Longevity Blue Zones (LBZs) are geographical areas of the planet harboring a measurably higher proportion of long-lived individuals compared with the usual average elsewhere [1
]. They are mostly isolated areas, such as the island of Okinawa in Japan, the peninsula of Nicoya in Costa Rica, the island of Ikaria in Greece, and the Ogliastra subregion on the Mediterranean island of Sardinia, all well known for hosting a large number of age-validated centenarians [3
]. In these populations exceptional longevity appears as a widespread phenomenon, which explains the term “population longevity” proposed in contrast to that of “individual longevity” [4
]. The analysis of LBZs has been claimed to facilitate the identification of longevity factors acting at the superindividual level (for a review, see [2
]). A number of hypotheses have been posed to explain the emergence of these long-lived populations, specifically targeted on genetic factors, environment, lifestyle, occupational activity, and social life [5
]. Among the lifestyle-related factors, dietary habits play a fundamental role: It is known that the ability of some individuals to reach an advanced age, by escaping most chronic non-transmissible diseases, derives at least in part from adopting a healthy diet for most of their lives.
Various food styles share the merit of promoting human longevity. Among them, the Mediterranean diet is usually considered one of the most capable of protecting against age-related disease, ensuring longer survival [6
], although the exact mechanism(s) by which the adherence to this dietary model acts positively are poorly known [7
] or controversial [8
]. Furthermore, the study of the relationship between the consumption of specific foods and health status does not yet allow definitive conclusions. Most of the putative beneficial aspects of the Mediterranean diet, widely publicized in popular literature, are generally attributed to the content of antioxidants [9
], the low consumption of processed meat [10
], and the consumption of olive oil [11
] and/or red wine [12
Ideally, a comparison between the dietary pattern of the elderly population of all four LBZs recognized so far would contribute to shed light on the role of diet in promoting successful aging. Yet this comparison is not easily achievable for various reasons, for example, the Ikaria population is numerically too small to be informative. On the other hand, the Okinawa population is quite different in terms of genetic structure, food history, ethnic characteristics and lifestyle from that of the other three LBZs, making the interpretation of such comparative analysis too complex. A realistic comparison is therefore feasible only between the population of Nicoya, Costa Rica, and Ogliastra in Sardinia, Italy. Besides, the cultural heritage of the two populations was historically influenced by Spanish rule, which may have left common traces in the food traditions [13
The main objective of this study was to evaluate comparatively the eating habits and functional ability of elderly people living in two LBZs, the Nicoya peninsula and Ogliastra.
2. Materials and Methods
2.1. Study Populations
2.1.1. Nicoya, Costa Rica
The Nicoya peninsula is a north-western region of Costa Rica (Central America) facing the Pacific Ocean at latitude North of 10° 04′ and longitude West 85° 25′. It encompasses the province of Guanacaste and hosts a population of about 326,000 inhabitants spread over an area of 778 km² [14
]. The area was once covered with tropical dry forests until it was converted into pastureland during the 1950s [15
]. The peninsula of Nicoya, compared to Costa Rica as a whole, appears to be a relatively isolated region (the Tempisque river separates it from the rest of the country), a characteristic shared by the other three LBZs [2
]. The ethnic composition of the population in the peninsula is slightly different from the whole of Costa Rica. Whereas in the latter the indigenous population is less than 2%, in the Nicoya peninsula this rises to 5% and includes, in particular, the Chorotega ethnic group, descendants of Native Americans whose traditions may have had some influence on the lifestyle and current behavior of the Nicoya population [16
In 2008, the demographer Luis Rosero-Bixby reported a life expectancy at birth of 76.2 years among the male population of Nicoya, i.e., higher than that of 74.8 recorded for white males in the United States [17
]. In this region, the overall mortality rate was 20% lower than that of the remaining part of the country; the proportion of people over 65 years of age was 8% and, as in other LBZs, economic indicators show a modest degree of underdevelopment compared to the rest of the country. The advantage of Nicoya’s males in terms of survival is absent in females, but also tends to disappear in emigrants abroad [17
], and according to the CRELES study is essentially due to a lower incidence of cardiovascular disease [18
]. This investigation, which also considered some bio-medical markers, showed that the average body height of the inhabitants of Nicoya was higher than the general population of Costa Rica, and their body mass index was lower, as was the prevalence of physical and mental disability [18
]. The leukocyte telomere length, considered an indicator of longevity, is higher among Nicoya’s inhabitants [19
]; however, this trait also depends on factors related to lifestyle, such as stress and daily physical activity, and does not exclusively reflect the individual genetic makeup [20
The functional and social profile of centenarians from the Nicoya peninsula has recently been described by Madrigal-Leer et al. [21
] and the eating habits of 18 men and 16 women between the ages of 90 and 109 have been analyzed by Momi-Chacón et al. [22
]. The latter study revealed a predominantly plant-based diet characterized by low consumption of red meat and a lower daily calorie intake than in the rest of Costa Rica.
2.1.2. Ogliastra, Sardinia
The central-eastern part of Sardinia, Italy, corresponding to the historical subregions of Ogliastra and Barbagia, at latitude North of 39° 55′ and longitude East 9° 31′, was among the first high-longevity areas to be identified worldwide [23
] during a comprehensive validation process of the age of Sardinian centenarians [24
]. An editorial appeared in 2001 in the Science journal that acknowledged the genuineness of the Sardinian phenomenon and outlined that the male population was especially involved [26
]. The longevity area encompasses a group of six municipalities (Arzana, Baunei, Seulo, Talana, Villagrande Strisaili and Urzulei) located around the central mountain, Gennargentu [5
]. The total population (currently 12,000 inhabitants) is mainly engaged in agricultural activities, maintaining a relatively traditional lifestyle. The causes of longevity in the Sardinian LBZ are currently the subject of intense scrutiny involving several disciplines. Early studies hypothesized a strong impact of genetic factors; however, the results of the AKEA study, which analyzed the transmission of parental longevity in 204 Sardinian centenarians [27
] did not reveal a significant vertical transmission of longevity in both the paternal and maternal lineage. In addition, genetic association studies have been performed on the oldest Sardinians, using markers notoriously associated with longevity; however, in terms of frequency, none of these markers have been shown to be significantly different from that of the general Sardinian population [28
]. Behavioral and socio-cultural factors, such as nutrition, physical activity and family support, seem to be relatively more important [2
2.2. Study Design
This cross-sectional study was conducted with 210 subjects (118 females and 92 males) aged between 80 and 109 years belonging to the Nicoya and Ogliastra populations, respectively. More specifically, the analyses included, (i) an evaluation of dietary habits; (ii) determination of some anthropometric indexes (body weight and height, body mass index (BMI), waist and limb circumferences) taken as long-term markers of nutritional status; and (iii) an evaluation of performance in daily activities.
2.3. Study Participants
The first sample consisted of 60 individuals who lived in the Nicoya peninsula and were examined directly by two of the authors (A.N. and L.V.) between July and August 2019. The identification of the subjects, extracted from an electronic database, was provided by the Asociación Península de Nicoya-Zona Azul. Inclusion criteria were Nicoyan origin (to ensure genetic homogeneity) and age of at least 80 years. Every Costa Rican citizen has, since his/her birth or the date of possible naturalization, an identification number reported on the cédula (identity card). To minimize error, the age of participants was double-checked through the Costa Rican electoral lists (padrón) that are updated every four years and made available by the Tribunal Supremo de Elecciones.
The second sample consisted of 150 subjects from Ogliastra, recruited during an ongoing study, the design and preliminary results of which were previously reported [5
]. Inclusion criteria were similar to those used for Nicoya. Age validation was performed as previously described [25
2.4. Data Collection
The interviews at the participants’ home were conducted in Spanish and Italian language to make participants feel comfortable. Information about food and daily activities were recorded, and in the case of subjects with moderate/severe dementia, family members were involved in the interview. Sociodemographic information recorded included age, marital status, education, smoking habits, and living conditions.
Body height was measured in centimeters using a stadiometer, with the patient’s head aligned according to the Frankfurt horizontal plane, and body weight was measured using an electronic scale with an accuracy up to 0.1 kg [29
The number of variables related to functional status was restricted to the functional ability in daily life, which has better relevance for quality of life measurement. Self-rated health was evaluated according to Idler at al. [30
]. Performance-based functional ability was tested using two validated tools: (i) The Basic Activities of Daily Living (BADL), which evaluates the autonomy in carrying out the activities of everyday life, through 6 domains (washing, dressing, using the bathroom, eating, checking urinary and intestinal functions, performing small movements) [31
]; and (ii) a modified version of Instrumental Activities of Daily Living (IADL), which estimates the autonomy in performing instrumental activities that are physically and cognitively more complex necessary for an independent life [32
]. Only three items were used in this study: telephone use, TV watching and use of money [33
2.5. Nutritional Evaluation
Information about dietary habits was collected using a simplified food frequency questionnaire (FFQ) already used for nutritional studies in Sardinia [34
] and adapted for the Costa Rican population, which included the following common foods: Meat, fish, vegetable, legumes, cereals, potatoes, pasta, sweets, milk, other dairy foods including soft and hard cheese, and coffee. A list of foods typical of the Nicoya and Ogliastra areas was also included. Nutritional evaluation was complemented by anthropometric measurements, using standardized methods [35
], and included the waist circumference (measured at the umbilical scar); the average circumference of the calf (in correspondence to the gastrocnemius muscle belly); the brachial circumference (in correspondence with the biceps muscle belly), as well as the knee-floor distance (measured from the patella lower edge to the floor) [35
]. Body mass index was calculated by dividing body weight (in kilograms) by height (in meters) squared (kg/m²).
2.6. Statistical Analysis
The basic descriptive statistics for each variable in both populations were reported as the mean and standard deviation for the continuous variables and the absolute and percentage frequencies for the categorical variables. Marital status was labelled as single, married or free union, widowed, and divorced. Education was expressed as the number of years spent at school, which in some developing populations is more informative than the achieved school level. Living conditions were expressed as two categories: (i) Residents in owned or leased houses, or (ii) residents in nursing homes. Smoking was stratified as (i) Non-smokers, (ii) former smokers, and (iii) current smokers. Intake of food categories was coded into an ordinal variable: (i) Never/rarely, (ii) 2–3 servings/month, (iii) 1–2 servings/week, (iv) 3–5 servings/week, and (v) every day. The BMI was divided into <18 (kg/m²), 18–24.9 (kg/m²), 25−29.9 (kg/m²), and ≥30 (kg/m²). The score obtained in the BADL and IADL was stratified into “severe disability” (score < 3) and “moderate disability or no disability” (score ≥ 3). The differences between the two populations were further analyzed by two-tailed Mann–Whitney U test for independent samples and the chi-square test for categorical variables. Correlation analysis was performed by calculating the Spearman correlation coefficient. All statistical analyses were performed using SPSS software (version 16.0, Chicago, IL, USA). p-values < 0.05 were considered statistically significant. The study was conducted in accordance with the Helsinki Declaration.
In the present study, an investigation of dietary habits was conducted in two of the longest-lived populations belonging to the LBZs [17
]. The analysis was done separately for the two sexes, in consideration of the diversity related to the different roles for men and women in these traditional societies, which are more prominent than in sophisticated post-modern societies. The social profile detected in the population of Nicoya was in agreement with a report by Madrigal-Leer et al. [21
] and somewhat similar for the Ogliastra community [5
]. Both are poor rural populations characterized by a remarkable history of long-standing isolation, not only in geographical terms but also genetic and cultural terms, which have been well documented in the literature (for Nicoya see [36
], for Ogliastra, see [38
]), although a discussion on the potential relationship between their genetic makeup and longevity is beyond the scope of this work. Although both areas are considered low-income regions compared to the rest of their respective countries, there is a difference of –56% in the average per capita income between Nicoya and Ogliastra. However, we must take into account that this is a mere indicator of “objective poverty” and does not include the subjective aspects (self-perceived poverty) [39
]. Indicators of air pollution are lower in the two locations compared to the rest of their countries, but that of soil, in particular from pesticides, is not negligible due to the intense agricultural activity [40
The analysis of anthropometric data shows that the elderly of Nicoya were on average taller and leaner than their Sardinian peers, in accordance with a previous observation [41
]. Moreover, in this article, Nicoyans were reported to be taller compared with the rest of the country. This outstanding height was attributed by the authors to a healthier growth of this population in the early stages of body development. On the other hand, the shorter stature of the Sardinian elderly cannot be attributed to insufficient nutrition during childhood and adolescence, but rather to a higher frequency of short-statured genetic variants [42
The analysis of the consumption frequencies of common foods in the two populations showed that cereals were the most frequently consumed food, with few differences between the two populations and the two sexes, followed by legumes and fruit, although their intake was significantly lower in the Ogliastra population. Interestingly, in the Nicoya subgroup there was a variable proportion, between 3% and 6%, who never or rarely ate this food. The salad consumption was around 1–2 servings a week in most interviewees and, although similar in the two populations, no Sardinian participants completely abstained from it, while among Nicoyans the percentage of those who did not eat salad was up to 15%. Furthermore, potato consumption was high in both populations: At least 1–2 servings per week in 50% of study participants with a 60% peak among Sardinian males. This seems in contrast with the alleged harmful health effect of these tubers, resulting from their high glycemic load potentially increasing the risk of diabetes [43
]. However, these negative aspects are mostly related to the cooking method, especially frying [45
]. Instead, in both populations, potatoes are mostly boiled and especially seasoned with fats that are able to reduce their glycemic index.
On the basis of these findings we can conclude that the diet of the two elderly populations is essentially “plant-based” [14
], although a non-negligible consumption of animal-derived foods was also recorded. Half of the individuals were meat-eaters at a frequency not less than of 3–5 servings per week, and a quarter of Sardinian and Nicoyan males consumed meat almost daily. Contrary to what has been reported recently in Nicoya centenarians [22
], the most consumed type of meat was pork and not chicken, although this was consumed, together with beef, in moderate quantities. Similarly, Sardinians consumed pork most frequently, followed by goat or lamb (data not shown). Of note, meat came from locally bred animals, and also ham, sausages, and salami were homemade. Therefore, this processed meat contains only salt and spices such as pepper and garlic without preservatives or chemical additives.
The non-negligible consumption of meat seems in contrast to what has been described in other populations [46
]. Based on the results of the NHANES III study [47
], the impact of meat consumption on health is age-dependent: Although meat products could be harmful before the age of 65, after this age the situation reverses, because meat may preserve the elderly from excessive loss of muscle mass, indirectly promoting longevity. Therefore, it is no wonder that it has been suggested to re-evaluate the role of meat in the daily diet, especially home-prepared meat from self-raised animals [48
A similar consideration must be made for dairy food: About half of Nicoyan males and females consumed it every day, while the percentage exceeded 80% among Sardinians. They are always typical homemade products: In Nicoya fresh cheese or in the form of cuajada
, in Sardinia mostly a fresh sour cheese (casu ajedu
), although aged cheese was consumed as well. For a long time, dairy products have not been considered particularly healthy; however, a positive association between their consumption and longevity has been reported among Japanese centenarians [49
], and it has been reported that they have a protective effect against dementia [50
] and cardiovascular disease [51
]. In this regard, it should be noted that, at least in Ogliastra, milk is almost never of bovine origin but comes from sheep and goat, which has less harmful effects on health and contains bioactive peptides that improve insulin activity [52
]. More importantly, the high consumption of milk was significantly and positively associated with functional capacity of BADL and IADL scores. These findings were consistent between the two ethnic groups and the two sexes, making the association reliable.
Although fish consumption is associated with better health, and is strongly recommended by nutritionists, it was very scarce in the two long-lived populations. The frequency of fish consumption was confirmed to be very low among Sardinians, as previously reported [53
], while it was a little higher among Nicoyans (more than 1–2 servings per week for only 10% of the total population). Another eating behavior shared by the two populations was the low consumption of sweets, since half of the Nicoyan males and two thirds of the Sardinian males ate less than 1–2 servings per month. Females from the two regions consumed slightly more.
Finally, coffee consumption was abundant among the study participants: More than 85% of the Nicoyans and more than 75% of the Sardinians drank coffee daily, a feature described also in Ikaria LBZ [54
]. Long-term dose-dependent benefits of coffee have been reported including a reduced risk of type 2 diabetes, Parkinson’s and Alzheimer’s disease, alcoholic cirrhosis, and gout [55
]. Moreover, several studies showed an inverse relationship between coffee consumption and mortality for any cause, albeit mild [57
The interest in the relationship between human longevity and the diet dates back to the classical period and is reflected in the Hippocratic writings [58
]. Only in modern times, however, the possibility of extending human lifespan by the adoption of a particular dietary regimen aroused the attention of scholars, as evidenced by the interest in famous fasters such as the Italian Alvise Cornaro in the Renaissance epoch [59
]. At present, there is a growing body of research is focused on the relationships between eating habits and human longevity [46
]. However, the media often spread news and statements not always based on evidence, making it urgent to accurately ascertain whether the information retrieved from long-lived populations is reliable and can provide guidance and recommendations generalizable to the broader population. Despite the difficulty in comparing the eating habits of populations geographically distant, and whose ethnic origins and evolutionary history are divergent, this effort has the advantage of strengthening the study’s findings, to a greater extent than an analysis performed on a single population, where the results could simply be due to chance.
Nonetheless, our study has some limitations. Firstly, the cross-sectional study design does not allow to determine cause-effect relationships, but only associations. Secondly, the FFQ used for the analysis, although widely used in many epidemiological studies, did not allow us to accurately estimate the calorie intake and is not able to ascertain any sort of calorie restriction. Moreover, being a “snapshot” of the current state of nutrition, our investigation lacks historical dimensions. However, the correlation between diet and health status in the LBZ research is a novelty and lays the foundations for future, more detailed studies on a greater number of variables collected. Finally, the large number of participants in our study ensured adequate statistical power to obtain reliable estimates.