Abstract
Overweight and obesity are associated with increased cardiovascular risk. Some studies have demonstrated that they also can result in renal damage. The aim of this study was to assess the prevalence of renal insufficiency (RI), defined as a GFR <60 ml/min per 1.73 m2, in a cohort of 4585 patients who attended primary care with essential hypertension and a body mass index ≥25 kg/m2. The patients were classified as overweight and obese according to body mass index (25 to 29.9 and ≥30 kg/m2, respectively). Abdominal obesity was defined as a waist circumference ≥88 and 102 cm in women and men, respectively. Both groups had a high prevalence of metabolic syndrome (Adult Treatment Panel III). The prevalence of RI was high in both the overweight group (22.7%; 95% confidence interval [CI] 20.6 to 24.9) and in the obese group (22.8%; 95% CI 21.0 to 24.7). The presence of diabetes increased the risk for RI (odds ratio 1.83; 95% CI 1.55 to 2.16). The prevalence of RI was greater in patients with abdominal obesity (23 versus 17%; P < 0.001). In the presence of abdominal obesity, cardiovascular risk factors and components of the metabolic syndrome also were more prevalent. The higher risk for RI with abdominal obesity persisted even after adjustment for dyslipidemia, elevated blood glucose levels, and other variables that are associated with RI (adjusted odds ratio 1.40; 95% CI 0.84 to 2.33). It was concluded that patients who have hypertension and visceral obesity and attend primary care present a higher prevalence of metabolic syndrome and RI.
Chronic kidney disease (CKD) is a widely known cardiovascular risk factor. Renal insufficiency (RI) and micro- or macroalbuminuria, both manifestations of CKD, are associated with increased cardiovascular morbidity and mortality (1–4).
The application of equations to estimate GFR has revealed an important and growing prevalence of CKD, associated with vascular events both in population-based studies and in patients with cardiovascular risk factors (5,6). Some epidemiologic studies have demonstrated an association between obesity and CKD. A high body mass index (BMI) increases the risk for a reduced GFR in both men and women (7). Obesity can be associated with glomerulosclerosis and also can facilitate a loss of renal function in patients with other kidney diseases (8,9). The risk for presenting RI as defined by a GFR <60 ml/min per 1.73 m2 and end-stage renal failure as defined by the need for kidney transplant or dialysis increases with the rise in BMI (10,11).
It therefore is likely that increased prevalence of CKD could be due, at least partially, to an increase in comorbidities such as overweight and obesity and the combination of associated hemodynamic and metabolic disorders that result in metabolic syndrome (MS). Awareness of the association between overweight/obesity and RI is important to adopt preventive and therapeutic measures for this risk factor of CKD. The present study assessed the prevalence of one specific manifestation of CKD, low GFR, in patients with essential hypertension and overweight/obesity seen in primary care.
Materials and Methods
This cross-sectional, multicenter study recruited a total of 4585 patients who attended Spanish primary care centers, previously received a diagnosis of essential hypertension, and a had body mass index (BMI) ≥25 kg/m2. Each investigator included four patients with hypertension and overweight (BMI 25 to 29.9 kg/m2) and four patients with hypertension and obesity (BMI ≥30 kg/m2). BP measurements were performed with a validated semiautomatic apparatus (Omron, Banockburn, IL) with a cuff size adapted to the arm circumference. Patients were considered to have hypertension when they had previously received a diagnosis of this condition and/or were taking antihypertensive treatment. The presence of abdominal obesity was defined by a waist circumference ≥88 cm (female) and ≥102 cm (male). Patients were considered to present MS when they fulfilled defining criteria of the Adult Treatment Panel III (12). The comparative data using the criteria established by the International Diabetes Federation also were included (13). Patients were considered to have diabetes when they had previously received a diagnosis of this condition and/or were taking antidiabetic treatment. All patients were asked about their smoking habits and the presence of any previous cardiovascular disease (ischemic heart disease, heart failure, stroke, or peripheral arterial disease) and any manifestation of chronic renal disease (renal insufficiency, hematuria, or proteinuria).
Within 7 d, the following parameters were analyzed in plasma after 8 h of fasting: Glucose, HbA1c, cholesterol, LDL cholesterol, HDL cholesterol, triglycerides, and creatinine. GFR was estimated from the serum creatinine using the simplified Modification of Diet in Renal Disease (MDRD) (14) and Cockroft-Gault (C-G) equations (15). The degree of renal function was established according to National Kidney Foundation guidelines (16). RI was defined as a GFR by MDRD <60 ml/min per 1.73 m2.
The primary objective of the Factores Adicionales que dificulTan el control en Hipertensos obesos (FATH) study was to analyze the prevalence of MS in patients with essential hypertension and overweight/obesity. In this post hoc substudy, the objective was to study the prevalence of RI in this population.
Statistical Analyses
Variables are expressed as the mean (SD) or frequency (95% confidence interval [CI]). Patients were classified by BMI into overweight or obese patients and by waist circumference into abdominal obesity/no abdominal obesity. The χ2 test was used to compare proportions of overweight and obese patients. Comparison of means between overweight and obese patients and between abdominal obesity or not was done using the t test. Consistency between GFR by MDRD and by C-G was estimated using the Bland-Altman method. Logistic regression was applied to estimate the risk of GFR <60 ml/min per 1.73 m2 as a result of the presence of abdominal obesity before and after adjustment for other covariates. Two-tailed comparisons were made throughout, and P < 0.05 was considered statistically significant. The analysis was carried out using SPSS for Windows (version 12.0; SPSS, Chicago, IL).
Results
A total of 2206 men and 2379 women with a mean age of 61.9 yr (10.6 yr) were studied. Of these, 32.9% (95% CI 30.7 to 33.4) had previously received a diagnosis of diabetes; 3.6% (95% CI 3.10 to 4.2%) were aware that they had chronic renal disease. Table 1 shows the characteristics of patients who were classified according to BMI into overweight or obese patients. The mean values of waist circumference were higher in the obese group, who also presented higher plasma glucose concentrations and a higher degree of dyslipidemia. The prevalence of MS by Adult Treatment Panel III criteria was 80.2% (95% CI 78.01 to 82.26) and 92.83% (95% CI 91.5 to 94.5) in the overweight and obese groups, respectively (P < 0.0001) and when International Diabetes Federation criteria were applied was 85.37 (95% CI 83.4 to 87.18) and 95.12 (95% CI 94.01 to 96.01) of the overweight and obese patients, respectively. There was a higher prevalence of diabetes in the obesity group. The overweight patients had similar systolic BP and diastolic BP values to those of the obese patients. There was a higher prevalence of smokers in the overweight group (28.9 versus 23%; P < 0.0001). The GFR by C-G was higher than that calculated by MDRD with a mean difference of 4.72 ml/m per 1.73 m2 in the overweight group and 24.7 ml/m per 1.73 m2 in the obesity group (Figure 1).
Bland-Altman plot comparing two methods to estimate the GFR (Cockroft-Gault and MDRD) in overweight (A) and obese (B) hypertensive patients.
Characteristics of the patientsa
There were no significant differences in the prevalence of renal insufficiency (GFR <60 ml/m per 1.73 m2) between overweight and obese patients (23% [95% CI 21 to 25%] versus 23% [95% CI 21 to 25%]; Table 2). In both the overweight and the obese groups, patients with diabetes had a higher prevalence of RI (30.1% [95% CI 24.4 to 32.9] versus 19.2% [95% CI 17.6 to 20.8; P < 0.0001] in the obese group and 29.1% [95% CI 24.6 to 33.9] versus 20.1% [95% CI 18.0 to 22.9] in the overweight patients). The risk for a GFR 30 to 60 ml/m per 1.73 m2 was 83% greater (odds ratio 1.83; 95% CI 1.55 to 2.16) in the presence of diabetes. When the distribution of GFR along quartiles of waist circumference was analyzed, there was a larger proportion of patients with GFR >90 ml/m per 1.73 m2 in the higher percentiles of waist circumference (P = 0.008 for the trend). A higher prevalence of RI was observed in patients with abdominal obesity (Table 2). The distribution of risk factors in patients with abdominal obesity is shown in Table 3. Patients with abdominal obesity tended to be older and to present more metabolic alterations and obesity (BMI ≥30 kg/m2). The presence of abdominal obesity increased the risk for presenting a GFR <60 ml/min per 1.73 m2 by 55%. After adjustment for all of the components of the MS, this risk was only slightly reduced (odds ratio 1.51; 95% CI 1.13 to 2.01).
GFR and prevalence of renal insufficiency (GFR <60 ml/min per 1.73 m2) according to BMI group and abdominal obesity
Proportion of patients with cardiovascular risk factors according to abdominal obesity
Discussion
This study shows a very high prevalence (23%) of RI (GFR by MDRD <60 ml/m per 1.73 m2) in a relatively large cohort of adult hypertensive patients with overweight/obesity. Given the difficulties with accurate estimation of GFR and the limitations of calculating GFR on the basis of serum creatinine alone, there is an increased interest in the use of equations (MDRD and C-G). These equations include variables such as age, weight, gender, and race and show a good correlation with accurate markers of GFR (17). When comparing both equations, the GFR values that were obtained with the C-G method were higher, and the differences were larger with higher BMI values. Other studies have shown that, in the presence of obesity/overweight, the C-G method overestimates GFR and consider the MDRD equation, especially in cases of reduced GFR, to be more accurate (18,19).
In the Spanish population pilot study, the prevalence of GFR <60 ml/m per 1.73 m2 was 5.1% (20), similar to that (5% of the population) performed in >500,000 patients in a Canadian population (21). However, when patients with hypertension are studied, there is a greater prevalence of RI. In a cohort of 721 patients who had essential hypertension, a mean age of 56 yr, and a BMI of 28.9 kg/m2 and attending a hospital clinic, a GFR <60 ml/min per 1.73 m2 was observed in 16.2% of the patients (22). In another recently published study (23), the prevalence of a GFR <60 ml/min per 1.73 m2 by MDRD in 13,687 patients who had hypertension and were seen in primary care in Spain was 27.7%. Patients who were included in this study were of similar characteristics to our study group. Most of them were overweight or obese, only 17% had normal body weight, and 30.6% had diabetes. The older age (mean 68.1 yr) could explain the higher prevalence of RI than that observed in our population. In the MicroAluminuria en pacientes con glucemia Basal ALterada (MAGAL) study published in this issue (24), the prevalence of RI in patients with hypertension and microalbuminuria was 19.9%, but 10% of these patients had BMI <25 kg/m2.
Given the coexistence of hypertension and overweight/obesity in our patients, it is difficult to establish the significance of each of these in the development of kidney damage. Both in hypertension and in overweight/obesity, as well as in diabetes, glomerular hyperfiltration can occur, which, over time, can contribute to kidney damage (25,26). Ribstein et al. (26) demonstrated in a comparative study in patients with hypertension that the presence of obesity causes a higher filtration fraction and, consequently, more microalbuminuria, thus confirming that the increase in weight intensifies hypertensive renal damage. Microalbuminuria was not measured in our study. Nonetheless, the greater prevalence of GFR >90 ml/m per 1.73 m2 in patients in the highest percentile of waist circumference suggest the presence of hyperfiltration, at least at some point during the renal life of patients with hypertension and obesity, a hyperfiltration that contributes to a steady decline of renal function. In the Hypertension Detection and Follow-Up Program (27), the incidence of chronic renal disease at 5 yr, defined by proteinuria and/or GFR <60 ml/min per 1.73 m2, was higher in patients with obesity and overweight (31 and 34%, respectively) than in hypertensive patients with ideal weight (28%).
No differences in prevalence of RI were observed between overweight or obese patients who were classified according to BMI in our study. A possible explanation is that a cutoff point of 25 kg/m2 in hypertensive patients with other risk factors already defines the increased risk for RI. Besides, BMI indicates only body corpulence, and it might be hypothesized that hypertensive patients with BMI between 25 and 29.9 kg/m2 have more body fat than nonhypertensive overweight individuals. Furthermore, it has been reported that hypertensive patients had more visceral adipose tissue accumulation, measured by multiscan magnetic resonance imaging, than nonhypertensive control subjects for a similar fat mass (28). In fact, our study shows that patients with abdominal obesity have a significantly lower GFR and that there are more patients with CKD compared with non(abdominal)obese patients, supporting the relevance of abdominal obesity in kidney damage. A study to assess body fat and its association with BMI in hypertensive patients is warranted. On the other side, it has been shown in patients without diabetes that, regardless of BMI, central distribution of fat (abdominal obesity) increases the risk for a reduction of GFR (29). The greater prevalence of RI in hypertensive patients with abdominal obesity could be due to the different metabolic alterations that frequently are associated with this type of obesity and that constitute the MS. A greater prevalence of metabolic alterations was seen in patients with abdominal obesity, although they still have a high risk for RI after adjustment for these variables. Therefore, other factors that were not determined in this study, such as hyperinsulinemia, increased sympathetic activity, renin-angiotensin system activation, inflammatory mediators, and other adipocyte-derived products, could play a role in the development of RI that is associated with abdominal obesity and MS (30). As expected, in the presence of diabetes, the prevalence of RI increased significantly in both overweight and obese patients.
Conclusion
Our study reveals that patients who have hypertension and overweight/obesity and are seen in a primary care setting show a high prevalence of MS and RI in which abdominal obesity plays an important role. Stepping up of preventive and therapeutic measures to control these frequent and important vascular risk factors therefore should be considered.
Acknowledgments
This study was supported by a Grant from Bristol-Myers Squibb.
The following investigators participated in the FATH Study: Abarca Bujan Benjamín, Abou Pestana Octavio, Abou Assali Boasli Radwan, Acedo Acedo Ángeles, Adroher Vallmajor Jordi, Aguera Mengual Fuensanta, Aguilar Jado José Manuel, Aguilera Hurtado Eva, Albarrán Juan Ma Elena, Albert Amorós Teresa, Alberto Vara Luis, Albors Valls Alberto, Alés Conejo Francisco, Alfageme Perez Jose María, Alfonso González Dacil C., Allué Callizo Davis, Almela Tejedo Teresa, Almirall Banque Carmen, Almiron Alverete Maria, Alonso Dura Carmen, Alonso Valladares Francisco, Alonso Fernandez Lola, Alonso Quintanilla Luis, Alonso Rosario, Alonso Val Antonio, Alpas Mabel, Alvarez Alvarez Alfredo, Alvarez Cosmea Artemio, Álvarez Taboas Jorge, Álvarez Gil José I., Álvaro Grande Epifanio, Alzua Blanco Luis, Amijibia Cabeza Iziar, Andrés Palomo Inmaculada, Andreu Martín Antonia, Antonio Fernandez Jose, Aparicio Velasco Josefina, Aramburu Aramburo Pedro, Arana Domenech Jesús, Arana Torres Monica, Aranda Vizcaíno Juan Jesús, Areas Medina Virginia, Argona Jesús Juan, Arias Concepción, Arias Garcia Maria Teresa, Arizaga Beatriz, Arranz Sanjurjo José Ángel, Arribas Aguirregaviría F. Javier, Arriola Mantxola Enrique, Arroyo Azpa Conchita, Artero Canals Fernando, Arteta Barrenetxea Iratxe, Aspiazu Rodríguez Juan Carlos, Ave José, Aviño Navarro Arturo, Ayala Gonzalez Ángel, Bacariza Riñón Francisco, Badell Gemma, Baeza Romero Manuel, Balaguer Belles Ismael, Balboa Jiménez José Luis, Bañuelos Gago Maria Jesús, Barbe Riesgo Margarita, Barbera Reus Ramón, Barrancos Heredia Maria Del Rosario, Barreiro Mourenian Carlos, Barrera Pinazo Rosa, Barrero Sanchez Carme, Barrios Santiago, Bartolome Resano Rafael, Basauri Bedoya Jose Manuel, Becerra Becerra A., Becerra Méndez Mercedes, Bellostas Imbert José, Benet Marti Josep Maria, Berdonces Jose L., Bernardo Quirós Victoria, Blanco Montes Jesús, Blanco Perdigón Luis, Blanco Iglesias Pedro, Blasco Lafarga Blanca, BlÁzquez Ma Luisa, Bordes García Laura, Bossom Diumenjo Maria, Botella Gregori Ana, Brunet I Costa Jordi, Burgazzoli Samper Juan Luis, Burgos Bravo Maria Jesus, Busselo Lete Luis Miguel, Buznego Álvarez Begoña, Caballe Godia José Luis, Caballero Domenech Joan Carles, Caballero Rodríguez Juan, Caballero Montanary Leonides, Cabana Gadea Andrés, Cabedo García Vicente, Cabero Garrido Manuel, Cabrera Aguilera Mercedes, Cabrera López Raúl, CaixÁs Pedragós Assumpta, Calatayud Rodríguez Antonio Luis, Calderón Pérez Rafael, Calles Romero Ignacio, Camacho Ibañez Juan Luis, Camacho Herrera Ma Jesús, Campanario Astete Pedro, Campos Rio Catherine, Campos Toimil Luis, Canales Alfredo, Candilejo Fortes Gabriela, Canelada Sanchez Jose Antonio, Cano Jiménez Agustín, Cantos Alcañiz Mari Sol, CapitÁn Caldas Mercedes, Carbonero Martínez Alejandro, Carrasco Herrera Jesus, Carreira Fonta Jose A., Carreras López Ángela, Carvajal Vión Isabel, Casado Moragón Concepción, Casado Navarro Joaquín, Casal Mendez Luis, Casanova Gil Miguel Ángel, Cascan Martín Jose Maria, Castilblanque Ballesteros Consuelo, Castillo Barea Encarnación, Castillo Ballesteros Jesus, Castrillon Rey Maria Jose, Cea Soria Luis, Celatti Gomez Blanca, Cerda Alfonso Vicente, Cerrada Machuca Maria José, Cerrato Rodríguez Maria, ChÁvez Egea Magdalena, Cinos Ramos Ma Lourdes, Clar Puig Cristina, Climent Ferri Victor, Cobas Varela Enrique, Cobos Toro Luis, Collado Navas Raquel, Conejero García Vicente, Corominas Sarrio Pilar, Correa Armero Rosario, Cortes Evaristo, Cortés Ugalde Fernando, Cortizo Torres Maria Emilia, Coscolla Checa Francisco, Costa Broch Pascual, Creixell Sanchez Jaume, Crespo Jiménez Floreal, Creus Rey Beatriz, Criado Campomanes Amparo, Cristofol López Isabel, Cruz Saldaña Francisco, Cuatrecasas Cambra Gabriel, Cuerpo Álvarez Francisco, Cuesta Menéndez Alfonso, Curado Garcia Carmen, Da Silva Gonzalez Álvaro, Daviña VÁzquez Ma Dolores, De Arriba Frade Fernando, De Barruetabeña Gutiérrez José Miguel, De Castro Peral LÁzaro, De Dios De Dios Ángel, De Dios Mora Juan, De Felipe Medina Ricardo, De Juan AlcarÁz Francisco, De Juan Puente Jesús, De La Torre Edo Jorge, De La Torre Vidal Montse, De Linares Del Río Carlos, De Rafael Marti Julio, De Tapia Polo Juan Jesús, Del Águila Padilla Pilar, Del As Gómez Enrique, Del Blanco Niembro Pablo, Del Río Bohorquez Cristobal, Del Río Alonso Jose María, Del Valle Pelayo Juan, Delgado Simón Félix, Delgado Santana Jesús, Diab Nafer, Díaz Alba Ángel, Díaz Gallardo Baltazar, Díaz Santiago Carlos, Díaz Paquez Francisco, Diaz Garcia Manuel, Diaz Jiménez Manuel, Diego Coll Carlos, Diego Dominguez Fernando, Diez Andrés María Luisa, Dominguez Velazquez Jesús, División Garrote Juan Antonio, Dolz Del Castelar Pareja Marcial, Domingo Sellart Francesc, Domingo Orduña Manuela, Dominguez Deben Daniel, Dominguez MÁrquez Juana, Domínguez Ávila JuliÁn, Dopico Perez Octavio, DurÁn Pérez Susana, Enfedaque Montes Belén, Enguidanos Garcia Marcia, Erlanz Abad Arturo, Escobar Muñoz Francisco, Escobedo Espinosa Francisca, Escorza Rodríguez Juan M., Esparcia Garcia Mariano, Espinel Álvarez José, Esplugues Chulvi Carmen, Esquembre Menor Raquel, Estables Recasens Pedro, Esteve Fuster Vicente, Exposito Coll Patricio, Falantes Parrado Manuel, Faus Mascarell Emilia, Faxas Margarita, Fernandez Dieguez Elena, Fernandez Martín JuliÁn, FernÁndez GÁlvez Cristóbal, FernÁndez Ares Jose A., FernÁndez García José María, FernÁndez Casado Pedro, Fernando López Carmen, Ferreiro Carmen, Ferrer Caballer Amparo, Fiallega Otero Rafael, Fle Pinilla Isidro, Foguet Boreu Quintí, Fonseca Capdeville Ernesto, Forcada Lozano Juan E., Fornieles Medina Miryam, Fortea Zaragoza Antonio, Fraga Cabado Jose, Fraga Diez Manuel, Francés Gómez Raquel, Franch Taix María Gemma, Franco Reche Luis, Fuentes Fernandez Fernando, Fuster Bellido Tomas, Gaisan Tomo Carmen, Galindo Tobal Francisca, Galindo Ruiz Jose M., Gallardo Díaz Miguel, Gallego Piote Sergio, Gallegos Castillero Raimundo, Garay Orte Jon, Garbayo Juan, Garchitorena Peiro Miguel, Garcia Sierra Alberto, Garcia Chevarría Belen, Garcia Galicia Félix, Garcia Jiménez Gerardo, Garcia Tell Guillermo, Garcia Nadal Ignacio, Garcia Blas J. Miguel, Garcia Campillo Joan Manuel, Garcia Sabater Joaquin, Garcia Cabarcos Jose Antonio, Garcia HernÁndez Luis, Garcia Cobelo Maria Emma, Garcia Prieto Mariano, Garcia-Reyes Ramos Mercedes, Garcia Conejero Olga, Garcia Peñafiel Rafael, Garcia Ochoa Rocío De Vicente, García García Alberto, García Vallano Isaac, García Allas Isabel, García Norro Javier, García Pérez Jordi, García Hidalgo José, García Aparicio Judit, García López Manuel, García Bernal Manuela, García Callejas Ricardo, García Urendez Jose, Garrido Sampedro Manuel, Gasalla Rodríguez Concepción, Gascó García PlÁcido, Gaspar HernÁndez Andrés, Gene García Jose R., Gené García Pedro, Gil Monje Maria, Gimenez Navarro María Antonia, Giménez Palop Olga, Giner Garrigues Francisco, Giner Lacuesta Isabel, Gippini Pérez Antonio, Girón Daviña Marta, Gispert Servitge Adria, Goikoetxea Arrillaga Alejandro, Gomara Sonia, Gómez Ruiz Javier, Gómez Gonzalez Laureano, Gómez Mendicuti Manuel, Gómez Fumero Sonsoles, Gómez Aguinaga Juan Manuel, Gómez Ribelles Rafael, Gonzalez López Belén, Gonzalez Gago Jose Antonio, Gonzalez Gonzalez Juana, Gonzalez Cuber Lamberto, GonzÁlez Lorrio Francisco, Gonzalez Gonzalez Luis, Gonzalez López Arce Luis, Gonzalez Moreiras Manuel, Gonzalez Cabrera Marcos, GonzÁlez Álvarez Antonio, GonzÁlez GalÁn Concepción, GonzÁlez Acuña Eduardo, GonzÁlez GonzÁlez Javier, GonzÁlez Rodríguez Luis, GonzÁlez Rodríguez Manuel, GonzÁlez Candela Rosario, Gonzalo Carlos, Gorriz Santamaría Elena, Gorrotxtegi Ereño Jesús, Goterris Pinto Marian, Granado Sanchez Francisco José, Gras Balaguer Santiago, Guardiola Grau Begoña, Guerrero Reina Salvador, Guillen Garcia Francisco, Guillen Hdez. Monserrat, Gutiérrez Delgado Eduardo, Gutiérrez Méndez José Luis, GuzmÁn Martí Juan A., Guzon Méndez Fernando, Helguera Jose Luis, Heredia Cabrera Francisco, Hernaez Cabañas Luis F., HernÁndez Pérez Ana, HernÁndez Surroca Daniel, HernÁndez Díaz Francisco, HernÁndez Gutiérrez Juana Isabel, HernÁndez Moreno Julio, HernÁndez Pedro, HernÁndez García Concepción, HernÁndez Rico Filomena, HernÁndez Iglesias Juan José, HernÁndez Rodríguez Maria Dolores, HernÁndez Herrera Ricardo, Herran Oteruelo Luis Ángel, Herrera HernÁndez Eduardo, Hevia Rodríguez Eduardo, Hidalgo Santiago Juan Carlos, Hinojosa Gallardo Juan Luis, Ibor Vidal Encarnación, Iglesias Fernandez Federico, Imaz Pérez Francisco, Inesta Mena Claudia, Iraola Sierra Begoña, Irizabal Navas Juan Cruz, Jane Jaures Antoni, Jiménez CÁmara Antonio, Jiménez Rodríguez Maria Ángeles, Jiménez Jerez Maria Del Carmen, Jiménez CÁmara Valentín, Jiménez Garijo Diego, Jiménez Herrera José María, Jiménez Notario Manuel, Jiménez Samper Milagros, Jorge Sanchez Ramón J., Juan Alberola Vicente, Kern Volcy Edouard José, Laborda Esteruelas Montse, Laiseca Sagardui Javier, Lalinde Herrero Martín, Lamarca Roca Angels, Lara Fornelino Luis Felipe, Lasso Oria Virginia, Latorre Atienza Marco A., Leal Correa Bartolome, Leira Paz Gloria, Lemus Gallego Juan Luis, Lezaun Indurain Ana, Lillo Gallego Paco, Linares Lorenzo Francisco, Llenares Orts José F., Llorente Gómez De Segura Iñaki, Lluna Gasco Carlos, López Abietar María Isabel, López García Celia, López Serrano Beatriz, Lopez Varela Carmen, López De La Iglesia Jaime, López VÁzquez Jose Luis, López Toledo Ma Luisa, López Quintero Purificación, López Luque Santiago Rafael, López Mitxelena Teresa, López Aisa Blanca, López Ortiz Francisco, López Cambeses Rosario, López Crespo Yolanda, Lozano Cobos Antonio, Luengo Agüero Jesus, Macia Pérez Ramón, Madero Ambrojo Emilio, Magadalena Belio José Félix, Mahiques García Elvira, Malagas Ferrera Herminio, Mansilla Rodríguez Calixta, Marco Segarra Emili, Marín De La Cueva Juan Antonio, Marín IbÁñez Alejandro, Marín Osorio Carmen, Marion Navasa Gonzalo, Marti Corominola Andreu, Martín Peces Blanca, Martín Pérez Enrique, Martín Sanchez Jose, Martín Jiménez Juan Antonio, Martín Collado Manolo, Martín BlÁzquez Mercedes, Martín Fresneda Soledad, Martín Alegre Amparo, Martín Ruiz Aurelio, Martín Domenech Ignacio, Martín Lafoz Juan Carlos, Martín Gonzalez Luis, Marín Moros José María, Martínez Garcia Agustín, Martínez Ruiz Andrés, Martínez Rosselló Antonio, Martínez Bravo Bernardino, Martínez Quess Dulce, Martínez Ortega Francisco, Martínez Piquer Joaquín, Martínez Orozco Marino, Martínez Llarena Marisa, Martínez Mercedes, Martínez Fernandez Montserrat, Martínez Pardo Rafael, Martínez Luque Francisco Javier, Martínez Martínez Ma Jesús, Martos Calzado José, Massana Toro Pere, Matellanes Matellanes Ángel, Mateos Freire Sergio, Mato Marcos Fernando, Matoses Nacher Daniel, Mayques Alos José Luis, Medina Maya Jose Antonio, Medina Cuenca Pedro, Melo Faus Juan Bta, Mena Garcia Candido, Mena Pena Maria, Méndez Gómez Begoña, Méndez Robles Jesús, Méndez Delagado Manuel, Merina Sanchez Rafael, Mesa Pedrero Carlos, Minchero Alberto, Mingo Belloso Yolanda, Minuesa Cortijo Francisco Javier, Miñana Aguado Sandra, Miñano FernÁndez Pilar, Molina Molina Felipe, Molina De Heras Miguel, Monblan Díaz Eva, Monge García José Manuel, Monraba Ferrer Jose M., Monroy Fuenmayor Nieves, Montalvillo Montalvillo Jose Luis, Montesinos E., Moñivas Lijaro Mariano, Morales Navarro Fernando, Morales Aranjuez Isabel María, Moralez Pérez Lola, Moreno Andújar Dolores, Moreno Moreno Eugenio, Morillo VÁzquez Álvaro, Mulero Garcia Maria José, Munguia Alcalde Vicente, Muñoz PelÁez Carmen, Muñoz Rodríguez J.A., Muñoz GalÁn Maria Dolores, Murguizu Garcia Ana, Murie Roig Ana, Muriel Díaz Paz, Murillo Torrado Diego, Murillo Torrado Mariano, Nader Ramirez Roberto, Nasser Rifai Adel, Navalón Martínez Amparo, Navalón Gómez Pascual, Navarro Navarrete Carmen, Navarro Pérez Jorge, Navarro Sanz Juan José, Navarro Villena Manuel, Nicolau Rerrer Francisca, Nieto Fernandez Arroyo Manuel, Nieto Hortal Pepe, Nieto Cervera Rafael, Nogales Rebollo Gregorio J., Noguera Bennaser Juan, Ocaña Cazalilla Carmelo, Ogallas Raya Fuensanta, Olalde Quintana Rafael, Oliva Gomez Fco Jose, Olivares Bautista Mari Carmen, Oliveras Montse, Oliveras Deulofeu Victor, Olmedo Peñaranda Javier, Orio Segura Esperanza, Orquín Vera Abelardo, Ortega Cantero Ángel, Ortega Cutillas Mariano, Ortega Jiménez Victor, Ortiz De Santa Maria Jose, Ortiz-Villajos Serrano Carmen, Osca Pellicer David, Osuna Dominguez José, Otero Toral Ángel, Otero Coton Jose, Otero Rodríguez Rocío, Paches Porcar Maria Dolores, Palacios Villanueva Cayetano, Palomares Moral Eduardo, Panero Alejandro, Pardo Otero Felipe, Paredes Saura José, Parralejo Cano Francisco, Pascual Fuster Vicente, Pastor Mira Percebal Isidro, Paz Rodríguez Fabiola, Pazos GonzÁlez Pilar, Peco Bermúdez Benjamín, Pedraza SÁnchez Sonia, Pellicer Muñoz Mónica, Pellit Ramil Ignacio, Pensado Pousa José, Peña Díaz Dolores, Perea Mostajo Janeth, Pereira Cuello Jesús, Pérez Pérez Carlos, Pérez Gil Javier S., Pérez Cebrian Maria José, Perez Mira Maria José, Pérez Zamora Susana, Pérez FernÁndez Aurelia, Pérez GonzÁlez Guillermo, Pérez Boronat Luis, Pérez Palmes Mari Paz, Pérez Rivero Miguel A., Perona Pagan Miguel, Picazo Romero Emilio, Piury Alonso Carlos, Pizarro López Mar, Ponce Martín Jose, Ponce Bejarano Manuel, Ponz Callen Antonio, Prat Mireia, Prieto Girón Jesús, Prieto Díaz Miguel A., Prieto Prieto Raquel, Puchades Chilet Ángeles, Pueyo Martínez Manuel, Pujol Dakme Pere, Quintana Ortíz Javier, Rabanal Carrera Sandra, Raigda Igada Guerra Antonio, Ramirez Marent Jose Ignacio, Ramírez Canca María Teresa, Ramírez GonzÁlez Rosa Ma, Ramos Rodriguez Consuelo, Ramos Martín Vidal, Razón Angulo Emilio, Regueiro Antonio, Requena Marín Carmen, Retuerta García María Dolores, Rey Gonzalez Pilar, Ribes Albert Jose, Riuas AlcÁzar Guillermo, Rivero Moreno Antonio, Roberto Echevarri Enrique, Robre Oriete Mariano, Roca Guanter Enric, Rodondo Rico Inmaculada, Rodriguez Arce Angeles, Rodríguez López Elisa, Rodríguez Vicente Isabel, Rodriguez Inchaustegui Jose Luis, Rodríguez Pino Jose Manrique, Rodríguez Sanchez Juan José, Rodríguez Apresa Ma Dolores, Rodríguez Solureano Maria Antonia, Rodríguez Rodríguez Miguel Ángel, Rodríguez HernÁndez Vidal, Rodríguez Poncela Antonio, Rodríguez López Mercedes, RoldÁn Sanchez Juan Jose, Romaní Del Castillo Javier, Romero GonzÁlez Elena, Romero Atanes Jesús, Romero Martín Julia, Rosa Gil Luis, Rubio HernÁndez Jose Félix, Rudolphi Carralero Teodoro, Ruiz Comellas Anna, Ruiz Diez Dolores, Ruiz Ferrando Ernestina, Ruiz Franzi Ignacio, Ruiz De Gordeguela Julio, Ruiz Pastor Luis, Ruiz Fernandez Manuel, Ruiz Aragón Rosalía, Ruvira Martínez Ernesto, SacristÁn Rubio Alberto, SÁenz Galeano Antonio, Sainz Salazar Ma Félix, Saiz Jose Antonio, Salas Fernando, Salas Tomas, Salgado Cachofeiro José Alfonso, Salgado Nieto Vicente, Sanchez Calso Antonio, Sanchez Garcia Fernado, Sanchez Mate Isabel, Sanchez Moran Isabel, Sanchez Viel Isabel, Sanchez Prieto Jaime, Sanchez Coureiro Manuel, Sanchez Santos Natividad, SÁnchez Berbel Baldomero, SÁnchez Carrillo Santiago, Sancho Soriano Natividad, Saniger Herrera José Manuel, Sanmartín Almenar Ana, Sansano Trives Rosario, Santana Benítez Jesús, Santiago SÁez Andrés, Santiago Antonio, Santos Altozano Carlos, Santos Bueso Isabel María, Santos Godoy Rafael, Sanz Rebollo Gloria, Sanz García Juan José, Sanz Bailón Luis, Sarria Ferrada Jesús, Segarra Codina Ramon, Segrera Manzano Silvia, Serrano Contreras Benjamín, Serrano Valverde Leticia, Serrano-Guerra Librero Fco. Javier, Silva Silva Manuela, Simón Gutierrez Raul, Sirvent Antolin Luis, Sorli Guerola Jose Vicente, Soubriet Velasco Ángel, SuÁrez HernÁndez Hector, SuÁrez Castro Nicanor Enrique, SuÁrez FernÁndez Eusebio, Tarradellas Bancus Jose María, Tejero Puerto Francisco, Tisaire Sanchez Javier, Tola Gutiérrez Beatriz, Toldos Villegas Gregorio, Torner Perarnau Lluis, Torres Izquierdo Jesus, Torres Exposito Juan, Trujillano Gerardo, Úbeda Pastor María, Valeriola Julvez José María, Valero Barcelo Carmen, Valero Lance Maria Pilar, Valladares Mateu Lluis Carles, Vargas Negrín Francisco, VÁzquez Rojo Carlos, VÁzquez García María Dolores, Velasco Escobar Pablo, Velayos Jiménez Enrique, Velazquez Ferro Juan Jesús, Ventura Rodriguez Silvestre, Vergara Martín Jesús, Vicente Arroyo Manuel J., Vigil-Escalera Francisco, Vila Villarte Carme, Vilano Vives Jordi, Villa Estebanez Rubén, Villahoz Castrillejo Rosa, Villalva Quintana Elena, Villanueva Budia Guillermo, Villanueva Gómez Isabel, Villanueva Telleria Jerusalén, Villanueva Rebollo José Manuel, Villanueva Zarate Jose Ramón, Villar Rivera Marcos, Villarte Perez Ofelia, Villena Machuca Maria Luisa, Viudes Plaza Emilio, Vizuete Gala Carmen, Zamorano Martín Juan Carlos, Zapata Medin Luisa, Zeloro GonzÁlez TomÁs, Zuazagoitia Nubla Jose Félix, Zubiri SÁenz Félix, Zugaza Gurruchaga Lucrecia.
- © 2006 American Society of Nephrology