|Year : 2021 | Volume
| Issue : 2 | Page : 110-116
Incidence of new-onset diabetes among sudanese renal transplant patients using different immunosuppressive regimens: A retrospective study
Alaa Mohammedazeem Elzain1, Safaa Badi1, Bashir Alsiddig Yousef2, Habab Khalid Elkheir3
1 Department of Clinical Pharmacy, Faculty of Pharmacy, Omdurman Islamic University, Omdurman, Sudan
2 Department of Pharmacology, Faculty of Pharmacy, University of Khartoum, Khartoum, Sudan
3 Department of Clinical Pharmacy, Faculty of Pharmacy, Omdurman Islamic University, Omdurman; Department of Clinical Pharmacy, Faculty of Pharmacy, University of Sciences and Technology, Khartoum, Sudan
|Date of Submission||03-May-2020|
|Date of Decision||12-Jul-2020|
|Date of Acceptance||23-Sep-2020|
|Date of Web Publication||27-Oct-2021|
Bashir Alsiddig Yousef
Department of Pharmacology, Faculty of Pharmacy, University of Khartoum, Al-Qasr Ave, Khartoum 11111
Source of Support: None, Conflict of Interest: None
Background: New onset diabetes after renal transplant (NODAT) is a serious complication of therapy with immunosuppressive drugs. The aim of this study was to estimate the incidence of NODAT and its association with immunosuppressant regimens within 6 months of the administration. Methodology: A descriptive retrospective case finding hospital-based study, conducted in the department of nephrology at Ahmed Gasim Hospital from January to September 2017, on patients who underwent renal transplantation between June 2015 and June 2016. The data were collected using a structured checklist. The collected data were analyzed by the Statistical Package for Social Sciences (SPSS). Results: A total of 110 patients were included, the majority of studied patients were males (71.8%) and in the age group of 20–40 years (50.9%). The most commonly prescribed immunosuppressant regimen was regimen, which consists of methylprednisolone as induction therapy and tacrolimus + azathioprine + prednisolone as maintenance therapy. Regarding the adverse effects, 11 (10%) of them developed NODAT throughout 6 months after transplantation. However, no significant association was found between the postulated risk factors and the incidence of NODAT. Conclusion: The incidence of NODAT was 10% throughout 6 months after transplantation. Correlations between sociodemographic characteristics, immunosuppressant regimens, episodes of rejection with the incidence of NODAT were found statistically insignificant.
Keywords: Immunosuppressive regimens, incidence, new-onset diabetes, renal transplantation
|How to cite this article:|
Elzain AM, Badi S, Yousef BA, Elkheir HK. Incidence of new-onset diabetes among sudanese renal transplant patients using different immunosuppressive regimens: A retrospective study. CHRISMED J Health Res 2021;8:110-6
|How to cite this URL:|
Elzain AM, Badi S, Yousef BA, Elkheir HK. Incidence of new-onset diabetes among sudanese renal transplant patients using different immunosuppressive regimens: A retrospective study. CHRISMED J Health Res [serial online] 2021 [cited 2021 Nov 27];8:110-6. Available from: https://www.cjhr.org/text.asp?2021/8/2/110/329447
| Introduction|| |
Chronic kidney disease (CKD) was nearly doubled as a cause of death worldwide between 1990 and 2010 and was the 18th highest cause of death worldwide in 2010. By 2030, more than 70% of patients with end-stage renal disease (ESRD) are estimated to be living in low-income countries, such as those in sub-Saharan Africa, where the gross domestic product per person is on average less than US$1500 per year., CKD is defined as kidney dysfunction or damage that persists for >3 months. Kidney transplantation is the best available therapy for ESRD, as it can improve the quality and length of life and decrease the risk of death for patients compared to chronic dialysis.,, Kidney transplantation is contraindicated in the context of active infection, malignancy, substance abuse, or nonadherence to therapy; or in cases where comorbidities are expected to limit life expectancy and the ability to benefit from kidney transplantation significantly.
The immunosuppressants are agents used to prevent rejection in organ transplant recipients and for the treatment of autoimmune disorders. Recent improvements after kidney transplantation are due to the introduction of effective immunosuppressive agents and improved surgical techniques. In general, there are three stages of clinical immunosuppression: induction therapy, maintenance therapy, and treatment of an established acute rejection episode. The most common maintenance immunosuppressive agents can be divided into five classes: the calcineurin inhibitors (cyclosporine and tacrolimus), costimulation blockers (belatacept), mammalian target of rapamycin inhibitors (sirolimus and everolimus), antiproliferative (azathioprine and mycophenolic acid derivatives), and corticosteroids., Although modern immunosuppression in kidney transplantation has led to significant reductions in allograft rejection, drug-specific complications, including new-onset diabetes mellitus, hyperlipidemia, and hypertension remain a serious concern.,
Posttransplantation diabetes mellitus, or now more commonly referred to in the transplant literature as new-onset diabetes after transplant (NODAT) is defined by the World Health Organization and American Diabetes Association (ADA) as diabetes that develops for the first time after kidney transplantation.,, NODAT is caused by the combination of insulin resistance and deficient insulin production., The immunosuppressant agents are the main cause for the induction of NODAT. The diabetogenic effect of glucocorticoids is primarily caused by insulin resistance, in vitro and biopsy studies in human and animal models suggest that both cyclosporine and tacrolimus impair pancreatic β-cell function. Many reports have shown the incidence of NODAT within 6 months after transplantation,,, and other have been carried to determine the risk factors for developing of NODAT, such as that indicated the older age, obesity, and diuretic therapy are important determinants of impaired β-cell function after renal transplantation., Despite the importance of this issue as many Sudanese population underwent renal transplantation, and they are using immunosuppressants, there is no single study done in this area in Sudan recently. Hence, our study aimed to determine the incidence of new-onset diabetes among renal transplant patients using different immunosuppressive regimens.
| Methodology|| |
This was a descriptive retrospective case findings hospital-based study. The study was conducted in the department of nephrology at Ahmed Gasim Hospital. The study was conducted from January to September 2017. The study population was adult Sudanese patients who underwent renal transplant between June 2015 and June 2016.
Inclusion and exclusion criteria
Adult renal transplant patients who were using immunosuppressants for at least 6 months after the transplant, patients with at least had one of the parameters of blood glucose measurement throughout 6 months after transplant were included in the study. Patients were excluded if they were diagnosed with diabetes before transplantation, lost to follow-up, had no blood glucose measurement during the first 6 months after the transplant, received transplantation of another organ before, and those who were taking immunosuppressants for nontransplant reasons such as lupus nephritis.
Sample size and sampling methods
All available medical charts of patients who underwent renal transplantation between June 2015 and June 2016 at Ahmed Gasim Hospital contained 267 patients. From these, 157 were excluded from the study for the following reasons: diabetes mellitus before transplantation (n = 2), lost to follow-up, and had no blood glucose measurement during the first 6 months after transplant (n = 154), used immunosuppressants before transplant for lupus nephritis (n = 1). Finally, 110 patients were included in the analysis.
Data were collected using a pretested designed data collection sheet. A pilot study was done for 10 patients and then was excluded from the study. Sociodemographic, clinical, and laboratory data were recorded from the patients' medical charts. The data were collected every day except Fridays and Saturdays from 9:00 a.m. to 4:00 p.m., and the data collection was finished after 60 days.
Identification of patients using fasting blood glucose measurements
Fasting blood glucose (FBG) was initially determined in all patients before transplantation. According to the criteria of the ADA, diabetes is present if FBG level is ≥126 mg/dl on repeated measures (more than one time measurement). Impaired fasting glucose (IFG) is defined as FBG level between 100.8 mg/dl and 124.2 mg/dl, whereas the normal value (N) for FBG is <100.8 mg/dl. Six months after the transplantation, check-up laboratory tests were observed in all patients, and patients were classified into one of the following three groups based on the glucose value: normal (N), impaired fasting glucose (IFG), and NODAT; the diagnosis of NODAT based on two separated readings of FBG ≥126 mg/dl. The incidence of NODAT is calculated by the following formula, Incidence = (number of NODAT patients/total number of samples) ×100.
Data were entered and analyzed using the International Business Machines (IBM). Statistical Package for Social Sciences for Windows, Version 24.0 software (Armonk, NY, USA: IBM Corp), and Microsoft excel. Univariate analysis was used to summarize the data related to sociodemographic, clinical, and laboratory characteristics of study participants. Bivariate analysis to determine associations between the incidence of NODAT and various independent factors was conducted. Independent sample t-test was used to predict the association of incidence of NODAT and the factors affecting it. The statistic associations were considered significant at P < 0.05.
The approval to conduct the study was obtained from Omdurman Islamic University, National Committee of Research Department at the Ministry of Health, Khartoum State. And Department of Renal Diseases and Surgery-Ministry of Health, Khartoum State, besides the approval obtained from the authorities of Ahmed Gasim Hospital. Data confidentiality was protected throughout the study phases.
| Results|| |
Patient's sociodemographic and clinical characteristics
Among studied patients, as shown in [Table 1], the majorities of them were male (71.8%), and almost of patients were in the age group of 20–40 years (50.9%). Concerning body mass index (BMI), (47.3%) of patients had normal weight. Among the study population, hypertension was the most common comorbid disease (84.5%). Regarding donors, 53.6% received kidneys from their siblings, 11.9% from their sons, 9.5% from their daughters, 9.5% from their mothers, 5.9% from their nephews, 4.8% from their cousins, 1.2% from their father, 1.2% from their aunt while 1.2% from their wives. Clinically, the vast majority of patients enrolled in this study (84.5%) had low hemoglobin, high serum creatinine level (97.3%), high potassium level (43.6%), and 64.5% of patients had elevated level of serum cholesterol before renal transplant. Regarding FBG the majority of patients had normal FBG before transplant (77.3%), and (13.6%) had impaired fasting glucose (IFG). Of all patients, glycated hemoglobin (HbA1c) was not reported before transplant, and only one had reported RBG, which was found high (0.9%).
|Table 1: Sociodemographic characteristics of the study participants (n=110)|
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Fasting blood glucose follow-up after transplant
On analysis, a few numbers of patients (13.6%) had impaired fasting glucose (IFG) since the 1st month, while (20%) had IFG in the 4th month after the transplant. In addition, in the 1st month after transplant, few numbers of patients (3.6%) had high FBG; while in the 2nd and 3rd month after transplant, the highest amount of patients had high FBG; (11.8%) and (10.9%), respectively as illustrated in [Table 2]. Furthermore, the vast majority of patients had low hemoglobin levels in the 1st month after transplant (96.4%), while only (18.2%) had low hemoglobin levels in the 4th month. After transplantation, serum creatinine was normal in 66.4%, while in the 6th month, it was normal in 81.8% of them. Cholesterol level was found elevated in the majority of patients during the 2nd month after transplant (71.8%).
|Table 2: Distribution of fasting blood glucose level follow-up after transplant among studied patients (n=110)|
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Tacrolimus level follow-up after transplant
Depending on kidney transplant protocol of Ahmed Gasim Hospital, immunosuppression regimens were different; depending on immunologic status of patient. In our study, the most commonly prescribed immunosuppressant regimen was regimen A (90.9%); which consist of methylprednisolone as induction therapy and tacrolimus + azathioprine + prednisolone as maintenance therapy. Among all studied patients, azathioprine was withdrawn due to its side effects; 10% were discontinued for certain period and reconstituted again. Regarding the tacrolimus levels, it was high among 70.9% of the participants after the 2nd month, 68.25% after the 3rd month, 57% after the 4th month, 52.7% after the 5th month, and 34.5% after the 6th months' posttransplant.
Regarding other drugs, calcium channel blockers were most commonly prescribed (80.9%), beta-blockers were prescribed for 27.3% and statins for 11.8%, angiotensin converting enzyme inhibitors for 21.6%. Insulin was prescribed for 17 (15.5%) and oral hypoglycemic agents for 10.9% patients after transplant. Of all studied patients, 11 (10%) developed an episode of acute rejection.
Incidence of new-onset diabetes after transplant (NODAT)
Patients who had two readings of hyperglycemia (FBG more than 126 mg/dl) in the first 6 months after transplantation was considered having NODAT, the total number of patients diagnosed with NODAT were 11 cases. Therefore, the incidence of NODAT is equal to 10%. Considering BMI, 19 (17.3%) participants were underweight, of them only 2 (10.5%) were developed NODAT while 17 (89.5%) were not. While 52 (47.3%) were had normal weight, of them 3 (5.8%) were developed NODAT. Only 2 (20.2%) participants of 10 (9.1%) obese participants were developed NODAT, while only 1 (7.1%) participant of 14 (12.7%) over weighted participants were developed NODAT. BMI records were not reported for 15 (13.6%) participants [Table 3].
|Table 3: Risk factors for the development of new-onset diabetes after renal transplant among patients with transplant recipients|
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Other risk factors related to development of diabetes were summarized in [Table 3]. Furthermore, Pearson Chi-Square test revealed that no significant associations between NODAT development with age (P = 0.56), BMI (P = 0.414), comorbidities (P = 0.715), and immunosuppressant regimens (P = 0.543). On another hand, the rejection's episodes in the study were reported in 11 (10%) of the cases, all of them were in the non-NODAT group. The association of number of rejection's episode with the presence of NODAT was not significant (P = 0.296).
Furthermore, no significant association was found between NODAT and tacrolimus level except for the tacrolimus level after the 1st month of transplantation. As those who developed NODAT, 45.5% of them had a high tacrolimus level in the 1st month of transplantation (P = 0.02). When an independent sample t-test was performed, we found that there was no significant difference between the means of concentration-dose ratios of tacrolimus throughout 6 months and the presence of NODAT (P > 0.05). Moreover, there was no significant difference between the means of tacrolimus blood level throughout 6 months and the presence of NODAT (P > 0.05) [Table 4].
|Table 4: Comparison between the means of concentration dose ratio of tacrolimus and tacrolimus blood level throughout 6 months using an independent sample t-test (n=110)|
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| Discussion|| |
Renal transplantation is a life-saving surgery indicated to patients with ESRD to prolong life and increase the survival of them. Following renal transplantation, posttransplant immunosuppressive protocols will be prescribed to provide long-term patient and graft survival. The main problem for using immunosuppressive agents is the development of adverse effects such as posttransplant diabetes. The current study was carried out to determine the incidence of NODAT among Sudanese kidney-transplanted patients. Of 110 studied patients, most of them were males (79%), and half of them were in the age group of 20–40 years (50.9%); this could be justified by the fact that elderly patients were not a candidate for surgery; due to risk of anesthesia, functional decline, and other surgery complications as clarified in a study done by Lagoo-Deenadayalan et al. Hypertension was the most common comorbid disease among the studied patients; this explained by the fact that CKD is a complication from long-term hypertension, also after transplant, hypertension is the most common condition as a complication of immunosuppressants. On the other hand, the vast majority of patients had low hemoglobin level before transplant and in the early period after transplant; this can be attributed to erythropoietin dysfunction due to CKD, and the possible explanation for low hemoglobin level in the early period after transplant is that blood loss related to the surgical procedure, and subsequent inflammation, the effects of delayed graft function, induction therapy causing bone marrow suppression, and the abrupt cessation of erythropoietin administration may play an important role in the development of anemia during this period. In addition, it was observed in this study that some patients had abnormalities in lipid profile readings after transplantation as reported in Iran and the Symphony study; this could be due to immunosuppressants effect.,
Concerning immunosuppressant regimen, the most commonly prescribed regimen which consists of methylprednisolone as induction therapy and tacrolimus + azathioprine + prednisolone as maintenance therapy; and this reflects adherence of prescribers to local hospital protocol, and similar to the National Kidney Foundation Kidney Disease Outcome Quality Initiative clinical practice guidelines and European Best Practice Guidelines. Among all studied patients, azathioprine was withdrawn due to its side effects, 10% were discontinued for a certain period and then was reinitiated again; the side effects that led to its discontinuation either elevated liver enzymes or pancytopenia as mention in a study done by Boer and his colleges. The reported incidence of elevated FBG as stated by more than 126 mg/dl were 11 (10%) patients throughout 6 months; actually, incidence may be more than estimated, but the number of unreported FBG was high. In spite of the fact, we have many missed data. Interestingly, the incidence of NODAT is consistent with that published in Japan.
Correlational tests were done between the incidence of NODAT and age, gender, BMI, comorbidities, tacrolimus level, immunosuppressant regimens, antihypertensive medication, and the episode of acute rejection; the results which were inconsistent with other studies,, this may be due to small size of the studied population. In spite of the fact that increasing weight is the most potentially modifiable risk factor for NODAT in patients on the waiting list for transplantation, obesity was insignificantly associated with NODAT. Hereby, only 7% of patients were obese. This in agreement with results reported by Montori et al. Furthermore, the glycosylated hemoglobin level was not performed regularly during the follow-up period. Therefore, the incidence of NODAT may have been underestimated. Immunosuppressant regimens were not significantly associated with the incidence of NODAT in this study, unlike other studies., Some studies found some induction therapy like basiliximab was associated with increased risk of NODAT, but in this study, this association was found statistically insignificant; that may be due to the small sample size of the studied population in our study.
The association between immunosuppressant regimens and impaired fasting blood glucose (IFG) showed no significant association, unlike that reported in studies done in Hungary, France, and India, the possible explanation for that, is the small sample size.,, This may due to 100% of the patients were taking prednisolone and tacrolimus in all regimes throughout the 6 months. Tacrolimus blood level throughout 6 months after transplant was not found to be a significant predictor of NODAT, similar to results reported in studies done in Spain and Canada., Therefore, knowledge of the kidney transplant recipient about tacrolimus blood level is important for graft survival and prevention of adverse effects.
This study is not without limitations. First, it was a retrospective single-center study. Second, the main limitation of our present study was the small sample size that might prevent adequate analysis of the risks connected to NODAT. In addition, there were many missing data in the patient's medical chart and lack of computerized databases, especially the HBA1c level, which may underestimate the incidence of NODAT. Despite these limitations, the findings of the current study are interested as it is a first report indicting the incidence of posttransplant diabetes among Sudanese kidney-transplanted recipients. Thus, further studies should be conducted to assess the incidence of NODAT by including different areas and more samples of the population.
| Conclusion|| |
The incidence of NODAT in this study was 10% throughout 6 months after transplantation. The correlations between sociodemographic characteristics, immunosuppressant regimens, episode of rejection, and incidence of NODAT were statistically insignificant. Further studies should be conducted to assess the incidence of NODAT by including different areas and more samples of the population.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4]