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Adipose tissue and metabolic alterations: regional differences in fat cell size and number matter, but differently: a cross-sectional study.
Abstract
OBJECTIVE: White adipose tissue can expand by increasing the size and/or number of fat cells. Although increased sc and visceral fat cell size associates with an adverse metabolic profile, the relationship with fat cell number in either depot is unknown. We hypothesized that adipocyte number and size displayed different relationships with clinically relevant metabolic variables. METHODS: This was a cross-sectional study of 204 patients scheduled for gastric bypass surgery. Fat cell size and number were determined in visceral and abdominal sc adipose tissue and related to insulin sensitivity (by hyperinsulinemic euglycemic clamp), fasting plasma levels of insulin, triglycerides and high-density lipoprotein (HDL) cholesterol. RESULTS: Visceral and sc fat cell volumes were positively correlated with insulin and triglyceride levels and negatively with insulin sensitivity and HDL-cholesterol (P = .0020 or better). In contrast, although visceral fat cell number did not associate with any metabolic parameter, sc adipocyte number displayed a positive association with insulin sensitivity and HDL-cholesterol and a negative relationship with insulin and triglyceride levels (P = .0014 or better). All results were independent of body fat mass. CONCLUSIONS: Variations in fat cell size and number correlate differently with metabolic parameters in obesity. Increased fat cell size in visceral and sc depots associates with a pernicious metabolic profile, whereas increased sc, but not visceral, fat cell number correlates with a more beneficial phenotype. Whether determination of sc fat cell number, in addition to adipocyte size, may have a predictive value for the risk of type 2 diabetes needs to be demonstrated in prospective or mechanistic studies.
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TL;DR
In 204 patients undergoing gastric bypass, visceral and subcutaneous fat cell volume associated with a worse metabolic profile, while subcutaneous fat cell number associated with a more favorable insulin/lipid profile. These relationships were independent of total body fat mass, but the cross-sectional design cannot establish causality.
Key findings
- Visceral and subcutaneous fat cell volume correlated positively with plasma insulin and triglycerides and negatively with insulin sensitivity and HDL-cholesterol (P = .0020 or better). For example, visceral fat cell volume vs plasma insulin: r = 0.45, P < .0001; vs insulin sensitivity: r = −0.42, P < .0001.
- Visceral fat cell number did not associate with any studied metabolic parameter (e.g., plasma insulin r = −0.080, P = .28; insulin sensitivity r = −0.0038, P = .96).
- Subcutaneous fat cell number showed the opposite pattern from fat cell volume: positive with insulin sensitivity (r = 0.25, P = .0014) and HDL-cholesterol (r = 0.29, P < .0001), negative with plasma insulin (r = −0.26, P = .0003) and triglycerides (r = −0.35, P < .0001).
- In multiple linear regression corrected for total body fat, subcutaneous fat cell number remained associated with plasma insulin (Std β = −0.34, P < .0001), insulin sensitivity (Std β = 0.31, P = .0002), triglycerides (Std β = −0.38, P < .0001), and HDL-cholesterol (Std β = 0.35, P < .0001).
Methods
- Cross-sectional study of 204 patients referred for Roux-en-Y gastric bypass surgery (age 18–60 years; BMI >30 kg/m² with obesity-related complications or BMI >35 kg/m²); ESAT/EVAT values were obtainable from 188 subjects.
- Abdominal subcutaneous fat biopsy was obtained by needle aspiration, and visceral fat biopsy from the greater omentum during surgery. Fat cell size was determined by measuring 100 isolated adipocytes; fat cell number was estimated from depot weight divided by mean fat cell weight.
- Insulin sensitivity was measured by hyperinsulinemic-euglycemic clamp; fasting plasma insulin, triglycerides, and HDL-cholesterol were measured. DEXA with CoreScan estimated visceral and subcutaneous abdominal fat masses. Analyses used Spearman correlation, ANCOVA, and multiple linear regression, with Bonferroni correction.
Limitations
- The paper states that correlations ranged from −0.5 to +0.5, suggesting relatively large interindividual differences in adipocyte size/number are needed to observe metabolic differences; the cohort was rather homogeneous, predominantly women, and larger studies including normal-weight subjects and more men might yield different or stronger correlations.
- The paper states that fat cell number is calculated from two independent parameters (depot size and mean adipocyte weight), so determinations are only relevant for ESAT and EVAT; DEXA/CoreScan measures are indirect, and no visceral adipose tissue phantom was used for calibration.
- The paper states that only a limited set of metabolic phenotypes was studied, the cohort included T2DM and/or hypertension with gender imbalance, and predictive/causal relationships require prospective or mechanistic validation. Evident from the text: the cross-sectional design cannot establish causality, and the bariatric-surgery population may not represent obese individuals in the general population.
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22 Not checked yet · 13 Own interpretation · 10 Own method · 10 Own result · 1 No basis given
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In the paper
“Nevertheless, when corrected for gender, diabetes, or hypertension, the observed correlations remained statistically significant with nominal P values Ͻ .05.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
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“The same was true if the Bonferroni correction was used (allowing P Ͻ .0042 to be significant).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
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In the paper
“In sc adipose tissue, similar correlations were observed regarding fat cell volume as for visceral adipose tissue (Table 2 and Figure 2).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaincorrelationaln = 188- Asserted: passes — The authors put it forward as true.
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In the paper
“After Bonferroni correction of P values in Table 2 (16 comparisons allowing P Ͻ .0031 to be significant), all significant correlations remained.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaincorrelationaln = 188- Asserted: passes — The authors put it forward as true.
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In the paper
“All correlations remained statistically significant after correction for total body fat expressed in kilograms (or as percentage of total body weight, values not shown).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
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In the paper
“In visceral adipose tissue, fat cell volume, but not number, correlated significantly with insulin sensitivity and plasma levels of insulin, triglycerides, or HDL-cholesterol.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plainn = 188- Asserted: passes — The authors put it forward as true.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In visceral adipose tissue, fat cell volume, but not number, correlated significantly with insulin sensitivity and plasma levels of insulin, triglycerides, or HDL-cholesterol.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaincorrelationaln = 188- Asserted: passes — The authors put it forward as true.
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In the paper
“It is well established that a phenotype characterized by large (hypertrophic) adipocytes, is associated with hyperinsulinemia, insulin resistance, and dyslipidemia (14 -18).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Abstract
What the sources say
- Not checked yetcites [14]
- Not checked yetcites [15]
- Not checked yetcites [16]
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Variations in fat cell size and number correlate differently with metabolic parameters in obesity.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Abstract
plaincorrelationaln = 204- Asserted: passes — The authors put it forward as true.
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In the paper
“In conclusion, this study shows that fat cell size and number, independently of body fat mass, associate differently with metabolic parameters in obese subjects.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
boostedcorrelational- Asserted: passes — The authors put it forward as true.
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- It may state two separate claims as one. 17
- Probably not a substantial claim. 21
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In the paper
“Thus, there was a positive relationship with insulin sensitivity and HDL-cholesterol and a negative relationship with insulin and triglycerides.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaincorrelationaln = 188- Asserted: passes — The authors put it forward as true.
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In the paper
“In contrast, although sc fat cell number correlated significantly with all variables, it did so in an opposite way compared with cell volume (Table 2 and Figure 2).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaincorrelationaln = 188- Asserted: passes — The authors put it forward as true.
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In the paper
“Furthermore, numerically similar and P values were obtained if insulin sensitivity was corrected for LBM (M/LBM, values not shown).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“The present study suggest that classifying overweight/obese patients according to their fat cell size and number might be clinically useful to estimate the risk of T2DM and related metabolic complications and thereby determine treatment strategies, at least in specialized clinics.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may be too vague to check against evidence. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Increased sc or visceral fat cell size correlates with an adverse insulin/lipid profile, whereas increased sc fat cell number is coupled to a less pernicious phenotype.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
plaincorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In abdominal sc fat, more adipocytes is related to a more favorable state, whereas fat cell number in the visceral depot does not correlate with any of the studied metabolic parameters.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
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In the paper
“Adipose inflammation has emerged as an important factor contributing to insulin resistance (27).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [27]
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“It is relatively easy to measure fat cell size in small sc needle biopsies (40), and fat mass in different regions can be assessed by DEXA, with the use of recently developed software.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [40]
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“It is relatively easy to measure fat cell size in small sc needle biopsies (40), and fat mass in different regions can be assessed by DEXA, with the use of recently developed software.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
plain- Asserted: passes — The authors put it forward as true.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“One subject was examined using different DEXA equipment, and in one individual, DEXA measurements were missing.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Nevertheless, a limitation of our study is that no visceral adipose tissue phantom was used for calibrations.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Moreover, our cohort included participants with non-insulin-dependent diabetes (T2DM) and/or hypertension, and there was a clear imbalance in gender.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
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In the paper
“Interestingly, adipocyte size correlates closely with the expression and secretion of the proinflammatory cytokine TNF␣ in lean healthy women (28) and insulin resistance/hyperlipidemia in morbidly obese women (14).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [28]
- Not checked yetcites [14]
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“A related possibility explaining the association between adipose cellularity and metabolic changes may be that the capacity of adipose tissue to store lipids is limited (32).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [32]
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“The subjects were scanned using standard imaging and positioning protocols and the same scan mode (set for obese subjects) was used throughout the study.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Up to one-third of overweight or obese subjects are metabolically healthy (37).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [37]
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“In the multiple regression analyses, normal distribution of the residual error was determined using the Shapiro-Wilk W test and the constant variance of the errors was further checked by rando/mLy distributed patterns in residual-by-predicted plots.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Statistics
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“We subsequently validated this in an independent cohort of obese women and men, comparing the weight of the greater omentum with visceral adipose tissue mass estimated using the presently used DEXA equipment/software and CT (22).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
What the sources say
- Not checked yetcites [22]
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“It has been suggested that the classical categorization of body fat status based on BMI and adipose distribution is insufficient (36).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [36]
hedged- Asserted: passes — The authors put it forward as true.
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In the paper
“Furthermore, surgical removal of large amounts of abdominal sc adipose tissue from obese patients does not improve insulin resistance or other metabolic abnormalities (7, 8).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Abstract
What the sources say
- Not checked yetcites [7]
- Not checked yetcites [8]
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“The Bonferroni test was used to correct for multiple comparison statistics in Tables 2 and 3.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Statistics
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“No hardware or software changes were made during the course of the trial.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“Automatic calibration checks of the DEXA were performed daily throughout the study, and thrice-weekly calibrations using a spine phantom (for bone mineral density, provided by the manufacturer) were performed.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
plain- Asserted: passes — The authors put it forward as true.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“In total, 204 subjects were included in the study where ESAT/EVAT values from 188 subjects could be obtained.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plainn = 188- Asserted: passes — The authors put it forward as true.
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“In 14 patients, EVAT and ESAT values could not be measured because of the severe obesity.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Results
plaindirectn = 14- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“In these studies, subjects with many small sc fat cells displayed lower TNF␣ secretion and better insulin sensitivity, respectively.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [28]
- Not checked yetcites [14]
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Consequently, when adipose expansion reaches a maximum, lipids are stored ectopically in skeletal muscle, liver, and pancreatic islets, which in turn leads to lipotoxic effects including abnormal lipoprotein metabolism, insulin dysfunction, and altered insulin secretion.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [32]
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Fat cell volume and weight were determined using a standard method in the field that has been described in detail previously (14,22).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
What the sources say
- Not checked yetcites [14]
- Not checked yetcites [22]
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“Furthermore, the association between body fat distribution and insulin resistance/T2DM is controversial (38,39).”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Discussion
What the sources say
- Not checked yetcites [38]
- Not checked yetcites [39]
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Because only total android fat mass and EVAT are used to determine ESAT and both are valid measures, it follows that also the calculation of ESAT should be valid.”
§ Adipose Tissue and Metabolic Alterations: Regional Differences in Fat Cell Size and Number Matter, But Differently: A Cross-Sectional Study > Examinations
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
The paper relies on this without support.
The relationship between adipocyte number and insulin resistance and other metabolic variables associated with T2DM risk was unknown at the time of the study.
“However, the relationship between adipocyte number and insulin resistance as well as other metabolic variables associated with T2DM risk is unknown.”
The authors state this as an assumption.
Mean fat cell weight can be obtained by multiplying fat cell volume by 0.915, assuming fat cell density equals that of human adipose triglycerides.
“Assuming a mean density of fat cells equal to that of human adipose triglycerides, mean fat cell weight was obtained by multiplying the volume by 0.915 (ie, the density in grams per milliliter of triolein).”
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?
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Regardless of its localization, AT content and function differ markedly between obese and healthy lean people”
From Effect of Exercise Training on Fat Loss—Energetic Perspectives and the Role of Improved Adipose Tissue Function and Body Fat Distribution (2021) · cites this paper as Rydén et al., 2014
Experimental — accuracy not yet measured
Citations
Cites
Dynamics of fat cell turnover in humans
Spalding, K. L., Arner, E., Westermark, P. O., Bernard, S., Buchholz, B. A., Bergmann, O., Blomqvist, L., Hoffstedt, J., Näslund, E., Britton, T., et al. (2008) · Nature · doi:10.1038/nature06902 · Cited by 2,357
Self-citationBariatric Surgery versus Conventional Medical Therapy for Type 2 Diabetes
Mingrone, G., Panunzi, S., De Gaetano, A., Guidone, C., Iaconelli, A., Leccesi, L., Nanni, G., Pomp, A., Castagneto, M., Ghirlanda, G., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1200111 · Cited by 1,791
Krotkiewski, M., Björntorp, P. A., Sjöström, L., & Smith, U. (1983) · Journal of Clinical Investigation · doi:10.1172/jci111040 · Cited by 1,475
Gloy, V. L., Briel, M., Bhatt, D. L., Kashyap, S. R., Schauer, P. R., Mingrone, G., Bucher, H. C., & Nordmann, A. J. (2013) · BMJ · doi:10.1136/bmj.f5934 · Cited by 1,351
Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome — An allostatic perspective
Virtue, S., & Vidal-Puig, A. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2009.12.006 · Cited by 1,013
Absence of an Effect of Liposuction on Insulin Action and Risk Factors for Coronary Heart Disease
Klein, S., Fontana, L., Young, V. L., Coggan, A. R., Kilo, C., Patterson, B. W., & Mohammed, B. S. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa033179 · Cited by 917
Methods for the determination of adipose cell size in man and animals
Hirsch, J., & Gallian, E. (1968) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)43151-7 · Cited by 894
Weyer, C., Foley, J. E., Bogardus, C., Tataranni, P. A., & Pratley, R. E. (2000) · Diabetologia · doi:10.1007/s001250051560 · Cited by 799
Bariatric surgery and prevention of type 2 diabetes in Swedish obese subjects
Carlsson, L. M. S., Peltonen, M., Ahlin, S., Anveden, Å., Bouchard, C., Carlsson, B., Jacobson, P., Lönroth, H., Maglio, C., Näslund, I., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1112082 · Cited by 794
Adipocyte Turnover: Relevance to Human Adipose Tissue Morphology
Arner, E., Westermark, P. O., Spalding, K. L., Britton, T., Rydén, M., Frisén, J., Bernard, S., & Arner, P. (2010) · Diabetes · doi:10.2337/db09-0942 · Cited by 645
Self-citation
Cited by
Sorted by citations
Metabolically healthy obesity: facts and fantasies
Smith, G. I., Mittendorfer, B., & Klein, S. (2019) · Journal of Clinical Investigation · doi:10.1172/jci129186 · Cited by 677
Lotta, L. A., Gulati, P., Day, F. R., Payne, F., Ongen, H., van de Bunt, M., Gaulton, K. J., Eicher, J. D., Sharp, S. J., Luan, J., et al. (2016) · Nature Genetics · doi:10.1038/ng.3714 · Cited by 599
Impaired adipogenesis and dysfunctional adipose tissue in human hypertrophic obesity
Hammarstedt, A., Gogg, S., Hedjazifar, S., Nerstedt, A., & Smith, U. (2018) · Physiological Reviews · doi:10.1152/physrev.00034.2017 · Cited by 462
Obesity and the risk of cardiometabolic diseases
Valenzuela, P. L., Carrera-Bastos, P., Castillo-García, A., Lieberman, D. E., Santos-Lozano, A., & Lucia, A. (2023) · Nature Reviews Cardiology · doi:10.1038/s41569-023-00847-5 · Cited by 452
Adipose tissue fibrosis, hypertrophy, and hyperplasia: Correlations with diabetes in human obesity
Muir, L. A., Neeley, C. K., Meyer, K. A., Baker, N. A., Brosius, A. M., Washabaugh, A. R., Varban, O. A., Finks, J. F., Zamarron, B. F., Flesher, C. G., et al. (2016) · Obesity · doi:10.1002/oby.21377 · Cited by 367
Metadata
- Authors
- Rydén, M., Andersson, D. P., Bergström, I. B., & Arner, P.
- Affiliations
- Karolinska University Hospital (SE)
- Corresponding author
- Rydén, Mikael
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2014-10
- Volume
- 99
- Issue
- 10
- Pages
- E1870-E1876
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2114647414
- Semantic Scholar
- d4539851f822e7fab616919f43ad2e7b017805f4
- Cited by
- 124
- References
- 43
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 10 · 2023: 10 · 2022: 11 · 2021: 10 · 2020: 10 · 2019: 9 · 2018: 18 · 2017: 12 · 2016: 4 · 2015: 15
- FWCI
- 7.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eli Lilly and Company
- Karolinska Institutet
- Novo Nordisk
- Vetenskapsrådet
- European Association for the Study of Diabetes
- Novo Nordisk Fonden (NNF14OC0010187, NNF12OC1016371)
- U.S. Food and Drug Administration
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- white adipose tissue, adipocyte size, adipocyte number, visceral adipose tissue, subcutaneous adipose tissue, insulin sensitivity, insulin resistance, type 2 diabetes risk, HDL cholesterol, triglycerides, obesity, gastric bypass, metabolic phenotypes
- MeSH terms
- Adolescent, Adult, Cross-Sectional Studies, Diabetes Mellitus, Type 2, Female, Humans, Insulin, Insulin Resistance, Cholesterol, HDL, Male, Middle Aged, Obesity, Morbid, Omentum, Triglycerides, Glucose Clamp Technique, Adipocytes, Cell Size, Subcutaneous Fat, Intra-Abdominal Fat, Young Adult, Preoperative Period
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.
A language model drew the claims from the paper on 2026-10-09, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-09 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
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 ›
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