The obesity paradox

Sánchez-Jiménez, Flora; Jiménez-Cortegana, Carlos
doi:10.1016/j.medcli.2023.09.004
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Obesity&#44; which is measured by the Body Mass Index &#40;BMI&#41; &#8805; 30<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#44; is a complex disease that leads to a chronic low-grade inflammation of the adipose tissue and is associated with several factors&#44; including &#40;but not limited to&#41; the increase of proinflammatory cytokines&#44; release of leptin and downregulation of adiponectin&#44; which ultimately promote the development of different metabolic alterations and diseases such as type 2 diabetes mellitus &#40;T2DM&#41;&#44; hypertension and dyslipidemia&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Although there is historical evidence that has associated excess weight with all-cause death in the obese population&#44; a huge number of studies have been published in the last two decades with contradictory results&#44; which is currently known as the &#8220;obesity paradox&#8221;&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Specifically&#44; the first study that reported beneficial effects of obesity was published in 1999 and showed that the one-year survival rate in hemodialysis patients with obesity was significantly higher compared to those with lower weight and the BMI increase in one unit reduced by 30&#37; the relative risk of death&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Since then&#44; the &#8220;obesity paradox&#8221;&#44; term by which this phenomenon has been known since 2002&#44;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> has also been described in different pathologies and diseases such as T2DM&#44;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> cancer&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> or cardiovascular diseases&#44;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> among many others&#46; The obesity paradox is particularly striking in cancer&#44; since it has been widely demonstrated that excess adipose tissue could be a modulator of both classical antitumor therapies &#40;chemotherapy and radiotherapy&#41; and current therapies &#40;combined treatments and immunotherapies&#41; due to its negative impact on the tumor microenvironment &#40;TME&#41;&#44; boosting tumor cell development and cancer progression&#46; However&#44; in recent years&#44; it has been suggested that adipose tissue may be a factor that improves not only clinical responses&#44; but also survival rates in both cancer murine models and oncological patients&#44; although the mechanisms of action carried out by the interaction among treatments&#44; adipose tissue and the TME are still unknown&#46; Identifying those mechanisms could be of great importance to develop new therapeutic approaches&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Altogether&#44; different hypothesis to explain the beneficial role of obesity have arisen in a variety of diseases&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">First&#44; it is believed that the anatomical distribution of adipose tissue may be crucial to explain the obesity paradox&#46; In this sense&#44; subcutaneous adipose tissue &#40;SAT&#41; could play a protective role against metabolic diseases&#44; whereas both intra-abdominal solid organ adipose tissue and visceral adipose tissue &#40;VAT&#41; could be harmful&#46; In line with this notion&#44; it has been demonstrated a positive association between VAT and the risk of atherosclerosis in a SAT-independent manner&#46; Importantly&#44; there are both genetic and biological differences between these two types of adipose tissue&#46; VAT expresses higher levels of the homeobox A4 gene &#40;also known as <span class="elsevierStyleItalic">HoxA4</span>&#41;&#44; <span class="elsevierStyleItalic">HoxA5</span> and the homeobox C8 gene &#40;also known as <span class="elsevierStyleItalic">HoxC8</span>&#41;&#44; while SAT predominantly expresses <span class="elsevierStyleItalic">HoxC9</span> or <span class="elsevierStyleItalic">HoxA10</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> In addition&#44; VAT releases higher amounts of proinflammatory cytokines compared to SAT&#44; which could accelerate insulin resistance and the risk of atherosclerosis&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> For these reasons&#44; some authors prefer to use the term &#8220;metabolic obesity&#8221; to refer to the anatomical location of the adipose tissue &#40;rather than the volume&#41;&#44; which may allow a better identification and stratification of individuals with cardiometabolic risk&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Nutrition may also play a key role in the obesity paradox since obese individuals have higher metabolic reserves that could allow to cope with the catabolic burden caused by some diseases and treatments&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> Casas-Vara et al &#40;2012&#41; demonstrated that the nutritional status measured by different clinical parameters &#40;e&#46;g&#46;&#44; hemoglobin&#44; lymphocyte count&#44; serum albumin&#44; prealbumin&#44; and cholesterol levels&#41; was better in obese patients with heart failure &#40;HF&#41; compared to their leaner counterparts&#46; This was associated with long-term survival<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> and&#44; therefore&#44; obese patients may have a greater immune capacity against diseases under certain nutritional status&#46; Related to this&#44; glucose levels seem to be important to reveal the apparent protective effect of obesity&#44; since an increase in BMI has been associated with a lower risk of hypoglycemia in patients with severe HF and&#44; in turn&#44; contributed to a lower risk of mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Blood pressure may also influence on the contradictory results found in obese patients&#46; As it is known&#44; hypertension increases the risk of cardiovascular diseases in the obese population and&#44; accordingly&#44; obesity-related pulmonary hypertension has shown to increase the risk of right ventricular dysfunction&#46; However&#44; obesity may paradoxically confer a beneficial effect on right ventricular function and be associated with a lower risk of death&#44; although the clinical impact of this event is still unknown&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> In addition&#44; the Avoiding Cardiovascular Events through Combination Therapy in Patients Living with Systolic Hypertension &#40;ACCOMPLISH&#41; clinical trial showed that obese subjects with hypertension responded successfully to specific treatments compared to patients with lower BMI&#44;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> which may explain&#44; at least in part&#44; why hypertension is involved in the obesity paradox&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">This phenomenon could also be related to age&#44; gender&#44; and ethnicity&#46; Although the ageing process can imply being more prone to certain diseases and have a shorter life expectancy&#44; it has been shown that obesity in older subjects could be associated with the same morbidities and reduced quality of life than younger adults&#46; Furthermore&#44; weight loss &#40;voluntarily or unconsciously&#41; in the elderly has been related to the loss of bone density&#44; and obesity could be associated with a lower risk of hip fracture because the adipose tissue located in the abdominal area could cushion falls and reduce the chances of suffering fractures&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Regarding gender and ethnicity&#44; it has been demonstrated that accumulation of VAT &#40;instead of SAT&#41; is more frequent in African American women&#44; white men&#44; and Indian and Japanese people of both sexes&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">It is interesting to mention that BMI has been used in most of the studies in which the obesity paradox has been found&#46; However&#44; BMI could not be a suitable index to measure adiposity because it only considers weight and height rather than other important factors such as the anatomical location of the adipose tissue &#40;visceral or subcutaneous&#41; or the type of mass &#40;fat or muscle&#41;&#46; For those reasons&#44; some authors use the term &#8220;BMI paradox&#8221; to explain this phenomenon&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> Probably&#44; it could be more suitable to consider other indexes to determine adiposity properly&#44; such as the waist circumference&#44; the waist-to-hip ratio&#44; or the waist-to-height ratio &#40;WHtR&#41;&#46; Butt et al&#46; &#40;2023&#41; recently found the obesity paradox in HF patients with BMI &#8805; 25<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#59; however&#44; anthropometric measurements by the WHtR not only reflected the location and amount of ectopic adipose tissue better than BMI&#44; but also associated adiposity with a higher risk of HF&#44; thus suggesting the non-existence of the BMI-related obesity paradox&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">We need to consider that all the previous hypothesis that try to explain the obesity paradox may be also caused by adipokines that are released by the adipose tissue&#46; The most known cell signaling adipokine is leptin&#44; which play a key role in several mechanisms&#44; including those involved in energy balance or promoting different pathologies and diseases&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> In a similar way to obesity&#44; leptin has also demonstrated to be beneficial in some settings&#44; which has been called the &#8220;leptin paradox&#8221;&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Adiponectin is another adipocyte-secreted molecule that plays an opposite role to leptin in energy balance and its downregulation has proved to be detrimental in some diseases&#46; However&#44; contradictory results have also been found in obese patients&#44; being renamed this time as the &#8220;adiponectin paradox&#8221;&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">In conclusion&#44; although obesity has been widely demonstrated over the years to participate in the development of different diseases and the increased risk of mortality in both murine models and clinical patients&#44; in the last couple of decades contradictory results has emerged to the point of considering the existence of a protective role of adiposity&#46; The real reasons of such an enigmatic function of obesity against diseases and favoring long-term survival rates are still unknown and further research is needed to elucidate this phenomenon&#44; but currently there are some hypotheses that try to explain this event&#46; There are a variety of factors that could influence and need to be born in mind to determine the obesity paradox&#44; such as the anatomical distribution of adipose tissue&#44; the use of different indexes to measure obesity &#40;e&#46;g&#46;&#44; BMI or WHtR&#41;&#44; nutrition status&#44; clinical parameters &#40;e&#46;g&#46;&#44; albumin&#44; lymphocyte count&#44; glucose level&#44; or blood pressure&#41;&#44; demography&#44; genetics&#44; or even unidentified confounding factors&#46; Identifying the pathways whereby the obesity paradox occurs in some patients could be of great importance to &#40;i&#41; better identify and stratify patients according to their fat status&#44; &#40;ii&#41; establish predictive and&#47;or prognostic clinical biomarkers&#44; and &#40;iii&#41; design new drugs&#47;investigate new therapeutic approaches to overcome certain diseases&#44; that may ultimately improve survival rates and decrease the risk of death in those obese patients in whom the obesity paradox has not been observed&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Author contribution</span><p id="par0050" class="elsevierStylePara elsevierViewall">FS-J and CJ-C contributed to conceptualization&#44; literature search&#44; writing and review of the manuscript&#46; The authors read and agreed to publish this version of the manuscript&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Conflicts of interest</span><p id="par0055" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest&#46;</p></span></span>"
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