Published online Mar 25, 2024. doi: 10.5527/wjn.v13.i1.88972
Peer-review started: October 18, 2023
First decision: December 7, 2023
Revised: December 20, 2023
Accepted: January 15, 2024
Article in press: January 15, 2024
Published online: March 25, 2024
Processing time: 155 Days and 12.3 Hours
The association between congenital heart disease and chronic kidney disease is well known. Various mechanisms of kidney damage associated with congenital heart disease have been established. The etiology of kidneydisease has commonly been considered to be secondary to focal segmental glomerulosclerosis (FSGS), however, this has only been demonstrated in case reports and not in observational or clinical trials.
To identify baseline and clinical characteristics, as well as the findings in kidney biopsies of patients with congenital heart disease in our hospital.
This is a retrospective observational study conducted at the Nephrology Depart
Ten patients with congenital heart disease and kidney biopsy were found. The average age was 29.00 years ± 15.87 years with pre-biopsy proteinuria of 6193 mg/24 h ± 6165 mg/24 h. The most common congenital heart disease was Fallot’s tetralogy with 2 cases (20%) and ventricular septal defect with 2 (20%) cases. Among the 10 cases, one case of IgA nephropathy and one case of membranoproliferative glomerulonephritis associated with immune complexes were found, receiving specific treatment after histopathological diagnosis, delaying the initiation of kidney replacement therapy. Among remaining 8 cases (80%), one case of FSGS with perihilar variety was found, while the other 7 cases were non-specific FSGS.
Determining the cause of chronic kidney disease can help in delaying the need for kidney replacement therapy. In 2 out of 10 patients in our study, interventions were performed, and initiation of kidney replacement therapy was delayed. Prospective studies are needed to determine the usefulness of kidney biopsy in patients with congenital heart disease.
Core Tip: Patients with congenital heart disease often have impaired kidney function, typically due to the presence of focal segmental glomerulosclerosis (FSGS). However, in many cases, this glomerular pathology is identified only once clinically established (nephrotic proteinuria). The aim of this study is to determine the presence of FSGS under baseline conditions (without proteinuria), and therefore, it could be speculated that a preventive treatment could delay the initiation of kidney replacement therapy.
- Citation: Juarez-Villa JD, Zepeda-Quiroz I, Toledo-Ramírez S, Gomez-Johnson VH, Pérez-Allende F, Garibay-Vega BR, Rodríguez Castellanos FE, Moguel-González B, Garcia-Cruz E, Lopez-Gil S. Exploring kidney biopsy findings in congenital heart diseases: Insights beyond cyanotic nephropathy. World J Nephrol 2024; 13(1): 88972
- URL: https://www.wjgnet.com/2220-6124/full/v13/i1/88972.htm
- DOI: https://dx.doi.org/10.5527/wjn.v13.i1.88972
The association between congenital heart disease and chronic kidney disease is well known, although its prevalence is not known. Dimopoulos et al[1] reported that 15.8% of adults with cyanotic congenital heart disease and 8% of patients with non-cyanotic heart disease have some degree of chronic kidney disease, and Rajpal et al[2] reported that 1 in 6 adults with congenital heart disease have albuminuria.
These patients are subjected to various insults associated with the disease, including pathophysiological changes such as polycythemia, cyanosis, chronic hypoxia, and alterations in renal blood flow that affect glomerular hemodynamics, as well as complex surgical interventions and prolonged stays in intensive care units, all of which can cause repeated episodes of acute kidney injury[3-7].
While there have been significant advances in understanding the pathophysiology behind the decline in kidney function in these patients, glomerular alterations associated with congenital heart disease have been reported histologically since 1960[8-11]. However, over the years, there have only been a few isolated case reports and autopsy records with histopathological descriptions of glomerular changes[12].
Among the histological findings in kidney biopsies, the most common pathological features found are glomerulomegaly, mesangial hypercellularity, glomerular capillary congestion, and segmental sclerosis[13]. The most frequently observed pattern of glomerular damage is focal segmental glomerulosclerosis (FSGS), all of these changes commonly found in maladaptive glomerulopathies[14-16], as reported in a documented case by Hida et al[13]. Other authors propose the term “cyanotic nephropathy” to describe the maladaptive histological manifestation of hyperfiltration due to the previously mentioned risk factors[17-19].
Nowadays, there are more tools to increase the survival of patients with cyanotic congenital heart disease. However, it is important to keep in mind that these patients still have a high risk of developing cyanotic nephropathy, even after undergoing corrective cardiovascular surgery.
The objective of this study is to determine the baseline and clinical characteristics, as well as the findings in kidney biopsies of patients with congenital heart disease.
This is a retrospective and observational study carried out at the Nephrology Department of the National Institute of Cardiology “Ignacio Chávez”. All patients over 16 years old who underwent percutaneous renal biopsy from January 2000 to January 2023 with congenital heart disease were included in the study. Patients with incomplete medical records were excluded.
The kidney biopsy was performed based on the indication and consideration of the attending nephrologist for each patient. The technique was guided by real-time ultrasound, and the approach as well as the number of needles used were determined by the responsible nephrologist.
Complications after the biopsy were classified as major or minor complications. A major complication was defined as an event that required therapeutic intervention for resolution (e.g., blood transfusion, placement of a foley catheter, cystoclysis, angiography, nephrostomy, or nephrectomy). In addition, death was also considered a major complication. A minor complication, on the other hand, was defined as an event that did not require any intervention for resolution, regardless of symptoms (e.g., pain on a visual analog scale greater than 5 out of 10, need for hospitalization for further monitoring).
Minor complications included macroscopic and microscopic hematuria, hematoma regardless of size, pain, arteriovenous fistula, infection, subcapsular hemorrhage, and retroperitoneal hemorrhage. All of the above-mentioned complications were elevated to major if they required any therapeutic intervention. The need for hospitalization for monitoring a complication was not included as a second complication.
As for late complications, all patients were scheduled for a follow-up consultation one month after the biopsy to evaluate the histopathological outcome. This consultation served to rule out any late complications and to ensure that patients did not visit the emergency department during this period.
The indication for kidney biopsy was a 50% increase in proteinuria and/or a ≥ 50% increase in serum creatinine compared to the previous consultation and/or active sediment defined by erythrocyturia or leucocyturia, without a clinical event justifying the deterioration of proteinuria or increase in serum creatinine.
The normal distribution of variables was evaluated using the Shapiro-Wilk test. Quantitative variables were described using means and SD or medians and interquartile ranges (IQR), depending on their distribution. Categorical variables were described using frequencies and proportions.
A total of 10 cases were found from January 2000 to January 2023, of which 3 (30%) patients were female. The average age was 29 years ± 15.87 years with a body mass index of 20.11 kg/m2 ± 7.90 kg/m2. The time from diagnosis of congenital heart disease to biopsy was 60 (39.60) months. Among the 10 patients, only 5 (50%) had a history of hypertension. Pre-biopsy proteinuria was 4843 (4079-6490) mg/24 h with a blood urea nitrogen level of 37.25 mg/dL ± 4.74 mg/dL.
Regarding ultrasonographic findings, kidney length was 9.16 centimeters ± 1.01 centimeters, 6 (60%) patients had lobulated borders, and only 2 (20%) patients had a preserved cortex to medulla ratio. In the kidney biopsy, 4 (40%) patients had insufficient samples for diagnosis; in all cases, a 16-gauge needle was used, and a transverse approach technique was employed. The number of glomeruli obtained was 13.00 ± 6.55. There were only minor complications in 3 (30%) patients, including 2 perirenal hematomas and a patient with hematuria. The rest of the baseline characteristics are presented in Tables 1 and 2.
Initial variables | Results, n = 10 |
Gender (female) | 3 (30) |
Age (yr) | 29.00 ± 15.87 |
Weight (kg) | 54.23 ± 27.17 |
Height (m) | 1.62 ± 0.08 |
Body mass index (kg/m2) | 20.11 ± 7.90 |
Diagnosis-biopsy time (months) | 60 (39-60) |
Hypertension | 5 (50) |
Use loop of Henle diuretics | 3 (30) |
Spironolactone use | 2 (20) |
Use of ACE inhibitors | 5 (50) |
Antiplatelet use | 2 (20) |
Warfarin use | 1 (10) |
Surgery prior to kidney biopsy | 5 (50) |
Serum creatinine (mg/dL) | 1.73 ± 2.10 |
Blood urea nitrogen (mg/dL) | 30.57 ± 29.32 |
Proteinuria (mg/24 h) | 4843 (4079-6490) |
Hemoglobin (g/L) | 15.33 ± 4.45 |
Hematocrit (%) | 48.07 ± 17.32 |
Platelets × 109/L | 288.00 ± 82.00 |
Hematuria | 0 (0) |
Variables prior to performing the renal biopsy | Results, n = 10 |
Serum creatinine (mg/dL) | 2.17 ± 1.88 |
Pre-biopsy BUN (mg/dL) | 37.25 ± 4.74 |
Proteinuria prior to biopsy (mg/24 h) | 6193.00 ± 6165.00 |
Hemoglobin (g/dL) | 14.10 ± 3.76 |
Hematocrit (%) | 43.90 ± 12.96 |
Hematuria | 2 (20%) |
Platelets × 109/L | 281.00 ± 78.15 |
Skin-kidney distance (cm) | 2.100 ± 0.264 |
Renal length (cm) | 9.160 ± 1.011 |
Renal width (cm) | 3.86 ± 0.64 |
Lobulated borders | 6 (60%) |
Ratio Cortex Medulla preserved | 2 (20%) |
Transverse biopsy technique | 10 (100%) |
Insufficient sample | 4 (40%) |
Number passes | 1 |
Glomeruli | 13.00 ± 6.55 |
Intersticial fibrosis (%) | 46.67 (45.00-50.00) |
Complications | 3 (30%) |
Histopathological findings included one case of IgA nephropathy and one case of membranoproliferative glomerulonephritis due to immune complexes. Among the remaining 8 (80%) cases, one case of FSGS with perihilar variety was found, while the other 7 cases were non-specific FSGS. The findings and diagnoses of congenital heart disease are shown in Table 3.
Gender | Age | Type of heart disease | Diagnosis | Glomeruli | Creatinine (mg/dL) | Proteinuria (g/g/24 h) | Renal measurements (cm) | Complications |
Male | 17 | Dextromorphism with common atrium, absence of right ventricular atrial septal defect | FSGS NOS | 14 | 2.89 | 1.70 | 8.0 × 3.6 | None |
Female | 23 | Acianogen VSD | FSGS NOS | 19 | 1.75 | 14.69 | 9.8 × 3.4 | None |
Male | 47 | Dextrocardia concordant atrioventricular and ventricular-arterial connection | FSGS NOS | 6 | 1.88 | 1.91 | 9.7 × 4.6 | None |
Female | 57 | ASD | IgA nephropathy | 18 | 1.41 | 3.23 | 8.7 × 4.2 | None |
Male | 38 | Persistent ductus arteriosus + Eisenmenger Syndrome | FSGS NOS | 25 | 1.02 | 4.09 | 10.1 × 5.3 | Haematuria |
Male | 33 | Pulmonary atresia | FSGS NOS | 6 | 8.25 | 10.89 | 9.4 × 4.3 | Perirenal hematoma |
Female | 20 | Infundibular VSD | GMN proliferative membrane immune complexes | 11 | 1.98 | 8.25 | 9.9 × 4.3 | None |
Male | 69 | Ebstein Anomaly | FSGS Perihiliar | 13 | 4.27 | 1.58 | 9.3 × 4.3 | None |
Male | 19 | Tetralogy of fallot | FSGS NOS | 6 | 3.24 | 5.18 | 8.4 × 4.2 | Perirenal hematoma |
Male | 41 | Tetralogy of fallot | FSGS NOS | 8 | 1.93 | 3.70 | 8.96 × 4.24 | None |
Research on cardio-renal syndrome has made great strides in recent times; however, there is limited evidence on kidney disease in patients with congenital heart diseases. As life expectancy in this population has increased due to therapeutic advances, a higher percentage of adults living with congenital heart diseases is expected[3-19].
The mechanisms of kidney injury in these patients include chronic hypoxia, intraglomerular hemodynamic changes, neurohormonal alterations, and even cardiac surgeries for the correction of congenital defects. These mechanisms are difficult to modify and consequently result in a significant increase in the prevalence of kidney disease in these patients[3-19].
Another significant obstacle is the identification of more accurate and sensitive diagnostic tools, as well as biomarkers for kidney function in this population. The international literature recommends requesting serum creatinine and cystatin C for the estimation of glomerular filtration rate from the first contact, given the biases in isolated creatinine mea
The findings from previous studies suggest a clinical association between FSGS and heart disease in pediatric patients, which may be speculated to be associated with an immune mechanism responsible for the development of FSGS that can also affect the heart. An important point to note is that these studies were performed with biopsies in the pediatric population, without studying the impact of these glomerulopathies in adulthood, both in renal and cardiac prognosis. Another disadvantage is that the prevalence of other glomerulopathies other than FSGS is unknown, as they are associated with maladaptive changes, and the biopsy result is often ignored in favor of empirical treatment[23].
In our center, within the congenital heart disease department, there is a registry of 3500 patients with congenital heart disease. We do not have the exact prevalence of chronic kidney disease in this population, but unpublished information indicates an approximate 13%[24]. Our study is one of the first to describe the long-term behavior of patients with congenital heart diseases who reach adulthood and evaluate the impact of renal damage on morbidity and mortality. One of the included patients, who had ventricular septal defect as the underlying heart disease and whose biopsy reported membranoproliferative glomerulonephritis, received treatment with steroids and calcineurin inhibitors, delaying the initiation of renal replacement therapy by 3 years. Another one of our patients with ventricular septal defect who underwent successful closure of the defect had IgA nephropathy as a finding in the kidney biopsy, and received immunosuppressive treatment with steroids, delaying the initiation of kidney replacement therapy by 24 years. In both cases, these treatments would not have been given without a histopathological report justifying these interventions.
Furthermore, another important point to highlight is the prognostic information provided by these renal biopsies, as they establish a percentage of tubulointerstitial damage or fibrosis, which gives us an idea of the likelihood of recovery[25].
Another advantage of the study is the low prevalence of minor complications in only one-third of the population and the absence of major complications, indicating the safety of the kidney biopsy procedure in this patient population.
Our study has limitations such as: (1) The retrospective nature of the study and small number of cases, with only 10 patients included; and (2) the study did not focus on the medical treatment instituted to modify the decline in kidney function, as this was determined by each attending physician for each patient. However, these findings motivate the need for a prospective study with the possibility of implementing interventions that could improve the renal and cardiac prognosis in these patients.
Congenital heart disease is a growing diagnosis in the adult population and is known to be associated with chronic kidney disease. However, the etiology of chronic kidney disease in this population is not well understood. Therefore, determining the cause can help intervene in delaying the progression to kidney replacement therapy. In two out of the ten patients in our study, interventions were performed based on the renal biopsy findings, this may probably delay the initiation of renal replacement therapy.
Our study serves as an initial proposal for prospective studies to determine the importance of renal biopsy in this population. By understanding the underlying renal pathology, appropriate interventions can be implemented to improve the renal and cardiac prognosis in these patients.
There is limited information available about the etiology of chronic kidney disease in patients with congenital heart disease today due to advanced surgeries providing an increased life expectancy, therefore it’s truly important to delay the onset of kidney replacement therapy.
There is a growing population of patients with congenital heart disease and chronic kidney disease which is an area of opportunity to evaluate the causes of this pathology and the impact on it’s treatment.
To determine that there may be other glomerulopathies in this population and treating them may possibly delay the onset of kidney replacement therapy.
We conducted a retrospective analysis of information from patients with congenital heart disease who underwent kidney biopsy.
We determined that there may be other glomerulopathies in which treatment could be given. It would be appropriate to determine in a larger population if the number of other glomerulopathies different from focal segmental glomerulosclerosis (FSGS) is higher and if treatment really delays kidney replacement therapy.
Chronic kidney disease in congenital heart disease is not always due to hypoxic damage that leads to FSGS.
Clinical trials that can clarify who truly benefits from biopsy and enable follow-up to perform interventions that could delay renal replacement therapy.
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Urology and nephrology
Country/Territory of origin: Mexico
Peer-review report’s scientific quality classification
Grade A (Excellent): 0
Grade B (Very good): B
Grade C (Good): 0
Grade D (Fair): 0
Grade E (Poor): 0
P-Reviewer: Ong H, Malaysia S-Editor: Chen YL L-Editor: A P-Editor: Zhao S
1. | Dimopoulos K, Diller GP, Koltsida E, Pijuan-Domenech A, Papadopoulou SA, Babu-Narayan SV, Salukhe TV, Piepoli MF, Poole-Wilson PA, Best N, Francis DP, Gatzoulis MA. Prevalence, predictors, and prognostic value of renal dysfunction in adults with congenital heart disease. Circulation. 2008;117:2320-2328. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 266] [Cited by in F6Publishing: 261] [Article Influence: 16.3] [Reference Citation Analysis (0)] |
2. | Rajpal S, Alshawabkeh L, Almaddah N, Joyce CM, Shafer K, Gurvitz M, Waikar SS, Mc Causland FR, Landzberg MJ, Opotowsky AR. Association of Albuminuria With Major Adverse Outcomes in Adults With Congenital Heart Disease: Results From the Boston Adult Congenital Heart Biobank. JAMA Cardiol. 2018;3:308-316. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 13] [Cited by in F6Publishing: 13] [Article Influence: 2.6] [Reference Citation Analysis (0)] |
3. | Li S, Krawczeski CD, Zappitelli M, Devarajan P, Thiessen-Philbrook H, Coca SG, Kim RW, Parikh CR; TRIBE-AKI Consortium. Incidence, risk factors, and outcomes of acute kidney injury after pediatric cardiac surgery: a prospective multicenter study. Crit Care Med. 2011;39:1493-1499. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 309] [Cited by in F6Publishing: 335] [Article Influence: 25.8] [Reference Citation Analysis (0)] |
4. | Nashat FS, Portal RW. The effects of changes in haematocrit on renal function. J Physiol. 1967;193:513-522. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 20] [Cited by in F6Publishing: 28] [Article Influence: 2.0] [Reference Citation Analysis (0)] |
5. | Passwell J, Orda S, Modan M, Shem-Tov A, Aladjem A, Boichis H. Abnormal renal functions in cyanotic congential heart disease. Arch Dis Child. 1976;51:803-805. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 13] [Cited by in F6Publishing: 14] [Article Influence: 0.3] [Reference Citation Analysis (0)] |
6. | Shankland SJ, Ly H, Thai K, Scholey JW. Increased glomerular capillary pressure alters glomerular cytokine expression. Circ Res. 1994;75:844-853. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 36] [Cited by in F6Publishing: 36] [Article Influence: 1.2] [Reference Citation Analysis (0)] |
7. | Perloff JK, Latta H, Barsotti P. Pathogenesis of the glomerular abnormality in cyanotic congenital heart disease. Am J Cardiol. 2000;86:1198-1204. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 48] [Cited by in F6Publishing: 49] [Article Influence: 2.0] [Reference Citation Analysis (0)] |
8. | Fine LG, Orphanides C, Norman JT. Progressive renal disease: the chronic hypoxia hypothesis. Kidney Int Suppl. 1998;65:S74-S78. [PubMed] [Cited in This Article: ] |
9. | Truong LD, Farhood A, Tasby J, Gillum D. Experimental chronic renal ischemia: morphologic and immunologic studies. Kidney Int. 1992;41:1676-1689. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 73] [Cited by in F6Publishing: 66] [Article Influence: 2.1] [Reference Citation Analysis (0)] |
10. | Ohuchi H, Takasugi H, Ohashi H, Yamada O, Watanabe K, Yagihara T, Echigo S. Abnormalities of neurohormonal and cardiac autonomic nervous activities relate poorly to functional status in fontan patients. Circulation. 2004;110:2601-2608. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 70] [Cited by in F6Publishing: 70] [Article Influence: 3.5] [Reference Citation Analysis (0)] |
11. | SPEAR GS. Glomerular alterations in cyanotic congenital heart disease. Bull Johns Hopkins Hosp. 1960;106:347-367. [PubMed] [Cited in This Article: ] |
12. | Ingelfinger JR, Kalantar-Zadeh K, Schaefer F; for the World Kidney Day Steering Committee. Averting the legacy of kidney disease-focus on childhood. Kidney Int. 2016;89:512-518. Kidney Int. 2016;89:1405. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 2] [Cited by in F6Publishing: 2] [Article Influence: 0.3] [Reference Citation Analysis (0)] |
13. | Hida K, Wada J, Yamasaki H, Nagake Y, Zhang H, Sugiyama H, Shikata K, Makino H. Cyanotic congenital heart disease associated with glomerulomegaly and focal segmental glomerulosclerosis: remission of nephrotic syndrome with angiotensin converting enzyme inhibitor. Nephrol Dial Transplant. 2002;17:144-147. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 14] [Cited by in F6Publishing: 14] [Article Influence: 0.6] [Reference Citation Analysis (0)] |
14. | Ogunkunle OO, Asinobi AO, Omokhodion SI, Ademola AD. Nephrotic syndrome complicating cyanotic congenital heart disease: a report of two cases. West Afr J Med. 2008;27:263-266. [PubMed] [Cited in This Article: ] |
15. | Ekulu PM, Kazadi-Wa-Kazadi O, Lumbala PK, Aloni MN. Nephrotic Syndrome in a Child Suffering from Tetralogy of Fallot: A Rare Association. Case Rep Pediatr. 2015;2015:128409. [PubMed] [DOI] [Cited in This Article: ] [Reference Citation Analysis (0)] |
16. | Sultana A, Chowdhury NAH, Hossain J, Kabir S, Islam MS. Nephrotic Range of Proteinuria in Congenital Cyanotic Heart Disease: A Rare Complication. Bangladesh J Child Heal. 2021;44:178-180. [DOI] [Cited in This Article: ] |
17. | Sagalowsky AI. Re: sensory disturbance of the thigh after renal transplantation. Y. Murata, K. Sakamoto, R. Hayashi, K. Takahashi, S.-I. Nakamura and H. Moriya. J Urol, 165: 770-772, 2001. J Urol. 2002;167:259. [PubMed] [DOI] [Cited in This Article: ] [Reference Citation Analysis (0)] |
18. | Flanagan MF, Hourihan M, Keane JF. Incidence of renal dysfunction in adults with cyanotic congenital heart disease. Am J Cardiol. 1991;68:403-406. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 52] [Cited by in F6Publishing: 54] [Article Influence: 1.6] [Reference Citation Analysis (0)] |
19. | Mair DD, Puga FJ, Danielson GK. Late functional status of survivors of the Fontan procedure performed during the 1970s. Circulation. 1992;86:II106-II109. [PubMed] [Cited in This Article: ] |
20. | Sharma S, Ruebner RL, Furth SL, Dodds KM, Rychik J, Goldberg DJ. Assessment of Kidney Function in Survivors Following Fontan Palliation. Congenit Heart Dis. 2016;11:630-636. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 42] [Cited by in F6Publishing: 44] [Article Influence: 5.5] [Reference Citation Analysis (0)] |
21. | Sandberg C, Johansson K, Christersson C, Hlebowicz J, Thilén U, Johansson B. Sarcopenia is common in adults with complex congenital heart disease. Int J Cardiol. 2019;296:57-62. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 24] [Cited by in F6Publishing: 24] [Article Influence: 4.8] [Reference Citation Analysis (0)] |
22. | Khajali Z, Aliramezany M, Jorfi F, Ghaderian H, Maleki M, Malek H, Lotfian S, Khalili Y, and Naderi N. Sarcopenia in young adults with congenital heart disease. JCSM Rapid Comm. 2022;5:77-85. [DOI] [Cited in This Article: ] |
23. | El Sayegh S, Ephrem G, Wish JB, Moe S, Lim K. Kidney disease and congenital heart disease: Partnership for life. Front Physiol. 2022;13:970389. [PubMed] [DOI] [Cited in This Article: ] [Cited by in F6Publishing: 4] [Reference Citation Analysis (0)] |
24. | García-Cruz E, Manzur-Sandoval D, Gopar-Nieto R, Plata-Corona JC, Montalvo-Ocotoxtle IG, Navarro-Martinez DA, Terán-Morales EM, Rivera-Buendía F, Antonio-Villa NE, García-González NE, Angulo-Cruzado ST, Sánchez-López SV, Torres-Martel JM, Díaz-Gallardo LG, Barrera-Real AJ, Quiroz-Martínez VA, Pedroza MV, Sánchez-Nieto J, Valdez-Ramos M, Ávila-Vanzzini N, Vera-Zertuche JM, Baranda-Tovar FM. Cardiometabolic Risk Factors in Mexican Adults With Congenital Heart Disease. JACC Adv. 2023;100596. [DOI] [Cited in This Article: ] [Cited by in Crossref: 2] [Cited by in F6Publishing: 1] [Article Influence: 1.0] [Reference Citation Analysis (0)] |
25. | Menn-Josephy H, Lee CS, Nolin A, Christov M, Rybin DV, Weinberg JM, Henderson J, Bonegio R, Havasi A. Renal Interstitial Fibrosis: An Imperfect Predictor of Kidney Disease Progression in Some Patient Cohorts. Am J Nephrol. 2016;44:289-299. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 40] [Cited by in F6Publishing: 55] [Article Influence: 6.9] [Reference Citation Analysis (0)] |