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Year : 2016  |  Volume : 12  |  Issue : 2  |  Page : 897-902

Serum adiponectin levels are inversely correlated with leukemia: A meta-analysis

1 Department of Hematology, Yantai Yuhuangding Hospital, Yantai 264000, Shandong, P.R. China
2 Department of Cardiology, Yantai Yuhuangding Hospital, Yantai 264000, Shandong, P.R. China

Date of Web Publication25-Jul-2016

Correspondence Address:
Jun-Jie Ma
Department of Hematology, Yantai Yuhuangding Hospital, No. 20, Yuhuangding East Road, Yantai 264000, Shandong
P.R. China
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0973-1482.186695

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 > Abstract 

Object: This study is aimed at exploring the correlation between serum adiponectin (ADPN) levels and leukemia.
Materials and Methods: Eligible studies were retrieved using both computerized and manual searches. Relevant case-control studies were enrolled in strict accordance to our inclusion and exclusion criteria.
Result: We searched 130 published studies and included 11 eligible studies for our meta-analysis according to our rigorous inclusion and exclusion criteria. The selected studies included 637 leukemia patients and 524 healthy controls. Our meta-analysis showed: (1) Serum ADPN levels of patients with leukemia were lower than healthy controls; (2) a subgroup analysis based on sample size verified that serum ADPN levels in patients with leukemia were significantly lower than that in healthy controls irrespective of a large sample size (n ≥ 80) or a small sample size (n < 80).
Conclusion: Our meta-analysis suggested that serum ADPN levels may be inversely correlated with leukemia, and ADPN levels can be used as an effective biologic marker in early diagnosis and therapeutic monitoring of leukemia.

Keywords: Acrp 30, AdipoQ, GBP28, leukemia, serum adiponectin

How to cite this article:
Ma JJ, Shang J, Wang H, Sui JR, Liu K, Du JX. Serum adiponectin levels are inversely correlated with leukemia: A meta-analysis. J Can Res Ther 2016;12:897-902

How to cite this URL:
Ma JJ, Shang J, Wang H, Sui JR, Liu K, Du JX. Serum adiponectin levels are inversely correlated with leukemia: A meta-analysis. J Can Res Ther [serial online] 2016 [cited 2020 Oct 21];12:897-902. Available from: https://www.cancerjournal.net/text.asp?2016/12/2/897/186695

 > Introduction Top

Leukemia, a blood cancer, is a kind of malignant tumor effecting the hematopoietic system that originates in bone marrow cells and subsequently, leukemic cells populate the peripheral blood.[1] Leukemia is a deadly disease with 250,000 new cases occurring annually in the USA.[2],[3] The main clinical symptoms of leukemia were presented with fever, pallor, bleeds peripheral edema, lymphadenopathy, organomegaly, and dyspnea.[4],[5] Leukemia has several subtypes, including chronic lymphoid leukemia, acute lymphoblastic leukemia (ALL), chronic myeloid leukemia, acute myeloid leukemia (AML) and other acute leukemia.[6],[7] Between 2005 and 2009, the incidence of childhood AML was estimated at 7.7 cases/million children aged 0–14 in the United States and continues to grow at an alarming rate.[8] ALL accounted for nearly 75% of newly diagnosed leukemias and 25% of all malignancies in pediatric patients.[9] The etiology of leukemia is complex and involves occupational exposures to benzene or other organic solvents and chemicals, chemotherapeutic agents, agrichemicals, tobacco smoke, genetic factors and obesity.[10],[11] Leukemia is treated by multiple treatment options such as chemotherapy, radiation, surgery, and bone marrow and stem cell transplants.[12] It was worth noting that alterations in serum adiponectin (ADPN) levels have been observed in leukemia patients.[13]

Adiponectin, also named Acrp 30, AdipoQ and GBP28 is an adipocyte-derived secretory protein that regulates several metabolic processes involving glucose regulation and fatty acid catabolism.[14],[15] ADPN presents in copious amounts in human serum, in the range 3–30 µg/ml, usually sequestered as oligomeric complexes.[16] The structure of ADPN is very similar to the complement factor C1q.[17] ADPN is a 244-amino acid protein containing four distinct domains: An amino-terminal signal peptide, followed by a species-specific variable domain, a collagen-like region of 22 Gly-X-Y repeats, and a carboxy-terminal orbicular domain that binds to ADPN receptors, similar to the complement factor C1q and the trimeric topology of tumor necrosis factor-alpha.[18],[19] ADPN is functionally in insulin-sensitivity, anti-inflammatory, and anti-atherogenic, which is a key role in development of insulin resistance in diseased states.[20] Higher circulating levels of ADPN show clear correlation with low Gleason score, lower tumor stage and decreased risk of incidence in prostate cancer.[21] Numerous studies have indicated the crucial relations between serum ADPN levels and various diseases including leukemia, hypertension, dyslipidemia, metabolic syndrome, hyperuricemia, atherosclerosis, chronic kidney disease and pulmonary disease.[13],[22],[23] Previous studies revealed an inverse relation between serum levels of ADPN and the risk of AML in children.[24],[25] However, there was study found no association between serum ADPN levels and leukemia.[26] In view of the conflicting results from previous studies, a meta-analysis was conducted by analyzing available previous studies aimed to further assess the correlations between serum ADPN levels and leukemia.

 > Materials and Methods Top

Data sources and keywords

In order to identify relevant published studies, the PubMed database was searched exhaustively (last updated search in September, 2014) by applying a sensitive search strategy using search terms: (“adiponectin” or “ADPN” or “insulin-sensitizing hormone”) and (“leukemia” or “blood cancer” or “hematologic neoplasms” or “acute leukemia”). Manual searches were carried on to retrieve other cross-references.

Inclusion and exclusion criteria

The following inclusion criteria for selection of studies for this meta-analysis were: (1) The studies must be designed as case-control and focused on the associations between serum ADPN levels and leukemia; (2) patients with leukemia were in case group, while the healthy individuals were selected as control group; (3) all the eligible studies contained complete information; (4) studies were published in Chinese or in English; (5) for overlapping publications, only the most recent or the most complete study was included in this meta-analysis. The exclusion criteria were: (1) The insufficient data; (2) significant differences in baseline characteristics between the case and control group; (3) duplicate publications; (4) the indeterminacy of diagnostic criteria.

Data extraction and quality assessment

In order to obtain reliable data extraction, we used a standardized form by two independent investigators to verify the extracted data from the enrolled studies. The following information was collected: The first author, publication year, country, ethnicity, language, disease, detection method, age, gender, the number of cases and controls. A third investigator was consulted in case of any disagreements during data collection. The quality of selected papers was assessed by two or more investigators independently, according to the Newcastle–Ottawa Scale (NOS) criteria.[27] The detailed NOS criteria were presented in [Table 1].
Table 1: Newcastle-Ottawa quality assessment scale for case-control studies

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Statistical analysis

The Stata statistical software (Version 12.0, Stata Corporation, College Station, TX, USA) was conducted in the meta-analysis. We counted the standard mean difference (SMD) and its 95% confidence intervals (95% CIs) to evaluate the differences of serum ADPN levels between the cases and the healthy controls by applying random effects model or fixed-effects model. Z-test was carried to evaluate the significance of pooled SMDs. The heterogeneity between all the studies was evaluated by the Cochran's Q-statistic (P < 0.05 was considered significant) and I2 test (0%, no heterogeneity; 100%, maximal heterogeneity).[28] Random effects model was used in the case of significant heterogeneity (P < 0.05 or I2 test exhibited >50%), otherwise, a fixed effect model was used.[29] In addition, the single factor and multi-factor meta-regression analysis was utilized to assess the potential sources of heterogeneity, and Monte Carlo method was employed to obtain further confirmation.[30],[31] Univariate and multivariate meta-regression analysis was used to assess whether the results had the significant influence on the overall results by deleting a single studies one by one. Furthermore, the funnel plot and Egger's linear regression test was used to assess publication bias in included studies.[32],[33]

 > Results Top

Baseline characteristics of included studies

Electronic database and manual searches resulted in the identification of 130 potential articles after excluding duplicates (n = 2), letters, reviews or meta-analysis (n = 1), nonhuman studies (n = 16), and studies not related to our research topic (n = 24). The remaining studies (n = 87) were reviewed and additional 73 studies were excluded because they did not represent case-control or cohort studies (n = 23), were not relevant to leukemia (n = 22), or not relevant to serum ADPN levels (n = 28). After further assessment, three studies were removed for not containing enough information. Finally, 11 eligible studies published between 2006 and 2014 were incorporated in our meta-analysis and included a total of 1161 samples (637 leukemia cases and 524 healthy controls).[15], 26, [34],[35],[36],[37],[38],[39],[40],[41],[42] Total four studies were performed in Asians (all from China), five studies were conducted in Caucasians (two studies from Turkey, one from USA and two from Greece) and two studies carried out in Africans (both from Egypt). The baseline characteristics for the 11 studies are shown in [Table 2].
Table 2: Baseline characteristics for the 11 eligible studies

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Pooled outcome of meta-analysis

Random effects model was applied because of heterogeneity among studies (I2 = 96.9%, P < 0.001). The result of our meta-analysis revealed that serum ADPN levels of patients with leukemia were significantly lower than in healthy controls (SMD = −2.19, 95% CI = −3.05–−1.33, P < 0.001) [Figure 1]. A subgroup analysis on the basis of sample size demonstrated that serum ADPN levels of patients with leukemia in large sample size (n ≥ 80) and small sample size (n < 80) were significantly lower than that in healthy controls (small: SMD = −2.20, 95% CI = −3.05–−1.36, P < 0.001; large: SMD = −2.09, 95% CI = −3.70–−0.47, P = 0.011) [Figure 2]. The meta-regression analysis present in [Figure 3] and [Table 3] indicated that publication year, sample size, country, ethnicity, language and detection method were not the potential sources of heterogeneity.
Figure 1: Forest plots to compare the differences of serum adiponectin levels between patients with leukemia and the healthy controls in the meta-analysis

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Figure 2: Forest plots of comparison between serum adiponectin levels in leukemia patients and the healthy controls in subgroup analyses by sample size

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Figure 3: Meta-regression analyses on publication year, country, ethnicity, language and detection method

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Table 3: Meta-regression analyses of potential source of heterogeneity

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Sensitivity analysis and publication bias

The result of sensitivity analysis showed that all enrolled studies had no significant effect on the pooled SMDs on correlations between serum ADPN levels and leukemia. The asymmetric funnel plots, suggested that there was publication bias in the enrolled studies and the Egger linear regression analysis further confirmed the lack of publication bias (P = 0.001) [Figure 4].
Figure 4: Sensitivity analysis and risk of publication bias of serum adiponectin levels in leukemia patients and the healthy controls

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 > Discussion Top

Leukemia begins in the bone marrow and eventually lead to the production of a large numbers of abnormal white blood cells.[43] Several previous studies detected low serum ADPN levels in various diseases, including leukemia.[22],[44],[45] However, there was also study questioned the correlation between ADPN and leukemia and required further investigation.[26] We conducted this meta-analysis to understand the specific association between ADPN and leukemia.

We find that the serum ADPN levels were significantly lower leukemia patients compared to healthy controls, indicating that ADPN reduction might be an important role in the development of leukemia. The research of El-Baz et al. in leukemia patients reported that low ADPN level at diagnosis showed their implication in leukemia pathogenesis and may serve as potential clinically significant diagnostic marker to detect leukemic relapse.[24] Ozturk et al. investigated ADPN receptors expressions in cell lines of leukemia patients and their study demonstrated that the increase in AdipoR1 and the decrease in AdipoR2 expressions were seen to be related with leukemia pathogenesis.[46] The potential mechanisms by which decrease of ADPN level might influence leukemia might be related to angiogenesis and it is shown to play an picotal rolein the progression of leukemia.[47],[48],[49] Furthermore, ADPN is an adipocytokine which is produced in significant amounts by adipocytes, which are the most abundant stromal cells in human adult bone marrow.[50] ADPN possesses multiple functions including anti-inflammatory, anti-proliferative, and pro-apoptotic properties.[51] ADPN activates caspase cascade in vascular endothelial cells to induce apoptosis, and thus plays a negative regulatory role in angiogenesis.[52] Therefore, lower serum level of ADPN might cause increased angiogenesis, which leads to the accumulation of lymphocytes in the peripheral blood, bone marrow, and secondary lymphoid organs and thereby aid in the progression of leukemia. Consistent with this, a previous study showed that ADPN exerted a remarkably protective effect in leukemia, although the specific mechanism remained to be elucidated.[36]

The subgroup analysis on the basis of sample size revealed that the serum levels of ADPN in patients in both small and large sample size were significantly lower than those in healthy controls, further confirming the reliability of the result of present meta-analysis that the serum ADPN levels are notably lower in leukemia patients than in healthy controls.

We also admit limitations of this study. Sample size in several selected studies was relatively small, which may influence the accuracy of final result in our meta-analysis. Moreover, the boundary of small and large sample size was not defined in accordance with relevant standard, and thereby the result of the subgroup analysis by sample size might be affected to some extent.

To summarize, serum ADPN level might play a protective role in leukemia, and therefore, ADPN could be considered as a reliable biological marker for early diagnosis and monitoring treatment of leukemia. Our conclusion needs to be confirmed in better designed research studies involving larger sample sizes and a more appropriate multivariate analysis.

 > Acknowledgments Top

We would like to acknowledge the reviewers for their helpful comments on this paper.

 > References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3]


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