Trends and outcomes of the use of percutaneous native kidney biopsy in the United States: 5-year data analysis of the Nationwide Inpatient Sample

Trends and outcomes of the use of percutaneous native kidney biopsy in the United States: 5-year... Background: Despite an inordinate share of health care resources being utilized by patients with kidney disease, morbidity and mortality in these patients remain high. Although renal biopsy is an intervention to identify potential treatment- modifiable causes of disease, large-scale data studying the safety and outcomes of percutaneous native kidney biopsy in hospitalized patients are lacking. Methods: We queried the Nationwide Inpatient Sample database from 2008 to 2012 and identified all hospital admissions during which a percutaneous renal biopsy was performed. Patients <18 years of age or with a transplanted kidney were excluded. Data regarding associated renal pathology and procedure-related complications were collected and analyzed. Outcomes studied were length of stay, mortality and cost adjusted for inflation. Results: A total of 118 064 hospital admissions were included in our analysis. The most common complications reported after percutaneous kidney biopsy were packed red blood cell transfusion (261/1000 cases), hematuria (129/1000 cases) and bleeding (78/1000 cases). Patients had an overall mortality of 1.8%. The mean length of stay for each hospitalization was 10.65 days, with a significant difference between elective and nonelective admissions (6.3 versus 11.7; P< 0.01). The average cost per hospitalization was US$22 917 after adjusting for inflation, again with a significant difference between elective and nonelective admissions (15 168 versus 24 780; P< 0.01). Conclusion: Overall, percutaneous renal biopsy is considered a safe procedure; however, our study based on a national database demonstrates a relatively higher complication rate as compared with the limited prior available studies. Key words: acute kidney injury, chronic kidney disease, kidney biopsy, kidney failure, Nationwide Inpatient Sample (NIS) Received: April 9, 2017. Editorial decision: August 4, 2017 V C The Author 2017. Published by Oxford University Press on behalf of ERA-EDTA. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 331 Classification of Disease, Revision 9 (ICD-9) procedure code 5523 Introduction was used to identify cases where percutaneous renal biopsy was The prevalence of chronic kidney disease (CKD) in the US adult performed. Data from patients 18 years of age were included, general population has increased slightly over the past 17 years, whereas those missing mortality or gender data elements were reaching 14.8% according to data from the National Health and excluded. Patients with a transplanted kidney were identified Nutrition Examination Survey (NHANES) database 2011–2014 [1]. and excluded using Diagnosis Related Group 24 (DRG24) code 302, In 2014, Medicare patients with CKD were twice as likely to be hos- ICD-9 diagnostic codes V420 and 99681 and ICD-9 procedure pitalized and had an adjusted all-cause mortality rate that was codes 5553, 5561 and 5569 (Appendix, Table A). twice as high as patients without CKD. In addition, Medicare Mean age, number of chronic conditions and baseline medi- expenditures on beneficiaries with CKD accounted for 44% of total cal comorbidities were described. Distribution of cases by gen- expenditures on adults between 18 and 64 years of age and for der, age groups, race, hospital region, hospital bed size, hospital 20% of expenditures on adults 65 years of age. In contrast, the academic status and primary coverage was reported. The preva- incidence of end-stage renal disease (ESRD) is decreasing, though lence of specific renal diseases and commonly associated diag- it remains as high as 1424 cases per million population in adults noses was determined. 65 years of age. Among patients on dialysis, the total number of The rate of occurrence of bleeding, transfusion, nephrec- deaths in 2014 was 172.8 per 1000 patient-years. Moreover, tomy and other frequently reported procedure complications Medicare expenditures on beneficiaries with ESRD reached was identified. Outcomes studied include mortality, length of US$32.8 billion during that period. Whereas it is estimated that stay and total cost adjusted for inflation. Data processing 40% of patients with CKD have diabetes, the incidence of ESRD and analysis was performed using Microsoft Excel 2013 and due to diabetes was 2282 per million population. Given the signifi- Statistical Package for the Social Sciences version 23 software cant cost and mortality associated with renal disease, accurate (IBM, Armonk, NY, USA). and timely diagnostic procedures are an essential part of the care Categorical variables were expressed as frequency, rate and of these patients. While renal biopsy has been used to identify the percentage while continuous variables were expressed as mean cause of renal disease since 1923, novel technologies involving (standard deviation). An independent sample t-test was used proteomics are now being evaluated as noninvasive alternatives for comparison between means at a 99% confidence level and a [2, 3]. Information from a renal tissue sample is not always con- binary logistic regression was used for risk analysis. clusive, however, it remains helpful in certain clinical scenarios [4]. Although renal biopsy is performed to identify treatment mod- ifiable causes of kidney disease, large-scale data studying the safety and outcome of percutaneous native kidney biopsy in hos- Results pitalized patients are lacking. A total of 175 831 hospital admissions where percutaneous renal Percutaneous renal biopsy is the most commonly used biopsy was performed were identified between 2008 and 2012. method to obtain renal tissue, with an open surgical procedure 11 190 hospitalizations involving patients <18 years of age were reserved for patients with contraindications to a percutaneous excluded. One hundred and fifty-six cases missing data ele- approach [4, 5]. Novel ways of obtaining renal tissue include ments on gender or mortality were also excluded. After exclud- transjugular and laparoscopic approaches [6–8]. Studies on the ing patients with a transplanted kidney, a total of 118 064 cases benefit and safety of a renal biopsy are available for review. In a were included in the subsequent analysis (Appendix, Table B). study by Kropp et al. [9], in 46 patients with CKD undergoing The mean age was 55.36 years and the average number of renal biopsy or nephrectomy, 9% of samples were inconclusive. chronic medical conditions was 6.27 (Appendix, Table C). Earlier studies [10, 11] concluded that a renal biopsy altered Deficiency anemia, congestive heart failure, diabetes, hyper- management in 19–42% of cases, but a recent study by Kitterer tension and renal failure were reported, among others, as exist- et al. [12] concluded that a disease responsive to treatment mod- ing medical comorbidities (Table 1). ification was identified in 74% of cases. Bleeding is a common Patients undergoing percutaneous renal biopsy were 52.5% complication occurring in 1.2% of cases of percutaneous native males. The majority of patients were between 38 and 77 years of kidney biopsy and in 0.2% of cases of percutaneous biopsy of a age. Patients were 55.8% White, 22.9% Black and 13.7% Hispanic. transplanted kidney [13, 14]. In a meta-analysis published in More cases were encountered in the South (40.5%) and in large 2012, 3.5% of patients had macroscopic hematuria and 0.9% of hospitals (71.3%). Cases from urban teaching hospitals compro- patients required erythrocyte transfusion after a percutaneous mised 57.2% compared with 42.8% from urban nonteaching or renal biopsy. Urinary tract obstruction, unilateral nephrectomy rural hospitals. Medicare or Medicaid were the primary payers and death occurred in 0.3, 0.01 and 0.02% of those cases, respec- in 54.4% of patients compared with 32.5% covered by private tively. Despite the number of studies available, a conclusive health insurance (Table 2). data on the use of inpatient percutaneous renal biopsy and the ICD-9 diagnostic code 58089 (acute glomerulonephritis with frequency of complications is still lacking at the national level. other specified pathological lesion in kidney) was the most fre- In this study we present data on the use of inpatient percutane- quently reported diagnosis among acute glomerulonephritis, ous native renal biopsy during inpatient hospitalization of US whereas 5821 (chronic glomerulonephritis with lesion of mem- adults between 2008 and 2012. We describe baseline patient branous glomerulonephritis) was the most frequently reported characteristics and medical comorbidities, identify the fre- diagnosis among chronic glomerulonephritis. ICD-9 diagnostic quency of complications, report associated renal pathologies code 5819 (nephrotic syndrome with unspecified pathological and discuss hospitalization outcomes. lesion in kidney) was the most frequently reported diagnosis among nephrotic group diagnoses, while 58381 (nephritis and nephropathy, not specified as acute or chronic, in diseases clas- Materials and methods sified elsewhere) was the most frequently reported diagnosis Data from the Nationwide Inpatient Sample (NIS) database, from among nephritis and nephropathy group. Code 5845 (acute kid- 1 January 2008 to 31 December 2012, was studied. International ney failure with lesion of tubular necrosis) was identified in Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 332 | A.A. Al Turk et al. Table 1. Baseline patient comorbidities Table 2. Distribution of cases by gender, age group, race, hospital region, hospital bed size, hospital academic status and primary Comorbidities Percentage coverage Acquired immune deficiency syndrome 0.8 Characteristic Percentage Alcohol abuse 3.9 Chronic blood loss anemia 2.6 Gender Chronic pulmonary disease 15.4 Male 52.5 Coagulopathy 11.2 Female 47.5 Collagen vascular disease/rheumatoid arthritis 6.4 Age group (years) Congestive heart failure 14.1 18–37 19.8 Deficiency anemia 49.1 38–57 31.6 Depression 8.3 58–77 37.8 Diabetes, uncomplicated 15.8 78 10.8 Diabetes with chronic complications 12.6 Race Drug abuse 3.9 White 55.8 Fluid and electrolyte disorders 49.7 Black 22.9 Hypertension 44.6 Hispanic 13.7 Hypothyroidism 10.7 Asian or Pacific Islander 3.2 Liver disease 5.2 Native American 0.7 Lymphoma 2.4 Other 3.7 Metastatic cancer 2.2 Hospital region Obesity 12.8 Northeast 17.8 Other neurological disorders 4.9 Midwest or North Central 22.2 Paralysis 1.6 South 40.5 Peripheral vascular disorders 4.9 West 19.5 Psychosis 3.5 Hospital bed size Pulmonary circulation disorders 4.1 Small 7.1 Renal failure 26.5 Medium 21.6 Solid tumor without metastasis 2.9 Large 71.3 Valvular disease 4.7 Hospital academic status Weight loss 9.7 Rural or urban nonteaching 42.8 Urban teaching 57.2 Primary coverage Medicare or Medicaid 54.4 15.2% of the cases. As a reported diagnosis, 1% of cases had Private 32.5 renal sclerosis (587—renal sclerosis, unspecified) (Table 3). Self-pay, no charge, or other 13.1 In CKD, more cases were classified into Stages 3 and 4, with 8.7% and 6.5%, respectively. As a reported diagnosis, 13.3% of cases had ESRD (Appendix, Table D). Among kidney-related neoplasm, 9.6% were malignant, 0.8% were benign and 0.7% comparing the length of stay between teaching and non- teaching hospitals. Patients admitted electively were discharged were secondary metastatic (Appendix, Table E). Among DRG 24 codes, 316 (renal failure) was the most fre- an average of 5.4 days earlier (P< 0.01) (Table 6). After adjusting for inflation, the average cost per hospitaliza- quent at 29.9%, followed by 331 (other kidney and urinary tract diagnoses with major complications or comorbidities) at 8%. tion was US$22 917 (Appendix, Table C). Males had a slightly lower but significant difference in the total cost compared with Connective tissue disorders with major complications or comorbidities (code 240) was next at 7.6%, followed by 315 (other females (22 639 versus US$23 224; P< 0.01). A nonelective nature of an admission and an admission to an urban teaching hospital kidney and urinary tract procedure) at 4.1%. Table 4 lists all the DRG 24 codes with a rate of occurrence 1%. were associated with a higher total cost. A nonelective admis- sion was US$9500 more expensive than an elective admission, The need for packed red blood cell (PRBC) transfusion was the most frequently reported complication (261/1000). This was while the difference between teaching and non-teaching hospi- tals approached US$3000 (Table 6). Hematuria was associated followed by hematuria, bleeding and hypotension (129/1000, 78/ 1000 and 40/1000, respectively). Death occurred in 18 of 1000 with a lower admission cost, however, the need for PRBC trans- fusion, occurrence of bleeding and hypotension were associated hospital admissions. Ileus was reported at a rate of 15/1000. Kidney laceration and the need for nephrectomy occurred less with a higher cost. Interestingly, performing a nephrectomy or an open renal biopsy had no significant impact on the mean frequently (1/1000 and 0.4/1000, respectively). During the course of hospitalization, a repeat percutaneous renal biopsy was cost of an admission (Appendix, Table F). In an attempt to identify predictors of increased mortality in needed in 14 of 1000 cases, whereas an open renal biopsy was performed in 0.2 of 1000 cases (Table 5). patients admitted for a percutaneous renal biopsy, a binary logistic regression analysis was performed using a forward like- While neither gender nor hospital academic status had an impact on inpatient mortality, patients admitted electively had lihood ratio model. Advanced age was found to be associated with the highest predicted mortality, with an odds ratio (OR) of significantly lower mortality rates when compared with non- electively admitted patients (0.99 versus 2.01%; P< 0.01) (Table 6). 18.8. Patients with metastatic cancer, acute kidney injury, coagulopathy or liver disease at baseline had a higher predicted The average length of stay was 10.65 hospital days (Appendix, Table C). Females had a slightly higher but statisti- mortality as well (OR 6.2, 3.9, 2.7 and 2.1, respectively). Among the studied complications, the need for PRBC transfusion was cally significant length of stay compared with males (10.9 ver- sus 10.5 days; P< 0.01). A similar effect was observed when the best predictor for increased mortality, followed by Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 333 Table 3. Frequency of reported pathology among patients undergoing percutaneous native kidney biopsy ICD-9 diagnosis code ICD-9 diagnostic code description Percentage Acute glomerulonephritis 5800 Acute glomerulonephritis with lesion of proliferative glomerulonephritis 0.4 5804 Acute glomerulonephritis with lesion of rapidly progressive glomerulonephritis 0.8 58081 Acute glomerulonephritis in diseases classified elsewhere 1.2 58089 Acute glomerulonephritis with specified pathological lesion in kidney 3.9 5809 Acute glomerulonephritis with unspecified pathological lesion in kidney 1.4 Nephrotic syndrome 5810 Nephrotic syndrome with lesion of proliferative glomerulonephritis 0.1 5811 Nephrotic syndrome with lesion of membranous glomerulonephritis 1.9 5812 Nephrotic syndrome with lesion of membranoproliferative glomerulonephritis 0.4 5813 Nephrotic syndrome with lesion of minimal change glomerulonephritis 0.4 58181 Nephrotic syndrome in diseases classified elsewhere 4.1 58189 Nephrotic syndrome with specified pathological lesion in kidney 0.4 5819 Nephrotic syndrome with unspecified pathological lesion in kidney 7.6 Chronic glomerulonephritis 5820 Chronic glomerulonephritis with lesion of proliferative glomerulonephritis N 5821 Chronic glomerulonephritis with lesion of membranous glomerulonephritis 1.2 5822 Chronic glomerulonephritis with lesion of membranoproliferative glomerulonephritis 0.1 5824 Chronic glomerulonephritis with lesion of rapidly progressive glomerulonephritis 0.1 58281 Chronic glomerulonephritis in diseases classified elsewhere 0.9 58289 Chronic glomerulonephritis with specified pathological lesion in kidney 0.5 5829 Chronic glomerulonephritis with unspecified pathological lesion in kidney 0.3 Nephritis and nephropathy 5830 Nephritis and nephropathy, not specified as acute or chronic, with lesion of proliferative glomerulonephritis 0.3 5831 Nephritis and nephropathy, not specified as acute or chronic, with lesion of membranous glomerulonephritis 0.6 5832 Nephritis and nephropathy, not specified as acute or chronic, with lesion of membranoproliferative 0.7 glomerulonephritis 5834 Nephritis and nephropathy, not specified as acute or chronic, with lesion of rapidly progressive 1.2 glomerulonephritis 5836 Nephritis and nephropathy, not specified as acute or chronic, with lesion of renal cortical necrosis N 5837 Nephritis and nephropathy, not specified as acute or chronic, with lesion of renal medullary necrosis N 58381 Nephritis and nephropathy, not specified as acute or chronic, in diseases classified elsewhere 10.9 58389 Nephritis and nephropathy, not specified as acute or chronic, with specified pathological lesion in kidney 3.2 5839 Nephritis and nephropathy, not specified as acute or chronic, with unspecified pathological lesion in kidney 4.7 Acute renal failure 5845 Acute kidney failure with lesion of tubular necrosis 15.2 5846 Acute kidney failure with lesion of renal cortical necrosis N 5847 Acute kidney failure with lesion of renal medullary [papillary] necrosis N 5848 Acute kidney failure with specified pathological lesion in kidney 1.7 5849 Acute kidney failure, unspecified 48.6 Renal sclerosis 587 Renal sclerosis, unspecified 1 N, negligible. Table 4. Most frequently associated DRG 24 code in patients undergoing percutaneous native kidney biopsy DRG 24 code DRG 24 code description Percentage 316 Renal failure 29.9 331 Other kidney and urinary tract diagnoses with major complications or comorbidities 8.0 240 Connective tissue disorders with major complications or comorbidities 7.6 315 Other kidney and urinary tract procedures 4.1 303 Kidney and ureter procedures for neoplasm 3.9 318 kidney and urinary tract neoplasm with major complications or comorbidities 3.3 332 Other kidney and urinary tract diagnoses 2.5 127 Heart failure and shock 2.4 576 Septicemia without mechanical ventilation >96 h 1.9 403 Lymphoma and nonacute leukemia with major complications or comorbidities 1.8 239 Pathological fractures and musculoskeletal and connective tissue malignancy 1.5 468 Extensive operating room procedure unrelated to principal diagnosis 1.4 304 Kidney and ureter procedures for nonneoplasm with major complications or comorbidities 1.0 452 Complications of treatment with major complications or comorbidities 1.0 Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 334 | A.A. Al Turk et al. Table 5. Frequency of reported complications of percutaneous native kidney biopsy Complication ICD-9 code Rate per 1000 cases PRBC transfusion 9904 261 Hematuria 5997, 59970, 59971, 59972 129 Bleeding 4590, 99811, 99812 78 Hypotension 4580, 45829, 4588, 4589 40 Death 18 Ileus 5601 15 Repeat percutaneous renal biopsy 5523 14 Kidney laceration 86600, 86601, 86602, 86603, 86610, 86611, 86612, 86613 1 Nephrectomy 554, 5551, 5552, 5554 0.4 Open renal biopsy 5524 0.2 ICD-9 procedure code. ICD-9 diagnostic code. Table 6. Variation in inpatient mortality, length of hospital stay and cost by gender, hospital academic status and admission urgency Gender Hospital academic status Admission urgency Male Female P-value Rural or urban nonteaching Urban teaching P-value Nonelective Elective P-value Mortality (%) 1.90 1.71 0.13 1.80 1.83 0.67 2.01 0.99 <0.01 Length of stay (days) 10.5 10.9 <0.01 10.2 10.9 <0.01 11.7 6.3 <0.01 Cost (US$) 22 639 23 224 <0.01 21 173 24 135 <0.01 24 780 15 168 <0.01 hypotension (OR 2.0 and 1.7, respectively). The Nagelkerke R - diseases were present, with focal segmental glomerulosclerosis value of this regression model was 0.158. (FSGS) and ATN being two of the top disorders found in dia- betics. While FSGS can be explained by hypertension and obe- sity being more prevalent in the diabetes population, the Discussion mechanism for the increased incidence of ATN has not been elucidated to date. Perhaps more importantly, up to 36% of The prevalence of CKD in the USA was 14.8% as recently as 2014. While CKD Stage 2 decreased in prevalence, CKD Stage 3 patients did not have signs of diabetic kidney disease at all, car- rying alternative diagnoses such as membranous nephropathy has increased over the period 1999–2014 and is currently present in >6% of the US adult population [1]. In our data and pauci-immune glomerulonephritis. Some of these causes are potentially amenable to immunosuppressive therapy, which search, renal failure was identified as the primary diagnosis in hospitalized patients undergoing kidney biopsy. A study per- can lead to increased renal survival. ~ Our study, while quantifying the number of renal biopsies formed by Liano et al. [15] found that acute tubular necrosis (ATN) was the most common cause of acute kidney injury performed, relied on ICD-9 and DRG coding for diagnostic infor- mation. Glomerulonephridities together composed nearly 10% treated by nephrologists. Typically ATN is a clinical diagnosis and is treated with supportive care. In our study, ATN was iden- of renal biopsies performed, however, identifying the specific etiologies of glomerulonephritis was beyond the scope of this tified in 15.2% of biopsies. As discussed by Haas et al. [16], in patients whose clinical presentations are not consistent with study due to the nature of the database and the ICD-9 and DRG coding systems. About 15% of renal biopsies were performed for ATN, obstructive or prerenal causes, prebiopsy and postbiopsy diagnoses differed in up to one-third of cases. We feel that this nephrotic syndrome; membranous nephropathy was diagnosed in 2% of cases. Renal malignancy was identified in nearly 10% highlights the utility and significance of renal biopsy to diag- nose renal dysfunction when the clinical presentation is not of patients. Previous data on percutaneous renal biopsy concluded that conclusive. Indications for percutaneous renal biopsy are largely driven it is a safe procedure, with several studies showing a significant complication rate of 1% [20, 21]. It was also shown to be highly by clinical presentation and expert opinion [17, 18]. Some com- mon indications include acute kidney injury lasting >3 weeks, sensitive and specific in diagnosing primary renal malignancy, with close to 100% accuracy [22]. In contrast to a study by proteinuria >1 g/day, renal involvement of systemic disease and hematuria presumed to be of renal origin. Diabetes mellitus Tondel et al. [23] where gross hematuria was the most fre- quently reported complication (1.9%), hematuria was reported is the most common cause of CKD and ESRD, with most patients not requiring biopsy for diagnosis. Our search revealed that in 12.9% of our patients while the rate of occurrence of PRBC transfusion was 26.1%. Bleeding without the need for PRBC 28.4% of biopsied patients carried a diagnosis of diabetes, which is consistent with the 25% figure proposed in a study performed transfusion was less frequently reported. This may be due to underreporting of bleeding as a complication or due to the use by Sharma et al. [19]. Indications for renal biopsy in diabetic patients are nephrotic-range proteinuria or significant decline of PRBC transfusion for indications other than acute blood loss. Of note, the frequency of PRBC transfusion, hematuria and in renal function that exceeds the patient’s natural history of their disease [18]. While initial evaluation can suggest diabetic bleeding were much higher in our study than in previous stud- ies. Given that our study included a national database, we think nephropathy, up to 60% of diabetic patients may have kidney findings other than diabetic nephropathy [19]. Several other that our study reveals the true incidence of the aforementioned Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 335 complications in the USA. Prior studies reporting lower compli- compared with other patients (23.6 versus 10.4 days; P< 0.01). In cation rates may be related to the selection of centers where elective admissions, the average length of stay was 6.3 days, renal biopsies were performed and perhaps is also related to a which decreased to 6.1 days when excluding deaths. This length selection bias, with patients enrolled in these studies being less of stay is longer than expected considering the trend towards sick. For example, 11.2% of patients in our study had preexisting outpatient observation after biopsy. Since the NIS database coagulopathy while, such patients were excluded in other includes information on hospitalized patients only, patients biopsy series [24]. The difference in complication rates observed who underwent a percutaneous renal biopsy under observation between our data and the data from the national registry for status were not studied. This is a potential source of bias toward renal biopsy in Norway may be partly related to the higher the longer length of stay reported in our study. mean age of patients analyzed in our study (55.36 years com- Due to advances in CKD and ESRD care, the life expectancy pared with 50.6 years) [23]. The Norwegian data included of patients with renal disease is increasing [1]. As a result, the patients with renal biopsies performed both in outpatient and expenditures for ESRD have doubled during the 2003–2014 inpatient settings; the data from the NIS database pertains to period, from 16 billion to US$32 billion. It is difficult to properly patients who are only admitted to the hospital, hence a sicker assess the economic burden of CKD, but a study by Wang et al. population. Identifying the true incidence of reported complica- [25] revealed a linear increase in health care utilization and eco- tions is an aid for clinicians when weighing the risks and bene- nomic burden as patients advance from early to advanced-stage fits of a percutaneous renal biopsy and in obtaining true CKD. In our study, a higher cost was observed both in patients informed consent. with nonelective admissions and with admissions to urban Due to the nature of the database used, several elements teaching hospitals. Whereas a shorter length of stay can explain were missing in our analysis. These elements include the use of the lower cost observed in elective admissions, a slightly longer real-time ultrasound technology, the needle size used for length of stay cannot fully account for the higher cost observed biopsy, the number of passes performed and the number of in teaching hospitals. One explanation could be the variation in cores obtained and the level of experience and specialty of the disease severity among hospitals, along with more advanced operator. In a prior study, however, the needle size used, the diagnostic testing and procedures done at academic centers, number of needle passes, and the specialty of the operator had resulting in higher hospital bills. With the exception of hematu- no influence on the rate of major complications of a percutane- ria, complications from a percutaneous renal biopsy resulted in ous renal biopsy [23]. Also not included were the number of an increase in admission cost. The lack of significance in cases patients on antiplatelet or anticoagulation therapy and the where a nephrectomy or an open renal biopsy was performed is number of patients who underwent arterial embolization ther- likely due to the small number of patients in these groups. apy in an attempt to control bleeding after a renal biopsy. In this analysis of percutaneous renal biopsies in hospital- Our database search showed an overall mortality of 1.8%. ized patients we found that PRBC transfusion and hematuria While this value could be directly related to the renal biopsy occurred at a rate of 26.1% and 12.9% respectively, and that performed, it is more likely due to the nature of the acute dis- occurrence of bleeding, ileus or PRBC transfusion was associ- ease leading to hospitalization and related complications. This ated with an increased hospitalization cost. Renal biopsy is further supported when comparing the mortality rate of elec- remains the gold standard for diagnostic, prognostic and thera- tive admissions (0.99%) with nonelective admissions (2.01%). peutic purposes in many renal diseases; however, other techni- Again we see the discrepancy in mortality rate between our ques, such as proteomics, are being increasingly studied as study and prior work, thus solidifying the idea of bias existing noninvasive alternatives [3, 24]. The use of these technologies towards a lower rate of complications in previous studies. may eventually replace renal biopsy as a primary means of Interestingly, there was no difference in mortality rate between determining individual renal pathology. Developing a compre- teaching and nonteaching hospitals. hensive national registry of renal biopsy findings would serve The appropriate observation period following a percutane- the dual purpose of being able to directly compare tissue diag- ous renal biopsy is still undefined. The practice varies from nosis to noninvasive techniques and to clearly identify those at 4–8 h of observation to an overnight admission. According to a highest risk for progression of renal disease. By revealing com- large biopsy series, up to 7.4% of major complications occur plication rates of percutaneous renal biopsy and identifying 12–24 h after biopsy [24]. Studies that advocate the safety of out- underlying renal disease in hospitalized patients while also pro- patient observation typically include doing a Doppler ultra- viding an in-depth analysis of hospitalization outcomes, we sound postprocedure, frequent vital checks and serial believe that our study helps to emphasize both the financial hemoglobin level monitoring [21]. However, this is labor inten- and scientific aspects of kidney disease in the USA. sive and costly, thus negating the cost benefit of preventing a hospitalization. Patients who have an increased mortality risk Supplementary data after renal biopsy may benefit from a prolonged observation period. Our study identified advanced age, the presence of Supplementary data are available online at http://ckj.oxford metastatic cancer, acute kidney injury, liver disease and coagul- journals.org. opathy as predictors of higher mortality. However, the Nagelkerker R-squared value of our model was low, 0.158. We also found that academic institutions perform renal biopsies at Conflicts of interest statement a rate 1.3 times that of nonacademic hospital institutions, likely None declared. due to a large referral base. A nonelective admission was found to be a major contribu- References tor to an increased length of stay, likely secondary to the nature of acute illness requiring hospitalization and a prolonged treat- 1. United States Renal Data System. 2016 USRDS Annual Data ment duration. Furthermore, patients who did not survive the Report: Epidemiology of Kidney Disease in the United States. admission had a statistically significant longer length of stay Bethesda, MD: National Institutes of Health, National Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 336 | A.A. Al Turk et al. 15. Liano ~ F, Pascual J. 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Bleeding complications of update and evidence for best practice. Clin J Am Soc Nephrol native kidney biopsy: a systematic review and meta-analy- 2016; 11: 354–362 sis. Am J Kidney Dis 2012; 60: 62–73 25. Wang V, Vilme H, Maciejewski ML et al. The economic bur- 14. Atwell TD, Spanbauer JC, McMenomy BP et al. The timing den of chronic kidney disease and end-stage renal disease. and presentation of major hemorrhage after 18,947 image- Semin Nephrol 2016; 36: 319–30 guided percutaneous biopsies. AJR Am J Roentgenol 2015; 205: 190–195 Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Clinical Kidney Journal Oxford University Press

Trends and outcomes of the use of percutaneous native kidney biopsy in the United States: 5-year data analysis of the Nationwide Inpatient Sample

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Abstract

Background: Despite an inordinate share of health care resources being utilized by patients with kidney disease, morbidity and mortality in these patients remain high. Although renal biopsy is an intervention to identify potential treatment- modifiable causes of disease, large-scale data studying the safety and outcomes of percutaneous native kidney biopsy in hospitalized patients are lacking. Methods: We queried the Nationwide Inpatient Sample database from 2008 to 2012 and identified all hospital admissions during which a percutaneous renal biopsy was performed. Patients <18 years of age or with a transplanted kidney were excluded. Data regarding associated renal pathology and procedure-related complications were collected and analyzed. Outcomes studied were length of stay, mortality and cost adjusted for inflation. Results: A total of 118 064 hospital admissions were included in our analysis. The most common complications reported after percutaneous kidney biopsy were packed red blood cell transfusion (261/1000 cases), hematuria (129/1000 cases) and bleeding (78/1000 cases). Patients had an overall mortality of 1.8%. The mean length of stay for each hospitalization was 10.65 days, with a significant difference between elective and nonelective admissions (6.3 versus 11.7; P< 0.01). The average cost per hospitalization was US$22 917 after adjusting for inflation, again with a significant difference between elective and nonelective admissions (15 168 versus 24 780; P< 0.01). Conclusion: Overall, percutaneous renal biopsy is considered a safe procedure; however, our study based on a national database demonstrates a relatively higher complication rate as compared with the limited prior available studies. Key words: acute kidney injury, chronic kidney disease, kidney biopsy, kidney failure, Nationwide Inpatient Sample (NIS) Received: April 9, 2017. Editorial decision: August 4, 2017 V C The Author 2017. Published by Oxford University Press on behalf of ERA-EDTA. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 331 Classification of Disease, Revision 9 (ICD-9) procedure code 5523 Introduction was used to identify cases where percutaneous renal biopsy was The prevalence of chronic kidney disease (CKD) in the US adult performed. Data from patients 18 years of age were included, general population has increased slightly over the past 17 years, whereas those missing mortality or gender data elements were reaching 14.8% according to data from the National Health and excluded. Patients with a transplanted kidney were identified Nutrition Examination Survey (NHANES) database 2011–2014 [1]. and excluded using Diagnosis Related Group 24 (DRG24) code 302, In 2014, Medicare patients with CKD were twice as likely to be hos- ICD-9 diagnostic codes V420 and 99681 and ICD-9 procedure pitalized and had an adjusted all-cause mortality rate that was codes 5553, 5561 and 5569 (Appendix, Table A). twice as high as patients without CKD. In addition, Medicare Mean age, number of chronic conditions and baseline medi- expenditures on beneficiaries with CKD accounted for 44% of total cal comorbidities were described. Distribution of cases by gen- expenditures on adults between 18 and 64 years of age and for der, age groups, race, hospital region, hospital bed size, hospital 20% of expenditures on adults 65 years of age. In contrast, the academic status and primary coverage was reported. The preva- incidence of end-stage renal disease (ESRD) is decreasing, though lence of specific renal diseases and commonly associated diag- it remains as high as 1424 cases per million population in adults noses was determined. 65 years of age. Among patients on dialysis, the total number of The rate of occurrence of bleeding, transfusion, nephrec- deaths in 2014 was 172.8 per 1000 patient-years. Moreover, tomy and other frequently reported procedure complications Medicare expenditures on beneficiaries with ESRD reached was identified. Outcomes studied include mortality, length of US$32.8 billion during that period. Whereas it is estimated that stay and total cost adjusted for inflation. Data processing 40% of patients with CKD have diabetes, the incidence of ESRD and analysis was performed using Microsoft Excel 2013 and due to diabetes was 2282 per million population. Given the signifi- Statistical Package for the Social Sciences version 23 software cant cost and mortality associated with renal disease, accurate (IBM, Armonk, NY, USA). and timely diagnostic procedures are an essential part of the care Categorical variables were expressed as frequency, rate and of these patients. While renal biopsy has been used to identify the percentage while continuous variables were expressed as mean cause of renal disease since 1923, novel technologies involving (standard deviation). An independent sample t-test was used proteomics are now being evaluated as noninvasive alternatives for comparison between means at a 99% confidence level and a [2, 3]. Information from a renal tissue sample is not always con- binary logistic regression was used for risk analysis. clusive, however, it remains helpful in certain clinical scenarios [4]. Although renal biopsy is performed to identify treatment mod- ifiable causes of kidney disease, large-scale data studying the safety and outcome of percutaneous native kidney biopsy in hos- Results pitalized patients are lacking. A total of 175 831 hospital admissions where percutaneous renal Percutaneous renal biopsy is the most commonly used biopsy was performed were identified between 2008 and 2012. method to obtain renal tissue, with an open surgical procedure 11 190 hospitalizations involving patients <18 years of age were reserved for patients with contraindications to a percutaneous excluded. One hundred and fifty-six cases missing data ele- approach [4, 5]. Novel ways of obtaining renal tissue include ments on gender or mortality were also excluded. After exclud- transjugular and laparoscopic approaches [6–8]. Studies on the ing patients with a transplanted kidney, a total of 118 064 cases benefit and safety of a renal biopsy are available for review. In a were included in the subsequent analysis (Appendix, Table B). study by Kropp et al. [9], in 46 patients with CKD undergoing The mean age was 55.36 years and the average number of renal biopsy or nephrectomy, 9% of samples were inconclusive. chronic medical conditions was 6.27 (Appendix, Table C). Earlier studies [10, 11] concluded that a renal biopsy altered Deficiency anemia, congestive heart failure, diabetes, hyper- management in 19–42% of cases, but a recent study by Kitterer tension and renal failure were reported, among others, as exist- et al. [12] concluded that a disease responsive to treatment mod- ing medical comorbidities (Table 1). ification was identified in 74% of cases. Bleeding is a common Patients undergoing percutaneous renal biopsy were 52.5% complication occurring in 1.2% of cases of percutaneous native males. The majority of patients were between 38 and 77 years of kidney biopsy and in 0.2% of cases of percutaneous biopsy of a age. Patients were 55.8% White, 22.9% Black and 13.7% Hispanic. transplanted kidney [13, 14]. In a meta-analysis published in More cases were encountered in the South (40.5%) and in large 2012, 3.5% of patients had macroscopic hematuria and 0.9% of hospitals (71.3%). Cases from urban teaching hospitals compro- patients required erythrocyte transfusion after a percutaneous mised 57.2% compared with 42.8% from urban nonteaching or renal biopsy. Urinary tract obstruction, unilateral nephrectomy rural hospitals. Medicare or Medicaid were the primary payers and death occurred in 0.3, 0.01 and 0.02% of those cases, respec- in 54.4% of patients compared with 32.5% covered by private tively. Despite the number of studies available, a conclusive health insurance (Table 2). data on the use of inpatient percutaneous renal biopsy and the ICD-9 diagnostic code 58089 (acute glomerulonephritis with frequency of complications is still lacking at the national level. other specified pathological lesion in kidney) was the most fre- In this study we present data on the use of inpatient percutane- quently reported diagnosis among acute glomerulonephritis, ous native renal biopsy during inpatient hospitalization of US whereas 5821 (chronic glomerulonephritis with lesion of mem- adults between 2008 and 2012. We describe baseline patient branous glomerulonephritis) was the most frequently reported characteristics and medical comorbidities, identify the fre- diagnosis among chronic glomerulonephritis. ICD-9 diagnostic quency of complications, report associated renal pathologies code 5819 (nephrotic syndrome with unspecified pathological and discuss hospitalization outcomes. lesion in kidney) was the most frequently reported diagnosis among nephrotic group diagnoses, while 58381 (nephritis and nephropathy, not specified as acute or chronic, in diseases clas- Materials and methods sified elsewhere) was the most frequently reported diagnosis Data from the Nationwide Inpatient Sample (NIS) database, from among nephritis and nephropathy group. Code 5845 (acute kid- 1 January 2008 to 31 December 2012, was studied. International ney failure with lesion of tubular necrosis) was identified in Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 332 | A.A. Al Turk et al. Table 1. Baseline patient comorbidities Table 2. Distribution of cases by gender, age group, race, hospital region, hospital bed size, hospital academic status and primary Comorbidities Percentage coverage Acquired immune deficiency syndrome 0.8 Characteristic Percentage Alcohol abuse 3.9 Chronic blood loss anemia 2.6 Gender Chronic pulmonary disease 15.4 Male 52.5 Coagulopathy 11.2 Female 47.5 Collagen vascular disease/rheumatoid arthritis 6.4 Age group (years) Congestive heart failure 14.1 18–37 19.8 Deficiency anemia 49.1 38–57 31.6 Depression 8.3 58–77 37.8 Diabetes, uncomplicated 15.8 78 10.8 Diabetes with chronic complications 12.6 Race Drug abuse 3.9 White 55.8 Fluid and electrolyte disorders 49.7 Black 22.9 Hypertension 44.6 Hispanic 13.7 Hypothyroidism 10.7 Asian or Pacific Islander 3.2 Liver disease 5.2 Native American 0.7 Lymphoma 2.4 Other 3.7 Metastatic cancer 2.2 Hospital region Obesity 12.8 Northeast 17.8 Other neurological disorders 4.9 Midwest or North Central 22.2 Paralysis 1.6 South 40.5 Peripheral vascular disorders 4.9 West 19.5 Psychosis 3.5 Hospital bed size Pulmonary circulation disorders 4.1 Small 7.1 Renal failure 26.5 Medium 21.6 Solid tumor without metastasis 2.9 Large 71.3 Valvular disease 4.7 Hospital academic status Weight loss 9.7 Rural or urban nonteaching 42.8 Urban teaching 57.2 Primary coverage Medicare or Medicaid 54.4 15.2% of the cases. As a reported diagnosis, 1% of cases had Private 32.5 renal sclerosis (587—renal sclerosis, unspecified) (Table 3). Self-pay, no charge, or other 13.1 In CKD, more cases were classified into Stages 3 and 4, with 8.7% and 6.5%, respectively. As a reported diagnosis, 13.3% of cases had ESRD (Appendix, Table D). Among kidney-related neoplasm, 9.6% were malignant, 0.8% were benign and 0.7% comparing the length of stay between teaching and non- teaching hospitals. Patients admitted electively were discharged were secondary metastatic (Appendix, Table E). Among DRG 24 codes, 316 (renal failure) was the most fre- an average of 5.4 days earlier (P< 0.01) (Table 6). After adjusting for inflation, the average cost per hospitaliza- quent at 29.9%, followed by 331 (other kidney and urinary tract diagnoses with major complications or comorbidities) at 8%. tion was US$22 917 (Appendix, Table C). Males had a slightly lower but significant difference in the total cost compared with Connective tissue disorders with major complications or comorbidities (code 240) was next at 7.6%, followed by 315 (other females (22 639 versus US$23 224; P< 0.01). A nonelective nature of an admission and an admission to an urban teaching hospital kidney and urinary tract procedure) at 4.1%. Table 4 lists all the DRG 24 codes with a rate of occurrence 1%. were associated with a higher total cost. A nonelective admis- sion was US$9500 more expensive than an elective admission, The need for packed red blood cell (PRBC) transfusion was the most frequently reported complication (261/1000). This was while the difference between teaching and non-teaching hospi- tals approached US$3000 (Table 6). Hematuria was associated followed by hematuria, bleeding and hypotension (129/1000, 78/ 1000 and 40/1000, respectively). Death occurred in 18 of 1000 with a lower admission cost, however, the need for PRBC trans- fusion, occurrence of bleeding and hypotension were associated hospital admissions. Ileus was reported at a rate of 15/1000. Kidney laceration and the need for nephrectomy occurred less with a higher cost. Interestingly, performing a nephrectomy or an open renal biopsy had no significant impact on the mean frequently (1/1000 and 0.4/1000, respectively). During the course of hospitalization, a repeat percutaneous renal biopsy was cost of an admission (Appendix, Table F). In an attempt to identify predictors of increased mortality in needed in 14 of 1000 cases, whereas an open renal biopsy was performed in 0.2 of 1000 cases (Table 5). patients admitted for a percutaneous renal biopsy, a binary logistic regression analysis was performed using a forward like- While neither gender nor hospital academic status had an impact on inpatient mortality, patients admitted electively had lihood ratio model. Advanced age was found to be associated with the highest predicted mortality, with an odds ratio (OR) of significantly lower mortality rates when compared with non- electively admitted patients (0.99 versus 2.01%; P< 0.01) (Table 6). 18.8. Patients with metastatic cancer, acute kidney injury, coagulopathy or liver disease at baseline had a higher predicted The average length of stay was 10.65 hospital days (Appendix, Table C). Females had a slightly higher but statisti- mortality as well (OR 6.2, 3.9, 2.7 and 2.1, respectively). Among the studied complications, the need for PRBC transfusion was cally significant length of stay compared with males (10.9 ver- sus 10.5 days; P< 0.01). A similar effect was observed when the best predictor for increased mortality, followed by Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 333 Table 3. Frequency of reported pathology among patients undergoing percutaneous native kidney biopsy ICD-9 diagnosis code ICD-9 diagnostic code description Percentage Acute glomerulonephritis 5800 Acute glomerulonephritis with lesion of proliferative glomerulonephritis 0.4 5804 Acute glomerulonephritis with lesion of rapidly progressive glomerulonephritis 0.8 58081 Acute glomerulonephritis in diseases classified elsewhere 1.2 58089 Acute glomerulonephritis with specified pathological lesion in kidney 3.9 5809 Acute glomerulonephritis with unspecified pathological lesion in kidney 1.4 Nephrotic syndrome 5810 Nephrotic syndrome with lesion of proliferative glomerulonephritis 0.1 5811 Nephrotic syndrome with lesion of membranous glomerulonephritis 1.9 5812 Nephrotic syndrome with lesion of membranoproliferative glomerulonephritis 0.4 5813 Nephrotic syndrome with lesion of minimal change glomerulonephritis 0.4 58181 Nephrotic syndrome in diseases classified elsewhere 4.1 58189 Nephrotic syndrome with specified pathological lesion in kidney 0.4 5819 Nephrotic syndrome with unspecified pathological lesion in kidney 7.6 Chronic glomerulonephritis 5820 Chronic glomerulonephritis with lesion of proliferative glomerulonephritis N 5821 Chronic glomerulonephritis with lesion of membranous glomerulonephritis 1.2 5822 Chronic glomerulonephritis with lesion of membranoproliferative glomerulonephritis 0.1 5824 Chronic glomerulonephritis with lesion of rapidly progressive glomerulonephritis 0.1 58281 Chronic glomerulonephritis in diseases classified elsewhere 0.9 58289 Chronic glomerulonephritis with specified pathological lesion in kidney 0.5 5829 Chronic glomerulonephritis with unspecified pathological lesion in kidney 0.3 Nephritis and nephropathy 5830 Nephritis and nephropathy, not specified as acute or chronic, with lesion of proliferative glomerulonephritis 0.3 5831 Nephritis and nephropathy, not specified as acute or chronic, with lesion of membranous glomerulonephritis 0.6 5832 Nephritis and nephropathy, not specified as acute or chronic, with lesion of membranoproliferative 0.7 glomerulonephritis 5834 Nephritis and nephropathy, not specified as acute or chronic, with lesion of rapidly progressive 1.2 glomerulonephritis 5836 Nephritis and nephropathy, not specified as acute or chronic, with lesion of renal cortical necrosis N 5837 Nephritis and nephropathy, not specified as acute or chronic, with lesion of renal medullary necrosis N 58381 Nephritis and nephropathy, not specified as acute or chronic, in diseases classified elsewhere 10.9 58389 Nephritis and nephropathy, not specified as acute or chronic, with specified pathological lesion in kidney 3.2 5839 Nephritis and nephropathy, not specified as acute or chronic, with unspecified pathological lesion in kidney 4.7 Acute renal failure 5845 Acute kidney failure with lesion of tubular necrosis 15.2 5846 Acute kidney failure with lesion of renal cortical necrosis N 5847 Acute kidney failure with lesion of renal medullary [papillary] necrosis N 5848 Acute kidney failure with specified pathological lesion in kidney 1.7 5849 Acute kidney failure, unspecified 48.6 Renal sclerosis 587 Renal sclerosis, unspecified 1 N, negligible. Table 4. Most frequently associated DRG 24 code in patients undergoing percutaneous native kidney biopsy DRG 24 code DRG 24 code description Percentage 316 Renal failure 29.9 331 Other kidney and urinary tract diagnoses with major complications or comorbidities 8.0 240 Connective tissue disorders with major complications or comorbidities 7.6 315 Other kidney and urinary tract procedures 4.1 303 Kidney and ureter procedures for neoplasm 3.9 318 kidney and urinary tract neoplasm with major complications or comorbidities 3.3 332 Other kidney and urinary tract diagnoses 2.5 127 Heart failure and shock 2.4 576 Septicemia without mechanical ventilation >96 h 1.9 403 Lymphoma and nonacute leukemia with major complications or comorbidities 1.8 239 Pathological fractures and musculoskeletal and connective tissue malignancy 1.5 468 Extensive operating room procedure unrelated to principal diagnosis 1.4 304 Kidney and ureter procedures for nonneoplasm with major complications or comorbidities 1.0 452 Complications of treatment with major complications or comorbidities 1.0 Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 334 | A.A. Al Turk et al. Table 5. Frequency of reported complications of percutaneous native kidney biopsy Complication ICD-9 code Rate per 1000 cases PRBC transfusion 9904 261 Hematuria 5997, 59970, 59971, 59972 129 Bleeding 4590, 99811, 99812 78 Hypotension 4580, 45829, 4588, 4589 40 Death 18 Ileus 5601 15 Repeat percutaneous renal biopsy 5523 14 Kidney laceration 86600, 86601, 86602, 86603, 86610, 86611, 86612, 86613 1 Nephrectomy 554, 5551, 5552, 5554 0.4 Open renal biopsy 5524 0.2 ICD-9 procedure code. ICD-9 diagnostic code. Table 6. Variation in inpatient mortality, length of hospital stay and cost by gender, hospital academic status and admission urgency Gender Hospital academic status Admission urgency Male Female P-value Rural or urban nonteaching Urban teaching P-value Nonelective Elective P-value Mortality (%) 1.90 1.71 0.13 1.80 1.83 0.67 2.01 0.99 <0.01 Length of stay (days) 10.5 10.9 <0.01 10.2 10.9 <0.01 11.7 6.3 <0.01 Cost (US$) 22 639 23 224 <0.01 21 173 24 135 <0.01 24 780 15 168 <0.01 hypotension (OR 2.0 and 1.7, respectively). The Nagelkerke R - diseases were present, with focal segmental glomerulosclerosis value of this regression model was 0.158. (FSGS) and ATN being two of the top disorders found in dia- betics. While FSGS can be explained by hypertension and obe- sity being more prevalent in the diabetes population, the Discussion mechanism for the increased incidence of ATN has not been elucidated to date. Perhaps more importantly, up to 36% of The prevalence of CKD in the USA was 14.8% as recently as 2014. While CKD Stage 2 decreased in prevalence, CKD Stage 3 patients did not have signs of diabetic kidney disease at all, car- rying alternative diagnoses such as membranous nephropathy has increased over the period 1999–2014 and is currently present in >6% of the US adult population [1]. In our data and pauci-immune glomerulonephritis. Some of these causes are potentially amenable to immunosuppressive therapy, which search, renal failure was identified as the primary diagnosis in hospitalized patients undergoing kidney biopsy. A study per- can lead to increased renal survival. ~ Our study, while quantifying the number of renal biopsies formed by Liano et al. [15] found that acute tubular necrosis (ATN) was the most common cause of acute kidney injury performed, relied on ICD-9 and DRG coding for diagnostic infor- mation. Glomerulonephridities together composed nearly 10% treated by nephrologists. Typically ATN is a clinical diagnosis and is treated with supportive care. In our study, ATN was iden- of renal biopsies performed, however, identifying the specific etiologies of glomerulonephritis was beyond the scope of this tified in 15.2% of biopsies. As discussed by Haas et al. [16], in patients whose clinical presentations are not consistent with study due to the nature of the database and the ICD-9 and DRG coding systems. About 15% of renal biopsies were performed for ATN, obstructive or prerenal causes, prebiopsy and postbiopsy diagnoses differed in up to one-third of cases. We feel that this nephrotic syndrome; membranous nephropathy was diagnosed in 2% of cases. Renal malignancy was identified in nearly 10% highlights the utility and significance of renal biopsy to diag- nose renal dysfunction when the clinical presentation is not of patients. Previous data on percutaneous renal biopsy concluded that conclusive. Indications for percutaneous renal biopsy are largely driven it is a safe procedure, with several studies showing a significant complication rate of 1% [20, 21]. It was also shown to be highly by clinical presentation and expert opinion [17, 18]. Some com- mon indications include acute kidney injury lasting >3 weeks, sensitive and specific in diagnosing primary renal malignancy, with close to 100% accuracy [22]. In contrast to a study by proteinuria >1 g/day, renal involvement of systemic disease and hematuria presumed to be of renal origin. Diabetes mellitus Tondel et al. [23] where gross hematuria was the most fre- quently reported complication (1.9%), hematuria was reported is the most common cause of CKD and ESRD, with most patients not requiring biopsy for diagnosis. Our search revealed that in 12.9% of our patients while the rate of occurrence of PRBC transfusion was 26.1%. Bleeding without the need for PRBC 28.4% of biopsied patients carried a diagnosis of diabetes, which is consistent with the 25% figure proposed in a study performed transfusion was less frequently reported. This may be due to underreporting of bleeding as a complication or due to the use by Sharma et al. [19]. Indications for renal biopsy in diabetic patients are nephrotic-range proteinuria or significant decline of PRBC transfusion for indications other than acute blood loss. Of note, the frequency of PRBC transfusion, hematuria and in renal function that exceeds the patient’s natural history of their disease [18]. While initial evaluation can suggest diabetic bleeding were much higher in our study than in previous stud- ies. Given that our study included a national database, we think nephropathy, up to 60% of diabetic patients may have kidney findings other than diabetic nephropathy [19]. Several other that our study reveals the true incidence of the aforementioned Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 Outcomes of percutaneous native kidney biopsy | 335 complications in the USA. Prior studies reporting lower compli- compared with other patients (23.6 versus 10.4 days; P< 0.01). In cation rates may be related to the selection of centers where elective admissions, the average length of stay was 6.3 days, renal biopsies were performed and perhaps is also related to a which decreased to 6.1 days when excluding deaths. This length selection bias, with patients enrolled in these studies being less of stay is longer than expected considering the trend towards sick. For example, 11.2% of patients in our study had preexisting outpatient observation after biopsy. Since the NIS database coagulopathy while, such patients were excluded in other includes information on hospitalized patients only, patients biopsy series [24]. The difference in complication rates observed who underwent a percutaneous renal biopsy under observation between our data and the data from the national registry for status were not studied. This is a potential source of bias toward renal biopsy in Norway may be partly related to the higher the longer length of stay reported in our study. mean age of patients analyzed in our study (55.36 years com- Due to advances in CKD and ESRD care, the life expectancy pared with 50.6 years) [23]. The Norwegian data included of patients with renal disease is increasing [1]. As a result, the patients with renal biopsies performed both in outpatient and expenditures for ESRD have doubled during the 2003–2014 inpatient settings; the data from the NIS database pertains to period, from 16 billion to US$32 billion. It is difficult to properly patients who are only admitted to the hospital, hence a sicker assess the economic burden of CKD, but a study by Wang et al. population. Identifying the true incidence of reported complica- [25] revealed a linear increase in health care utilization and eco- tions is an aid for clinicians when weighing the risks and bene- nomic burden as patients advance from early to advanced-stage fits of a percutaneous renal biopsy and in obtaining true CKD. In our study, a higher cost was observed both in patients informed consent. with nonelective admissions and with admissions to urban Due to the nature of the database used, several elements teaching hospitals. Whereas a shorter length of stay can explain were missing in our analysis. These elements include the use of the lower cost observed in elective admissions, a slightly longer real-time ultrasound technology, the needle size used for length of stay cannot fully account for the higher cost observed biopsy, the number of passes performed and the number of in teaching hospitals. One explanation could be the variation in cores obtained and the level of experience and specialty of the disease severity among hospitals, along with more advanced operator. In a prior study, however, the needle size used, the diagnostic testing and procedures done at academic centers, number of needle passes, and the specialty of the operator had resulting in higher hospital bills. With the exception of hematu- no influence on the rate of major complications of a percutane- ria, complications from a percutaneous renal biopsy resulted in ous renal biopsy [23]. Also not included were the number of an increase in admission cost. The lack of significance in cases patients on antiplatelet or anticoagulation therapy and the where a nephrectomy or an open renal biopsy was performed is number of patients who underwent arterial embolization ther- likely due to the small number of patients in these groups. apy in an attempt to control bleeding after a renal biopsy. In this analysis of percutaneous renal biopsies in hospital- Our database search showed an overall mortality of 1.8%. ized patients we found that PRBC transfusion and hematuria While this value could be directly related to the renal biopsy occurred at a rate of 26.1% and 12.9% respectively, and that performed, it is more likely due to the nature of the acute dis- occurrence of bleeding, ileus or PRBC transfusion was associ- ease leading to hospitalization and related complications. This ated with an increased hospitalization cost. Renal biopsy is further supported when comparing the mortality rate of elec- remains the gold standard for diagnostic, prognostic and thera- tive admissions (0.99%) with nonelective admissions (2.01%). peutic purposes in many renal diseases; however, other techni- Again we see the discrepancy in mortality rate between our ques, such as proteomics, are being increasingly studied as study and prior work, thus solidifying the idea of bias existing noninvasive alternatives [3, 24]. The use of these technologies towards a lower rate of complications in previous studies. may eventually replace renal biopsy as a primary means of Interestingly, there was no difference in mortality rate between determining individual renal pathology. Developing a compre- teaching and nonteaching hospitals. hensive national registry of renal biopsy findings would serve The appropriate observation period following a percutane- the dual purpose of being able to directly compare tissue diag- ous renal biopsy is still undefined. The practice varies from nosis to noninvasive techniques and to clearly identify those at 4–8 h of observation to an overnight admission. According to a highest risk for progression of renal disease. By revealing com- large biopsy series, up to 7.4% of major complications occur plication rates of percutaneous renal biopsy and identifying 12–24 h after biopsy [24]. Studies that advocate the safety of out- underlying renal disease in hospitalized patients while also pro- patient observation typically include doing a Doppler ultra- viding an in-depth analysis of hospitalization outcomes, we sound postprocedure, frequent vital checks and serial believe that our study helps to emphasize both the financial hemoglobin level monitoring [21]. However, this is labor inten- and scientific aspects of kidney disease in the USA. sive and costly, thus negating the cost benefit of preventing a hospitalization. Patients who have an increased mortality risk Supplementary data after renal biopsy may benefit from a prolonged observation period. Our study identified advanced age, the presence of Supplementary data are available online at http://ckj.oxford metastatic cancer, acute kidney injury, liver disease and coagul- journals.org. opathy as predictors of higher mortality. However, the Nagelkerker R-squared value of our model was low, 0.158. We also found that academic institutions perform renal biopsies at Conflicts of interest statement a rate 1.3 times that of nonacademic hospital institutions, likely None declared. due to a large referral base. A nonelective admission was found to be a major contribu- References tor to an increased length of stay, likely secondary to the nature of acute illness requiring hospitalization and a prolonged treat- 1. United States Renal Data System. 2016 USRDS Annual Data ment duration. Furthermore, patients who did not survive the Report: Epidemiology of Kidney Disease in the United States. admission had a statistically significant longer length of stay Bethesda, MD: National Institutes of Health, National Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018 336 | A.A. Al Turk et al. 15. Liano ~ F, Pascual J. 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Bleeding complications of update and evidence for best practice. Clin J Am Soc Nephrol native kidney biopsy: a systematic review and meta-analy- 2016; 11: 354–362 sis. Am J Kidney Dis 2012; 60: 62–73 25. Wang V, Vilme H, Maciejewski ML et al. The economic bur- 14. Atwell TD, Spanbauer JC, McMenomy BP et al. The timing den of chronic kidney disease and end-stage renal disease. and presentation of major hemorrhage after 18,947 image- Semin Nephrol 2016; 36: 319–30 guided percutaneous biopsies. AJR Am J Roentgenol 2015; 205: 190–195 Downloaded from https://academic.oup.com/ckj/article-abstract/11/3/330/4562540 by Ed 'DeepDyve' Gillespie user on 20 June 2018

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Clinical Kidney JournalOxford University Press

Published: Oct 23, 2017

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