|Year : 2016 | Volume
| Issue : 7 | Page : 24-30
|Cardiovascular and cerebrovascular comorbidities in hemodialysis patients from the Gulf Cooperation Council countries enrolled in the dialysis outcome and practice pattern study phase 5 (2012-2015)
Faissal A. M. Shaheen1, Jamal Al Wakeel2, Saeed M. G. Al-Ghamdi3, Bassam Alhelal4, Sumaya AlGhareeb5, Ali Abdulkarim Al Obaidli6, Issa AlSalmi7, Hani Ezzat Abdulaziz8, Brian A Bieber9, Ronald L Pisoni9, GCC-DOPPS 5 Study Group10
1 Saudi Center for Organ Transplantation, Riyadh, Kingdom of Saudi Arabia
2 King Saud University, Riyadh, Kingdom of Saudi Arabia
3 King Abdulaziz University, Jeddah, Kingdom of Saudi Arabia
4 Adan Hospital, Adan, Kuwait
5 Salmaniya Medical Complex, Manama, Bahrain
6 Abu Dhabi Health Services Company (SEHA), Abu Dhabi, United Arab Emirates
7 Royal Hospital, Muscat, Oman
8 Hamad General Hospital, Doha, Qatar
9 Arbor Research Collaborative for Health, Ann Arbor, MI, USA
10 List of Study Group in Acknowledgement
Click here for correspondence address and email
|Date of Web Publication||1-Dec-2016|
| Abstract|| |
To determine the prevalence of cardiovascular comorbidities and their active risk factors in the selected hemodialysis centers in the Gulf Cooperation Council (GCC) countries, the Dialysis Outcome and Practice Pattern Study (DOPPS) was performed on 40 dialysis centers in the six GCC countries from June 2012 to May 2015. There were 21 dialysis centers from Saudi Arabia, nine from the United Arab Emirates (UAE), four from Kuwait, four from Oman, two from Qatar, and one from Bahrain. There were 922 patients participating in the study; 419 patients from Saudi Arabia, 144 from the UAE, 164 from Kuwait, 89 from Oman, 58 from Qatar, and 25 from Bahrain. Baseline data and laboratory investigations were obtained from every study patient, and the patients with any new events, change of dialysis prescription, or death were reported to the DOPPS main center during follow-up. The median age of the patients in the GCC centers was 55 years (range 32- 80 years), and the median percentage of males was 57%. The most common cause of chronic kidney disease among the study patients was diabetes mellitus (median: 43%) followed by hypertension (median: 29%) and glomerulonephritis (median: 9%). Hypertension (median 90%) and diabetes mellitus (median 52%) were the most common predisposing comorbidities to cardiovascular events in the study patients. The median ratios of patients with coronary artery disease, peripheral vascular disease, and congestive heart failure were 34%, 23%, and 24%, respectively. The median ratio for cerebrovascular comorbidities was 9%. The median prevalence of the factors that may predispose to the cardiovascular and cerebrovascular comorbidities such as gender of the patients, adequacy of dialysis, diabetes, hypertension, hypercholesterolemia, levels of anemia, parathormone levels, and calcium and phosphorus levels in the GCC countries were comparable with those in the previous DOPPS in other countries.
|How to cite this article:|
Shaheen FA, Al Wakeel J, Al-Ghamdi SM, Alhelal B, AlGhareeb S, Al Obaidli AA, AlSalmi I, Abdulaziz HE, Bieber BA, Pisoni RL, GD. Cardiovascular and cerebrovascular comorbidities in hemodialysis patients from the Gulf Cooperation Council countries enrolled in the dialysis outcome and practice pattern study phase 5 (2012-2015). Saudi J Kidney Dis Transpl 2016;27, Suppl S1:24-30
|How to cite this URL:|
Shaheen FA, Al Wakeel J, Al-Ghamdi SM, Alhelal B, AlGhareeb S, Al Obaidli AA, AlSalmi I, Abdulaziz HE, Bieber BA, Pisoni RL, GD. Cardiovascular and cerebrovascular comorbidities in hemodialysis patients from the Gulf Cooperation Council countries enrolled in the dialysis outcome and practice pattern study phase 5 (2012-2015). Saudi J Kidney Dis Transpl [serial online] 2016 [cited 2017 Jan 20];27, Suppl S1:24-30. Available from: http://www.sjkdt.org/text.asp?2016/27/7/24/194886
| Introduction|| |
The cardiovascular comorbidities among hemodialysis (HD) patients have been linked to morbidity and mortality in this population. ,,, The original kidney diseases could be secondary to systemic immunological (e.g., lupus nephritis and vasculitis) or non-immunological diseases (hypertension and diabetes mellitus). The patients with active systemic diseases that cause chronic kidney disease (CKD) have a higher risk for cardiovascular and cerebrovascular complications with mortality rate more than those with primary kidney disease. ,,,
Once established, advanced CKD becomes an independent risk factor for the cardiovascular and cerebrovascular complications through the metabolic and hormonal disturbances including hyperparathyroidism and vascular metastatic calcifications. ,, Even the state of malnutrition and the state of inflammation induced by uremia accelerate atherosclerosis in the vessels and cause further damage to the cardiovascular system. ,
Dialysis as a method of renal function replacement therapy may not resolve or control many of the cardiovascular comorbidities,  and various factors related to prescription of dialysis such as inadequate dialysis and ultrafiltration may adversely affect the cardiovascular system. , Moreover, the risk of systemic inflammation is increased due to certain practices (e.g., infected catheters used as accesses for HD). 
Epidemiological studies such as Dialysis Outcome and Practice Pattern Study (DOPPS), is a comparative observational multinational study to determine the differences and similarities of dialysis practices globally.  The study was carried out in phases, and in its phase 5, it involved the Gulf Cooperative Council (GCC) countries, which have six states in its membership including Bahrain, Kuwait, Qatar, Saudi Arabia, Oman, and the United Arab Emirates (UAE).
The aim of this study was to determine the prevalence of cardiovascular comorbidities and their active risk factors in the HD centers in the GCC countries and to compare them with those in the other countries in the world.
| Patients and Methods|| |
The DOPPS was carried out at 40 dialysis units in the six GCC countries from June 2012 to May 2015. There were 21 dialysis centers from Saudi Arabia, nine centers from the UAE, four centers from Kuwait, four centers from Oman, two centers from Qatar, and one center from Bahrain. There were 922 patients participating in the study. The distribution of patients was as follows: 419 patients from Saudi Arabia, 144 patients from the UAE, 164 patients from Kuwait, 89 patients from Oman, 58 patients from Qatar, and 25 patients from Bahrain. The baseline data on the patients included age, gender, body mass index (BMI), smoking habits, dialysis duration (vintage) and prescription, the social status and life, primary cause of ESRD, comorbidities including the cardiovascular and other systems, and medications (iron, erythropoietin, antihypertensive agents, Vitamin D, and cinacalcet). In addition, the quality of life was reported based on its physical and mental components.
The laboratory investigations included hemoglobin, ferritin, transferrin saturation (TSAT) albumin, normalized protein catabolic rate (PCR), total calcium, phosphorus, parathormone, creatinine, serum sodium, serum potassium, total cholesterol, and C-reactive protein.
During follow-up, the patients with any new events, change of dialysis prescription, or death were reported to the DOPPS main center during the three years of the study.
| Results|| |
The median age of the patients in the GCC centers was 55 years (range 32-80 years), and the median percentage of males was 57%. The median percentage of non-smokers was 58%. The median BMI was 25.3. The median percentage of patients with urine output more than 200 mL/day was 55% (range: 29-70%).
The median duration (vintage) on dialysis for the patients was 2.9 years. On average, 89% (range: 79-98%) of the patients received 3 times per week dialysis with a median treatment time of 210 min of dialysis each session. The median single pool Kt/V for the patients was 1.33. The median interdialytic weight gain for the patients was 3.4 kg. The medians of systolic and diastolic blood pressure measurements of patients before dialysis sessions were 145 and 76 mm Hg, respectively.
The most common cause of CKD in the study patients was diabetes mellitus (median: 43%) followed by hypertension (median: 29%) and glomerulonephritis (median: 9%).
The median levels of the laboratory parameters in the study patients were as follows: hemoglobin 10.9 g/L, ferritin 394 ng/mL, TSAT 26%, albumin 3.50 g/dL, normalized PCR 0.85, total calcium 8.7 mg/dL, phosphorus 4.90 mg/ dL, parathormone 295 pg/mL, cholesterol 144 mg/dL, C-reactive protein 28 mg/L, s. sodium 137 mmol/L, and potassium 4.90 mmol/L.
The median percentage of the study patients treated with erythropoiesis-stimulating agent was 87% with a median dose of 8700 units/ week, and the median i.v. iron dose per month was 333 mg. The median percentage of patients treated with phosphate binders was 81.4% and 65% with calcium-based phosphate binders. The median percentage of patients treated with oral Vitamin D was 36%, whereas it was 62% for patients treated with oral and i.v. Vitamin D. There were 23% patients on cinacalcet for the treatment of hyperparathyroidism. The median ratios of patients treated with calcium channel blockers and beta blockers for hypertension were 31% and 25%, respectively, while much fewer patients were being treated with angiotensin receptor blockers and converting enzyme inhibitors with median ratios of 5% and 6%, respectively. The median ratio of the patients treated with statins was 30%.
The median score of the physical component of the patients' quality of life was 35.0, whereas that for the mental component was 43.0 in the patients. The median of the Center for Epidemiological Studies Depression Scale was 9.0, and the depressive symptoms were evident in patients with a median value of 35%.
The most common non-cardiovascular comorbidity included hepatitis C (median 15%). The less common non-cardiovascular comorbidities included neurologic disorders (median 6%), lung disease (median 4%), recurrent cellulitis (median 8%), cancer (median 1%), gastrointestinal bleeding (median 1%), psychological disorder (median 1%), and hepatitis B (median 4%).
Hypertension (median 90%) and diabetes mellitus (median 52%) were the most common predisposing comorbidities to cardiovascular events in the study patients. The details of cardiac events or comorbidities are shown in [Table 1]. The median ratio of patients with coronary artery disease comorbidity was 34%, included prior diagnosis of coronary heart disease/CAD (median 28%), history of angina (median 19%), myocardial infarction ever (median 8%), coronary artery bypass surgery (median 6%), and angioplasty or stent (median 7%). The peripheral vascular disease (PVD) median ratio in the study patients was 23%, included claudication (median 17%), PVD prior diagnosis (median 7%), arterial bypass or stent for PVD (median 2%), and amputation for PVD (median 3%). The congestive heart failure (CHF) median ratio was 24%, included prior diagnosis of CHF (median 3%) and pulmonary edema (median 13%).
|Table 1: The common cardiovascular comorbidities of the dialysis patients in the Gulf Cooperative Council countries.|
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Other cardiovascular comorbidities included cardiac arrest (median 0.5%), atrial fibrillation (median 6%), other arrhythmias (median 3.5%), permanent pacemaker (median 1.5%), pericarditis (median 1%), and prosthetic heart valve (median 2%).
The median ratio for cerebrovascular comorbidities was 9%, included stroke with neurological deficit (median 5%), stroke without neurological deficit (median 4%), and transient ischemic attacks (median 1%).
| Discussion|| |
The results of the DOPPS in the GCC countries show comparable prevalence in the major categories of the cardiovascular and cerebrovascular complications in the chronic HD patients and other parts of the world.  The prevalence of coronary disease in the dialysis patients was not more than 40% of the patients, and the PVD and CHF each was encountered in <25% of the HD patients in all the centers. The CKD patients who survive the disease till they reach the stage of dialysis usually are those with the low levels of damage of cardiovascular system, whereas those with high levels of damage die at an earlier stage. , The surveys of percentages of patients in the different stages of CKD revealed that the patients in Stages 3 and 4 formed 3%-4% each of the prevalence of the disease, whereas Stage 5 formed 0.1%, which means that most patients succumb to death before reaching the stage needing dialysis. ,
Despite the low prevalence of the manifestations of cardiovascular morbidities seen in our study, the continuing risk factors of hypertension (88%) and diabetes mellitus (50%) among the HD patients in the GCC countries eventually would be responsible for more advanced damage to the cardiovascular and cerebrovascular systems and increased morbidity and mortality. ,, Moreover, the diagnosis of the status of the vascular tree in any HD patient needs meticulous testing and may not be very accurate in an epidemiological study such as the DOPPS.
Old age is a risk factor for the incidence and prevalence of cardiovascular complications in the general population;  the complications appear earlier in the CKD patients compared with the general population and the cardiovascular system in the young HD patients may behave similar to that in the persons with advanced age.  However, the significant finding of younger age population of HD dialysis patients in the GCC centers compared with those in the other parts of the world was intriguing, since the prevalence of the cardiovascular and cerebrovascular complications was similar in all the centers; the GCC HD patients had more compromised cardiovascular systems at a younger age. This could be peculiar to the population in the GCC countries and may be genetic in nature or due to less compliance with medications prescribed to them. The dialysis prescription data in the study patients did not reveal any significant contribution to the explanation. The adequacy of dialysis was comparable between all centers in the GCC. The metabolic disturbances including hyperparathyroidism and calcium and phosphorus levels were also comparable. The other risk factors that predispose to the cardiovascular and cerebrovascular complications including the male gender, obesity, and C-reactive protein and hypercholesterolemia levels in the GCC patients were also comparable among the centers. The prevalence of the habit of smoking tobacco was higher (40% among the GCC HD patients). The status of malnutritioninflammation and atherosclerosis (MIA) syndrome was not well defined in the study population and depended on limited data from the centers.
The limitations of this study include small patients sample contributed from some GCC countries such as Bahrain and Qatar, but taken collectively the limitations in the GCC may seem minor. In addition, inadequate reporting from some centers about several parameters such as inadequate data about how some of the complications were diagnosed such as the coronary artery disease. As an observational study, DOPPS may generate hypotheses to be tested in the GCC countries in further future studies.
| Conclusion|| |
The DOPPS is a tool to compare the different dialysis populations around the world. The GCC countries had a similar profile of prevalence of cardiovascular and cerebrovascular complications in a relatively young age population. The cause of that is clear and may need larger future studies.
| Acknowledgments|| |
The authors wish to thank the devoted efforts of GCC-DOPPS 5 Study Group members for their numerous contributions to this study including Country Investigators (Dr. Sameer Al-Arrayed, Dr. Sumaya Al Ghareeb, Dr. Bassam Al Helal, Dr. Naser Alkandari, Dr. Ali Alsahow, Dr. Anas AlYousef, Dr. Mohammad AlAzmi, Dr. Yaqob Ahmed Almaimani, Dr. Issa Alsalmi, Dr. Nabil Salmeen Mohsin, Dr. Fadwa Al Ali, Dr. Mohamed El-Sayed Abdel Fatah, Dr. Ashraf Fawzy, Dr. Abdulla Hamad, Dr. Saeed M. G. Al-Ghamdi, Dr. Mohammed Al Ghonaim, Dr. Jamal Al Wakeel, Dr. Fayez Hejaili, Dr. Ayman Karkar, Dr. Faissal Shaheen, Dr. Samra Abouchacra, Dr. Ali Abdulkarim Al Obaidli, Dr. Mohamed Hassan, Dr. Mona Nasir Al Rukhaimi, Dr. Abdul Kareem Saleh, Dr. Sylvia Ramirez, Dr. Bruce Robinson, and Dr. Ronald Pisoni), Clinical Research Associates and Project Coordinators/Managers (Dr. Amgad El-Baz El-Agroudy, Dr. Balaji Dandi, Ms. Cherry Flores, Mrs. Ph. Fatma Al Raisi, Ms. Ibtisam Al-Hasni, Dr. Ashraf Fawzy, Dr. Haroun Zakaria Ahmed, and Mr. Dan Santiago from the Saudi Center for Organ Transplantation; Mr. Muhammad Awwad, Ms. Roberta Al HousaniBlakely, Christina Pustulka, Anne Vandermade, Melissa Fava, Anna Hogan, Michelle Maxim, Justin Albert), Biostatisticians (Brian Bieber), and Study Site Medical Directors, and Study Coordinators: Dr. Hamid Ali Alyousif, Ms. Sohair Abdulroof Albably, Dr. Ahmed EidAlkady, Dr. Samir Al Muielo, Dr. Fakreldein Elamien Ali, Dr. Ayman El Monger, Dr. Sameh Mohammed Al-sammad, Dr. Baraa Rajab, Dr. AtifHanan, Tarek Abdelfattah Ahmed Ali, Dr. Ayman Karkar, Dr. Mohammed Abdelrahman, Dr. Mohammed Hussein, Dr. Wael Abdlah, Dr. Faisal Mushtaq, Dr. Salah Eldin El Sheik Beshir, Dr. Medhat Abdelmonem Shalaby, Dr. Mustafa Khaleel Al Obeid, Dr. Mohamad El Hadary, Dr. Alaa Al Shamy; Dr. AboudMamari, Dr. Mohammed Raily, Dr. Mustafa Ahmed; Ramzi Abou-Ayache, Dr. Hormoz Dastoor, Dr. Mohamed Hassan, Dr. Bassam Bernieh, Dr. Hareth Muthanna Mohammed Saaed, Dr. Mustafa Kamel, Prof. Abdel Basset Hassan, MD, PhD, FASN, Dr. Hassan Khammas, Dr. BalajiDandi, Dr. Sumaya Al-Ghareeb, Dr. Fadwa Al Ali, Dr. Anas Alyousef, Dr. Nasser AlKandari, Dr. Ali Alsahow, Dr. Bassam AlHelal, Dr. Ahmed Mandour, Dr. Yaqob Ahmed Almaimani, Dr. Amer Ahmed Alaamri, Dr. Ibrahim Sayed Ibrahim, Dr. El Badri Abdelgadir, Dr. Mohammed Al-Sayed Seleem, Dr. Ali Hassan Hakami; Dr. Samir Beshay, Dr. Nayer Morsy, Mr. Menwer Al-ofi, Ms. Sohair Abdulroof Albably, Dr. Huda Mohammed Saeed Ahmed, Ola Al-Marhoon; Dr. Samir Al Muielo, Ms. Joynalyn Barrios, Ms. Fatima Cruza; Ligaya Battad, Mr. Abdullah A. K. Al Harbi, Dr. Sameh Mohammed Al-sammad, Ms. Manal Ahmed Hamdan, Jennifer Samson, Mr. Ahmed Mousa Khawaji, Ms. Eman Al-Hejji, Ms. Rosalinda Lamis, Ms. Lagrimas Codotco, Dr. Wael Abdlah, Mrs. Priyanka Prasad, RN, Mr. Bander Faisal Justinia, Mr. Faisal Al Enazy, Sarah Brazil, Dr. Naemah Abdullah, Dr. Alaa Al Shamy, Dr. AboudMamari, Mely Gari Piling, Dr. Fakhriya Al Alwai, Rusmina Binti Sudin, Dr. Chandra Mauli Jha, MD; Katheryn Jamilano, Basima Khaddah, Hilal Al Rasbi, Muhy Eddin Hashem Hasan, Sr. Ekram Awadh Salem, Walid Gouiaa, Mini Issac, Jiby Mammen, Mary Ellen Monday, Mrs. Afrah Al Jamri, Mr. Yasser Khalil Abbas, Mrs. Rania Abd El-Aziz, Rania Abd El-Aziz, Cherry Flores, Mini Kumari Ramakrishnan, Shanty Mannaraprayil, Maria Charisse Bernardo, Bassam AlHelal, Evangeline Valdez, Rosily Joseph, Mrs. Ghaniyaal Shukaili, Adel Mohamed Bayoumy, Hamid Alshahri, Amira Balkhair, Amina Said Al Shezawi, Sultan Saif Ali Alroshdi, Dr. Shaninaz Faisal Bashir, Dr. Ahmed Mousa Dawood, Keirin Porras, Dr. Anthonimuthu Victor, and Mr. Sultan Al-Toqi.
| Source of Support|| |
The DOPPS Phase 5 Study in the GCC has been supported by Amgen without restrictions on publications. The DOPPS Program is supported by Amgen, Kyowa Hakko Kirin, AbbVie Inc, Sanofi Renal, Baxter Healthcare, and Vifor Fresenius Medical Care Renal Pharma, Ltd. Additional support for specific projects and countries is also provided by Amgen, BHC Medical, Janssen, Takeda, and Kidney Foundation of Canada (for logistics support) in Canada; Hexal, Deutsche Gesellschaft für Nephrologie (DGfN), Shire, and WiNe Institute in Germany; and the Japanese Society for Peritoneal Dialysis for Peritoneal Dialysis Outcomes and Practice Patterns Study in Japan. Funding for the DOPPS Program is provided without restrictions on publications.
Conflict of interest: None declared.
| References|| |
Parfrey PS, Foley RN. The clinical epidemiology of cardiac disease in chronic renal failure. J Am Soc Nephrol 1999;10:1606-15.
Collins AJ, Foley RN, Herzog C, Chavers B, Gilbertson D, Herzog C, et al. US renal data system 2012 annual data report. Am J Kidney Dis 2013;61 1 Suppl 1:A7, e1-476.
Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, et al. Kidney disease as a risk factor for development of cardiovascular disease: A statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 2003;108: 2154-69.
Weiner DE, Tighiouart H, Amin MG, Stark PC, MacLeod B, Griffith JL, et al. Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: A pooled analysis of community-based studies. J Am Soc Nephrol 2004;15:1307-15.
Barrera-Vargas A, Quintanar-Martínez M, Merayo-Chalico J, Alcocer-Varela J, GómezMartín D. Risk factors for systemic lupus erythematosus flares in patients with end-stage renal disease: A case-control study. Rheumatology (Oxford) 2016;55:429-35.
Flossmann O. Risks of treatments and long-term outcomes of systemic ANCA-associated vasculitis. Presse Med 2015;44(6 Pt 2):e251-7.
Ku E, Glidden DV, Johansen KL, Sarnak M, Tighiouart H, Grimes B, et al. Association between strict blood pressure control during chronic kidney disease and lower mortality after onset of end-stage renal disease. Kidney Int 2015;87:1055-60.
Bejan-Angoulvant T, Bergerot C, Juillard L, Mezergues A, Morelon E, Pouteil-Noble C, et al. Myocardial microvascular disease and major adverse cardiovascular events in patients with end-stage renal disease: Rationale and design of the MICROCARD study. Nephrol Dial Transplant 2012;27:2886-91.
Block GA, Klassen PS, Lazarus JM, Ofsthun N, Lowrie EG, Chertow GM. Mineral metabolism, mortality, and morbidity in maintenance hemodialysis. J Am Soc Nephrol 2004;15:2208-18.
Goodman WG, Goldin J, Kuizon BD, Yoon C, Gales B, Sider D, et al. Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N Engl J Med 2000;342:1478-83.
Goodman WG, London G, Amann K, Block GA, Giachelli C, Hruska KA, et al. Vascular calcification in chronic kidney disease. Am J Kidney Dis 2004;43:572-9.
Cheung AK, Sarnak MJ, Yan G, Dwyer JT, Heyka RJ, Rocco MV, et al. Atherosclerotic cardiovascular disease risks in chronic hemodialysis patients. Kidney Int 2000;58:353-62.
Ducloux D, Bresson-Vautrin C, Kribs M, Abdelfatah A, Chalopin JM. C-reactive protein and cardiovascular disease in peritoneal dialysis patients. Kidney Int 2002;62:1417-22.
Rahman M, Fu P, Sehgal AR, Smith MC. Interdialytic weight gain, compliance with dialysis regimen, and age are independent predictors of blood pressure in hemodialysis patients. Am J Kidney Dis 2000;35:257-65.
Selby NM, McIntyre CW. The acute cardiac effects of dialysis. Semin Dial 2007;20:220-8.
Herzog CA, Ma JZ, Collins AJ. Poor long-term survival after acute myocardial infarction among patients on long-term dialysis. N Engl J Med 1998;339:799-805.
Roca-Tey R, Arcos E, Comas J, Cao H, Tort J; Catalan Renal Registry Committee. Starting hemodialysis with catheter and mortality risk: Persistent association in a competing risk analysis. J Vasc Access 2016;17:20-8.
Goodkin DA, Bragg-Gresham JL, Koenig KG, Wolfe RA, Akiba T, Andreucci VE, et al. Association of comorbid conditions and mortality in hemodialysis patients in Europe, Japan, and the United States: The Dialysis Outcomes and Practice Patterns Study (DOPPS). J Am Soc Nephrol 2003;14:3270-7.
Thambyrajah J, Landray MJ, McGlynn FJ, Jones HJ, Wheeler DC, Townend JN. Abnormalities of endothelial function in patients with predialysis renal failure. Heart 2000;83:205-9.
Sharma S, Farrington K, Kozarski R, Christopoulos C, Niespialowska-Steuden M, Moffat D, et al. Impaired thrombolysis: A novel cardiovascular risk factor in end-stage renal disease. Eur Heart J 2013;34:354-63.
Fink HA, Ishani A, Taylor BC, Greer NL, MacDonald R, Rossini D, et al. Screening for, monitoring, and treatment of chronic kidney disease stages 1 to 3: A systematic review for the US Preventive Services Task Force and for an American College of Physicians Clinical Practice Guideline. Ann Intern Med 2012;156: 570-81.
Coresh J, Astor BC, Greene T, Eknoyan G, Levey AS. Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey. Am J Kidney Dis 2003;41:1-12.
Van Dijk PC, Jager KJ, Stengel B, GrönhagenRiska C, Feest TG, Briggs JD. Renal replacement therapy for diabetic end-stage renal disease: Data from 10 registries in Europe (1991-2000). Kidney Int 2005;67:1489-99.
Schroijen MA, van de Luijtgaarden MW, Noordzij M, Ravani P, Jarraya F, Collart F, et al. Survival in dialysis patients is different between patients with diabetes as primary renal disease and patients with diabetes as a comorbid condition. Diabetologia 2013;56:1949-57.
Gupta J, Mitra N, Kanetsky PA, Devaney J, Wing MR, Reilly M, et al. Association between albuminuria, kidney function, and inflammatory biomarker profile in CKD in CRIC. Clin J Am Soc Nephrol 2012;7:1938-46.
Manjunath G, Tighiouart H, Coresh J, Macleod B, Salem DN, Griffith JL, et al. Level of kidney function as a risk factor for cardiovascular outcomes in the elderly. Kidney Int 2003;63: 1121-9.
Faissal A. M. Shaheen
Saudi Center for Organ Transplantation, P. O. Box 27049, Riyadh 11417
Kingdom of Saudi Arabia