What is "normal weight": a story of misquotation

Image from JAMA. https://jamanetwork.com/data/Journals/JAMA/0/jmn180006fa.png

I am interested in the relationship between weight and bone health. And, that question, "what is 'normal weight'," has dogged me for many years. A recent paper, published in Menopause last week (1), concludes that "BMI cut-point of 30 kg/m^2 does not appear to be an appropriate indicator of true obesity status in postmenopausal women." The finding caught the attention of JAMA (2). However, I think the conclusion is a bit strong ...

In the mentioned study, the authors analyzed data from a cohort study that included 1329 postmenopausal women. The women aged between 53 and 85 yrs (at study entry). All women had body mass index (BMI) and DXA-derived percent body fat (PBF). They defined obesity was BMI ≥ 30 kg/m2 and body fat percent (PBF) greater than 35%. After setting up the scene, the authors then analyzed the correlation between BMI and PBF.

Using PBF>35% as 'reference criteria', the authors found that the sensitivity of BMI≥30 was 32.4%. In other words, out of 100 cases of presumably obesity (defined by PBF), only 32 cases were picked up by the current BMI-based criteria. After a series of sensitivity analyses, the authors found that the optimal BMI for defining obesity was 24.9 kg/m2.

I think the main problem with the above study is that the authors used PBF≥35% as a 'gold standard' for defining obesity. Although the 35% cut-off has been repeatedly used by many investigators over the past 20 years, it has no scientific basis. It is actually a result of ... misquotation!

Let me explain ...

In 1998, a paper published in the International Journal of Obesity (3) stated that “Obesity is characterised by an increased amount of body fat, defined in young adults as body fat >25% in males and >35% in females, corresponding to a body mass index (BMI) of 30 kg/m2 in young Caucasians,” with reference for this statement being the 1995 WHO Technical Report (4).

Subsequent papers from other authors continued referring to the 1998 IJO paper (3) and/or the 1995 WHO Report (4) as the primary source for the PBF thresholds. For example, a 1999 paper published in the European Journal of Clinical Nutrition (5) states that “In obesity or adiposity the body fat percent (BF%) exceeds 25% in males and 35% in females,” and the source of this statement was attributed to the 1998 IJO paper (3) and the 1995 WHO Report (4).

Since then, several other authors (6-11) have repeatedly cited the two works supporting the PBF thresholds. Indeed, a paper stated that “The gold standard definition of obesity BF>25% in men and >35% in women proposed by the World Health Organization” (11) without reference for this statement.

A series of studies examining the association between BMI and PBF used the PBF≥35% as gold standard for defining obesity (3, 11, 12). The supposedly PBF thresholds of 25% (for men) and 35% (for women) were also used as a rationale for proposing a lower BMI cut-off value for defining obesity in Asian populations (13).

As a matter of fact, neither the 1998 IJO paper (3) nor the WHO Technical Report (4) developed any PBF threshold for defining obesity. So, what does the WHO Technical Report state? Here is the text:

"A BMI of 30 in Dutch men implies a body fat content of about 30% at age 20 years and about 40% at age 60; in women aged 20 and 60, these figures are 40% and 50%, respectively” (page 327). In a subsequent section, the Report states that “using underwater weighing of 200 healthy Swedish men and women aged 45-78 years, Bjontorp and Evans (14) reported changes in the percentage of weight that is represented by body fat. At 45-49 years, men averaged 25% fat; this seemed to stabilize at 38% at age 60-65 years. Women had more body fat than men at 45-49 years (30%) and stabilized at an average of 43% at 55-59 years. Between 60 and 78, neither men nor women showed much change in percentage body fat” (page 378)."

So, as can be seen, The WHO Technical Report did not set any threshold of percent body fat for defining obesity. It seems reasonable to state that this particular area of research into obesity and body fat over the past 15 years has been built on a misquotation.

Surprisingly, misquotation is common in clinical medical literature (15-18), including a well-known case of hand surgery study (19). An analysis of citation and quotation accuracy in 3 anatomy journals revealed that the prevalence of quotation errors was 14%; of which, the majority (94%) was classified as major error (i.e., contradicted or unrelated to the author’s assertions) (20). One of the reasons for quotation error was secondary quotations, also known as the “lazy author syndrome” (21). A recent modelling study suggested that between 70 and 90% of scientific quotations are based on secondary sources, including citing single or multiple examined references from other papers (22). The example presented in this commentary suggests that some researchers do not read all papers they cite, and this resulted in a case of faulty citation, which could damage the subsequent obesity research.

In summary, an initial misrepresentation of a WHO Technical Report has led to a trail of subsequent misquotations, which appear to affect policy at the international level. I think it is reasonable to say that to date, there is no validated threshold of body fatness for defining obesity.

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1. Banack HR, Wactawski-Wende J, Hovey KM, Stokes A. Is BMI a valid measure of obesity in postmenopausal women? Menopause. 2018;25(3):307-13.

2. Rubin R. Postmenopausal Women With a "Normal" BMI Might Be Overweight or Even Obese. JAMA. 2018.

3. Deurenberg P, Yap M, van Staveren WA. Body mass index and percent body fat: a meta analysis among different ethnic groups. Int J Obes Relat Metab Disord. 1998;22(12):1164-71.

4. WHO. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Consultation. WHO Technical Report Series 1995;854(Geneva: World Health Organization).

5. Gurrici S, Hartriyanti Y, Hautvast JG, Deurenberg P. Differences in the relationship between body fat and body mass index between two different Indonesian ethnic groups: the effect of body build. Eur J Clin Nutr. 1999;53(6):468-72.

6. Ko GT, Tang J, Chan JC, Sung R, Wu MM, Wai HP, et al. Lower BMI cut-off value to define obesity in Hong Kong Chinese: an analysis based on body fat assessment by bioelectrical impedance. Br J Nutr. 2001;85(2):239-42.

7. Chang CJ, Wu CH, Chang CS, Yao WJ, Yang YC, Wu JS, et al. Low body mass index but high percent body fat in Taiwanese subjects: implications of obesity cutoffs. Int J Obes Relat Metab Disord. 2003;27(2):253-9.

8. Deurenberg P. Universal cut-off BMI points for obesity are not appropriate. Br J Nutr. 2001;85(2):135-6.

9. Deurenberg-Yap M, Chew SK, Deurenberg P. Elevated body fat percentage and cardiovascular risks at low body mass index levels among Singaporean Chinese, Malays and Indians. Obes Rev. 2002;3(3):209-15.

10. He M, Tan KC, Li ET, Kung AW. Body fat determination by dual energy X-ray absorptiometry and its relation to body mass index and waist circumference in Hong Kong Chinese. Int J Obes Relat Metab Disord. 2001;25(5):748-52.

11. Romero-Corral A, Somers VK, Sierra-Johnson J, Thomas RJ, Collazo-Clavell ML, Korinek J, et al. Accuracy of body mass index in diagnosing obesity in the adult general population. Int J Obes (Lond). 2008;32(6):959-66.

12. Okorodudu DO, Jumean MF, Montori VM, Romero-Corral A, Somers VK, Erwin PJ, et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes (Lond). 2010.

13. WHO. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363(9403):157-63.

14. Bjorntorp P, Evans W. The effect of exercise on body composition. In: Watkins J, Roubenoff R, Rosenberg IH, Eds Body composition: the measure and meaning of changes with aging. 1992;Boston: Foundation for Nutrition Advancement.

15. Wright M, Armstrong JS. The Ombudsman: verification of citations: Fawlty towers of knowledge? Interfaces. 2008;38(2):125-39.

16. Eichorn P, Yankauer A. Do authors check their references? A survey of accuracy of references in three public health journals. Am J Public Health. 1987;77(8):1011-2.

17. Oren G, Watson M. Accuracy of references in the ophthalmic literature. J Med Libr Assoc. 2009;97(2):142-5.

18. Whitworth JA. Who said that? Lancet. 2007;370(9593):1128.

19. Porrino JA, Jr., Tan V, Daluiski A. Misquotation of a commonly referenced hand surgery study. J Hand Surg Am. 2008;33(1):2-7.

20. Lukic IK, Lukic A, Gluncic V, Katavic V, Vucenik V, Marusic A. Citation and quotation accuracy in three anatomy journals. Clin Anat. 2004;17(7):534-9.

21. Gavras H. Inappropriate attribution: the "Lazy Author Syndrome". Am J Hypertens. 2002;15(9):831.

22. Simkin MV, Roychowdhury VP. Stochastic modeling of citation slips. Scientometrics. 2005;62:367-84.