The Impact of Sleeve Gastrectomy on Hyperlipidemia: A Systematic Review

Background. Weight loss and reduction in comorbidities can be achieved by longitudinal sleeve gastrectomy (LSG). Existing evidence suggests that LSG resolves or improves hyperlipidemia in morbidly obese patients. The aim of this study was to systematically review the effect of LSG on hyperlipidemia. Methods. A systematic literature search was conducted from English-language studies published from 2000 to 2012 for the following databases: MEDLINE, EMBASE, CINAHL, PubMed, Clinical evidence, Scopus, Dara, Web of Sciences, TRIP, Health Technology Database, Cochrane library, and PsycINFO. Results. A total of 4,211 articles were identified in the initial search, and 4,185 articles were excluded based on the exclusion criteria. Twenty-six studies met the inclusion criteria for this systematic review, involving 3,591 patients. The mean preoperative body mass index (BMI) was 48 ± 7.0 kg/m2 (range 37.2–65.3). The mean postoperative BMI was 35 ± 5.9 kg/m2 (range 26.3–49). The mean percentage of excess weight loss (EWL) was 63.1% (range 37.7–84.5), with a mean followup of 19.1 months (range 6–60). The mean levels of pre and post operative cholesterol were 194.4 ± 12.3 mg/dL (range 178–213) and 181 ± 16.3 mg/dL (range 158–200), respectively. Conclusion. Most patients with hyperlipidemia showed improvement or resolution of lipid profiles after LSG. Based on this systematic review, LSG has a significant effect on hyperlipidemia in the form of resolution or improvement in the majority of patients.


Introduction
Laparoscopic sleeve gastrectomy (LSG) was introduced initially as a first stage of the biliopancreatic diversion with duodenal switch (BPDDS) for severely obese patients who were regarded as high risk surgical candidates [1]. Due to its greater efficiency [2], technical simplicity [3], and low complication rates [4], LSG has become more widely accepted as a definitive treatment for morbidly obese patients [5]. In LSG, the stomach is divided vertically, while removing most of the fundus of the stomach and preserving the continuity of the digestive tract [6].
LSG leads to long-term weight loss and improvement or resolution of its associated comorbidities such as diabetes mellitus (DM), hypertension, and hyperlipidemia [7,8]. In a recent systematic review on the effect of the LSG on co-morbidities, Sarkhosh et al. [8] reported resolution of hypertension in 58% and resolution or improvement of hypertension in 75% of patients following LSG. In another systematic review, Alamo et al. [9] reported resolution of type 2 diabetes mellitus (T2DM) in 84% of patients after LSG. To our knowledge, the effect of LSG on hyperlipidemia was not reviewed systematically.
Most patients with obesity present with lipid abnormalities; however, only 20% of the obese patients population are not showing classical metabolic lipid changes [10]. Patients with abdominal obesity are more likely to have atherogenic dyslipidemia than those who have increased levels of the Low density lipoprotein (LDL) [11]. Hyperlipidemia is widely recognized as one of the main co-morbidities in severe obesity. It is therefore not surprising that research and treatment are increasingly focused on lipid profiles in the drive to potentially reduce cardiovascular related-diseases [12,13]. The aim of this study is therefore to systematically review the Based on discussions among the three coders, we achieved 100% agreement on the studies to be included. The initial search yielded 4,211 articles as described in Figure 1. Of these, 351 were duplicates, 3,163 articles were excluded based on the title, further 570 articles were excluded based on the abstract, and another 101 studies were eliminated after reading the full paper. Finally, we agreed on 26 articles to be included in the present systematic review.

Outcome Measures.
Studies included in this systematic review were LSG either as a single procedure or as a first procedure of staged surgery. The primary outcome of this study was resolution or improvement of hyperlipidemia. The resolution of hyperlipidemia was defined as discontinuation of all hyperlipidemia medications. The improvement of hyperlipidemia was defined as dose reduction of lipid lowering medications. The secondary outcome included changes in body mass index (BMI) postoperatively and the percentage of excess weight loss (%EWL). However, (% EWL) was calculated as follows: (% EWL) = (weight loss/excess weight) × 100, where excess weight is the total preoperative weight minus the ideal weight [14]. Ideal weight is the desirable weight which would indicate those persons with the lowest mortality rates and can be calculated through the metropolitan life table which is based on height, weight, and gender. (1) were studies of any design that involved LSG, (2) included reports on the effect of LSG on lipid profile, (3) compared LSG versus any other type of bariatric surgery, (4) were studies where a second stage procedure was planned, (5) reported data on cholesterol, triglyceride, LDL, and high density lipoprotein (HDL), (6) were published in English in peer-reviewed journals, and (7) were classified as relevant or possibly relevant based on two independent authors.

Selection Criteria. Studies were included if they
We excluded studies if (1) repeated LSG was performed, (2) they were conducted on patients who participated in health and/or nutrition program, (3) they provided only general descriptions and information about LSG without empirical data, (4) they combined LSG with another bariatric procedure results, (5) LSG was performed as revision surgery, (6) they provided information on the effect of LSG on other co-morbidities, and (7) they were nonhuman and non-English studies.

Assessment of Risk of Bias in Included Studies.
All included studies were assessed independently by two authors for methodological quality using the Cochrane and risk of bias tools [15]. Within the 26 studies included in this systematic review, 11 reported both resolution and improvement of hyperlipidemia after LSG and 83.5% of the patients had experienced resolution or improvement of hyperlipidemia. Another 7 studies reported only hyperlipidemia resolution and 54% of patients had complete resolution of hyperlipidemia. One study reported improvement of hyperlipidemia in 42% of the patients.

Search Results
Five studies compared the lipid profile results pre and post-surgery [19,23,37,39,41]. Only three studies showed minimal changes between pre and post operative cholesterol and LDL levels [18,19,41]. However, the same three studies reported significant changes in triglyceride level and HDL level post LSG (Table 2).

Discussion
The main purpose of this systematic review was to investigate further the effect of LSG on hyperlipidemia. LSG was initially used as a first stage operation for high risk surgical patients prior to undergoing a gastric bypass or biliopancreatic diversion. Existing evidence has suggested that LSG is effective as a single procedure for the treatment of morbid obesity and improvement or resolution of co-morbidities.
Our systematic review showed that LSG resolved or improved hyperlipidemia in a majority of patients. 83.5% of patients had resolution or improvement of their hyperlipidemia and 54% experienced complete resolution of their hyperlipidemia. These results correspond with other bariatric procedures. Omana et al. [32] found a greater resolution or improvement of hyperlipidemia with LSG in comparison with laparoscopic adjustable gastric banding. Hyperlipidemia improved in 87% of patients after LSG and in 50% of patients after gastric banding after a 15-month followup period.
Benaiges et al. [19] reported lower improvement or resolution rates for hyperlipidemia in the LSG group than in the laparoscopic Roux-en-Y gastric bypass (LRYGB). The hyperlipidemia improvement or resolution rate was 100% for LRYGB versus 75% for LSG. Researchers argued that the decrease in LDL cholesterol observed for LRYGB could be related to the malabsorption effect produced by this technique. This hypothesis is supported by several data [14,42].
Similarly, Kehagias et al. [28] found less resolution of hyperlipidemia in patients after LSG versus patients who underwent LRYGB. The rate of hyperlipidemia resolution was 90% for patients who had LRYGB and 75% for patients who had LSG. Lakdawala et al. [29] reported almost similar results for patients who had LSG and patients who had LRYGB. At one-year followup, hyperlipidemia resolved in 75% of patients who underwent LSG and in 78% of those who underwent LRYGB. Skroubis et al. [36] reported 90%, 78.4%, 55%, and 48.7% resolutions of hyperlipidemia after a 5-year followup for patients who underwent biliopancreatic diversion, vertical banded plasty, LSG, and Roux-en-Y gastric bypass (RYGB) respectively.
In regard to the secondary outcome, our systematic review showed a reduction in the %EWL over a one-year followup. The percentage of EWL after LSG was 63.1% (range 37.7-84.5). In comparison with other bariatric procedures, Kehagias et al. [28] reported greater loss of the %EWL in the LSG group in the first 2 years of their study and greater in the third year but with no statistical significance. Kehagias et al. [28] went further and found that the proportion of patients who achieved a %EWL greater than 50% at 3 years postoperatively was 77% after LRYGB and 83% after LSG.

Limitation
The primary studies included in this systematic review were case series and nonrandomized controlled trials, which are inherently biased. There were no published randomized controlled studies comparing LSG and medical therapy assessments of the resolution of hyperlipidemia on obese patients. Given this fact, the result of our systematic review should be interpreted with caution to avoid misleading results. This fact, however, appears to be applied to the majority of bariatric  Journal of Obesity surgical data. Furthermore, a formal meta-analysis could not feasibly be conducted due to the high degree of heterogeneity in the study's design, intervention, and the population in the studies. With all these limitations, nevertheless, our review supports the idea that LSG is associated with the resolution and/or improvement of hyperlipidemia after LSG.

Conclusion
This systematic review shows that LSG has a significant effect on hyperlipidemia, producing resolution or improvement in most of the cases. Therefore, LSG remains a viable surgical option for weight loss and reduction in co-morbidities such as hyperlipidemia.