Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study

Juliana Amaro Borborema Bezerra; Eduardo Pachu Raia dos Santos; Carlos Teixeira Brandt

doi:10.12688/f1000research.110214.1

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Research Article

Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study

[version 1; peer review: 1 approved with reservations]

Juliana Amaro Borborema Bezerra ¹, Eduardo Pachu Raia dos Santos², Carlos Teixeira Brandt³

PUBLISHED 12 Apr 2022

Author details Author details

¹ Faculty of Medical Sciences - UNIFACISA, CAMPINA GRANDE, Brazil
² Endoscopic and Obesity Surgery Institution – ICOEP, Campina Grande, Brazil
³ Federal University of Pernambuco, Recife, Brazil

Juliana Amaro Borborema Bezerra
Roles: Conceptualization, Investigation, Supervision, Validation, Writing – Original Draft Preparation

Eduardo Pachu Raia dos Santos
Roles: Investigation, Validation, Visualization, Writing – Review & Editing

Carlos Teixeira Brandt
Roles: Conceptualization, Data Curation, Formal Analysis, Project Administration, Supervision, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

Abstract

Background: Obesity is a global pandemic, caused by genetic, biological and social factors, increasing the risk of many chronic diseases, including kidney disease. Bariatric surgery can control associated comorbidities and also improve renal function. Thus, the aim of this study was to evaluate the effect of bariatric surgery on renal function and associated factors, through bivariate analysis.
Methods: A cohort, prospective, analytical study was carried out in the Department of surgery and obesity, in Campina Grande - Paraíba, Brazil. Thirty-five obese patients were evaluated in the preoperative period of bariatric surgery and after one year of bariatric surgery. Sociodemographic and anthropometric data were collected, body mass index was calculated, and renal function was estimated through the glomerular filtration rate.
Results: Predominantly female (71.4%) and white (77.1%) patients were observed. Regarding the type of bariatric surgery, most patients (65.7%) underwent the sleeve technique. There was no significant difference between the mean levels of cystatin C pre and post bariatric surgery. There was a significant improvement in the mean glomerular filtration rates in the postoperative period (p=0.09). In further analysis of the association between the variables: type of bariatric surgery, diabetes or hypertension outcomes, no association was observed with the outcome improvement in glomerular filtration rate, without statistical significance, respectively (p = 0.312; p =0.217; p = 0.476). Similarly, there was no statistically significant difference between the variable loss of body mass index, under the effect of bariatric surgery, in relation to the outcome of the glomerular filtration rate (p = 0.904).
Conclusion: After analyzing the association between outcome of glomerular filtration rate and the studied variables, no association was observed between these variables, under the effect of bariatric surgery, with improvement in glomerular filtration rate. Thus, bariatric surgery is associated with improvement of renal function independently.

Keywords

Obesity, Bariatric surgery, Glomerular filtration rate, Cystatin C, Renal function

Corresponding author: Juliana Amaro Borborema Bezerra

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2022 Amaro Borborema Bezerra J et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Amaro Borborema Bezerra J, Pachu Raia dos Santos E and Teixeira Brandt C. Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study [version 1; peer review: 1 approved with reservations]. F1000Research 2022, 11:409 (https://doi.org/10.12688/f1000research.110214.1) First published: 12 Apr 2022, 11:409 (https://doi.org/10.12688/f1000research.110214.1) Latest published: 12 Apr 2022, 11:409 (https://doi.org/10.12688/f1000research.110214.1)

Introduction

Obesity is a global pandemic related to excessive adiposity and mediated by inflammation, with long-term damage that impairs the quality of life of obese people.¹^,² It may affect all age groups and ethnicities in many countries.³^–⁵

Adopted life-style and genetic factors are related to the genesis of obesity and associated with an increase in cancer, cardiovascular diseases, blood hypertension, type 2 diabetes mellitus (DM) and chronic kidney disease (CKD).⁶^–¹⁰

The causes of obesity-related renal impairment are multifactorial, ranging from the deleterious mechanisms of obesity-associated comorbidities in the kidneys, as well as the production of adiponectin by adipose tissue. In addition to weight gain itself with deleterious renal action leading to the onset or worsening of CKD.¹¹^,¹²

Other mechanisms for the onset of kidney injury in obesity involve oxidative stress, activation of the renin-angiotensin-aldosterone system and insulin resistance.¹³^–¹⁷

Bariatric surgery has become the main method for controlling morbidities associated with obesity, with adequate glycemic and blood pressure control, in addition to promoting sustained weight loss.¹⁸^–²²

The effect of bariatric surgery on the renal function is a subject of intensive research. In most studies, one can observe, after bariatric surgery, an improvement of glomerular filtration rate (GFR) and in preventing the onset of CKD and its progression. But in other papers, the improvement of kidney function is not so clear.²³^–²⁵

The aim of this study was to evaluate the impact of bariatric surgery on patients' renal function and associated factors through a bivariate analysis, corroborating the findings of improvement in GFR in most studies.

Methods

Study design

A cohort, prospective, analytical study was carried out in a Department of surgery and obesity, in Campina Grande - Paraíba, Brazil, between February 2019 and August 2020. The study was approved by the Ethics and Research Committee of the Faculty of Medical Sciences - UNIFACISA - Campina Grande - Paraíba, Brazil, registration number - 79501417.0.0000.5175. All patients gave written informed consent before inclusion.

Sample size

The sampling process took place in a non-probabilistic way. To calculate the sample size, the free software G*Power version 3.1.9.7 (RRID:SCR_013726, http://www.gpower.hhu.de/); was used, with a significance level of 0.05 and a test power commonly used in the literature equal to 0.80. The existence of an average effect size equal to 0.5 was also considered. The minimum number of patients estimated for the research were 34. Sixty-five patients were recruited to participate in this research.

Inclusion and exclusion criteria

Obese individuals undergoing bariatric surgery were included in this study. Those with microalbuminuria ≥ 30 mg/g were excluded, to avoid previous kidney disease, and patients with thyroid disease were excluded too. Hyperthyroidism has been shown to increase, while hypothyroidism is shown to decrease cystatin C serum concentrations, the reason why participants with thyroid disease were excluded in this study.²⁶

Procedures

All the patients were evaluated using a form regarding sociodemographic characteristics (age, gender, ethnicity, schooling and health insurance), comorbidities (pre-existing diseases) and types of surgery they would undergo. At the same time, blood pressure, weight and height were measured. The body mass index (BMI) was calculated by weight (kilograms), divided by height (by meter squared).²⁷

Later, blood samples were collected to measure serum creatinine and cystatin C. The cystatin C was measured by nephelometry and calibrated to recent cystatin C standardization, with a result expressed in mg/L. This is an endogenous marker of glomerular filtration rate (GFR) for renal function due to its high sensitivity and specificity and it is not influenced by the weight loss.²⁸^,²⁹ The GFR was estimated using Nefrocalc version 2.0 (http://www.nefrocalc.net/filtracao-7.html) through the Chronic Kidney Disease Epidemiology (CKD-Epi) collaboration equation creatinine-cystatin C and corrected for the corresponding body surface.³⁰ Hypofiltration was defined by GFR < 90 mL/min/1.73 m², normal GFR ranged between 90 and 120 mL/min/1.73 m² and hyperfiltration was defined by GFR > 120mL/min/1.73 m².³¹

Only 35 patients could be re-evaluated one year after the bariatric surgery. The others refused to undergo any type of re-evaluation because of the Covid-19 pandemic. Therefore, only 35 patients were able to continue in this cohort study out of a total of 65 obese patients were included initially.

Statistical methods

Quantitative variables were expressed as means ± standard deviation. Qualitative variables were expressed by their absolute and relative frequencies. p ≤ 0.05 was established for rejection of the null hypothesis.

In order to investigate the effect of bariatric surgery on means (pre-surgery vs post-surgery), Student's t test for paired samples was applied. In the case of variables that did not meet the normality assumption, the bootstrapping procedure (1000 re-samplings; 95% CI) was performed to obtain greater reliability of the results. Similarly, one-way ANOVA with bootstrapping correction was applied in order to verify a possible influence of the GFR outcome (remained, improved or worsened GFR between pre-surgery and post-surgery) on the mean effects of loss of BMI (loss of BMI = BMI (pre-surgery) – BMI (post-surgery)). In the case of dichotomous variables, McNemar's test was performed. Fisher's exact test was used to investigate the association between variables created in order to express the effect of bariatric surgery. Such variables were: GFR outcome, type of diabetes outcome (DM: remained non-diabetic, improved or remained diabetic) and type of hypertension outcome (Hypertension: remained non-hypertensive, improved or remained hypertensive).

Results

Predominantly, female (71.4%) and white (77.1%) patients were observed in this study. All had high school education and health insurance. The mean time of follow-up was 16.2 ± 2.6 months. Ages ranged from 24.0 to 57.0 years. Regarding the type of bariatric surgery, most underwent the sleeve type (65.7%).

In the preoperative bariatric surgery, it was observed that 31.4% were diabetic patients and 40.0% were hypertensive patients. In the postoperative surgery, among the patients with hypertension and diabetes, the majority of obese patients obtained control. Of the total of 11 pre-surgery diabetic patients, seven were no longer diabetic, and of the total of 14 pre-surgery hypertensive patients, 12 became non-hypertensive post-surgery (Table 1).

Table 1. Morbidity measured pre and post bariatric surgery.

Diabetes
		Post-surgery
		Diabetic	Non-diabetic	Total	p*
Pre-surgery	Diabetic	4 (11.4%)	7 (20.0%)	11 (31.4%)
	Non-diabetic	0 (0.0%)	24 (68.6%)	24 (68.6%)
	Total	4 (11.4%)	31 (88.6%)	35 (100.0%)	< 0.05

Hypertension
		Post-surgery
		Hypertensive	Non-hypertensive	Total	p*
Pre-surgery	Hypertensive	2 (5.7%)	12 (34.3%)	14 (40.0%)
	Non-hypertensive	0 (0.0%)	21 (60.0%)	21 (60.0%)
	Total	2 (5.7%)	33 (94.3%)	35 (100.0%)	< 0.001

* McNemar's test. Binomial distribution used.

In the post bariatric surgery there was a significant reduction in the mean abdominal circumference (p < 0.0001) and in the mean BMI in postoperative period of bariatric surgery (p < 0.0001) (Table 2). No significant difference was observed between the mean levels of cystatin C pre and post bariatric surgery (p = 0.094) (Table 2). There was a significant improvement in glomerular filtration rates in obese patients undergoing bariatric surgery (Table 2) (Figure 1).

Table 2. Clinical markers measured pre and post bariatric surgery.

Variables	Pre-surgery Mean ± SD	Post-surgery Mean ± SD	p	d of Cohen
BMI (kg/m²)*	40.3 ± 5.7	29.5 ± 4.5	<0.0001**	3.37
Glomerularfiltrationrate (mL/min/1.73 m²)***	91.9 ± 17.8	100.5 ± 14.3	0.009**	0.47
Abdominal circumference (cm)****	120.7 ± 17.8	100.6 ± 14.8	<0.0001*****	2.4
Cystatin C (mg/L)******	0.83 ± 0.196	0.77 ± 0.126	0.094*****	0.29

* BMI: body mass index kg/m² (kilograms per square meter);

** paired t test with bootstrapping procedure;

*** GFR: Glomerular filtration rate mL/min/1.73 m² (milliliters per minute per1.73 square meters);

**** Abdominal circumference cm (centimeters);

***** paired t test;

****** Cystatin C mg/L (milligrams per liter); SD: Standard Deviation.

Figure 1. **p < .001. paired t test with bootstrapping procedure.

On analyzing the association between the outcome of the variables: type of bariatric surgery, diabetes outcome and hypertension outcome, no association was observed with the outcome improvement in GFR, under the effect of bariatric surgery, without statistical significance, respectively (p = 0.312; p = 0.217; p = 0.476) (Table 3).

Table 3. Relationship between the outcome of the Glomerular Filtration Rate (GFR) and the outcome of some variables under the effect of bariatric surgery.

		GFR			Total	p*
		Remained	Improved	Worsened	Total	p*
Types of surgery
	Bypass	0	11	1	12	0.312
	Bypass	0.0%	91.7%	8.3%	100.0%
	Sleeve	4	15	4	23
	Sleeve	17.4%	65.2%	17.4%	100.0%
Diabetes
	Remained non-diabetic	4	18	2	24	0.217
	Remained non-diabetic	16.7%	75.0%	8.3%	100.0%
	Improved	0	6	1	7
	Improved	0.0%	85.7%	14.3%	100.0%
	Remained diabetic	0	2	2	4
	Remained diabetic	0.0%	50.0%	50.0%	100.0%
Hypertension
	Remained non-hypertensive	2	17	2	21	0.476
	Remained non-hypertensive	9.5%	81.0%	9.5%	100.0%
	Improved	2	8	2	12
	Improved	16.7%	66.7%	16.7%	100.0%
	Remained hypertensive	0	1	1	2
	Remained hypertensive	0.0%	50.0%	50.0%	100.0%
Total		4	26	5	35
Total		11.4%	74.3%	14.3%	100.0%

* Fisher's exact test.

There is an indication that bypass surgery tends to lead a greater number of patients to an improvement in the GFR (91.7%), although this result is not statistically significant (p = 0.312) (Table 3).

One-Way ANOVA results demonstrated that there was no difference between the mean BMI losses associated with the GFR outcome groups (p = 0.904). The type of GFR outcome under the effect of surgery did not affect the result of BMI expressed by the loss between pre and postoperative periods (Figure 2).

Figure 2. *ns: not significant.

ANOVA One-Way with bootstrapping procedure.

Discussion

According to the literature, in this cohort study one can observe a prevalence of white, females with an average age of 41 years, having high school education and health insurance, as women tend to take more care of themselves. They had a good socioeconomic level, given the difficulties of access to bariatric surgery in public services.³²

Bariatric surgery has shown encouraging results in the control of comorbidities in obese individuals, proving to be effective in sustained weight loss, corroborating the findings of the present study.³³^,³⁴

With regard to comorbidities (hypertension and diabetes), a significant decrease in the prevalence of these diseases can be observed in rated obese individuals after bariatric surgery, similar to most studies.³⁵

Some studies have pointed out the improvement of renal function after bariatric surgery, but not in other studies.³⁶^–³⁸ In the present result, an improvement in renal function was observed after bariatric surgery.

In this study there was trend towards an improvement in the GFR in the bypass technique in relation to the sleeve as opposed to the one observed in the literature.³⁹ The explanation for this would be the evidence of the relationship of the bypass technique with urinary calculus formation, as well as malabsorption syndrome.³⁹

Kidney disease can be caused by hypertension, diabetes as well as obesity.¹⁰^,⁴⁰ However, obesity is also associated with the emergence of diabetes, hypertension and kidney disease. In this sense, bariatric surgery promotes a reduction in BMI, glycemic control and blood pressure, and is even associated with improved renal function.⁶^–¹² Therefore, it is hard to know what came first in this cascade of improvements.

After performing a bivariate analysis between outcome of glomerular filtration rate and factors such as outcome of hypertension, outcome of diabetes and surgical techniques, no association of these factors with improved renal function was found. Furthermore, the type of GFR outcome under the effect of bariatric surgery does not affect the result of BMI which reinforces evidence suggesting that there is a strong and independent association between obesity and development of kidney disease.²⁴

Conclusion

After bariatric surgery, there was a significant improvement in the GFR, abdominal circumference and BMI, in addition to the control of associated comorbidities in obese patients with diabetes and hypertension. After bivariate analysis, no association was found between the improvement in GFR in the post-operative period of bariatric surgery and the analyzed variables. However, other prospective and more robust studies, as well as those with a larger sample size are needed to answer this challenging question: “Does bariatric surgery have an effect on improving renal function as an independent factor?”

Limitations

The sample size that followed in this longitudinal study was too small because of the Covid-19 pandemic. The short follow-up time for assessing renal function after bariatric surgery stems from the fact that this manuscript is part of an ongoing PhD thesis research in surgery, from the Federal University of Pernambuco.

Data availability

Underlying data

Harvard Data verse: Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study. https://doi.org/10.7910/DVN/5C4F0I⁴¹

The project contains the following underlying data:

- 01_bariatric_surgery_nephrological_study_database.tab (raw data).

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

Author contribution

Bezerra JAB: collected the data, contributed in interpretation of data and prepared the manuscript.

Brandt CT: contributed in interpretation of data and made the final revision.

Santos EPR: contributed in interpretation of data.

Acknowledgement

• Gilberto S. Matos: PhD. Associate Professor of Statistics at The Federal University of Campina Grande (UFCG), Brazil- contributed to the statistical analysis.
• Edmilson de Albuquerque Borborema Filho: PhD. Associate Professor of English and Linguistics at The Federal University of Paraiba (UFPB), Brazil- contributed in english language review.

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Author details Author details

¹ Faculty of Medical Sciences - UNIFACISA, CAMPINA GRANDE, Brazil
² Endoscopic and Obesity Surgery Institution – ICOEP, Campina Grande, Brazil
³ Federal University of Pernambuco, Recife, Brazil

Juliana Amaro Borborema Bezerra
Roles: Conceptualization, Investigation, Supervision, Validation, Writing – Original Draft Preparation

Eduardo Pachu Raia dos Santos
Roles: Investigation, Validation, Visualization, Writing – Review & Editing

Carlos Teixeira Brandt
Roles: Conceptualization, Data Curation, Formal Analysis, Project Administration, Supervision, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

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Published: 12 Apr 2022, 11:409

https://doi.org/10.12688/f1000research.110214.1

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Amaro Borborema Bezerra J, Pachu Raia dos Santos E and Teixeira Brandt C. Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study [version 1; peer review: 1 approved with reservations]. F1000Research 2022, 11:409 (https://doi.org/10.12688/f1000research.110214.1)

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Reviewer Report 29 May 2024

Tarek Arabi, Alfaisal University, Riyadh, Saudi Arabia

Approved with Reservations

https://doi.org/10.5256/f1000research.121793.r218469

The study by Bezerra et al. is interesting and is still a topic of controversy and discussion. However, there are a few comments that must be addressed:

The language of the manuscript can be better refined.

The study by Bezerra et al. is interesting and is still a topic of controversy and discussion. However, there are a few comments that must be addressed:

The language of the manuscript can be better refined.
I believe the statistical methods used are weak. The authors relied heavily on comparing categorical variables instead of continuous ones. Instead of categorizing patients into 'improved', 'worsened', and 'remained', it might be more adequate to compare the value of the GFR change itself. For example, the change of GFR in bypass vs. sleeve patients. I think this would help strengthen the statistical value and would give the readers an accurate representation of how much the change was.
The authors stated their method of calculating sample size. I do not think they mentioned what the population size they based off their calculations off was.
I believe it is important to provide a mean and SD of the age itself, instead of simply a range.
The tables are difficult to follow, in my opinion. I think the tables would need to restructured after adding the GFR change instead of just categories. Furthermore, a table describing the general demographics and relevant parameters of the study sample is needed.
The discussion is too simple. Authors should delve deeper into the role of obesity in renal function and better compare with studies in the literature.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Partly
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Kidney transplantation, obesity, chronic kidney disease, molecular mechanisms, immunology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Tarek Arabi, Alfaisal University, Riyadh, Saudi Arabia

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29 May 2024 | for Version 1

Tarek Arabi, Alfaisal University, Riyadh, Saudi Arabia

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Approved With Reservations

The study by Bezerra et al. is interesting and is still a topic of controversy and discussion. However, there are a few comments that must be addressed:

The language of the manuscript can be better refined.
I believe the statistical methods used are weak. The authors relied heavily on comparing categorical variables instead of continuous ones. Instead of categorizing patients into 'improved', 'worsened', and 'remained', it might be more adequate to compare the value of the GFR change itself. For example, the change of GFR in bypass vs. sleeve patients. I think this would help strengthen the statistical value and would give the readers an accurate representation of how much the change was.
The authors stated their method of calculating sample size. I do not think they mentioned what the population size they based off their calculations off was.
I believe it is important to provide a mean and SD of the age itself, instead of simply a range.
The tables are difficult to follow, in my opinion. I think the tables would need to restructured after adding the GFR change instead of just categories. Furthermore, a table describing the general demographics and relevant parameters of the study sample is needed.
The discussion is too simple. Authors should delve deeper into the role of obesity in renal function and better compare with studies in the literature.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Partly
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Kidney transplantation, obesity, chronic kidney disease, molecular mechanisms, immunology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Effects of bariatric surgery on renal function and associated factors with bivariate analysis: a cohort study

Abstract

Keywords

Introduction

Methods

Study design

Sample size

Inclusion and exclusion criteria

Procedures

Statistical methods

Results

Table 1. Morbidity measured pre and post bariatric surgery.

Table 2. Clinical markers measured pre and post bariatric surgery.

Figure 1. **p < .001. paired t test with bootstrapping procedure.

Table 3. Relationship between the outcome of the Glomerular Filtration Rate (GFR) and the outcome of some variables under the effect of bariatric surgery.

Figure 2. *ns: not significant.

Discussion

Conclusion

Limitations

Data availability

Underlying data

Author contribution

Acknowledgement

References

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