that three cases had acute rejection (AR) and eight cases had features of CAN [Table 1]. All patients with AR had ACR. The glomeruli showed an increase in MNCs in some cases, while two cases showed thickening of the Bowman's capsule. The tubules revealed features of tubulitis while the in terstitium revealed infiltration with MNC. In two cases, few neutrophils and eosinophils were also present. Based on the Banff's criteria for rejection, two out of three cases of ACR were diagnosed to have grade 1A and one had grade 1B rejection [Table 1].
Table 1: Types of rejection based on Banff's criteria ('97) in renal transplant rejection cases and the levels of complement and immunoglobulins in these cases.

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In the eight cases with CAN, all showed segmental and/or global glomerulosclerosis. Hyalinized crescent was seen in two cases and thickening and duplication of the glomerular basement membrane (GBM) were each seen in two glomeruli. In three cases, the glomeruli showed thrombi in the capillary lumen. The tubules revealed varying degrees of atrophy in all cases with thickening of the tubular basement membrane (TBM). The interstitium in all cases showed varying degree of fibrosis and infiltration with MNC. Lymphoid follicles were present in the interstitium in two cases and a granuloma was noted in one case. Blood vessels revealed fibromuscular hyperplasia and hyaline thickening. Classification of CAN according to Banff's criteria revealed that four cases belonged to CAN grade I, two belonged to CAN grade II and two were grouped under CAN grade III [Table 1].

Serum complement component C3 was assayed in all the groups. In the NHC group, the level varied from 56.20 to 157.40 mg/dL. About 83.33% of these individuals had C3 level between 80 and 160 mg/dL, while six cases in the NHC group had a slightly lower value of C3, varying between 56.20 and 74.26 mg/dL. In patients in the CRF, Tx Stb and Tx Rej groups, about 80-82% of the cases had C3 levels close to the normal range. Although the mean value of C3 in cases with Tx Rej (93.40 ± 13.87 mg/dL) was lower than that in the Tx Stb, CRF and NHC groups, it was not statistically significant [Table 2].
Table 2: Serum C3 level in the CRF, Tx Stb, Tx Rej and NHC groups.

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The complement C4 level was between 20 and 40 mg/dL in 75% in the NHC group, while in 22.22% of the cases, the C4 level was lower than the normal range, and it varied from 15.01 to 19.85 mg/dL. In cases with Tx Rej, 45.45% had low C4 level between 17.5 and 19.0 mg/dL. In contrast, 66.67% of the Tx Stb and 62.85% of the patients with CRF had C4 between 20 and 40 mg/dL. The low level of C4 in cases with Tx Rej was statistically significant when compared with Tx Stb and NHC groups [Table 3]. When the C4 level was correlated with the histological type of rejection, it was found that one case with ACR had a level below 20 mg/ dL while in those with CAN, four cases (50%) had low C4 value below 20 mg/dL [Table 1]. The difference in the mean value of C4 between ACR and CAN was not statistically different.
Table 3: Serum C4 level in the CRF, Tx Stb, Tx Rej and NHC groups.

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The serum IgG level in the NHC group varied between 1279.72 and 1674.19 mg/dL. Majority of the cases (97.23%) had a value between 700 and 1600 mg/dL. All Tx Stb cases had IgG levels within the normal range, but the mean level was significantly lower than normal. In the Tx Rej cases, 90.91% had a normal value, but more toward the lower side. Again, the mean value was significantly reduced when compared with the NHC group. In CRF cases also, three patients (8.57%) had value less than 700 mg/dL while the level was in the normal range in the remaining patients. Thus, the mean level of IgG was significantly lower in the CRF, Tx Stb and Tx Rej groups when compared with the NHC group [Table 4]. There was no significant correlation between serum IgG levels and histological types of rejection, either ACR or CAN.
Table 4: Serum IgG level in the CRF, Tx Stb, Tx Rej and NHC groups.

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The serum IgA level in healthy controls varied from 101.11 to 362.20 mg/dL. All study cases (NHC, Tx Stb, Tx Rej and CRF) had IgA levels in the normal range of 70-400 mg/ dL. However, in the Tx Stb and Tx Rej groups, majority had value toward the lower side of the normal range. The mean value of IgA in both the Tx Stb and the Tx Rej groups was significantly reduced as compared with the NHC and CRF groups. This suggests that serum IgA synthesis is slightly suppressed after renal transplantation [Table 5]. Correlation of serum IgA with histopathology of rejection showed that a lower mean level of IgA was recorded in ACR as compared with CAN (124.13 ± 76.67 vs 148.70 ± 51.48 mg/dL). This difference was not statistically significant.
Table 5: Serum IgA level in in CRF, Tx Stb, Tx Rej and NHC groups.

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The serum IgM level in the NHC group ranged from 61.79 to 285.67 mg/dL. Only one case in this group had an increased IgM level (more than 230 mg/dL). Patients with CRF and Tx Stb had IgM between 45.54 and 190.92 mg/dL. The mean value of serum IgM in the CRF and Tx Stb groups was significantly reduced ascompared with NHC while in the Tx Rej cases, the mean IgM level was more or less equal to the NHC group, suggesting that serum IgM synthesis is unaffected in rejection [Table 6]. Correlation of serum IgM with renal histo-pathology did not reveal any significant difference between ACR and CAN.
Table 6: Serum IgM level in CRF, Tx Stb, Tx Rej and NHC groups.

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Correlation of the complement and immunoglobulins in the Tx Stb group showed that C3 had a positive significant correlation with IgG (r = +0.50, P < 0.05). No other significant correlation was found between the various markers in the transplant rejection group [Table 7] and [Table 8].
Table 7: Correlation of immunological markers in the transplant-stable group.

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Table 8: Correlation of immunological markers in the transplant rejection group.

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   Discussion Top


Deficiency in complement levels predisposes patients to infection via two mechanisms, [11] ineffective opsonization and defects in lytic activity (defects in MAC). It has also been reported that patients with malnutrition have low complement levels. [12] Humoral rejection occurs in 20-30% of the cases with rejection, and has a poorer prognosis than cellular rejection. The serum levels of C3 and C4 decrease significantly during rejection episodes compared with both pre-transplant and control values. [4]

The complement components and its split products have led workers to investigate its role in the field of renal disease and transplantation. It is not only an important component of the innate immune system but it also plays an essential role in the initiation and control of the adaptive immune response. [13]

In our study, we measured the serum complement components C3 and C4 by the single radial immunodiffusion method. The mean level of serum C3 and C4 in the NHC group was 103.76 ± 26.55 mg/dL (range 56.20-157.40 mg/dL) and 25.83 ± 6.51 mg/dL (range 15.01-40.80 mg/dL), respectively. Engstrom et al [14] reported in their study on C3 and C4 in diabetics and non-diabetics that the mean value of C3 in the non-diabetic control group was 98 ± 21 mg/dL (range 67-129 mg/dL) and C4 was 24.6 ± 8 mg/dL (range 13-32 mg/dL). Al-Saimary et al [15] reported the mean level of C3 in 100 normal controls to be lower than in patients with atopic dermatitis (139.90 vs 218.30 mg/dL). They reported the mean level of C4 also to be significantly higher in patients than in controls (42.90 vs 30.10 mg/dL).

In our study, CRF patients had a mean C3 level of 99.85 ± 19.04 mg/dL, which was found to be not significant when compared with the NHC group. Tang et al [16] have reported a mean C3 level of 93.8 mg/dL in transplant recipients and 96.6 mg/dL in healthy subjects.

In many studies, complement components have been reported in renal histology. The introduction of C4d, a split product of C4, staining in biopsies from renal transplant recipients has led to the idea of the role of humoral rejection. Studies have shown a strong correlation of C4d staining of peri-tubular capillaries with panel-reactive [17] or donor-specific antibodies, [18] which is indicative of humoral rejection. In several other studies, C4d staining has been shown to predict poor graft survival. [19],[20] These results show that the complement activation occurs by the classical pathway. In a study by Watanabe and Scornik, [21] complement activity in the serum of liver, heart and lung transplantation that was tested by a standard antibody was similar to normal serum. In contrast, patients with kidney transplantation exhibited higher complement activity. They further suggested from their study that complements are activated by HLA antibodies, leading to the highest deposition of C3b followed by C4b and C5b. Sund et al [22] have reported from their study on complement activation in kidney graft biopsies that diffuse deposition of C4d in the capillaries of kidney graft relates to acute humoral rejection.

In a study from France [23] on 24 kidney transplant recipients having thrombotic microangiopathy (TMA), six patients showed low C3 plasma level and/or low factor B levels suggesting activation of the alternate complement pathway. Their molecular study suggested that of these 24 patients, seven patients showed a mutation in complement factors H and I (CFH and CFI), and two of them showed mutation in both the genes. Contrary to this, in renal transplant patients without TMA, no mutation was found. One-third of the patients with TMA lost their graft within one year of transplant, which included six patients with a CFH mutation or a decrease of C3 or CFB in plasma. In a recent study, [24] it has been shown that C3 is produced in the liver in response to pro-inflammatory cytokines such as IL-6 and IL-1. Our study has shown a positive correlation of IL-6 and C3 in Tx Stb cases, but not in the CRF and Tx Rej groups.

The study data of Regele et al [25] have concluded that activation of complement in renal microvasculature indicates humoral allo-reactivity, contributing to chronic rejection characterized by chronic transplant glomerulopathy and basement membrane multi-layering in peritubular capillaries. Some studies have shown that C4 deposition in the capillary endothelium of human cardiac and renal allografts represents chronic rejection. [25],[26] In one small study, [27] 17% of the recipients with the deposition of C4d in the capillaries developed chronic allograft dysfunction. Contrary to the above findings, Namba et al [28] recently concluded that in cases with positive C4d showing long-term survival, no significant differences were observed with chronic rejection.

In our study, we found that serum C3 was normal in all cases with ACR while in CAN, in a majority of the cases (6/8), C3 was normal (more than 80 mg/dL), while in two cases, mild borderline reduction was noted. Both these cases had segmental and global sclerosis without any vasculitis. In contrast, C4 level was normal in two cases of ACR and reduced in one case (less than 20 mg/dL). There was a significant reduction of C4 in the serum of rejection cases, supporting the hypothesis that humoral immunity is also one of the factors in chronic rejection.

The levels of serum immunoglobulins IgG, IgA and IgM have also been studied in relation to rejection. White et al [29] reported the mean value of IgG in 100 normal controls to be 1463 ± 252 mg/dL, ranging from 960 to 2160 mg/dL. Edan et al [30] have reported the mean value of IgG in NHC to be 1115.80 mg/dL. Earlier studies reported contradictory results. Barnes et al [4] had reported that serum IgG levels were significantly lower in controls than in patients with end-stage renal failure (ESRF). Recent studies have supported our observations. Sarmiento et al [31] found decreased levels of IgG in heart transplant recipients and proposed that it was responsible for infection after transplantation. In our CRF cases, the mean level of IgG was 1186.85 mg/dL, which was significantly lower than NHC. Lessan-Pezeshki et al [6] have also supported our observations that the IgG level decreases after undergoing renal transplantation. In their study, the mean IgG was higher in the Tx Stb group as compared with the Tx Rej group (1361 vs 1201 mg/dL).

White et al [29] reported a slightly higher mean value of IgA of 238 mg/dL with a range of 67- 478 mg/dL in normal healthy Omanis. The mean level of IgA reported by Edan et al [30] in their study in 2006 in NHC was 200.50 mg/dL, which was more or less similar to our findings. The mean level of IgA was higher in the Tx Stb group as compared with the Tx Rej group. [6] We also noticed a significantly lower level of IgA in the Tx Rej group as compared with the Tx Stb group.

A recent study [32] reported that IgA nephropathy is present in up to 60% of the graft recipients within ten years post-transplant, leading to loss of graft. In contrast, Chacko and colleagues [33] showed that the 5-year graft survival in those who previously had IgA nephropathy was not significantly different from the group that did not have IgA nephropathy and underwent renal transplant.

The mean serum IgM was reported to be 130.72 ± 46.11 mg/dL in our NHC. Other workers have reported a mean level of IgM of 145.70 mg/dL [29] and 114 mg/dL. [30] In the CRF group, the mean level was found to be 106.47 mg/dL, which was significantly lower than the NHC. Barnes et al [4] reported significantly lower serum IgM levels in controls than in patients with ESRF. They also reported that IgM levels increased during rejection episodes. We also found that the IgM level was significantly higher in the Tx Rej group as compared with the Tx Stb group; however, the IgM level in the Tx Rej group was similar to that in the NHC group.

Yamani et al [34] and Broeders et al [35] have concluded from their study on heart and renal transplantation, respectively, that hypogammaglobulinemia is associated with the occurrence of rejection or infection due to the intense immunosuppression. In our study, all the patients in the Tx Stb group were taking a low dose of azathioprine and cyclosporine, whereas patients in the Tx Rej group were irregular in taking drugs due to financial reasons. Hence, low levels of IgM could be due to immunosuppression occurring due to drugs. Similarly, in CRF also, low IgM may be due to immunosuppression.

Thus, our study suggests that cell-mediated immunity is the main cause of rejection in both ACR and CAN, while in CAN, humoral immunity may also be involved in some cases along with cellular immunity.


   Acknowledgment Top


We are thankful to the UGC Advanced Immunodiagnostic Training and Research Centre, Division of Immunopathology, Department of Pathology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, India.

 
   References Top

1.Halloran PF, Schlaut J, Solez K, Srinivasa NS. The significance of the anti-class I antibody response. II. Clinical and pathologic features of renal transplants with anti-class I-like antibody. Transplantation 1992;53:550-5.  Back to cited text no. 1
    
2.Collins AB, Schneeberger EE, Pascual MA, et al. Complement activation in acute humoral renal allograft rejection: diagnostic significance of C4d deposits in peritubular capillaries. J Am Soc Nephrol 1999;10:2208-14.  Back to cited text no. 2
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3.Kooijmans-Coutinho MF, Hermans J, Schrama E, et al. Interstitial rejection, vascular rejection, and diffuse thrombosis of renal allografts. Predisposing factors, histology, immunohistochemistry, and relation to outcome. Transplantation 1996;61:1338-44.  Back to cited text no. 3
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4.Barnes RM, Hart CA, Alexander LC, Steen S. Immunological evaluation of renal transplant patients: changes in levels of beta-2-microglobulin, immunoglobulins and complement components during graft rejection. J Clin Lab Immunol 1983;12(1):17-22.  Back to cited text no. 4
    
5.Bouts AH, Davin JC, Krediet RT, et al. Immunoglobulins in chronic renal failure of childhood: Effects of dialysis modalities. Kidney Int 2000;58:629-37.  Back to cited text no. 5
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11.Liszewski MK, Atkinson JP. Regulatory proteins of complement. In MM Frank, JE Volanakis (eds), The human Complement System in Health and Disease, Marcel Dekker, New York, 1998;149-66.  Back to cited text no. 11
    
12.Frank MM. Primary immune deficiencies: presentation, diagnosis, and management. Pediatr Clin North Am 2000;47:1-7.  Back to cited text no. 12
    
13.Berger SP, Roos A, Daha MR. Complement and the kidney: What the nephrologists needs to know in 2006? Nephrol Dial Transplant 2005;20:2613-9.  Back to cited text no. 13
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14.Engstrom G, Hedblad B, Eriksson KF, Janzon L, Lindgarde F. Complement C3 Is a Risk Factor for the Development of Diabetes. A Population-Based Cohort Study. Diabetes 2005;54:570-5.  Back to cited text no. 14
    
15.Al-Saimary IE, Bakr SS, Al-Hamdi K. Immunoglobulin and complement components levels in patients with atopic dermatitis. The Internet J Dermatol 2006;3:2.  Back to cited text no. 15
    
16.Tang S, Zhou W, Sheerin S, Vaughan RW, Sacks SH. Contribution of renal secreted complement C3 to the circulating pool in humans. J Immunol 1999;162:4336-41.  Back to cited text no. 16
    
17.Feucht HE, Schneeberger H, Hillebrand G, et al. Capillary deposition of C4d complement fragment and early renal graft loss. Kidney Int 1993;43:333-8.  Back to cited text no. 17
    
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23.Le Quintrec M, Lionet A, Kamar N, et al. Complement mutation associated de novo thrombotic microangiopathy following kidney transplanytation. Am J Transplant 2008;8(8):1 694-701.  Back to cited text no. 23
    
24.Ritchie RF, Palomaki GE, Neveux LM, Navolotskaia O, Ledue TB, Craig WY. Reference distributions for complement proteins C3 and C4: a practical, simple and clinically relevant approach in a large cohort. J Clin Lab Anal 2004;18:1-8.  Back to cited text no. 24
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25.Regele H, Böhmig GA, Habicht A, et al. Capillary deposition of complement split product C4d in renal allografts is associated with basement membrane injury in peritubular and glomerular capillaries: a contribution of humoral immunity to chronic allograft rejection. J Am Soc Nephrol 2002;13(9):2371-80.  Back to cited text no. 25
    
26.Mauiyyedi S, Pelle P, Saidman S, et al. Chronic humoral rejectin: Identification of antibody mediated chronic renal allograft rejection by C4d deposits in peritubular capillaries. J Am Soc Nephrol 2001;12:574-82.  Back to cited text no. 26
    
27.Theruvath TP, Saidman SL, Mauiyyedi S, et al. Control of antidonor antibody production with tacrolimus and mycophenolate mofetil in renal allograft recipients with chronic rejection. Transplantation 2001;72:77-83.  Back to cited text no. 27
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29.White AG, Al Riyami HA, Kuchipudi P, Daar AS. Immunglobulins, immunoglobulin subclasses and complement in adult omanis. Ann Saudi Med 1997;17(1):39-42.  Back to cited text no. 29
    
30.Edan I, Bakr SS, Al-Hamdi. Serum immunoglobulin and complement component levels in patients with atopic dermatitis. The Internet J Dermatol 2006;3:2.  Back to cited text no. 30
    
31.Sarmiento E, Rodriguez-Molina J, Munoz P, et al. Decreased levels of serum immunoglobulins as a risk factor for infection after heart transplantation. Transplantation 2005;37:4046-9.  Back to cited text no. 31
    
32.Choy BY, Chan TM, Lai KN. Recurrent glomerulonephritis after kidney transplantation. Am J Transplant 2006;6:2535-42.  Back to cited text no. 32
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33.Chacko B, Jhn GT, Neelkantan N, Korula A, Jacob CK. Outcomes of renal transplantation in patients with IgA nephropathy in India. J Postgrad Med 2007;53:92-5.  Back to cited text no. 33
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34.Yamani MH, Avery RK, Mawhorter SD, et al. Hypogammaglobulinemia following cardiac transplantation: a link between rejection and infection. J Heart Lung Transplant 2001;20(4): 425-30. 35.   Back to cited text no. 34
    
35.Broeders EN, Wissing KM, Hazzan M, et al. Evolution of immunoglobulins and mannose binding protein levels after renal transplanttation: association with infectious complications. Transpl Int 2008;21(1):57-64.  Back to cited text no. 35
    

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Correspondence Address:
Gyanendra Kumar Sonkar
Department of Biochemistry, C.S.M Medical University (Formerly King George's Medical University), Lucknow - 226003
India
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Source of Support: None, Conflict of Interest: None


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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]

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    Abstract
   Introduction
    Materials and Me...
   Statistical Analysis
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