Anthropometric Indices and Nutritional Parameters in Centenarians
Centenarians as Model of Longevity and Healthy Aging
The number of centenarians should witness a substantial increase worldwide during the twenty-first century. The Population Division of the United Nations enunciated it should reach more than 20 million people in 2100, rising from 0.5 million in 2017 (Robine and Cubaynes 2017; United Nations 2017). Indeed, the older adults are actually the fastest growing segment of the population. While aging has been studied for many years, it is only recently that longevity has attracted the interest of scientists who started to consider centenarians as “special people” because they avoided or postponed the onset of major age-related diseases. Centenarians can be considered the most informative human model of healthy aging with minimal influence of diseases and comorbidities. This model allows the identification of the pathophysiological mechanisms involved in the successful aging and of protective factors (genetic, nutritional, or environmental) against the most widespread age-related diseases. The oldest old have lower incidence of chronic diseases such as cardiovascular disease, hypertension, chronic obstructive pulmonary disease, cancer, stroke, renal disease, hypercholesterolemia, and diabetes than elderly people (Franceschi et al. 2018). A part of them has quite good mental status, with absent episodes of anxiety and depression (Franceschi et al. 2018). Also, from a molecular and cellular point of view, centenarians manifest some peculiarities. Indeed, they show a reduction in oxidative stress and a low basal metabolic rate (He et al. 2015). In fact, low concentrations of triglycerides, total cholesterol, and low-density lipoprotein (LDL) cholesterol, as well as preserved insulin sensitivity and low levels of serum insulin-like growth factor-1 are peculiar characteristics of these subjects (Franceschi et al. 2018). The older people show a progressive increase in physiological inflammatory state defined “inflammaging” (Franceschi et al. 2000) that is a chronic, low-grade inflammation caused by increased stimulation of innate immune and accumulation of senescent cells secreting proinflammatory mediators (Franceschi et al. 2017). Although centenarians manifest signs of inflammaging, they do not show most of its negative consequences. A balance between pro- and anti-inflammatory factors is a predominant characteristic of these people (Ostan et al. 2008) and a well-preserved complement system distinguishes their peculiar immune profile (Bellavia et al. 1999).
Research on centenarians is not easy because of their low prevalence and the lack of an appropriate control group. As a large amount of studies indicates a familiarity of the features predisposing to long life, centenarians’ offspring may have inherited advantageous characteristics from their parents, thus providing an alternative and useful approach to study healthy aging and longevity (Gueresi et al. 2013). Centenarians’ offspring are healthier than age-matched controls not born from long-lived parents, suggesting that the biological components of longevity might overlap with the biological components of healthy aging (Bucci et al. 2016).
Nutritional Portrait of Centenarians
The phenotype of longevity is complex and multifactorial and results from a unique reciprocal interaction between environment, genetics, epigenetics, and stochastic factors (Franceschi et al. 2018). Centenarians are the result of biological processes, and nutritional and social habits that exert their effects throughout life (Franceschi et al. 2018). In particular, an Italian centenarians’ peculiar trait is their varied diet, taken slowly and in little portions at fixed times of day. Because of their education, geographical location, and historical events, for most of their life they followed a provegetarian diet, rich in vegetables and legumes, eggs and cheese, and poor in meat. The heterogeneity of their diet might be a key element promoting exceptional longevity. In the specific case of Italian centenarians, for most of their life they complied with a nutritional and lifestyle profile compatible with the Mediterranean diet (Martucci et al. 2017), a well-balanced diet providing a balanced mix of nutrients with antioxidant, anti-inflammatory, and prebiotic effects (Martucci et al. 2017). The heterogeneity of this diet allows to counterbalance pro- and anti-inflammatory pathways delaying the detrimental effects of inflammaging and the onset of the most widespread age-related diseases (Martucci et al. 2017; Ostan et al. 2015). Large amounts of recent studies have shown an association among the Mediterranean diet and the calorie restriction considered a nutritional intervention able to modulate aging and to increase the lifespan (Martucci et al. 2017). The Mediterranean diet contains resveratrol, quercetin, olive oil secorroids, phenolic antioxidants and carotenoids (Rattan 2008), able to stimulate and upregulate cellular and molecular defense pathways (i.e., nuclear factor kappa-light-chain-enhancer of activated B cells [NF-κB], mammalian target of rapamycin [mTOR], and sirtuins [SIRT]), that mimic the calorie restriction (Martucci et al. 2017; Pallauf et al. 2013). Ristow et al. proposed the theory that calorie restriction acts as mild stressor promoting hermetic responses and activating longevity-promoting pathways (Ristow and Schmeisser 2014). In particular, the reduced intake of proteins and amino acids is the most effective prolongevity “treatment” (Mirzaei et al. 2014).
The line between calorie restriction and malnutrition is blurred. Malnutrition is defined as a state of nutrition in which a deficiency or excess of energy, protein, and micronutrients causes measurable adverse effects on tissue/body form (body shape, size, and composition) and function, and clinical outcomes. The older adults worldwide and, in particular, the centenarians are often limited in their food assumption by a list of factors, such as compromised oral health, altered taste and smell, loss of appetite, unwillingness to cook, impaired vision and cognitive function, and difficulty moving (Marsman et al. 2018). Evidences show a reduction of biochemical parameters and an impairment of anthropometric values associated with lost cognitive function, cardiovascular disease, cancer, eye disease, and other conditions common in older people (Marsman et al. 2018). All these negative factors contribute to alter metabolism, appetite, and absorption of proteins and nutrients and consequently lead to malnutrition (Wang et al. 2018). Typically, malnutrition has a low prevalence in free-living elderly (2–10%) and a higher prevalence in the hospitalized or institutionalized elderly (30–60%) (Wang et al. 2018).
The question of whether centenarians share a condition of malnutrition or have a phenotype similar to individuals on calorie-restricted diet is still under debate. Many studies reporting centenarians’ nutritional status involve the use of nutritional biomarkers measured in biological fluids and selective anthropometric indices as suitable tools for solving this dilemma and distinguishing malnutrition from the calorie restriction phenotype (Hausman et al. 2011).
Key Research Findings
Nutritional Screening Tools in Older People
Malnutrition screening is the recommended first step in the nutrition care process in older persons and, in particular, in centenarians allowing the early identification of nutritional concerns (Mueller et al. 2011). The multifactorial nature of protein-energy malnutrition in the older adults shows up the need to use suitable nutrition screening tools with adequate requirements of high sensitivity and specificity. For an accurate evaluation, it is necessary to perform multiple tests in order to collect as much information as possible to detect the nutritional status and, in most cases, to diagnose malnutrition.
Nutritional Indices in the Biological Fluids
Albumin is the most abundant plasmatic protein, but its metabolic functions are not known in detail. This protein is a good marker of nutritional status in clinically stable people, thus this is considered one of the major indicators of malnutrition. Unfortunately, there is a limitation in the use of albumin as biomarker of malnutrition. Indeed, its long half-life (about 20 days) makes it inadequate to assess recent changes in nutritional status. The normal range of albumin makes up 3.2–5.2 g/dL. According to the concentration of albumin, it is possible to classify the severity of malnutrition in mild, moderate, and severe (Cabrerizo et al. 2015). A large amount of studies showed a progressive reduction of albumin concentration in serum between 0.08 and 0.17 g/L per year associated to aging with a greater reduction in men than in women (Gom et al. 2007). Despite these age-related changes, albumin levels in healthy elderly people stay above 3.8 g/dL until after the age of 90 (Campion et al. 1988). Hypoalbuminemia is the greatest prognostic indicator for complications, onset of disability, and mortality in older people (Cabrerizo et al. 2015).
Serum cholesterol can be considered an indicator of protein-calorie malnutrition when it shows a reduction of more than 25% in the last year and when other causes of hypocholesterolemia have been excluded. Epidemiological studies suggest that serum cholesterol levels tend to increase in adult persons, but decrease in older people (Wilson et al. 1994). Therefore, a reduction of whole body (and probably hepatic) cholesterol synthesis occurs with ongoing age (Bertolotti et al. 2014). Contrarily, a study involving a Northern Europe cohort of very old age (up to 85 years) has observed a tendency for serum cholesterol levels to plateau with reduced concentrations in women (Tilvis et al. 2011). Taken together, all these findings suggest a decreased metabolic need of cholesterol in older persons with a reduction of LDL uptake as well as a reduced expression and/or activity of both the enzymes of cholesterol synthesis (Galman et al. 2011) and the markers of cholesterol absorption (Galman et al. 2011; Tilvis et al. 2011).
Anthropometric Parameters of Body Composition
Body Mass Index
Body mass index (BMI) is an indicator of weight-for-height and is one of the most common tools used in the assessment of nutritional status. It is calculated by dividing the weight in kilograms by the square of height in meters (kg/m2) and allows the classification of individuals as underweight (BMI<18.5), normal weight (18.5–24.99), overweight (25.0–29.99), or obese (≥30.0). A low BMI is associated with an increased risk of mortality in older people, whereas a high BMI is related to chronic health conditions at advanced ages (Villareal et al. 2005). The use of a simple anthropometric index of body composition, such as BMI, is considered as a practical approach to the assessment of adiposity for a long time. However, there are some problems associated with the use of BMI as an indicator of health and nutritional status in older adults. In fact, this parameter does not allow in distinguishing between muscle mass and adipose tissue and provides little information on fat distribution (Ruhl and Everhart 2010). In addition, the measures are affected by the loss of height that occurs with age and the difficulty to get a realistic measure of height due to inability to stand (Hausman et al. 2011). Despite these problems, BMI has been usually used as an indicator of nutritional status in several centenarians’ studies (Hausman et al. 2011). Typically, BMI of centenarians is lower than that of their older adult controls (Magri et al. 2002) and further decreases over 100 years (Magri et al. 2002).
Waist circumference is the major clinical parameter used for the indirect evaluation of visceral fat and abdominal obesity. Nevertheless, it is unclear whether to what extent the range of waist circumference depends on body size (Hsieh and Yoshinaga 1999). As the previously described indices, also the use of waist circumference has some disadvantages. First, waist circumference does not allow in distinguishing between visceral and subcutaneous fats (Pouliot et al. 1994). Second, this measure underestimates the amount of visceral fat in short people and overestimates it in tall people because it does not consider height. These results highlight the limitations of using BMI and waist circumference individually as indices of abdominal adiposity (and/or muscle mass) (Nazare et al. 2015). To avoid the underestimation of abdominal obesity related to their use in isolation, it is advisable to make use of the combined application of both BMI and waist circumference (Nazare et al. 2015). The recommended cut-off values for waist circumference are ≤94 cm in men and ≤80 cm in women. Evidences have revealed that high waist circumference values correlates with a more unfavorable cardiometabolic risk profile (Zhang et al. 2018) as well as it has been positively associated with all-cause mortality in most studies. Waist circumference predicts mortality risk better than BMI (Zhang et al. 2018).
Hand Grip Strength
A change in muscle function may be an early indication of malnutrition (Windsor and Hill 1988). Hand grip strength (HGS) is the objective tool used to assess muscle strength and to measure physical function, particularly in circumstances where weight and/or accurate physical assessment are difficult to detect. HGS is a rapid, low-cost, and user-friendly tool with high test and re-test reliability and high inter-rater reliability (Mathiowetz et al. 1985), suggesting to be a good indicator of nutritional status (Norman et al. 2011). A significant association between HGS and nutritional status has been observed in a heterogeneous group of nourished and malnourished hospital patients (Flood et al. 2014). Moreover, monitoring the HGS variation over time, it is possible to predict changes in the nutritional status (Flood et al. 2014). HGS is significantly lower in malnourished state where the main fuel source of the body is the skeletal muscle. This fact may be the cause of the loss of protein stores and the decline in muscle strength/functionality that occur in these subjects (Kenjle et al. 2005). The predictive property of HGS suggests the important role of this tool in the clinical practice.
Examples of Application
Nutritional Status Indices and Anthropometric Parameters: The Case of Centenarians from Northern Italy
The above-mentioned nutritional indices measured in the biological fluids and anthropometric parameters of body composition could be useful in the clinical practice to investigate the nutritional status of centenarians and could be used to further evaluate the inherited advantageous features of longevity in relation to lifestyle. From this perspective, in a cohort of subjects composed of about one hundred centenarians born in Northern Italy between the 1899 and 1908, the multidimensional geriatric assessment shows that both the nutritional biological indices and the anthropometric parameters display values within the normal range. In particular, the data suggest that the phenotype of centenarians is similar to that observed in adult persons who followed calorie restriction regimens, even if centenarians never followed a specific calorie restriction paradigm through their long life. This cohort of centenarians from Northern Italy reveals a condition of calorie restriction without malnutrition already observed in a previous study which included Okinawan centenarians (Willcox et al. 2007). The nutritional biological indices and the anthropometric parameters taken into consideration in this example of application result to be not only within the normal range but also very closed to the optimal values, and exclude the presence of malnutrition.
The centenarians’ offspring show normal albumin concentrations and regular HGS, but higher values than the normal range for total cholesterol, BMI, and waist circumference. Investigating these parameters, in centenarians’ offspring, the BMI is lower compared to a group of sex and age-matched healthy subjects born from non-long-lived parents. This evidence reinforces the notion that longevity runs in families (Gueresi et al. 2013). The albumin and the total cholesterol concentrations in centenarians’ serum are lower than those of their offspring and of a group of healthy septuagenarians. Interestingly, centenarians showed averages closed to the optimal values. In the same cohort, BMI and HGS are significantly lower in centenarians, while the values of waist circumference are very similar between centenarian women and their offspring, but significantly lower compared to healthy septuagenarians with non-long-lived parents.
The normal albumin values found in centenarians are similar to those observed in healthy older people, suggesting that the oldest old are not malnourished (Cabrerizo et al. 2015). The decrease of serum cholesterol levels in centenarians is in agreement with the progressive reduction of cholesterol synthesis that occurs during the aging process, maybe a consequence of an extended slowed metabolic rate (Bertolotti et al. 2014). The low BMI detected in centenarian population confirms that these people are less predisposed to develop chronic health conditions as hypertension, diabetes, cardiovascular disease, and osteoarthritis (Villareal et al. 2005), while a low waist circumference denotes a more favorable cardiometabolic risk profile as suggested by the literature (Zhang et al. 2018). Moreover, both centenarians’ low BMI and low waist circumference point out the absence of abdominal obesity (Zhang et al. 2018). The low HGS of the oldest old could be linked to the condition of extreme vulnerability of these subjects. This result is in agreement with different studies confirming that low HGS correlates with sarcopenia, frailty, and a loss of bone mineral density (Turusheva et al. 2017), typical features of the aging process.
Future Directions of Research
The role of diet and nutrition is pivotal to promote the good quality of the aging process. Therefore the identification of biomarkers to evaluate the nutritional status is needed. The detection of nutritional indices in the biological fluids and the use of simple anthropometric indices of body composition are practical and suitable approaches for the easy assessment of the centenarians’ nutritional status. The combined application of the above-mentioned tools might be the more effective method to measure the nutritional status in the successful aging. As little is known about specific nutritional interventions that effectively promote healthy aging, the future research will focus on the identification of lifestyle interventions that could promote longevity.
Centenarians are the result of a mixture of peculiarities that allow them to avoid or postpone the major age-related diseases, staying cognitively and physically active until age 90 and above. Aging and, in particular, longevity appear to be a continuum of biological processes characterized by progressive adaptations which can be influenced by geographical, cultural, socio-economic, and anthropological aspects and both genetic and physiological factors. Altogether, the nutritional habits and lifestyle in a specifically favorable environment contributed to centenarians’ healthy aging and longevity. In the last few years, the large amount of studies on centenarians has revealed the need to employ quantitative biomarkers as an essential component to study healthy aging and longevity.
For this reason, the researchers have developed tools, which can measure improvements/impairments in physiological integrity throughout life and can be used to predict factors, habits, and traits that contribute to successful aging.
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