ORIGINAL CONTRIBUTIONS

Influence of Excess Weight Loss and Weight Regainon Biochemical Indicators During a 4-Year Follow-up AfterRoux-en-Y Gastric Bypass

Carolina Ferreira Nicoletti & Bruno Affonso Parenti de Oliveira &

Marcela Augusta Souza de Pinhel & Bruna Donati & Julio Sergio Marchini &Wilson Salgado Junior & Carla Barbosa Nonino

# Springer Science+Business Media New York 2014

AbstractBackground Bariatric surgery produces a substantial weightloss and improves the comorbidities associated with obesitysuch as diabetes mellitus and dyslipidemia, although inabilityto lose weight or weight regain has been estimated to occur in20% of cases. The objective of the present study was to assessthe influence of weight variations on biochemical indicatorsduring a 4-year period after bariatric surgery.Methods A4-year retrospective longitudinal studywas conduct-ed on 138 patients with grade III obesity submitted to Roux-en-Ygastric bypass, with the assessment of anthropometric

measurements and biochemical indicators. The patients weredivided into two groups according to percent excess weight loss(%EWL): %EWL>50 % and %EWL<50 %, and into twogroups according to weight regain: <10 % and >10 %. TheStudent t test for independent samples was used to assess thedifferences in biochemical indicators between groups (p≤0.05).Results Four years after surgery, there was a weight loss of49.4±21.8 kg and %EWL of 61±21.2 %, with 73.2 % (n=101) of the patients showing %EWL of 50 % or more.Significant weight regain occurred in 24.6 % of the sample.There was a difference in weight, BMI, total cholesterol,LDL-cholesterol, triglycerides, and albumin between patientswith different%EWL.No difference in biochemical indicatorswas observed between subjects with and without regain.Conclusion Four years after surgery, greater %EWL was as-sociated with a better lipid profile. In addition, weight regaindid not change the biochemical indicators of this patient series.

Keywords Bariatric surgery . Excess weight loss .Weightregain . Biochemical profile

Introduction

Among the various treatments of obesity, bariatric surgery isbeing pointed out as the most effective tool for achieving thenecessary weight loss and mainly the maintenance of weightloss along time [1, 2]. Roux-en-Y gastric bypass (RYGB), asurgical technique that combines the reduction of gastriccapacity and intestinal malabsorption, is the surgical proce-dure most frequently used [3, 4]. RYGB permits the loss of 30to 40 % of the initial weight and of 60 to 75 % of excess

C. F. Nicoletti : B. A. P. de Oliveira :M.A. S. de Pinhel :B.Donati :J. S. Marchini : C. B. Nonino (*)Department of Internal Medicine, Faculty of Medicine of RibeiraoPreto, University of São Paulo, Avenida dos Bandeirantes, 3900,Ribeirao Preto, SP 14049-900, Brazile-mail: carla@fmrp.usp.br

C. F. Nicolettie-mail: carol_nicolettif@yahoo.com.br

B. A. P. de Oliveirae-mail: bruno_parenti@usp.br

M. A. S. de Pinhele-mail: marcelapinhel@yahoo.com.br

B. Donatie-mail: brunadonati@msn.com

J. S. Marchinie-mail: jsmarchi@fmrp.usp.br

W. Salgado JuniorDepartment of Surgery and Anatomy, Faculty of Medicine ofRibeirao Preto, University of São Paulo, Ribeirão Preto, SP, Brazile-mail: wsalgado@fmrp.usp.br

C. F. Nicoletti I B. A. P. Oliveira I M. A. S. Pinhel I B. Donati IJ. S. Marchini I C. B. Nonino (*)

M. A. S. Pinhel

B. A. P. Oliveira

OBES SURGDOI 10.1007/s11695-014-1349-0

weight over a period of 1 year, the reduction and/or resolutionof the major comorbidities related to excess weight, and animproved quality of life [4]. Studies have pointed out a loss ofat least 50 % of excess weight to indicate successful surgicaltreatment [5, 6].

In addition to the weight changes caused by surgical treat-ment, improved biochemical indicators have been reported tooccur, with a reduction of serum triglycerides, low densitylipoprotein (LDL)-cholesterol fractions, and fasting glycemialevels 6, 12, or 18 months after surgery, reaching normalvalues [7].

On the other hand, failure of this therapeutic approachrepresented by the incapacity of weight loss or weight regainhas been estimated to occur in 20 % of cases [6]. Weightregain after the minimum weight achieved has been observed2 to 5 years after surgery [8]. Some of the predictive factors ofweight regain after the surgical procedure are the surgicaltechnique used, the presence of eating compulsion and disor-ders [9, 10], the dilatation of the gastric pouch, patient adhe-sion to follow-up and support groups, reduction of physicalactivity, and hormonal adaptations [5, 11, 12].

Few long-term studies have assessed the impact of excessweight loss or of weight regain on the biochemical indicatorsafter surgery. Thus, the objective of the present study was toassess the influence of weight variations such as excess weightloss and weight regain on the biochemical indicators during a4-year period after bariatric surgery.

Material and Methods

A longitudinal retrospective study was conducted on patientswith grade III obesity followed up at the Center of BariatricSurgery of the University Hospital, Faculty of Medicine ofRibeirão Preto, University of São Paulo for at least 4 yearsafter RYGB. Patients with surgical complications, patientswho became pregnant, and patients with cancer or patientswho died were excluded from the study. The EthicsCommittee of the institution approved the study, and all pa-tients gave written informed consent to participate.

Roux-en-Y gastric bypass, the most frequently used bariat-ric surgery technique, restricts absorption by combining re-duction of the gastric reservoir to between 20 and 50 mL andsecondary dysabsorption with bypass of the duodenum andproximal jejunum. Both the alimentary and the biliopancreaticlimb measured 100 cm. All the surgeries were performed byopen surgery and under the supervision of two experiencedsurgeons.

Preoperative data and data for 1, 2, 3, and 4 years aftersurgery were collected from the medical records. The follow-ing variables were analyzed: weight (kg), height (m), bodymass index—BMI (kg/m2), weight loss (kg and %), excessweight loss (%EWL), fasting glycemia (mg/dl), lipid profile

[total cholesterol (mg/dl), triglycerides (mg/dl), low densitylipoprotein (LDL-cholesterol) (mg/dl), and high density lipo-protein (HDL-cholesterol) (mg/dl)], albumin (g/dl), total pro-teins (g/dl), iron (μg/dl), unbound iron binding capacity(UIBC) (μg/dl), ferritin (ng/ml), and hemoglobin (Hb) (g/dl).

The %EWL was calculated as the percent difference be-tween preoperative weight and ideal weight. Ideal weight wascalculated as proposed by the Metropolitan Life InsuranceCompany [13]. To determine the influence of %EWL on thebiochemical indicators, the sample was divided into twogroups: patients with %EWL less than 50 % and patients with%EWL of 50 % or more.

Weight regain (%) was assessed by calculating the percentdifference between the final weight detected during the 4-yearpostoperative period and the lowest weight reached postoper-atively. A 10 % cut-off point was established to indicate theoccurrence of significant weight regain. For the analysis of theinfluence of percent weight regain on the biochemical indica-tors, the patients were divided into two groups: weight regainof less than 10 % and weight regain of 10 % or more.

Biochemical parameters were determined according to theroutine exams performed in the service. The concentrations oftotal cholesterol, triglycerides, LDL-cholesterol, HDL-cholesterol, albumin, total proteins, iron, UIBC, and ferritinwere determined by automated colorimetry; fasting glycemiawas determined by an enzymatic method; and hemoglobin bythe global analysis method (Coulter T 890 equipment).

Statistical Analysis

Data are reported as mean±SD. Mixed effect models wereused for the longitudinal evaluation of the anthropometric andbiochemical variables with PROC MIXED in SAS 9.3. TheStudent t test for independent samples was used to determinethe difference in biochemical indicators between patients with%EWL higher and lower than 50% and between patients withweight regain higher and lower than 10 % using SAS 9.2. Thechi-square test was used to compare frequencies between%EWL and weight regain. The level of significance was setat p≤0.05.

Results

Of the 550 patients submitted to RYGB in the service understudy, 302 completed a 4-year postoperative follow-up. Ofthese, 138 (81.2 % females, mean age 42.4±10.4 years) hadcomplete information in their medical records and were in-cluded in the study. Table 1 shows a comparison betweenpatients enrolled in the study and not.

Table 2 shows the weight measurements and the BMIvalues for the periods studied. A 33.2 % reduction of theinitial weight was observed in the first year after surgery and

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a 6.7 % reduction was observed in the second year. At the endof the study, the mean weight loss was 49.4±21.8 kg (34.9±12.7 % of the initial weight). The minimum weight reachedwas 86.3±16.8 kg. In the third and fourth postoperative years,there was weight regain compared to preoperative values andto the first 2 years of the study (p<0.05).

By 4 years after surgery, %EWL was 61.0±21.2 %, with73.2 % (n=101) of the patients having a %EWL of 50 % ormore. A significant weight regain occurred in 24.6 % of thesample, with 73.5 % of these patients regaining 10 to 20 %and 26.5 % more than 20 % of their minimum weight. Of thepatients who had %EWL lower than 50 %, 54.0 % did notregained weight and 46.0 % regained >10 %. Consideringthose with %EWL greater than 50 %, 83.2 % did not regainedweight and 16.8 % regained >10 % (p<0.001).

A reduction of glycemia, total cholesterol, triglycerides,LDL-cholesterol, total proteins, iron, and hemoglobin wasobserved in the first year after surgery, with these values beingmaintained until the end of the study (Table 3).

Analysis of %EWL revealed that, by 4 years after RYGB,there was a difference in weight, BMI, total cholesterol, LDL-cholesterol, triglycerides, and albumin between patients with a%EWL higher and lower than 50 % (Fig. 1). No difference inthe biochemical indicators was observed during this periodbetween subjects with and without weight regain (Table 4).

Discussion

The results of the present study show that there was a weightloss up to the third year after RYGB and that some patientsmaintained this loss while others regained weight. Surgicaltreatment led to an improvement of the biochemical indicatorssuch as dyslipidemia and altered fasting glycemia. An impactof higher %EWLwas observed on serum total cholesterol andLDL-cholesterol concentrations. In contrast, no differences inbiochemical indicators were detected between individualswith and without weight regain, whose values were withinnormal limits.

The weight reduction observed after the first year of thepresent study (33.2 % of the initial weight) was similar to thatobserved in a Swedish study [14], a Finnish study [15], and ameta-analysis study [16–18]. Also, Pedrosa et al. [19] reporteda gradual weight and BMI reduction, with differences in allphases (6, 12, 18, and 24 months), with the lowest weight andBMI and the highest percentage of weight loss occurringbetween 18 and 24 months. Valesiet et al. [20] studied 250cases and reported a weight reduction of the order of 37.5% atthe end of the first year after surgery. In contrast, Quadros et al.(2007) [21] detected lower percentages during the same period(30.7 %).

As observed in the present study, the higher rates of weightloss occur during the first year after RYGB, with the losscorresponding to 30 to 40 % of the initial weight. The rateof weight loss then tends to decrease, with stability beingreached at 12 to 24 months, and with a possible weight regainoccurring after the second postoperative year. It has beenobserved that approximately 10 to 20 % of the patients showa significant weight regain in the long term [22, 23], with animportant impact on health, including the recurrence of co-morbidities related to obesity and a worse quality of life [23,

Table 1 Characterization of the total sample of patients with obesitygrade III in preoperative period

Variables Included patients(n=138)

Not included patients(n=412)

Age (years) 42.4±10.4 39.8±9.8*

BMI (kg/m2) 52.2±7.8 51.8±7,5

Glycemia (mg/dL) 108.9±40.2 104.2±39.2

Cholesterol (mg/dL) 187.9±39.3 180.6±39.8

Triglycerides (mg/dL) 149.5±78.5 147.8±78.6

LDL (mg/dL) 118.6±32.9 112.2±32.9

HDL (mg/dL) 39.8±9.8 40.7±11

Albumin (g/dL) 3.9±0.4 4.2±2.3

Total protein (g/dL) 7.0±0.5 7.0±0.5

Iron (μg/dL) 78.1±28.3 73.5±27.2

UIBC (g/dL) 252.8±66 245.0±65.2

Ferritin (ng/mL) 159.5±148.2 171±152.8

Hemoglobin (g/dL) 13.9±1.8 13.5±1.6

BMI body mass index, LDL low density lipoprotein, HDL high densitylipoprotein, UIBC unbound iron binding capacity

*p<0.05 (Student’s t test)

Table 2 Weight and body mass index (BMI) values of the patients before surgery and over a 4-year follow-up period after surgery

Preoperative Postoperative

1 year Δ% 2 years Δ% 3 years Δ% 4 years Δ%

Weight (kg) 138.5±23.0 92.5±18.5* −33.2 86.3±16.7*, ** −6.7 87.1±16.9*, ** 0.9 89.1±18.1*, ***, **** 2.3

BMI (kg/m2) 52.2±7.8 34.8±6.5* −33.3 32.4±5.6*, ** −6.9 32.8±5.8*, ** 1.2 33.5±6.1*, ***, **** 2.1

BMI body mass index* p<0.05 compared to the preoperative value; ** p<0.05 compared to 1 year; *** p<0.05 compared to 2 years; **** p<0.05 compared to 3 years

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24]. In addition, weight regain has substantial economic re-percussions, with recurrent costs associated with these condi-tions [25]. In agreement with our findings, a Brazilian studywith a 5-year follow-up after RYGB showed a significantweight regain by 48 months after surgery, with an increasein BMI [8]. Weight regain is associated with compulsiveovereating, loss of control of intake [25], failure to adhere tonutritional guidelines, and low schooling [26].

There is still controversy about the influence of previousBMI on the results of surgery. In the present study, the mean

preoperative BMI was 52.2±7.8 kg, characterizingsuperobese individuals. Higa et al. [27] observed that patientswith a preoperative BMI <50 kg/m2 showed a better %EWL.An extremely high preoperative BMI has been associated witha rapid weight loss after surgery, although also with highpostoperative regain rates [8, 28].

In the present study, there was a significant improvement ofserum total cholesterol, LDL-cholesterol, and triglycerides1 year after RYGB, with an increase of HDL-cholesterol anda reduction of the remaining lipids. These data agree with

Table 3 Evolution of the biochemical indicators of the patients from preoperative values to the values observed over a follow-up period of 4 years aftersurgery

Preoperative Postoperative

1 year 2 years 3 years 4 years

Glycemia (mg/dL) 108.9±40.2 85.4±10.5* 84.8±12.4* 84.4±12.1* 85.0±11.9*

Total cholesterol (mg/dL) 187.9±39.3 164.8±34* 164.9±35.1* 167.5±32.9* 173.5±37.8*, ***

Triglycerides (mg/dL) 149.5±78.5 87.0±35.2* 80.1±34.9* 77.4±32.5* 80.7±37.5*

LDL-cholesterol (mg/dL) 118.6±32.9 99.1±27.9* 94.6±27.2* 98.1±27.7* 102.9±29.9*

HDL-cholesterol (mg/dL) 39.8±9.8 47.5±10.5* 53.8±13.4*, ** 54.3±11.8*, ** 54.5±12.3*, **

Albumin (g/dL) 3.9±0.4 4.0±0.3 4.1±0.2*, ** 4.4±3.2*, ** 4.1±0.2*

Total proteins (g/dL) 7.0±0.5 7.2±4.6* 6.8±0.4* 6.7±0.4* 6.7±0.4*

Iron (μg/dL) 78.1±28.3 84.4±34.2 86.4±38.1 78.2±35.9 84.9±43.3

UIBC (g/dL) 252.8±66 225.5±82.1* 252.7±97.1 264.4±95.9** 266.3±95.5**

Ferritin (ng/mL) 159.5±148.2 123.7±121.5* 101.7±107.3*, ** 86.7±117.0*, ** 69.6±98.2*, **, ***

Hemoglobin (g/dL) 13.9±1.8 12.8±2.2* 12.6±2.0* 12.2±2.3* 12.3±2*

UIBC unbound iron binding capacity* p<0.05 compared to the preoperative period; ** p<0.05 compared to 1 year; *** p<0.05 compared to 2 years

p<0.05 compared to 3 years (mixed effect models)

Fig. 1 Mean (±SD) values of weight, BMI and biochemical parameters among patients who obtained a %EWL higher or lower than 50 %. *p<0.05

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those reported in other Brazilian studies [19, 20] and fordifferent populations also submitted to bariatric surgery [29,30]. Studies have reported high preoperative triglyceride andLDL-cholesterol concentrations that reached normalization by12 months after surgery [7, 31]. The improvement of lipidprofile of obese patients determined by gastroplasty seems tobe related to weight reduction and to the consequent improve-ment of hepatic insulin sensitivity. However, the exact mech-anism of these benefits has not been fully clarified [32].

The %EWL of 61.2 % detected in the present study waslower than the value reported by Beleli et al. [33], whoobserved a 75.7 % excess weight loss within 2 years aftersurgery. Studies have shown that the reduction of comorbid-ities related to obesity after bariatric surgery depends onweight loss [17, 22]. Analysis of the groups with %EWLhigher or lower than 50 % showed that total cholesterol,triglyceride, and LDL-cholesterol values differed betweengroups, revealing the benefit of a greater %EWL for the lipidprofile. There was no difference in serum glycemia concen-trations between groups, so that the reduction of this param-eter does not depend on%EWL. Studies have pointed out thatthe metabolic effect of bariatric surgery has a great impact onglycemia levels [2, 34]. Conversely, Brethauer et al. [34]showed that a lower weight loss after surgery and weightregain may lead to the recurrence of diabetes.

Late effects of bariatric surgery showed no direct results onserum iron, but changed the values of components of ironmetabolism as a reduction in ferritin and hemoglobin.However, the greater or lesser loss of excess weight has notdetermined the changes in the iron profile. Thus, changes inthe anatomy and physiology of the gastrointestinal tract, suchas the reduction of gastric secretion and jejunal exclusion, and

food intolerance are the main causes of worsening of ironmetabolism [35, 36].

Weight regain is directly related to health impairment dueto a possible return of obesity and recurrence of comorbidities.In the present study, no difference in biochemical indicatorswas observed between the groups with and without weightregain. However, a literature review by Shah et al. [11] dem-onstrated that percent weight regain is proportional to the riskof a return of diseases associated with obesity. We suggest thatthe marked weight loss detected in the present study wassufficient to improve the biochemical indicators, so thatweight regain did not change the benefits provided by theinitial loss. It should be pointed out that, if these patientsshould continue to regain weight along the years, changesmay occur in their biochemical profile.

It is important to consider that the follow-up rate is lowduring the 4 years which represents an important limitation ofour study.

Taken together, the present results demonstrate the impor-tance of the maintenance of nutritional and behavioral actionsthat will contribute to the achievement of the ideal weight forthese patients and to the prevention of weight gains that willcause them to return to the risk situations which they facedbefore the intervention.

We conclude that RYGB is an important tool for weightloss and for the control of dyslipidemia and blood glucoselevels. Also, a greater excess weight loss was associatedwith abetter lipid profile 4 years after surgery. In addition, weightregain did not change the biochemical indicators of the presentseries.

Acknowledgments None.

Conflict of Interest All authors declare no conflict of interest.

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