The DOI matches its Crossref record; 72 of the 72 references it cites were found in a registry or an index.
Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis
Abstract
BACKGROUND: Conflicting results regarding adiponectin levels in women with polycystic ovary syndrome (PCOS) have been reported. To evaluate adiponectin levels in PCOS, a systematic review of all studies comparing adiponectin levels in women with PCOS with healthy controls and a meta-analysis of those involving women with similar body mass index (BMI) were performed. The influence of possible effect modifiers, such as insulin resistance (IR) and testosterone, was investigated. The influence of obesity was investigated through a 'nested' meta-analysis after within-study BMI stratification and appropriate pooling. METHODS: Literature search was conducted through MEDLINE, EMBASE, Cochrane CENTRAL (through June 2008), references from relevant studies and personal contact with the authors. Thirty-one studies, reporting data on 3469 subjects, were reviewed and 16 included in the main meta-analysis. RESULTS: Women with PCOS demonstrated significantly lower adiponectin values [weighted mean difference (95% confidence interval) -1.71 (-2.82 to -0.6), P < 10(-4)], yet with significant between-study heterogeneity. Lower adiponectin levels are associated with the IR observed in women with PCOS, compared with controls. IR, but not total testosterone, was found significant among biological parameters explored in the meta-regression model. Hypoadiponectinaemia was present in both lean and obese women with PCOS when compared with non-PCOS counterparts. Data on high molecular weight (HMW) adiponectin are limited (three studies). CONCLUSIONS: After controlling for BMI-related effects, adiponectin levels seem to be lower in women with PCOS compared with non-PCOS controls. Low levels of adiponectin in PCOS are probably related to IR but not to testosterone. Total adiponectin should not be used as a biomarker of PCOS severity. Further investigation is needed for HMW adiponectin levels in PCOS.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“after controlling for BMI-related effects, adiponectin levels appear to be lower in women with PCOS than in controls without PCOS [44].”
From PCOS and nutritional approaches: Differences between lean and obese phenotype (2021) · cites this paper as [44]
Citations
Cites
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139
Meta-analysis in clinical trials
DerSimonian, R., & Laird, N. (1986) · Controlled Clinical Trials · doi:10.1016/0197-2456(86)90046-2 · Cited by 39,552
Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., & Turner, R. C. (1985) · Diabetologia · doi:10.1007/bf00280883 · Cited by 31,502
Meta-analysis of Observational Studies in Epidemiology<SUBTITLE>A Proposal for Reporting</SUBTITLE>
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623
(2014) · Medical Entomology and Zoology · Cited by 17,633
Wasserman, S. S., Hedges, L. V., & Olkin, I. (1988) · Journal of Educational Statistics · doi:10.2307/1164953 · Cited by 10,377
(2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.10.004 · Cited by 9,050
The Rotterdam ESHRE/ASRM-sponsored PCOS consensus workshop group (2004) · Human Reproduction · doi:10.1093/humrep/deh098 · Cited by 6,138
Statistical Methods for Meta-Analysis.
Freeman, P. R., Hedges, L. V., & Olkin, I. (1986) · Biometrics · doi:10.2307/2531069 · Cited by 4,840
Weyer, C., Funahashi, T., Tanaka, S., Hotta, K., Matsuzawa, Y., Pratley, R. E., & Tataranni, P. A. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.5.7463 · Cited by 3,541
Adiponectin and Adiponectin Receptors
Kadowaki, T., & Yamauchi, T. (2005) · Endocrine Reviews · doi:10.1210/er.2005-0005 · Cited by 2,634
Franks, S. (1995) · New England Journal of Medicine · doi:10.1056/nejm199509283331307 · Cited by 2,463
Ehrmann, D. A. (2005) · New England Journal of Medicine · doi:10.1056/nejmra041536 · Cited by 1,920
Pajvani, U. B., Hawkins, M., Combs, T. P., Rajala, M. W., Doebber, T., Berger, J. P., Wagner, J. A., Wu, M., Knopps, A., Xiang, A. H., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311113200 · Cited by 1,163
Language bias in randomised controlled trials published in English and German
Egger, M., Zellweger-Zähner, T., Schneider, M., Junker, C., Lengeler, C., & Antes, G. (1997) · The Lancet · doi:10.1016/s0140-6736(97)02419-7 · Cited by 1,028
Adjusting for publication bias in the presence of heterogeneity
Terrin, N., Schmid, C. H., Lau, J., & Olkin, I. (2003) · Statistics in Medicine · doi:10.1002/sim.1461 · Cited by 809
Franks, S. (1997) · Archives of Disease in Childhood · doi:10.1136/adc.77.1.89 · Cited by 802
Adiponectin – journey from an adipocyte secretory protein to biomarker of the metabolic syndrome
TRUJILLO, M. E., & Scherer, P. E. (2005) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2004.01426.x · Cited by 782
Hara, K., Horikoshi, M., Yamauchi, T., Yago, H., Miyazaki, O., Ebinuma, H., Imai, Y., Nagai, R., & Kadowaki, T. (2006) · Diabetes Care · doi:10.2337/dc05-1801 · Cited by 584
Wang, C., Catlin, D. H., Demers, L. M., Starcevic, B., & Swerdloff, R. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031287 · Cited by 580
Decreased Plasma Adiponectin Concentrations in Women with Dyslipidemia
Matsubara, M., Maruoka, S., & Katayose, S. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.6.8550 · Cited by 544
Adiponectin Multimeric Complexes and the Metabolic Syndrome Trait Cluster
Lara‐Castro, C., Luo, N., Wallace, P., Klein, R. L., & Garvey, W. T. (2006) · Diabetes · doi:10.2337/diabetes.55.01.06.db05-1105 · Cited by 480
Morales, A. J., Laughlin, G. A., Bützow, T. L., Maheshwari, H., Baumann, G., & Yen, S. S. C. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.8.8768842 · Cited by 453
Xu, A., Chan, K. W., Hoo, R. L. C., Wang, Y., Tan, K. C. B., Zhang, J., Chen, B., Lam, M. C., Tse, C. A., Cooper, G. J. S., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414231200 · Cited by 424
Adiponectin - Its Role in Metabolism and Beyond
Stefan, N., & Stümvoll, M. (2002) · Hormone and Metabolic Research · doi:10.1055/s-2002-34785 · Cited by 293
Elkind-Hirsch, K., Marrioneaux, O., Bhushan, M., Vernor, D., & Bhushan, R. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0115 · Cited by 276
Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study
Escobar-Morreale, H. F. (2006) · Human Reproduction · doi:10.1093/humrep/del146 · Cited by 200
Endothelial Dysfunction in PCOS: Role of Obesity and Adipose Hormones
Carmina, E., Orio, F., Palomba, S., Longo, R. A., Cascella, T., Colao, A. A. L., Lombardi, G., Rini, G. B., & Løbo, R. A. (2006) · The American Journal of Medicine · doi:10.1016/j.amjmed.2005.10.059 · Cited by 199
Young Obese Women with Polycystic Ovary Syndrome Have Evidence of Early Coronary Atherosclerosis
Juran, R., Kerchner, A., Maifeld, M., van Beek, E. J. R., Jagasia, D. H., & Dokras, A. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1343 · Cited by 194
Meta-analysis. Beyond the grand mean?
Smith, G. D., Egger, M., & Phillips, A. N. (1997) · BMJ · doi:10.1136/bmj.315.7122.1610 · Cited by 174
Can meta-analysis help target interventions at individuals most likely to benefit?
Thompson, S. G., & Higgins, J. P. (2005) · The Lancet · doi:10.1016/s0140-6736(05)70200-2 · Cited by 174
Adiponectin Levels in Women with Polycystic Ovary Syndrome
Orio, F., Palomba, S., Cascella, T., Milan, G., Mioni, R., Pagano, C., Zullo, F., Colao, A., Lombardi, G., & Vettor, R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-022033 · Cited by 173
Ibáñez, L., & de Zegher, F. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031281 · Cited by 172
Plasma adiponectin and insulin resistance in women with polycystic ovary syndrome
Ardawi, M. S. M., & Rouzi, A. A. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.077 · Cited by 165
Serum adiponectin levels in women with polycystic ovary syndrome
Panidis, D. (2003) · Human Reproduction · doi:10.1093/humrep/deg353 · Cited by 156
Ducluzeau, P., Cousin, P., Malvoisin, E., Bornet, H., Vidal, H., Laville, M., & PUGEAT, M. M. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030219 · Cited by 137
Evidence for altered adipocyte function in polycystic ovary syndrome
Carmina, E., Orio, F., Palomba, S., Cascella, T., Longo, R. A., Colao, A., Lombardi, G., & Løbo, R. A. (2005) · European Journal of Endocrinology · doi:10.1530/eje.1.01868 · Cited by 134
Glintborg, D., Andersen, M., Hagen, C., Frystyk, J., Hulstrøm, V., Flyvbjerg, A., & Hermann, A. P. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02207 · Cited by 133
Spranger, J., Möhlig, M., Wegewitz, U. E., Ristow, M., Pfeiffer, A. F. H., Schill, T., Schlösser, H. W., Brabant, G. E., & Schöfl, C. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02159.x · Cited by 130
Ibáñez, L., Valls, C., Marcos, M. V., Ong, K. K., Dunger, D. B., & de Zegher, F. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0463 · Cited by 123
Methods correcting for multiple testing: operating characteristics
Brown, B. W., & Russell, K. E. (1997) · Statistics in Medicine · doi:10.1002/(sici)1097-0258(19971130)16:22 · Cited by 118
Carmina, E., Bucchieri, S., Mansueto, P., Rini, G., Ferin, M., & Løbo, R. A. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.03.007 · Cited by 103
Ruutiainen, K., & Seppälä, M. T. (1991) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-199106000-00004 · Cited by 99
Xita, N. V., Georgiou, I. A., Chatzikyriakidou, A., Vounatsou, M., Papassotiriou, G.-P., Papassotiriou, I., & Tsatsoulis, A. A. (2005) · Clinical Chemistry · doi:10.1373/clinchem.2004.043109 · Cited by 92
Majuri, A., Santaniemi, M., Rautio, K., Kunnari, A., Vartiainen, J., Ruokonen, A., Kesäniemi, Y. A., Tapanainen, J. S., Ukkola, O. H., & Morin-Papunen, L. C. (2007) · European Journal of Endocrinology · doi:10.1530/eje.1.02331 · Cited by 89
Siemińśka, L., Marek, B., Kos‐Kudła, B., Niedziolka, D., Kajdaniuk, D., Nowak, M., & Głogowska-Szeląg, J. (2004) · Journal of Endocrinological Investigation · doi:10.1007/bf03347474 · Cited by 85
Carmina, E., Chu, M. C., Morán, C., Tortoriello, D. V., Vardhana, P. A., Tena, G., Preciado, R., & Løbo, R. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.03.085 · Cited by 84
Adiponectin Levels in Women With Polycystic Ovary Syndrome and Severe Insulin Resistance
Sepilian, V., & Nagamani, M. (2004) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2004.09.003 · Cited by 70
Glintborg, D., Frystyk, J., Højlund, K., Andersen, K. K., Henriksen, J. E., Hermann, A. P., Hagen, C., Flyvbjerg, A., & Andersen, M. (2007) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2007.03015.x · Cited by 69
Genetic Determinants of Insulin Action in Polycystic Ovary Syndrome
Haap, M. M., Machicao, F. E., Stefan, N., Thamer, C., Tschritter, O., Schnuck, F., Wallwiener, D. R., Stümvoll, M., Häring, H.-U., & Fritsche, A. (2005) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-2005-837665 · Cited by 67
Moran, L. J., Noakes, M., Clifton, P. M., Wittert, G. A., Belobrajdic, D. P., & Norman, R. J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2336 · Cited by 66
Schwarz, P. E. H., Towers, G. W., Fischer, S., Govindarajalu, S., Schulze, J., Bornstein, S. R., Hanefeld, M., & Vasseur, F. (2006) · Diabetes Care · doi:10.2337/dc05-2123 · Cited by 66
Tan, B. K., Chen, J., Digby, J. E., Keay, S. D., Kennedy, C. R., & Randeva, H. S. (2006) · Diabetologia · doi:10.1007/s00125-006-0419-9 · Cited by 64
Aroda, V. R., Ciaraldi, T. P., Chang, S., Dahan, M. H., Chang, R. J., & Henry, R. R. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.04.046 · Cited by 63
Lewandowski, K. C., Szosland, K., O’Callaghan, C. J., Tan, B. K., Randeva, H. S., & Lewiñski, A. (2005) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2004.12.014 · Cited by 62
Weerakiet, S., Bunnag, P., Phakdeekitcharoen, B., Wansumrith, S., Chanprasertyothin, S., Jultanmas, R., & Thakkinstian, A. (2007) · Gynecological Endocrinology · doi:10.1080/09513590701214158 · Cited by 59
Zhang, N., Shi, Y., Hao, C., Gu, H. F., Li, Y., Zhao, Y., Wang, L., & Chen, Z. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0576 · Cited by 54
Orio, F., Palomba, S., Cascella, T., Biase, S. D., Labella, D., Russo, T., Savastano, S., Zullo, F., Colao, A. A. L., Vettor, R., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0109 · Cited by 52
Panidis, D. (2004) · Human Reproduction · doi:10.1093/humrep/deh336 · Cited by 51
Xita, N. V., Papassotiriou, I., Georgiou, I. A., Vounatsou, M., Margeli, A., & Tsatsoulis, A. A. (2007) · Metabolism · doi:10.1016/j.metabol.2007.01.008 · Cited by 51
Jalovaara, K., Santaniemi, M., Timonen, M., Jokelainen, J. J., Kesäniemi, Y. A., Ukkola, O. H., Keinanen-Kiukaanniemi, S. M., & Rajala, U. (2008) · Metabolism · doi:10.1016/j.metabol.2008.03.019 · Cited by 50
Barber, T. M., Hazell, M., Christodoulides, C., Golding, S. J., Alvey, C., Burling, K., Vidal‐Puig, A., Groome, N. P., Wass, J. A. H., Franks, S., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2759 · Cited by 50
Assessment of insulin resistance in young women with polycystic ovary syndrome
Jensterle, M., Weber, M. M., Pfeifer, M., Preželj, J., Pfützner, A., & Janež, A. (2008) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2008.03.017 · Cited by 43
Thomann, R., Rossinelli, N., Keller, U. B., Tirri, B. F., Geyter, C. D., Ruiz, J. C., Kränzlin, M., & Puder, J. J. (2008) · Gynecological Endocrinology · doi:10.1080/09513590801893398 · Cited by 43
Endothelial Function Varies According to Insulin Resistance Disease Type
Beckman, J. A., Goldfine, A. B., Dunaif, A. E., Gerhard‐Herman, M. D., & Creager, M. A. (2007) · Diabetes Care · doi:10.2337/dc06-2142 · Cited by 42
Bik, W., Baranowska-Bik, A., Wolińska‐Witort, E., Chmielowska, M., Martyńska, L., & Baranowska, B. (2007) · Gynecological Endocrinology · doi:10.1080/09513590701260169 · Cited by 36
Gülçelik, N. E., Aral, Y., Serter, R., Demir, Y., & Çulha, C. (2006) · Gynecological Endocrinology · doi:10.1080/09513590600917943 · Cited by 32
Factors contributing to the risk of cardiovascular disease reflected by plasma adiponectin
Zyriax, B., Algenstaedt, P., Hess, U. F., Schoeffauer, M., Bamberger, C. M., Boeing, H., & Windler, E. E. T. (2008) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2007.12.033 · Cited by 26
Gülçelik, N. E., Aral, Y., Serter, R., & Koç, G. (2008) · Journal of the National Medical Association · doi:10.1016/s0027-9684(15)31176-7 · Cited by 25
Determinants of Circulating Adiponectin in Women with Polycystic Ovary Syndrome
Vrbíková, J., Dvořáková, K., Hill, M., Včelák, J., Stanická, S., Vaňková, M., Vejražková, D., Vondra, K., Bendlová, B., & Stárka, L. (2005) · Gynecologic and Obstetric Investigation · doi:10.1159/000086273 · Cited by 24
Panidis, D., Farmakiotis, D., Rousso, D., Koliakos, G., Kaltsas, T., & Krassas, G. E. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.05.105 · Cited by 18
Can adiponectin predict abnormal glucose tolerance in Thai women with polycystic ovary syndrome?
Weerakiet, S., Tingthanatikul, Y., Boonnag, P., Wansumrith, S., Rattanasiri, S., & Leelaphiwat, S. (2008) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2007.00704.x · Cited by 6
Flagged first, then by citations
Cited by
Sorted by citations
Diamanti-Kandarakis, E., & Dunaif, A. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1034 · Cited by 1,947
Dumesic, D. A., Oberfield, S. E., Stener-Victorin, E., Marshall, J. C., Laven, J. S., & Legro, R. S. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1018 · Cited by 1,020
Obesity and polycystic ovary syndrome
Barber, T., McCarthy, M. I., Wass, J. A. H., & Franks, S. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02587.x · Cited by 655
The adverse effects of obesity on conception and implantation
Brewer, C., & Balen, A. H. (2010) · Reproduction · doi:10.1530/rep-09-0568 · Cited by 498
“Women with PCOS appear to have lower levels of adiponectin than non-PCO controls, and obese anovulatory women with PCOS have lower levels still, although this is not a consistent finding in the literature (Carmina et al. 2005, 2009, Toulis et al. 2009).”
ResultIbáñez, L., Oberfield, S. E., Witchel, S., Auchus, R. J., Chang, R. J., Codner, E., Dabadghao, P., Darendeliler, F., Elbarbary, N. S., Gambineri, A., et al. (2017) · Hormone Research in Paediatrics · doi:10.1159/000479371 · Cited by 463
Metadata
- Authors
- Toulis, K. A., Goulis, D. G., Farmakiotis, D., Georgopoulos, N. A., Katsikis, I., Tarlatzis, B. C., Papadimas, I., & Panidis, D.
- Affiliations
- Aristotle University of Thessaloniki (GR)
- University of Patras (GR)
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2009
- Volume
- 15
- Issue
- 3
- Pages
- 297-307
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W2131241159
- Cited by
- 262
- References
- 72
- Citations by year
- 2026: 10 · 2025: 9 · 2024: 8 · 2023: 10 · 2022: 14 · 2021: 20 · 2020: 19 · 2019: 13 · 2018: 12 · 2017: 17 · 2016: 10 · 2015: 21 · 2014: 17 · 2013: 23 · 2012: 25
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Warwick
- University of Adelaide
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Keywords
- polycystic ovary syndrome, adiponectin, insulin resistance, testosterone, obesity, body mass index, high molecular weight adiponectin
- MeSH terms
- Female, Humans, Insulin Resistance, Obesity, Polycystic Ovary Syndrome, Regression Analysis, Testosterone, Adiponectin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review