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Clinical Chemistry 52: 680-685, 2006. First published February 23, 2006; 10.1373/clinchem.2005.062562
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(Clinical Chemistry. 2006;52:680-685.)
© 2006 American Association for Clinical Chemistry, Inc.

Proteomics and Protein Markers

B-Type Natriuretic Peptide (BNP) and N-Terminal Pro-BNP in Obese Patients without Heart Failure: Relationship to Body Mass Index and Gastric Bypass Surgery

John V. St. Peter1,3,a, Guilford G. Hartley2,3, MaryAnn M. Murakami4 and Fred S. Apple2,4

1 College of Pharmacy and 2 School of Medicine, University of Minnesota, Minneapolis, MN.
Departments of3 Medicine and 4 Laboratory Medicine and Pathology, Hennepin County Medical Center, Minneapolis, MN.

aAddress correspondence to this author at: Experimental & Clinical Pharmacology, University of Minnesota, College of Pharmacy, Weaver Densford Hall 7-115A, 308 Harvard Street SE, Minneapolis, MN 55455-0343. Fax 612-625-3927; e-mail stpet003{at}umn.edu.


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Further investigations are warranted to better characterize variables that may confound the clinical interpretation of plasma natriuretic peptide measurements, which are increasingly recognized to have diagnostic and predictive importance.

Methods: Blood samples (EDTA plasma) from patients (n = 206) attending clinics for the medical treatment and follow-up of obesity were analyzed for B-type natriuretic peptide (BNP; Bayer assay) and the N-terminal segment of its prohormone (NT-proBNP; Roche assay). Natriuretic peptide concentration ranges were evaluated in those without diagnosis of congestive heart failure (CHF) or chronic kidney disease (CKD).

Results: BNP and NT-proBNP were directly correlated (r = 0.87; P = 0.01), with NT-proBNP concentrations higher relative to BNP. Of obese patients without CHF or CKD, 21.6% (40 of 185) had NT-proBNP concentrations greater than the published assay upper reference limit. Concentrations of both natriuretic peptides were higher in patients currently exposed to beta blockers, patients with the diagnosis of hypertension or type 2 diabetes, and patients with a history of gastric bypass surgery. An inverse relationship between body mass index (BMI) and both BNP and NT-proBNP was evident. According to the National Institutes of Health, National Heart, Lung, and Blood Institute classification, more than 95% of the participants sampled in this study were either obesity class 2 (35 kg/m2 < BMI < 39.9 kg/m2) or class 3 (BMI ≥40 kg/m2)

Conclusions: A substantial proportion of obese patients without CHF or CKD have concentrations greater than the upper reference limit for NT-proBNP but not for simultaneously measured BNP. A history of gastric bypass surgery appeared to be a significant predictor of increased natriuretic peptide concentrations when assessed in a population of patients with class 2 or 3 obesity.


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Physiologic and pathologic states leading to volume expansion and/or increased tension on cardiac myocytes lead to up-regulation of signals for the production and secretion of cardiac natriuretic prohormones, including A-, B-, and C-type natriuretic peptides (1). Plasma concentrations of the cardiac natriuretic peptides B-type natriuretic peptide (BNP) 1 and its N-terminal prohormone (NT-proBNP) are used in various clinical settings to aid in the real-time diagnosis of heart failure (2)(3). Additionally, recent prospective investigations have highlighted the possible prognostic potential of BNP and NT-proBNP in patients with and without heart failure (4)(5)(6).

Controlled clinical trials continue to define the potential utility of measuring natriuretic peptide concentrations, but no consensus exists regarding standardization and application of cardiac natriuretic peptides as biomarkers for diagnostic and prognostic applications (3)(7)(8)(9). Many variables, such as age, sex, and diseases and their related drug therapies, as well as assay methods have been found to affect or confound the interpretation of blood natriuretic peptide concentrations (5)(6)(10) and may be independent predictors of increased natriuretic peptide concentration (11)(12)(13). In the context of other demographic and diagnostic markers of clinical status or disease, obesity is not generally noted to be an independent predictor of natriuretic peptide concentrations (11); however, body size measured as body mass index (BMI, kg/m2) appears to exhibit a consistent inverse relationship to natriuretic peptide concentrations. In large cohort studies of patients with or without heart failure, greater obesity or BMI was significantly associated with lower natriuretic peptide concentrations compared with concentrations in leaner cohort members (11)(14).

The many different assay methods for BNP and NT-proBNP further confound the comparability of reports of the diagnostic significance of various peptide concentrations (10). Therefore, confusion may arise among clinicians regarding the collection, processing, and storage of biological samples for measurement of natriuretic peptide concentrations; the interpretation of concentration results; and most importantly, the biological variability of these various peptide moieties.

Despite extensive research, simultaneous assessment of BNP and NT-proBNP in large numbers of patients and controls has not been performed. We therefore undertook a prospective, cross-sectional study to determine the percentage of severely obese patients with BNP and NT-proBNP concentrations outside the reference intervals to assess relationships between simultaneously determined natriuretic peptide concentrations and severe obesity, common medication therapies, and common comorbidities.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
A wide cross-section of consecutive patients (n = 206) attending an obesity clinic donated a blood sample for simultaneous assay of BNP and NT-proBNP concentrations. The protocol was reviewed and approved by the local Human Subjects Research Committee, and all participants gave signed informed consent. One of the authors (G.G.H.) extracted individual demographic data from medical records, including health history, diagnoses, current medications, pertinent physical examination findings, and laboratory results. All patients with evidence of kidney dysfunction at the time the blood sample was obtained were considered to have chronic kidney disease (CKD). All patients whose serum creatinine was >124 µmol/L (1.4 mg/dL) on the date of specimen acquisition or of the most recent prior determination or who had episodically recurring increases in serum creatinine to >124 µmol/L (1.4 mg/dL) before specimen acquisition were identified. All patients whose clinical history revealed a diagnosis of heart failure (based on a combination of assessments of the patient over a period of time and with a range of modalities, including symptoms, physical findings, cardiac imaging, and response to therapy) were considered to have congestive heart failure (CHF). Complete demographic information could not be obtained for 2 patients, and they were excluded before summarization of the demographic data of the screened population.

All blood samples were collected in glass tubes containing EDTA as anticoagulant and centrifuged within 4 h; the resulting plasma was frozen in plastic tubes at –20 °C until analyzed. NT-proBNP concentrations were determined with an electrochemiluminescent assay on the Elecsys® 2010 platform (Roche Diagnostics). The limit of detection was 5 ng/L with total imprecision (as CV) <3% at concentrations of 200 to 500 ng/L. BNP concentrations were determined with a 2-site sandwich chemiluminescent immunoassay on the ADVIA® Centaur® platform (Bayer Diagnostics Corporation). The limit of detection for this assay was 2 ng/L with total imprecision (as CV) <5% at concentrations of 29 to 1400 ng/L.

Patient information was coded and grouped by the presence or absence of diagnostic and/or medication categories. For both the BNP and NT-proBNP assays, plasma concentrations less than the respective lower limits of detection were assigned values equal to the detection limits for analysis purposes. Plasma concentrations of NT-proBNP and BNP did not follow a gaussian distribution and were log-transformed before statistical analysis. Correlation between the simultaneously measured natriuretic peptides was assessed by Pearson correlation. For the primary analysis, data from patients with a diagnosis of heart failure or kidney disease were excluded. We used the independent Student t-test for univariate comparisons of log-transformed peptide concentrations within each demographic category, grouped by the presence or absence of the condition or drug therapy. We used log-transformed BNP and NT-proBNP concentrations as the dependent variable and factors identified from univariate comparisons to construct analyses of covariance general linear models. Potential interaction between terms was assessed. Final models were identified by stepwise addition of significant factors and observation of the relative stability of each sequential model.

We used linear regression analysis with BMI as a continuous independent variable to assess the relationship between obesity and log-transformed BNP and NT-proBNP concentrations. Values for the continuous variables are given as the mean (SD) unless otherwise specified. Categorical variables are noted as counts (percentage of within-sex total). We used Pearson {chi}2 analysis to identify differences in distributions of categorical variables. All statistical analyses were performed with SPSS for Windows (Ver. 12.0), and statistical significance was assumed at P = 0.05.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The demographics of all study participants with complete demographic information (n = 204) are outlined in columns 1 and 2 of Table 1 . Approximately 76% (156 of 204) of participants were women. According to the National Institutes of Health, National Heart, Lung, and Blood Institute recognized classification of obesity, more than 95% of the participants sampled in this study were either obesity class 2 (35 kg/m2 < BMI < 39.9 kg/m2) or class 3 (BMI ≥40 kg/m2) (15). Compared with female participants, males were older, heavier, and more likely to have diagnoses of hypertension and sleep apnea. Men used diuretics and insulin more frequently than did women. Cohort demographic data after exclusion of 19 individuals with diagnoses of CHF (n = 13), CKD (n = 5), or concurrent CHF and CKD (n = 1) are shown in columns 3 and 4 of Table 1 . For participants with a diagnosis of CHF, BNP concentrations were 2–308 ng/L and NT-proBNP concentrations were 31–1572 ng/L. For the 5 patients excluded for CKD, BNP concentrations were 2–511 ng/L and NT-proBNP concentrations were 22–2771 ng/L. The 1 patient with both CHF and CKD had BNP and NT-proBNP concentrations of 325 and 2708 ng/L, respectively.


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  		Table 1. Patient demographics for the entire patient group (uncensored) and the obese patients without CKD or CHF (censored).

Assessment of the entire sample (n = 204; r = 0.87; P = 0.01) and the censored sample (n = 185; r = 0.85; P = 0.01) showed that plasma concentrations of BNP and NT-proBNP were directly correlated. As expected, NT-proBNP concentrations were higher than those of BNP. A plot of the paired concentrations of each natriuretic peptide for all patients without CHF or CKD (n = 185) is shown in Fig. 1 , which includes lines representing the stated upper reference limit for each peptide. Of the 185 patients in the censored sample, 40 (21.6%) had NT-proBNP concentrations above the upper reference limit, with a median value of 208 ng/L (range, 126–684 ng/L). None of the BNP measurements were above the stated upper reference limit.


Figure 1
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  		Figure 1. Plasma concentrations of BNP vs NT-proBNP in 185 severely obese patients without CHF or CKD.

Dashed lines represent the stated upper reference limits for BNP (100 ng/L) and NT-proBNP (125 ng/L).

For the entire cohort (n = 204), linear regression of log-transformed natriuretic peptide concentrations vs BMI demonstrated nonsignificant inverse trends. The censored cohort (n = 185; Fig. 2 ) showed similar inverse but weak relationships for both BNP (r = –0.172; P = 0.019) and NT-proBNP (r = –0.133; P = 0.070).


Figure 2
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  		Figure 2. BMI vs plasma natriuretic peptide concentrations (n = 185).

(A), BNP. Solid line represents the linear regression relationship: BNP = –0.98(BMI) + 33 (r = 0.17; P = 0.019). (B), NT-proBNP. Solid line represents the linear regression relationship: NT-proBNP = –0.98 (BMI) + 130 (r = 0.13; P = 0.07).

Patients with class 3 obesity had lower NT-proBNP concentrations than those with class 2; however, this difference was not observed with BNP. When we considered other variables, including history of gastric bypass surgery, presence of type 2 diabetes, diagnosis of hypertension, and current use of beta-blocker therapy, we observed significant differences for both BNP and NT-proBNP (Table 2 ).


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  		Table 2. Univariate P values for significant differences in natriuretic peptide concentrations grouped by demographic categories and assay type (n = 185).

The results of the final general linear model used to investigate potential predictors of natriuretic peptide concentrations, adjusting for age and BMI and using sex, history of gastric bypass surgery, presence of type 2 diabetes, diagnosis of hypertension, and current beta-blocker therapy as fixed effects, are shown in Table 3 . Age and history of gastric bypass surgery were related to higher concentrations for both BNP and NT-proBNP. Current beta-blocker therapy was identified as a predictor of increased concentrations of BNP but not of NT-proBNP. Model-adjusted mean estimates indicated that a positive gastric bypass surgery history increased BNP concentrations by ~66% compared with a negative history (mean, 20 ng/L with surgical history vs 12 ng/L without). For NT-proBNP, a history of gastric bypass surgery increased the model mean estimate by 90% (mean, 109 ng/L with surgical history vs 57 ng/L without).


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  		Table 3. Independent predictors of log(BNP) or log(NT-proBNP) in patients with obesity (n = 185) by univariate ANOVA.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The relationship between ambient plasma concentrations of natriuretic peptides and various clinical conditions, concomitant medications, and assay conditions is of intense interest at present. We prospectively investigated several of these issues by simultaneously assessing 2 different BNP moieties, BNP and NT-proBNP, by 2 distinct assays. We observed the predictive nature of age with respect to both natriuretic peptides but did not observe the significant sex-based differences reported by others (16). Our study confirms a recognized inverse relationship between BMI and both BNP and NT-proBNP in patients with class 2 or 3 obesity without obvious CHF or CKD by history and physical examination. However, although statistically significant, the regression relationships between BMI and peptide concentrations account for only a small portion of the variability observed in BNP and NT-proBNP concentrations. Additionally, as noted by others, when taken in the context of other factors, BMI is not significantly predictive (11)(12)(14).

A novel finding from our investigation is the observation that previous gastric bypass surgery was predictive of increases in both BNP and NT-proBNP concentrations. Specifically, we detected an ~2-fold increase in both median and model-estimated mean concentrations of NT-proBNP. Although interpretation of the pathologic or physiologic significance of this finding cannot be addressed by our study, it is interesting to note that clearance of natriuretic peptides has been directly linked to the degree of adiposity and fat tissue (17)(18)(19)(20). On the basis of this observation, it could be conjectured that loss of adiposity after gastric surgery leads to loss of natriuretic peptide clearance pathways and attainment of a new, higher steady-state peptide concentration. Contrary to this line of thought are the recent findings of significant lowering of NT-proBNP concentrations 12 months after laparoscopic adjustable gastric banding in a small number (n = 34) of obese patients (21). In that study, however, both the surgical procedure and the analytic technique used for natriuretic peptide quantification were different from ours.

Limitations of this study include the use of history and physical examination from medical records as the method for characterizing CHF and CKD status. Additionally, previous studies have assessed BMI–peptide relationships across a larger BMI range. Our study had only 1 participant with BMI <30 kg/m2, all others were in the 32–68 kg/m2 range. Lastly, several variables and comorbid conditions that were not specifically screened in this project may potentially affect natriuretic peptide disposition.

In conclusion, we identified a history of gastric bypass surgery as a new factor that is related to increased plasma concentrations of BNP and NT-proBNP in a cohort of patients with a high degree of obesity. As noted previously, an overall trend for decreasing plasma concentrations of natriuretic peptides was observed. The relationship between prior gastric bypass surgery and higher concentrations of both BNP and NT-proBNP is intriguing. This observation persisted with adjustment for previously identified factors known to affect natriuretic peptide concentrations and supports the potential for the presence of a complex relationship between weight variables and natriuretic peptide concentrations. Continued investigation of the relationship between gastric bypass surgery and the physiologic or pathologic effects related to natriuretic peptide plasma concentrations is warranted.


   Acknowledgments
 
Bayer Diagnostics partially funded this investigation; however, the design and analysis of the findings were performed independent of Bayer. We thank the staff and patients of the Hennepin Center for Diabetes & Endocrinology for their efforts and participation in this project.


   Footnotes
 
1 Nonstandard abbreviations: BNP, B-type natriuretic peptide; NT-proBNP, N-terminal pro-B-type natriuretic peptide; BMI, body mass index; CKD, chronic kidney disease; and CHF, congestive heart failure.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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