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Obesity Surgery (2023) 33:789–806

https://doi.org/10.1007/s11695-022-06444-8

ORIGINAL CONTRIBUTIONS

Change in Adipokines and Gastrointestinal Hormones After Bariatric


Surgery: a Meta‑analysis
Jiayun Huang1 · Yanya Chen1,2 · Xuan Wang1 · Cunchuan Wang3 · Jingge Yang3 · Bingsheng Guan3 

Received: 30 June 2022 / Revised: 21 December 2022 / Accepted: 27 December 2022 / Published online: 6 January 2023
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2023

Abstract
Purpose  The study aimed to perform a meta-analysis about the change in adipokines and gastrointestinal hormones after
bariatric surgery in patients with obesity.
Materials and Methods  We searched the Cochrane Central Register of Controlled Trials, EMBASE, and PubMed for related
articles and used Review Manager 5.4 for data aggregation. Sensitivity and subgroup analysis were also conducted when
feasible.
Results  As a result, 95 articles involving 6232 patients were included in the meta-analysis. After bariatric surgery, the levels
of leptin, ghrelin, C-reactive protein (CRP), interleukin-6 (IL-6), high-sensitivity C-reactive protein (Hs-CRP), tumor necro-
sis, factor-α (TNF-α), and interleukin-1β (IL-1β) reduced, while adiponectin, glucagon-like peptide-1 (GLP-1), and peptide
YY (PYY) levels increased significantly. Subgroup analysis indicated that there was a more significant reduction in leptin
level with a longer follow-up time. OAGB had a greater effect on increasing adiponectin level compared with other proce-
dures. SG procedure would bring about reduced ghrelin, while BPD resulted in increased ghrelin. Meta-regression analysis
found that publication year, study design, number of patients, preoperative age, preoperative BMI, and quality assessment
score were not significantly related to change in leptin, adiponectin, and ghrelin levels.
Conclusion  Bariatric surgery was associated with a significant decrease in leptin, ghrelin, CRP, IL-6, Hs-CRP, TNF-α, and
IL-1β, as well as increase in adiponectin, GLP-1, and PYY levels.

Keywords  Bariatric surgery · Adipokine · Gastrointestinal hormone · Meta-analysis · Obesity

Introduction

Nowadays, obesity has become a global health problem,


which can bring about a range of obesity-related metabolic
Jiayun Huang, Yanya Chen, and Bingsheng Guan contributed
equally to this work. diseases and a substantial economic burden to humans [1].
It was reported that more than 650 million people world-
Key Points  wide are suffering from obesity [2]. Several clinical studies
1. Bariatric surgery was associated with a significant decrease in showed that bariatric surgery is one of the most effective
leptin, ghrelin, CRP, IL-6, Hs-CRP, TNF-α, and IL-1β levels.
2. The levels of adiponectin, GLP-1, and PYY increased after
treatment methods for morbid obesity, which can help to lose
bariatric surgery. weight and relieve related metabolic diseases [3–5].
3. Publication year, study design, number of patients, preoperative Although the clinical effect of bariatric surgery has been
age, preoperative BMI, and quality assessment score were not studied a lot, the mechanism behind bariatric surgery has
significantly related to change in leptin, adiponectin, and ghrelin
levels.
not been well-known yet. Some potential mechanisms have
been proposed, including change in the intestinal flora, bile
* Jingge Yang acid metabolism, and small intestine refactoring [6]. Moreo-
dryangjg@126.com ver, the change in adipokines and gastrointestinal hormones
* Bingsheng Guan have also been reported as a mechanism of action. How-
guanbingshengxy@163.com ever, there are different research outcomes in the literature;
Extended author information available on the last page of the article

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790 Obesity Surgery (2023) 33:789–806

some reported decreased leptin level after Roux-en-Y gas- hormone, including leptin, peptide YY (PYY), ghrelin,
tric bypasses (RYGB) and no significant change after gastric glucagon-like peptide-1 (GLP-1), adiponectin, insulin-like
banding (GB) [7]. Some said reduced ghrelin after sleeve growth factor-1 (IGF-1), interleukin-1β (IL-1β), IL-6, tumor
gastrectomy (SG) [8], while others found elevated ghrelin necrosis factor-α (TNF-α), C-reactive protein (CRP), and
after RYGB [9]. There are also opposite results in interleu- high-sensitivity C-reactive protein (Hs-CRP). If more than
kin-6 (IL-6) change after RYGB and biliopancreatic diver- one postoperative adipokine/gastrointestinal hormone level
sion (BPD) [10, 11]. Given this inconsistent evidence, it was provided, we only selected the measurement value at the
is difficult to conclude the exact change in adipokines and longest follow-up time.
gastrointestinal hormones after bariatric surgery. We excluded non-English articles, conference abstracts,
Although a previous meta-analysis had pooled the change reviews, and studies on laboratory animals, studies with
in glucagon-like peptide-1 (GLP-1) after RYGB, it included patients aged < 18 years, and studies with fewer than 30
only one gastrointestinal hormone and one type of bariatric participants. The threshold number of 30 was chosen for
surgery [12]. Many other kinds of adipokines, gastrointesti- practicality and to avoid the small study effects potentially
nal hormones, and bariatric surgeries have yet to be pooled. distorting the pooled results of this meta-analysis.
Therefore, this study aimed to make a meta-analysis regard-
ing the change in various adipokines and gastrointestinal Data Extraction and Quality Assessment
hormones after bariatric surgery.
After a literature search and deleting the duplicated articles,
we screened the titles and abstracts of each article for pre-
Methods liminary evaluation. And then, we downloaded the full text
for further evaluation if necessary. For all the included litera-
The meta-analysis was performed in accordance with some ture, we used a pre-specified data extraction form to extract
guidelines, including the meta-analysis of observational the following data: the first author, publication year, country,
studies in epidemiology (MOOSE), the Cochrane Handbook, study design, surgical procedure, number of patients, age,
and the Preferred Reporting Items for Systematic Reviews body mass index (BMI), follow-up duration, and outcomes.
and Meta-Analyses (PRISMA). Because the completion of For the missing data, we would contact the authors by email
this article does not include clinical intervention for patients, for complete information if possible. The quality of included
informed consent and ethical approval can be exempted. trials was assessed by the Newcastle–Ottawa Scale (NOS),
which consists of three dimensions (patient selections, com-
Literature Search parability, and the assessment of outcomes). And the score
for this scale ranged from 0 to 9.
A literature search was made on the Cochrane Central Reg-
ister of Controlled Trials (CENTRAL), EMBASE, and Pub- Statistical Analysis
Med from inception to 14 October 2022, with no language
restrictions. Free terms and subject headings were applied We used Review Manager 5.4 and Stata (version 12.0) for
to search literature flexibly, including (bariatric surgery OR statistical analysis. For continuous variables, calculate the
metabolic surgery OR weight loss surgery OR obesity sur- mean difference (MD) or standardized mean difference
gery OR gastric bypass OR sleeve gastrectomy OR gastric (SMD) with a corresponding 95% confidence interval (95%
banding OR biliopancreatic diversion OR duodenojejunal CI) as appropriate, depending on whether the same scale
bypass) AND (obese OR obesity) AND (adipocyte factor measurement is used. Cochran Q- = statistic and I2 statistics
OR adipocytokines OR cytokines OR inflammatory factor were adopted to evaluate the between-study heterogeneity,
OR gut hormone OR leptin OR PYY OR ghrelin OR gluca- with P < 0.1 and I2 > 50% representing significant heteroge-
gon-like peptide-1 OR adiponectin OR insulin-like growth neity. A random-effects model would be used to pool data
factor-1 OR IL-1 OR IL-6 OR TNF OR CRP). In addition, when significant heterogeneity was found. Otherwise, we
we also searched for other possible articles based on the would use a fixed effects model. When necessary and feasi-
references of screened articles. ble, subgroup analyses would be performed to identify pos-
sible sources of between-study heterogeneity. Pre-specified
Inclusion and Exclusion Criteria subgroup analyses included surgical type (SG, RYGB, BPD,
GB, one-anastomosis gastric bypass), region (America,
Studies that met the following inclusion criteria would be Europe, Asia, Africa), and follow-up time (≤ 6  months,
included: (1) patients with obesity who underwent bariatric 6–12  months, > 12  months). A meta-regression analysis
surgery and (2) providing baseline and postoperative data was conducted to evaluate if the change in adipokine and
for at least one of the following adipokine or gastrointestinal gastrointestinal hormone levels was affected by publication

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Obesity Surgery (2023) 33:789–806 791

year, study design, number of patients, preoperative age, pre- more substantial leptin level reduction with a longer fol-
operative BMI, and NOS score. Regarding the sensitivity low-up time. Meta-regression analysis showed that publica-
analyses, the methods of changing the pooled model (fixed tion year (P = 0.198), study design (P = 0.093), number of
effects model or random-effects model) and removing one patients (P = 0.528), preoperative age (P = 0.651), preopera-
study were conducted. The possible publication was evalu- tive BMI (P = 0.529), and NOS score (P = 0.062) were not
ated with Begg and Egger tests through Stata software. significantly associated with leptin change.
In sensitivity analysis, the pooled results did not sig-
nificantly alter when excluding one research in turn, with
Results a range from − 2.48 (95% CI − 2.76 to − 2.20) to − 2.32
(95% CI − 2.57 to − 2.07). Also, the change in leptin level
Search Process, Study Characteristics, and Quality was confirmed by changing the random-effects model to a
Assessment fixed effects model (SMD =  − 1.85, 95% CI − 1.91 to − 1.79,
P < 0.00001).
Primary database searches provided a total of 7057 related Furthermore, potential publication bias was seen with
articles, and additional manual search did not provide Begg (P = 0.000) and Egger (P = 0.000) tests. Therefore, we
any other new trials that met the inclusion criteria. After conducted a trim and filled analysis with the software Stata
removing duplicate surveys, 5984 titles and abstracts were and found that both the pooled results before and after trim
reserved. Subsequently, 780 articles were retained, and the and fill analysis were statistically significant (both P < 0.05),
full text was downloaded for further evaluation. Finally, indicating that the pooled estimate for leptin was robust.
a total of 6232 patients from 95 articles were included in
the meta-analysis [7–11, 13–102]. Of the included studies, Meta‑analysis of Adiponectin
twelve had two arms, six had three arms, and one had four
arms; these arms were analyzed separately in the meta-anal- Forty-three trials involving a total of 2197 patients dem-
ysis. Figure 1 shows the detailed process of study selection. onstrated the result of adiponectin. Due to the significant
The study characteristics are shown in Table 1. Among heterogeneity between the studies (P < 0.00001, I2 = 92%),
these studies, the types of bariatric surgeries were not con- we chose a random-effects model to summarize the data
sistent, including malabsorptive surgery (e.g., BPD), restric- and found that bariatric surgery is effective in raising
tive surgery (e.g., SG, GB), and mixed surgery (e.g., RYGB, adiponectin levels (SMD = 1.35, 95% CI 1.1 to 1.61,
one-anastomosis gastric bypass). The follow-up period P < 0.00001) (Fig. 3).
ranged from 3 weeks to 60 months. The quality of the stud- Regarding subgroup analysis, we found that the change
ies is assessed in Table 1. in adiponectin level was not statistically significant in
different subgroups of follow-up duration (P = 0.94).
Meta‑analysis of Leptin Compared with other surgical modalities, OAGB had a
more considerable impact on the elevation of adiponectin
Seventy-one trials involving 3501 patients reported results (SMD = 3.08, 95% CI 2.56 to 3.61, P < 0.00001). Addi-
for leptin. Because there was significant heterogeneity tionally, patients from America and Africa had more
between these studies (P < 0.00001, I2 = 95%), the data was remarkable adiponectin reduction than Europe and Asia
pooled using a random-effects model. The result showed (P < 0.00001).
that bariatric surgery could significantly reduce leptin lev- Meta-regression analysis showed that publication year
els in patients with obesity (SMD =  − 2.46, 95% CI − 2.73 (P = 0.372), study design (P = 0.257), number of patients
to − 2.19, P < 0.00001) (Fig. 2). (P = 0.325), preoperative age (P = 0.698), preoperative
For the purpose of exploring the possible source of het- BMI (P = 0.683), and NOS score (P = 0.844) were not sig-
erogeneity, we conducted subgroup analyses according to nificantly associated with adiponectin change. Concern-
different types of bariatric surgery, patient region, and fol- ing sensitivity analysis, the pooled result remained similar
low-up duration (Table 2). Among these types of bariatric when removing one study in turn. And changing the ran-
surgery, SG, RYGB, BPD, and GB procedures could lead dom-effects analysis into fixed effects model (SMD = 0.93,
to significant leptin reduction, while one-anastomosis gas- 95% CI 0.87 to 1.00, P < 0.00001) also did not significantly
tric bypass (OAGB) had no significant effect on leptin level impact the pooled result. There was significant publication
(SMD =  − 9.98, 95% CI − 24.90 to 4.94, P = 0.19). Among bias with Begg (P = 0.000) or Egger (P = 0.000) test. We
patients in different regions, African patients seem to gain tried to conduct trim and fill analysis, but no trimming could
the most significant influence (SMD =  − 5.75, 95% CI − 7.45 be performed, and the data was unchanged, which meant that
to − 4.04, P < 0.00001). The subsequent analysis showed a the pooled estimate for adiponectin was robust.

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792 Obesity Surgery (2023) 33:789–806

Fig. 1  PRISMA flow diagram


of the study selection

Meta‑analysis of Ghrelin related to CRP change. By means of moving one study out
in turn and changing the analysis model, sensitivity analysis
Ghrelin from 40 articles involving 1480 patients was revealed that the pooled result for ghrelin is robust.
included for analysis. Because of significant heterogeneity
between the included studies (P < 0.00001, I2 = 95%), we
Meta‑analysis of CRP
chose a random-effects model to pool the data. According to
the final results, the level of ghrelin reduced after bariatric
Thirty-six trials involving 1690 patients were included
surgery (SMD =  − 0.50, 95% CI − 0.88 to − 0.12, P = 0.009)
in the meta-analysis on CRP. We used a random-effects
(Fig. 4).
model to aggregate results because of the high heteroge-
Regarding various types of bariatric surgery, we found
neity between studies (P < 0.00001, I2 = 83%). The result
that SG procedure would bring about reduced ghrelin
showed that bariatric surgery was effective in reducing
(SMD =  − 1.35, 95% CI − 2.00 to − 0.69, P < 0.00001),
the level of CRP (SMD =  − 1.04, 95% CI − 1.23 to − 0.85,
while BPD resulted in increased ghrelin (SMD = 0.59, 95%
P < 0.00001) (Fig. 5).
CI 0.25 to 0.94, P = 0.0007). When looking at the region’s
There was no statistically significant difference between
impact, it was shown that patients from America and Africa
the data obtained by subgroup analysis based on the type of
had significant ghrelin change (P < 0.05), while Europe and
surgery (P = 0.21) and follow-up duration (P = 0.22). The
Asia had no. Compared with preoperative data, there was
differences between the data caused by different regions
no statistically significant change in ghrelin level in short-
were statistically significant (P < 0.00001), and partici-
term postoperative follow-up (≤ 6  months). However, it
pants from Africa gained more reduction in CRP level
turned out to be statistically significant in longer follow-up
(SMD =  − 1.97, 95% CI − 2.25 to − 1.70, P < 0.00001)
(> 6 months). Meta-regression analysis found that publica-
when compared with participants from America, Europe,
tion year, study design, number of patients, preoperative age,
and Asia. In sensitivity analysis, the pooled data was not
preoperative BMI, and NOS score were not significantly

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Table 1  Characteristics of included trails
Authors Year Country Study design Intervention Number Age (years) BMI (kg/m2) Follow-up (months) Outcomes NOS

El-Zawawy 2022 Egypt Prospective SG 40 33.22 ± 10.32 49.30 ± 8.85 12 Hs-CRP 9


Farup 2022 Norway Retrospective RYGB, SG 62 44.7 ± 8.5 39 ± 2 12 Leptin, adiponectin, ghrelin 9
Frühbeck (1) 2022 Spain NA RYGB 31 47 ± 2 42.0 ± 1.2 7 Leptin 9
Frühbeck (2) 2022 Spain NA RYGB 63 46.7 ± 15.6 32.3 ± 6.3 12 CRP, leptin, adiponectin 9
Hany 2022 Egypt Prospective SG 70 33.8 ± 11.45 45.17 ± 6.61 12 Leptin, PYY, GLP-1, ghrelin 9
Khanaghaei 2022 Iran Prospective RYGB 35 18—54 42.06 4 CRP 8
Obesity Surgery (2023) 33:789–806

Moriconi (1) 2022 Italy NA RYGB 30 44 ± 10 46.1 ± 5.5 6 CRP, IL-1β 8


Moriconi (2) 2022 Italy NA RYGB 8 40 ± 6 49.0 ± 6.1 6 CRP, IL-1β 9
Moriconi (3) 2022 Italy NA RYGB 8 41 ± 8 50.1 ± 7.0 6 CRP, IL-1β 9
Pacheco (1) 2022 Spain NA BPD 37 50.0 ± 5.2 46.7 ± 5.1 36 Leptin, adiponectin 9
Pacheco (2) 2022 Spain NA BPD 75 49.6 ± 6.1 46.5 ± 4.3 36 Leptin, adiponectin 9
Pacheco (3) 2022 Spain NA BPD 37 49.8 ± 6.1 46.3 ± 4.1 36 Leptin, adiponectin 9
Sachan (1) 2022 India Prospective SG, gastric bypass 30 38.33 ± 1.99 46.11 ± 1.18 6 CRP, TNF-α, IL-6, adiponectin 8
Salman (2) 2022 Egypt NA SG 54 44.3 ± 7.0 41.6 ± 2.6 12 GLP-1, Hs-CRP 9
Tas 2022 Turkey NA SG 60 40.72 ± 9.27 45.09 ± 2.97 12 Leptin 8
Zhou 2022 China Retrospective SG 72 29 ± 9.43 39.6 ± 6.30 6.7 CRP 9
Lautenbach 2021 Germany Retrospective RYGB, SG 163 41.3 ± 11.6 51.63 ± 8.02 48 CRP, Hs-CRP 8
Salman 2021 Egypt Prospective SG 120 43.7 ± 8.5 43.8 ± 5.2 12 CRP 8
Tabasi 2021 Iran Prospective SG 126 37.3 ± 6.3 43.27 ± 5.40 12 IL-1β, IL-6 8
Carmona-Maurici 2020 Spain Prospective RYGB, SG 66 20—65  ≥ 35 12 CRP, TNF-α, adiponectin, leptin, IL-6 8
Salman (1) 2020 Egypt Prospective SG 50 41.8 ± 8.6 44.2 ± 3.3 12 Leptin, ghrelin 8
Salman (2) 2020 Egypt Prospective RYGB 50 42.5 ± 8.8 43.79 ± 3.4 12 Leptin, ghrelin 8
Salman (3) 2020 Egypt Prospective OAGB 62 43.9 ± 6.8 42.2 ± 2.9 12 Adiponectin, leptin, Hs-CRP, IL-6, 9
TNF-α
Sharma 2019 India NA SG 90 24—68 49.25 ± 3.96 6 Ghrelin 9
Yin 2019 China Prospective SG 60 35.9 42.0 ± 8.9 12 Leptin, ghrelin 7
Arhire 2018 Romania Prospective SG 75 42.11 ± 11.45 45.16 ± 6.78 12 Ghrelin, leptin, adiponectin 8
Demerdash 2018 Egypt Prospective SG 92 42.6 ± 5.4 47.36 ± 5.45 12 Ghrelin, leptin 8
Belligoli 2017 Italy Prospective SG 180 43 ± 11 47.4 ± 7.3 12 Hs-CRP, IL-6, TNF-α, leptin 8
Chen 2017 China Retrospective RYGB 33 47.7 ± 11.6 30.9 ± 4.6 12 Leptin 8
de Luis 2017 Spain Prospective BPD 64 46.5 ± 8.2 48.9 ± 5.8 36 Adiponectin 9
Kalinowski (1) 2017 Poland Prospective SG 36 44.9 ± 10.6 46.1 ± 5.9 12 Ghrelin, leptin 9
Kalinowski (2) 2017 Poland Prospective RYGB 36 43.9 ± 10.8 48.6 ± 5.4 12 Ghrelin, leptin 9
Piche 2017 Canada Prospective BPD 73 NA 49.8 ± 7.1 12 Hs-CRP, IL-6, TNF-α, leptin, adiponec- 8
tin
Rao (1) 2017 USA Prospective GB 9 43.4 ± 3.4 42.5 ± 2.7 7 Leptin, PYY 9
Rao (2) 2017 USA Prospective RYGB 22 43.1 ± 2.4 47.8 ± 1.7 7 Leptin, PYY 9

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793

Rao (3) 2017 USA Prospective SG 11 39.9 ± 2.9 46.4 ± 1.7 7 Leptin, PYY 9


Table 1  (continued)
794

Authors Year Country Study design Intervention Number Age (years) BMI (kg/m2) Follow-up (months) Outcomes NOS

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Sans 2017 France Prospective RYGB 103 40.6 ± 11.2 43.3 ± 4.9 12 CRP 8
Schmatz (1) 2017 Brazil Prospective RYGB 20 36.7 ± 10.5 43.09 ± 1.95 12 Ghrelin, IL-6, IL-1β, TNF-α, adiponec- 9
tin
Schmatz (2) 2017 Brazil Prospective RYGB 20 52.0 ± 10.7 43.40 ± 3.65 12 Ghrelin, IL-6, IL-1β, TNF-α, adiponec- 9
tin
Sell 2017 France Prospective RYGB, GB 53 44.8 ± 10.6 47.0 ± 6.3 12 Adiponectin, CRP, IL-6 8
Thereaux 2017 France Prospective RYGB, SG 37 44.0 ± 10.4 45.2 ± 5.5 12 CRP 8
Tirado 2017 Spain Prospective RYGB, SG 66 42.3 ± 10.2 45.6 ± 6.19 12 Adiponectin, CRP, IL-6, TNF-α, IL-1β 8
Urbanavicius 2017 Lithuania Retrospective GB 103 45.9 ± 11.7 47.5 ± 7.3 48 Leptin, adiponectin 8
Yadav 2017 UK Prospective RYGB 37 49 52 ± 9 12 CRP, leptin, adiponectin, TNF-α 8
Zhu (1) 2017 China Retrospective RYGB 35 39.5 ± 11.8 36.7 ± 4.6 6 GLP-1, ghrelin 9
Zhu (2) 2017 China Retrospective SG 32 42.3 ± 12.8 36.5 ± 6.3 6 GLP-1, ghrelin 9
Adami 2016 Italy Prospective BPD 30 NA 36.3 ± 8.4 60 Leptin, adiponectin 9
Dogan 2016 Turkey NA SG 30 41.23 ± 10.37 49.30 ± 7.92 6 Ghrelin 9
Gentili 2016 Italy NA SG 80 43 ± 11 44.6 ± 7.2 10 Leptin, adiponectin 9
Illan 2016 Spain Prospective VBG-RYGB 73 38.53 ± 10.00 47.56 ± 7.02 12 Hs-CRP, IL-6 8
Molin 2016 Brazil NA RYGB 39 39.4 ± 10.9 44.3 ± 6.4 6 Leptin, RYY​ 9
Morshed 2016 Egypt Prospective SG 30 40.3 ± 8.5 42.71 ± 4.3 12 CRP 8
Nosso (1) 2016 Italy Prospective RYGB 14 49 ± 7 42 ± 6 12 GLP-1, ghrelin 9
Nosso (2) 2016 Italy Prospective SG 19 44 ± 10 46 ± 9 12 GLP-1, ghrelin 9
Pelascini 2016 France Retrospective RYGB 102 45.6 ± 10 45 ± 6.6 24 CRP 9
Richette 2016 France Prospective RYGB, SG, GB 154 41.5 ± 12.3 47.8 ± 7.2 6 Leptin, adiponectin, IL-6, Hs-CRP 9
Shih 2016 China Prospective RYGB, VBG 93 18—65  > 30 12 CRP, IL-6 8
Yu 2016 China Retrospective RYGB 42 46.3 ± 12.8 31.6 ± 4.8 12 Adiponectin 8
Alosco 2015 USA Prospective RYGB 84 43.86 ± 10.39 46.88 ± 6.08 12 Leptin, ghrelin 8
Fellici 2015 Brazil Prospective RYGB 36 18—60 32.1 ± 0.3 12 Hs-CRP, adiponectin 9
Ferrer 2015 Spain Prospective RYGB 32 21—61  > 35 12 Leptin, adiponectin, ghrelin 8
Flores 2015 Spain Prospective RYGB, SG 37 52 ± 8 45 ± 5 12 Leptin 8
Gandolfini 2015 France Prospective RYGB 34 36 ± 11 46.3 ± 5.9 16 GLP-1 9
Hawkins 2015 America Prospective RYGB 77 43.4 ± 10.6 46.7 ± 5.3 12 CRP 8
Netto 2015 Brazil Prospective RYGB 41 39.4 ± 10.9 44.6 ± 6.3 6 Adiponectin, TNF-α, leptin 8
Abdennour 2014 USA Prospective RYGB 345 42 ± 12 47.9 ± 7.4 12 Leptin, adiponectin, IL-6, Hs-CRP 8
Auguet 2014 Spain Prospective RYGB, SG 30 47.2 ± 8.9 46.5 ± 5.0 12 CRP 8
Bužga 2014 Czech Prospective SG 37 43.5 ± 10.2 43.0 ± 4.9 12 Ghrelin, leptin, adiponectin 9
Carrasco (1) 2014 Chile Prospective SG 20 33.5 ± 8.6 37.4 ± 2.9 12 Ghrelin, adiponectin 9
Carrasco (2) 2014 Chile Prospective RYGB 23 36.9 ± 8.4 42.0 ± 3.8 12 Ghrelin, adiponectin 9
Obesity Surgery (2023) 33:789–806
Table 1  (continued)
Authors Year Country Study design Intervention Number Age (years) BMI (kg/m2) Follow-up (months) Outcomes NOS

Ferrannini 2014 USA Prospective BPD, RYGB 182 41 ± 103 48.0 ± 7.8 12 Leptin 8
Lips (1) 2014 Netherlands Retrospective GB 11 46.3 ± 1.9 43.1 ± 0.9 3 weeks GLP-1, PYY, ghrelin 9
Lips (2) 2014 Netherlands Retrospective RYGB 16 48.6 ± 1.6 44.2 ± 0.8 3 weeks GLP-1, PYY, ghrelin 9
Lips (3) 2014 Netherlands Retrospective RYGB 15 51.3 ± 1.9 43.5 ± 1.1 3 weeks GLP-1, PYY, ghrelin 9
Rojano-Rodríguez 2014 Mexico Retrospective RYGB, SG 36 37 ± 7.94 42.48 ± 5.97 6 CRP 9
Yang 2014 China Prospective RYGB, GB, SG, OAGB 178 32.9 ± 10.0 42.0 ± 6.6 12 Hs-CRP 8
Obesity Surgery (2023) 33:789–806

Caron-Cantin 2013 Canada Prospective BPD 70 41.3 ± 10.7 50.0 ± 7.2 12 CRP, IL-6, TNF-α 8
Jimene 2013 Spain Retrospective RYGB, SG 104  ≥ 18  ≥ 35 12 Hs-CRP 8
Terra 2013 Spain NA RYGB, SG 30 47.2 ± 8.9 46.5 ± 5.0 12 Ghrelin, leptin 9
Hady 2012 Poland NA SG 100 NA 52.15 ± 8.5 6 Ghrelin 9
Pardina 2012 Spain Prospective RYGB 34 21–61 48.8 12 Leptin, ghrelin 8
Saleh 2012 Brazil Prospective RYGB 47 41 47.1 ± 5.5 10 Hs-CRP 9
Breitman 2011 USA Prospective RYGB 30 46.9 ± 8.4 43.3 ± 4.1 8 weeks CRP, IL-6, IGF-1, leptin, ghrelin, GLP-1 9
Dalmas 2011 France Prospective RYGB 51 NA 49.8 ± 1.1 12 IL-6, Hs-CRP, leptin, adiponectin 8
Tschoner 2011 Austria Prospective GB, Gastric bypass 36 21—53 42.95 ± 4.22 18 Hs-CRP, TNF-α, IL-6, leptin, adiponec- 9
tin
Broch 2010 Spain Prospective RYGB 63 45.0 ± 9.3 49.7 ± 8.0 12 CRP, adiponectin 8
de Luis 2010 Spain Prospective BPD 41 42.9 ± 10.1 50.6 ± 7.5 12 Leptin, adiponectin, IL-6, TNF-α 8
Handisurya 2010 Austria Prospective RYGB 33 43.75 ± 11.95 47.12 ± 6.78 12 CRP, leptin 8
Ress 2010 Austria Prospective GB, gastric bypass 32 34.6 ± 8.7 42.65 ± 3.99 18 Leptin, adiponectin, Hs-CRP 9
Carroll 2009 USA NA RYGB 34 NA 43.4 ± 5.0 6 CRP, leptin, ghrelin, GLP-1 9
Korner (1) 2009 USA Prospective GB 15 47.1 ± 2.5 41 ± 1 12 Ghrelin, GLP-1, leptin, PYY 8
Korner (2) 2009 USA Prospective RYGB 28 45.0 ± 2.0 48 ± 1 12 Ghrelin, GLP-1, leptin, PYY 8
Moschen 2009 Austria Prospective GB 30 37.5 ± 58.61 42.6 ± 3.86 12 CRP, TNF-α 8
Garcia-Fuentes (1) 2008 Spain NA BPD 38 43.2 ± 11.5 54.0 ± 5.9 7 Leptin, PYY, ghrelin 9
Garcia-Fuentes (2) 2008 Spain NA RYGB 13 42.8 ± 7.4 53.0 ± 9.1 7 Leptin, PYY, ghrelin 9
Karamanakos (1) 2008 Greece Prospective RYGB 16 37 ± 8.25 46.6 ± 3.7 12 Ghrelin, PYY 9
Karamanakos (2) 2008 Greece Prospective SG 16 30.6 ± 7.8 45.1 ± 3.6 12 Ghrelin, PYY 9
Liou 2008 China Prospective OAGB 68 31.6 ± 8.9 39.7 ± 7.2 12 Leptin, ghrelin, CRP 8
Riedl (1) 2008 Austria Prospective RYGB 30 42.9 ± 10.95 47.7 ± 6.02 12 Leptin 8
Riedl (2) 2008 Austria Prospective GB 10 43.9 ± 14.23 47.6 ± 6.64 12 Leptin 8
Czupryniak 2007 Poland Prospective RYGB 68 36.4 ± 10.2 44.4 ± 6.8 24 Leptin 9
Couce 2006 Austria Prospective GB 31 40 ± 11 46 ± 5 6 Leptin, adiponectin 9
Morínigo (1) 2006 Spain Prospective RYGB 12 41.8 ± 2.7 49.7 ± 1.7 6 weeks GLP-1 9
Morínigo (2) 2006 Spain Prospective RYGB 12 46.8 ± 3.2 48.6 ± 1.8 6 weeks GLP-1 9
Morínigo (3) 2006 Spain Prospective RYGB 10 50.5 ± 3.0 49.0 ± 2.1 6 weeks GLP-1 9

13
795

796 Obesity Surgery (2023) 33:789–806

significantly changed when removing any study in turn.

SG, sleeve gastrectomy; RYGB, Roux-en-Y gastric bypass; BPD, biliopancreatic diversion; GB, gastric banding; OAGB, one-anastomosis gastric bypass; VBG-RYGB, vertical banded gastro-
plasty-Roux-en-Y gastric bypass; VBG, vertical banded gastric; NA, not available, CRP, C-reactive protein; IL-6, interleukin-6; Hs-CRP, high-sensitivity C-reactive protein; TNF-α, tumor necro-
NOS Additionally, a fixed effects model yielded a similar result

8
9
9
9
8
8
9
8

8
8
9
Leptin, adiponectin, IL-6, TNF-α, Hs- (SMD =  − 1.03, 95% CI − 1.11 to − 0.96, P < 0.00001) with
the random-effects analysis.

Meta‑analysis of IL‑6

Adiponectin, IL-6, leptin


Twenty-six studies with a total of 1796 patients providing
CRP, adiponectin, IL-6

IL-6 data were included in the meta-analysis. We adopted a

sis factor-α; PAI-1, plasminogen activator inhibitor-1; MCP-1, chemoattractant protein-1; IL-10, interleukin-10; NOS, Newcastle–Ottawa Quality Assessment Scale
random-effects model to aggregate the data because of the
Leptin, ghrelin

high between-study heterogeneity (P < 0.00001, I2 = 90%).


CRP, IL-6
BMI (kg/m2) Follow-up (months) Outcomes

The final summary showed that bariatric surgery could

Leptin
Leptin
Leptin
Leptin
Leptin
Leptin
CRP

reduce patients’ IL-6 levels (SMD =  − 0.59, 95% CI − 0.82


to − 0.35, P < 0.00001) (Fig. 6).
There was no statistically significant difference between
the data obtained by subgroup analysis according to the type
of surgery (P = 0.19) and follow-up duration (P = 0.22).
Although the studies with follow-up duration ≤ 6 months
pooled a non-significant change in IL-6 level, the studies
45.8 ± 7.6 24
41.8 ± 0.8 24
54.1 ± 9.1 12
50.7 ± 9.67 12
47.2 ± 8.5 12
12
17
42.5 ± 4.9 12
12

34.6 ± 13.03 53.01 ± 5.14 6
35.1 ± 13.1 54.24 ± 6.36 6

with > 6 months follow-up led to significant IL-6 reduction.


In addition, sensitivity analysis, through changing analy-
49.8 ± 8.2

48 ± 7
48 ± 7

sis model and one-study-out method, displayed the robust


pooled estimate for I-6.
39.8 ± 10.1
41.3 ± 8.87
Number Age (years)

39.7 ± 6.3
42.7 ± 8.7
42.2 ± 9.3

42.0 ± 10
42 ± 11

Meta‑analysis of Hs‑CRP, TNF‑α, MLP‑1, PYY,


40 ± 9

34

and IL‑1β

Twenty-one articles on Hs-CRP involving 1687 patients


were included for meta-analysis. We chose a random-effects
154
43
40
20
45
65
20
36
30
41
60

model to aggregate the result because of high heterogene-


ity (P < 0.00001, I2 = 83%). The final result demonstrated
a statistically significant reduction of Hs-CRP level after
GB, gastric bypass

bariatric surgery (SMD =  − 1.15, 95% CI − 1.35 to − 0.96,


VBG-RYGB

P < 0.00001).
Intervention

Totally, 439 patients from 17 trials were included in the


meta-analysis of GLP-1. A random-effects model was used
BPD
BPD

GB
GB
GB
GB
GB
GB

SG

to pool the data by reason of between-study heterogene-


ity (P < 0.00001, I2 = 74%). The pooled result showed that
Study design

Prospective
Prospective
Prospective
Prospective
Prospective
Prospective
Prospective
Prospective
Prospective

bariatric surgery was related to the change in ghrelin level


(SMD = 0.30, 95% CI 0.02 to 0.58, P = 0.04).
NA
NA

A total of 794 patients in 16 articles reported TNF-α


results. Because of the heterogeneity between studies
Switzerland

(P < 0.00001, I2 = 97%), we adopted a random-effects model


Year Country

German
Austria

Turkey
Turkey
France
France
2006 France

Brazil
Spain

to summarize the result. The result showed that bariatric sur-


Italy

gery could reduce TNF-α level (MD =  − 0.63, 95% CI − 1.11


1998
2003
2001
2005
2004
2004
2005
2005
2005
2005

to − 0.15, P = 0.01).
Fourteen articles on PYY involving 318 patients were
Table 1  (continued)

included for meta-analysis. We chose a random-effects


García-Unzueta

model to aggregate the result because of high heterogene-


ity (P < 0.00001, I2 = 84%). The final result demonstrated a
Geloneze
Uzun (1)
Uzun (2)
Coupaye

Infanger
Authors

Laimer

statistically significant increase in PYY level after bariatric


Adami
Poitou
Poitou

Kopp

surgery (SMD = 0.63, 95% CI 0.20 to 1.06, P = 0.004).

13
Obesity Surgery (2023) 33:789–806 797

Fig. 2  Forest plots showing change in leptin

Seven articles involved 278 patients reporting the result analyze the result. According to the analysis result, bariatric sur-
of IL-1β. Because of the high heterogeneity of the study gery has a statistically significant effect on the change in MCP-1
(P < 0.00001, I2 = 99%), a random-effects model was adopted to level (MD =  − 9.02, 95% CI − 11.32 to − 6.73, P < 0.00001).

13

798 Obesity Surgery (2023) 33:789–806

Table 2  Subgroup analyses of some adipokines and gastrointestinal hormones


Subgroup Stratification No. of studies P value for I2 Pooled standardized P value
heterogeneity mean differences for pooled
results

Leptin
Bariatric surgery
SG 12  < 0.00001 95%  − 2.87 [− 3.54, − 2.21]  < 0.00001
RYGB 23  < 0.00001 91%  − 2.16 [− 2.53, − 1.78]  < 0.00001
BPD 10  < 0.00001 94%  − 2.46 [− 3.25, − 1.67]  < 0.00001
GB 12  < 0.00001 97%  − 2.42 [− 3.48, − 1.36]  < 0.00001
OAGB 2  < 0.00001 99%  − 9.98 [− 24.90, 4.94] 0.19
Region
America 14  < 0.00001 90%  − 2.21 [− 2.64, − 1.78]  < 0.00001
Europe 44  < 0.00001 94%  − 2.19 [− 2.51, − 1.87]  < 0.00001
Asia 5  < 0.00001 91%  − 1.74 [− 2.54, − 0.94]  < 0.00001
Africa 7  < 0.00001 97%  − 5.75 [− 7.45, − 4.04]  < 0.00001
Follow-up duration
 ≤ 6 months 8  < 0.00001 82%  − 1.61 [− 2.04, − 1.18]  < 0.00001
 > 6 months and ≤ 12 months 51  < 0.00001 93%  − 2.40 [− 2.70, − 2.11]  < 0.00001
 > 12 months 12  < 0.00001 98%  − 3.08 [− 4.15, − 2.01]  < 0.00001
Adiponectin
Bariatric surgery
SG 5  < 0.0001 86% 1.07 [0.55, 1.60]  < 0.0001
RYGB 14  < 0.00001 93% 1.75 [1.24, 2.27]  < 0.00001
BPD 9  < 0.00001 94% 2.03 [1.26, 2.79]  < 0.00001
GB 4 0.80 0% 0.42 [0.21, 0.62]  < 0.0001
OAGB 1 - - 3.08 [2.56, 3.61]  < 0.00001
Region
America 8  < 0.00001 96% 2.80 [1.84, 3.75]  < 0.00001
Europe 31  < 0.00001 90% 1.13 [0.87, 1.39]  < 0.00001
Asia 2 0.18 44% 1.17 [0.64, 1.69]  < 0.00001
Africa 1 - - 3.08 [2.56, 3.61]  < 0.00001
Follow-up duration
 ≤ 6 months 4  < 0.00001 97% 1.44 [0.08, 2.80] 0.04
 > 6 months and ≤ 12 months 28  < 0.00001 92% 1.36 [1.07, 1.66]  < 0.00001
 > 12 months 11  < 0.00001 92% 1.26 [0.75, 1.78]  < 0.00001
Ghrelin
Bariatric surgery
SG 13  < 0.00001 96%  − 1.35 [− 2.00, − 0.69]  < 0.00001
RYGB 20  < 0.00001 93%  − 0.20 [− 0.71, 0.30] 0.43
BPD 2 0.59 0% 0.59 [0.25, 0.94] 0.0007
GB 2 0.25 25% 0.29 [− 0.35, 0.93] 0.38
OAGB 1 - -  − 0.22 [− 0.56, 0.12] 0.20
Region
America 9  < 0.00001 96%  − 1.38 [− 2.36, − 0.40] 0.006
Europe 21  < 0.00001 86% 0.04 [− 0.28, 0.36] 0.80
Asia 6  < 0.00001 97%  − 0.41 [− 1.55, 0.73] 0.48
Africa 4  < 0.00001 98%  − 1.91 [− 3.57, − 0.24] 0.02
Follow-up duration
 ≤ 6 months 10  < 0.00001 96%  − 0.30 [− 1.10, 0.49] 0.46
 > 6 months and ≤ 12 months 30  < 0.00001 95%  − 0.57 [− 1.01, − 0.13] 0.01
CRP

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Obesity Surgery (2023) 33:789–806 799

Table 2  (continued)
Subgroup Stratification No. of studies P value for I2 Pooled standardized P value
heterogeneity mean differences for pooled
results

Bariatric surgery
SG 4  < 0.00001 89%  − 1.46 [− 2.08, − 0.84]  < 0.00001
RYGB 17  < 0.00001 81%  − 1.17 [− 1.47, − 0.86]  < 0.00001
BPD 1 - -  − 0.81 [− 1.16, − 0.47]  < 0.00001
GB 2 0.04 77%  − 0.80 [− 1.52, − 0.07] 0.03
Region
America 4 0.03 66%  − 0.94 [− 1.36, − 0.52]  < 0.0001
Europe 23  < 0.00001 78%  − 1.05 [− 1.27, − 0.84]  < 0.00001
Asia 6  < 0.00001 89%  − 0.80 [− 1.33, − 0.26] 0.003
Africa 2 0.93 0%  − 1.97 [− 2.25, − 1.70]  < 0.00001
Follow-up duration
 ≤ 6 months 8  < 0.00001 80%  − 0.68 [− 1.18, − 0.18] 0.008
 > 6 months and ≤ 12 months 24  < 0.00001 86%  − 1.15 [− 1.40, − 0.91]  < 0.00001
 > 12 months 4 0.22 32%  − 1.00 [− 1.24, − 0.76]  < 0.00001
IL-6
Bariatric surgery
SG 3  < 0.00001 98%  − 0.88 [− 2.01, 0.25] 0.13
RYGB 5  < 0.00001 95%  − 1.31 [− 2.24, − 0.38] 0.006
BPD 4 0.78 0%  − 0.40 [− 0.61, − 0.19] 0.0002
GB 2 0.71 0.0%  − 0.32 [− 0.58, 0.05] 0.02
Region
America 6  < 0.00001 94%  − 1.02 [− 1.65, − 0.39] 0.002
Europe 15  < 0.00001 73%  − 0.54 [− 0.72, − 0.35]  < 0.00001
Asia 4  < 0.00001 97%  − 0.34 [− 1.54, 0.86] 0.58
Follow-up duration
 ≤ 6 months 3 0.0002 88% 0.21 [− 0.54, 0.96] 0.59
 > 6 months and ≤ 12 months 21  < 0.00001 91%  − 0.71 [− 0.98, − 0.44]  < 0.00001
 > 12 months 2 0.81 0%  − 0.53 [− 0.85, − 0.21] 0.001

SG, sleeve gastrectomy; RYGB, Roux-en-Y gastric bypass; BPD, biliopancreatic diversion; GB, gastric banding; OAGB, one-anastomosis gastric
bypass; CRP, C-reactive protein; IL-6, interleukin-6

Discussion leptin can induce a high metabolic rate, thermogenesis,


and anorexic status [103]. After high-calorie food con-
Given that bariatric surgery is becoming increasingly sumption, serum leptin level would be increased to keep
widely used, sufficient knowledge about its underlying the balance of energy control and body weight. Generally
mechanism is essential, which can help to choose the speaking, the amount of leptin is proportional to body fat
most suitable surgical procedure for patients. Change in content; patients with obesity would have higher leptin lev-
adipokines and gastrointestinal hormones after bariatric els than patients with normal weight [104]. But it is worth
surgery has been proposed with inconsistent results. To our noting that high leptin level in patients with obesity was
knowledge, this is the first study that took a series of adi- not related to anorexia or body fat loss, possibly explained
pokines and gastrointestinal hormones into meta-analysis. by the effect of endogenous leptin resistance [105]. Our
We found that the levels of leptin, ghrelin, CRP, IL-6, Hs- pooled results showed that after weight reduction caused
CRP, TNF-α, and IL-1β reduced significantly after bari- by bariatric surgery, serum leptin level would decrease
atric surgery, while adiponectin, GLP-1, and PYY levels significantly (P < 0.05). Some previous studies reported
increased significantly. comparable, significant reduction in serum leptin levels
This study’s most reported adipokine was leptin, a poly- after either RYGB or SG [74, 106]; our subgroup analy-
peptide hormone secreted by adipose tissues and stomach ses also had similar results. The fact that OAGB had no
fundus cells. By acting centrally in the hypothalamus, significant effect on leptin level may be attributed to few

13

800 Obesity Surgery (2023) 33:789–806

Fig. 3  Forest plots showing change in adiponectin

included studies. Regarding the region’s impact, patients regardless of gender and menopausal status [107]. There-
from Africa have more substantial leptin reduction than fore, sufficient attention should be paid to the fracture risk
patients from other regions, revealing that ethnic factors after bariatric surgery and enough calcium and vitamin D
may be related to the change in leptin level. needed to be administered. Subgroup analysis showed that
As the highest content of adipokines in peripheral blood, OAGB, RYGB, and BPD procedures brought about a more
adiponectin is expressed exclusively by adipocytes. Pre- significant increase in adiponectin than GB procedure. A
vious literature demonstrated low circulating adiponec- possible reason for this is that GB is just a restrictive sur-
tin level in obesity [43], which was proved by our meta gery, while OAGB, RYGB, and BPD are mixed procedures
results that an increased level of adiponectin was found which can combine intake limitation and malabsorption
after bariatric surgery. Adiponectin is an insulin-sensitizing and will provide better weight loss.
hormone; increased adiponectin after surgery can partly Ghrelin is a hormone produced mainly by P/D1 cells
explain why blood glucose status can be improved after in the gastric fundus. It was widely believed that bariatric
bariatric surgery in patients with diabetes [43]. In addition, surgery could reduce ghrelin level. The whole pooled result
adiponectin was reported as the most crucial adipokine that of ghrelin in our study also confirmed this (SMD =  − 0.50,
is negatively connected with bone mineral density (BMD) P = 0.009). What should be noteworthy in our subgroup

13
Obesity Surgery (2023) 33:789–806 801

Fig. 4  Forest plots showing change in ghrelin

analyses is that ghrelin levels reduced significantly in postoperative time points [26]. With respect to the impact
patients who received LSG (SMD =  − 1.35, P < 0.00001), of follow-up, our pooled data revealed no significant dif-
increased in BPD (P = 0.0007), and remained unchanged ference in CRP change in postoperative follow-up. But a
in RYGB and GB. The reduced ghrelin level after SG can longer follow-up is needed because a study showed that
be attributed to having the gastric fundus resected. Few the decline in CRP and Hs-CRP could be at the U-shaped
included studies on BPD and GB may also have an impact curve, with the lowest level at postoperative 2 years fol-
on the pooled data. Further studies considering the effect lowed by a gradual increase [26]. TNF-α is another marker
of surgical procedures are needed. that reflects an inflammatory state. Data from previous
CRP and Hs-CRP are both common inflammatory mark- studies reported unaltered TNF-α after bariatric surgery
ers. As a chronic inflammatory status, obesity is associated [29, 108]. This meta-analysis concluded that bariatric sur-
with elevated CRP and Hs-CRP levels. Our pooled data gery was associated with significant decreased TNF-α.
indicated that CRP and Hs-CRP levels would reduce after IL-6 is a proinflammatory cytokine with many functions
bariatric surgery. Regarding the comparison among vari- and participates actively in the immune response. Patients
ous surgeries, we found no significant differences in mean with obesity always encounter high chronic subclinical
change before and after surgery between different surgical inflammation. Therefore, increased serum IL-6 level was
procedures. This was not inconsistent with Lautenbach’s found in our pooled result compared to the postoperative
study, which found that CRP level were significantly higher level. Additionally, we found no significant relationship
in patients undergoing SG compared to RYGB at some between IL-6 change and surgical procedures and regions,

13

802 Obesity Surgery (2023) 33:789–806

Fig. 5  Forest plots showing change in CRP

but the literature indicated that IL-6 had some association their potential as weight-loss drugs, such as Seiglutide.
with obesity-related diseases. For example, a positive cor- Increased GLP-1 level found in our study also supported
relation between IL-6 and CT90 (the percentage of total the effect of GLP-1 on weight reduction. IL-1β is a proin-
sleep time in which the oxygen saturation remains below flammatory factor, and the pooled result of postoperative
90%) was found before bariatric surgery [42], suggesting IL-1β level decreased when compared with preoperative
that the status of obstructive sleep apnea in patients with data (SMD =  − 9.02, P < 0.00001).
obesity can impact both inflammatory and metabolic lev- Some limitations of this meta-analysis should be pointed
els. Behinds, IL-6 change after bariatric surgery is earlier out. The first limitation is between-study heterogeneity; type
and more obvious in patients with diabetes than without of bariatric surgery, study region, and follow-up duration
diabetes, which may be explained by the fact that diabetes are different between studies and may result in reporting
is also an inflammatory disease and correcting adiposity biases. Nevertheless, the random-effects model was used
alone is probably not enough to improve the inflammatory when appropriate to provide the most conservative results.
state [53]. In addition, sensitivity analysis and subgroup analysis were
Some other vital adipokines and gastrointestinal hor- conducted and showed that the pooled data were relatively
mones have also been included in this analysis. PYY is robust. Another limitation is that available data about BPD
secreted from the distal gut cells, which can suppress appe- and OAGB procedures are limited. All in all, more studies
tite by reducing gastric emptying and slowing down the gut taking the type of bariatric surgery and patient characteris-
flow. Our study found elevated PYY level after bariatric tics into account are needed, so as to determine the impact of
surgery. Due to the fact that GLP-1 has significant anti-type specific bariatric surgery on adipokines and gastrointestinal
2 diabetes effects, GLP-1 analogs have been evaluated for hormones in particular populations.

13
Obesity Surgery (2023) 33:789–806 803

Fig. 6  Forest plots showing change in IL-6

Conclusion 2. Afshin A, Forouzanfar MH, Reitsma MB, et al. Health effects of


overweight and obesity in 195 countries over 25 years. New Engl
J Med. 2017;377(1):13–27.
Based on the currently available evidence, bariatric surgery 3. Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus
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in adiponectin, GLP-1, and PYY levels.
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Funding  The work was supported by the Fundamental Research Funds 5. Robert M, Espalieu P, Pelascini E, et al. Efficacy and safety of
for the Central Universities (21622304) and the Basic and Applied one anastomosis gastric bypass versus Roux-en-Y gastric bypass
Basic Research Project of Guangzhou Basic Research Program for obesity (YOMEGA): a multicentre, randomised, open-label,
(SL2023A04J01245). non-inferiority trial. The Lancet. 2019;393(10178):1299–309.
6. Valentí V, Cienfuegos JA, Becerril MS, et al. Mechanism of bari-
Data Availability  The analyzed datasets generated during the study are atric and metabolic surgery: beyond surgeons, gastroenterologists
available from the corresponding author on reasonable request. and endocrinologists. Rev Esp Enferm Dig. 2020;112(3):229–33.
7. Riedl M, Vila G, Maier C, et al. Plasma osteopontin increases
Declarations  after bariatric surgery and correlates with markers of bone
turnover but not with insulin resistance. J Clin Endocrinol
Ethical Approval  This article does not contain any studies with human Metab. 2008;93(6):2307–12.
participants or animals performed by any of the authors. 8. Salman MA, El-Ghobary M, Soliman A, et  al. Long-term
changes in leptin, chemerin, and ghrelin levels following Roux-
Consent to Participate  Informed consent does not apply. en-Y gastric bypass and laparoscopic sleeve gastrectomy. Obes
Surg. 2020;30(3):1052–60.
9. Pardina E, Ferrer R, Baena-Fustegueras JA, et al. Only C-reactive
Conflict of Interest  The authors declare no competing interests.
protein, but not TNF-alpha or IL6, reflects the improvement in
inflammation after bariatric surgery. Obes Surg. 2012;22(1):131–9.
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Authors and Affiliations

Jiayun Huang1 · Yanya Chen1,2 · Xuan Wang1 · Cunchuan Wang3 · Jingge Yang3 · Bingsheng Guan3 

1 3
School of Nursing, Jinan University, Guangzhou 510632, Department of Gastrointestinal Surgery, First Affiliated
China Hospital of Jinan University, Guangzhou 510632, China
2
Department of Infectious Diseases and Public Health, Jockey
Club College of Veterinary Medicine and Life Sciences, City
University of Hong Kong, Hong Kong 999077, China

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