Does the trained immune system play an important role in the extreme longevity that is seen in the Sardinian blue zone?

Villages in the island of Sardinia in the Mediterranean that display exceptional longevity are clustered within a defined mountainous region. Because of their unique location we hypothesize that these villages had a unique infectious disease exposure relevant to the observed successful longevity. These highland villages had a significant exposure to malaria in the first half of the 20th century after which malaria was eliminated due to vector control mechanisms. In addition, there is likely a high incidence of Helicobacter pylori infections among shepherds in Sardinia, the primary occupation of many living in the LBZ, as well as helminth infections among children. This suggests that individuals living in the LBZ had a unique infectious disease exposure. Specifically, we hypothesize that the continued high exposure of residents in the LBZ to these infectious agents prior to the 1950s lead to the generation of a uniquely trained (or imprinted) immune system. Once some of these diseases were eliminated in the latter half of the century, individuals within the LBZ were equipped with a trained immune system that was uniquely capable of not only responding effectively to common infections but also responding in a manner that maximized maintaining tissue health. In addition, there are lifestyle factors that also favor such a trained immune system. This hypothesis may help explain the slow progression of chronic immune mediated diseases as well as other chronic non-transmissible age-related diseases seen in the Sardinian LBZ and serve as a template for future studies that support or refute this hypothesis.

[1]  B. Everts,et al.  Antigens from the parasitic nematode Trichuris suis induce metabolic reprogramming and trained immunity to constrain inflammatory responses in macrophages. , 2022, Cytokine.

[2]  P. Ramsland,et al.  Helicobacter pylori and the Role of Lipopolysaccharide Variation in Innate Immune Evasion , 2022, Frontiers in Immunology.

[3]  Gernot Posselt,et al.  Beyond the gastric epithelium - the paradox of Helicobacter pylori-induced immune responses. , 2022, Current opinion in immunology.

[4]  M. Dore,et al.  Increased Risk to Develop Hypertension and Carotid Plaques in Patients with Long-Lasting Helicobacter pylori Gastritis , 2022, Journal of clinical medicine.

[5]  T. Seeman,et al.  Social stressors associated with age-related T lymphocyte percentages in older US adults: Evidence from the US Health and Retirement Study , 2022, medRxiv.

[6]  D. Boraschi,et al.  Helicobacter pylori Infection of Primary Human Monocytes Boosts Subsequent Immune Responses to LPS , 2022, Frontiers in Immunology.

[7]  M. C. Fastame Well-being, food habits, and lifestyle for longevity. Preliminary evidence from the sardinian centenarians and long-lived people of the Blue Zone , 2022, Psychology, health & medicine.

[8]  R. Xavier,et al.  Single-cell transcriptomic profiles reveal changes associated with BCG-induced trained immunity and protective effects in circulating monocytes. , 2021, Cell reports.

[9]  D. Monti,et al.  Immunosenescence and inflammaging in the aging process: age-related diseases or longevity? , 2021, Ageing Research Reviews.

[10]  C. Franceschi,et al.  Specific features of the oldest old from the Longevity Blue Zones in Ikaria and Sardinia , 2021, Mechanisms of Ageing and Development.

[11]  M. Nahrendorf,et al.  Infectious and lifestyle modifiers of immunity and host resilience. , 2021, Immunity.

[12]  J. Asara,et al.  Pre-operative exercise therapy triggers anti-inflammatory trained immunity of Kupffer cells through metabolic reprogramming , 2021, Nature Metabolism.

[13]  M. Dore,et al.  Evolution of the Dietary Patterns across Nutrition Transition in the Sardinian Longevity Blue Zone and Association with Health Indicators in the Oldest Old , 2021, Nutrients.

[14]  M. C. Fastame,et al.  Mental Health and Religiosity in the Sardinian Blue Zone: Life Satisfaction and Optimism for Aging Well , 2021, Journal of Religion and Health.

[15]  M. Szyf,et al.  Potential reversal of epigenetic age using a diet and lifestyle intervention: a pilot randomized clinical trial , 2021, Aging.

[16]  L. Joosten,et al.  Trained Immunity: Reprogramming Innate Immunity in Health and Disease. , 2021, Annual review of immunology.

[17]  M. Dore,et al.  Does the longevity of the Sardinian population date back to Roman times? A comprehensive review of the available evidence. , 2021, PloS one.

[18]  Jie Zhou,et al.  Trained immunity contributes to the prevention of Mycobacterium tuberculosis infection, a novel role of autophagy , 2021, Emerging microbes & infections.

[19]  M. Dore,et al.  Spatial Association between Gastric Cancer Mortality and Goiter in Sardinia , 2021, Asian Pacific journal of cancer prevention : APJCP.

[20]  Gemma L. Kay,et al.  Metagenomics and microscope revealed T. trichiura and other intestinal parasites in a cesspit of an Italian nineteenth century aristocratic palace , 2020, Scientific Reports.

[21]  A. R. Silva,et al.  Mediterranean Diet: Lipids, Inflammation, and Malaria Infection , 2020, International journal of molecular sciences.

[22]  M. Dore,et al.  Dietary Habits, Anthropometric Features and Daily Performance in Two Independent Long-Lived Populations from Nicoya peninsula (Costa Rica) and Ogliastra (Sardinia) , 2020, Nutrients.

[23]  M. Netea,et al.  Trained Immunity: a Tool for Reducing Susceptibility to and the Severity of SARS-CoV-2 Infection , 2020, Cell.

[24]  J. Ferluga,et al.  Natural and trained innate immunity against Mycobacterium tuberculosis. , 2020, Immunobiology.

[25]  A. Hoischen,et al.  Catecholamines Induce Trained Immunity in Monocytes In Vitro and In Vivo , 2020, Circulation research.

[26]  P. Imhof,et al.  Molecular Dynamics Simulations of a Chimeric Androgen Receptor Protein (SPARKI) Confirm the Importance of the Dimerization Domain on DNA Binding Specificity , 2020, Frontiers in Molecular Biosciences.

[27]  A. Müller,et al.  Mechanisms of persistence, innate immune activation and immunomodulation by the gastric pathogen Helicobacter pylori. , 2020, Current opinion in microbiology.

[28]  M. Dore,et al.  Sociodemographic, Clinical and Functional Profile of Nonagenarians from Two Areas of Sardinia Characterized by Distinct Longevity Levels. , 2020, Rejuvenation research.

[29]  C. Nicco,et al.  Trained immunity modulates inflammation-induced fibrosis , 2019, Nature Communications.

[30]  Alejandro Lucia,et al.  Chronic inflammation in the etiology of disease across the life span , 2019, Nature Medicine.

[31]  E. Chiappini,et al.  Immune Response to Mycobacterium tuberculosis: A Narrative Review , 2019, Front. Pediatr..

[32]  A. Verrall,et al.  Beyond memory T cells: mechanisms of protective immunity to tuberculosis infection , 2019, Immunology and cell biology.

[33]  C. Penha-Gonçalves Genetics of Malaria Inflammatory Responses: A Pathogenesis Perspective , 2019, Front. Immunol..

[34]  T. Cover,et al.  Helicobacter pylori VacA Targets Myeloid Cells in the Gastric Lamina Propria To Promote Peripherally Induced Regulatory T-Cell Differentiation and Persistent Infection , 2019, mBio.

[35]  M. Drancourt,et al.  Trained Immunity Carried by Non-immune Cells , 2019, Front. Microbiol..

[36]  P. Malfertheiner,et al.  Helicobacter pylori Infection: New Facts in Clinical Management , 2018, Current Treatment Options in Gastroenterology.

[37]  Jake K. Byrnes,et al.  Estimates of the Heritability of Human Longevity Are Substantially Inflated due to Assortative Mating , 2018, Genetics.

[38]  Joseph H. Marcus,et al.  Genomic history of the Sardinian population , 2018, Nature Genetics.

[39]  M. Bonafè,et al.  Age-related M1/M2 phenotype changes in circulating monocytes from healthy/unhealthy individuals , 2018, Aging.

[40]  B. Peleteiro,et al.  The occupational risk of Helicobacter pylori infection: a systematic review , 2018, International Archives of Occupational and Environmental Health.

[41]  Dan Geiger,et al.  Quantitative analysis of population-scale family trees with millions of relatives , 2017, Science.

[42]  C. Franceschi,et al.  The Continuum of Aging and Age-Related Diseases: Common Mechanisms but Different Rates , 2018, Front. Med..

[43]  M. C. Fastame,et al.  Resilience in Elders of the Sardinian Blue Zone: An Explorative Study , 2018, Behavioral sciences.

[44]  M. Netea,et al.  Cutting Edge: Plasmodium falciparum Induces Trained Innate Immunity , 2018, The Journal of Immunology.

[45]  M. Oosting,et al.  Western Diet Triggers NLRP3-Dependent Innate Immune Reprogramming , 2018, Cell.

[46]  M. Dore,et al.  Analysis of Physical Activity Among Free-Living Nonagenarians From a Sardinian Longevous Population. , 2017, Journal of aging and physical activity.

[47]  Paolo Garagnani,et al.  Immunobiography and the Heterogeneity of Immune Responses in the Elderly: A Focus on Inflammaging and Trained Immunity , 2017, Front. Immunol..

[48]  C. Franceschi,et al.  The genetics of human longevity: an intricacy of genes, environment, culture and microbiome , 2017, Mechanisms of Ageing and Development.

[49]  P. Murray Macrophage Polarization. , 2017, Annual review of physiology.

[50]  R. Xavier,et al.  Functional and Genomic Architecture of Borrelia burgdorferi-Induced Cytokine Responses in Humans. , 2016, Cell host & microbe.

[51]  L. Joosten,et al.  Innate immune cell activation and epigenetic remodeling in symptomatic and asymptomatic atherosclerosis in humans in vivo. , 2016, Atherosclerosis.

[52]  R. Maizels,et al.  Host parasite communications—Messages from helminths for the immune system , 2016, Molecular and biochemical parasitology.

[53]  R. Maizels,et al.  Parasitic helminth infections and the control of human allergic and autoimmune disorders. , 2016, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[54]  M. Gerhard,et al.  Helicobacter pylori γ-Glutamyltranspeptidase Induces Tolerogenic Human Dendritic Cells by Activation of Glutamate Receptors , 2016, The Journal of Immunology.

[55]  R. Xavier,et al.  Trained immunity: A program of innate immune memory in health and disease , 2016, Science.

[56]  Dan Buettner,et al.  Blue Zones , 2016, American journal of lifestyle medicine.

[57]  J. Hirschhorn,et al.  Small island, big genetic discoveries , 2015, Nature Genetics.

[58]  M. Dore,et al.  Male longevity in Sardinia, a review of historical sources supporting a causal link with dietary factors , 2014, European Journal of Clinical Nutrition.

[59]  Peter D. Crompton,et al.  Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. , 2014, Annual review of immunology.

[60]  C. Prinz,et al.  Helicobacter pylori Cytotoxin-Associated Gene A Impairs Human Dendritic Cell Maturation and Function through IL-10–Mediated Activation of STAT3 , 2014, The Journal of Immunology.

[61]  E. Riley,et al.  Piecing Together the Puzzle of Severe Malaria , 2013, Science Translational Medicine.

[62]  Robert J Wilkinson,et al.  The immune response in tuberculosis. , 2013, Annual review of immunology.

[63]  N. Battistini,et al.  Lifestyle and nutrition related to male longevity in Sardinia: an ecological study. , 2013, Nutrition, metabolism, and cardiovascular diseases : NMCD.

[64]  A. Maisa,et al.  Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function , 2012, Aging cell.

[65]  R. Xavier,et al.  Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. , 2012, Cell host & microbe.

[66]  L. Contu,et al.  Genome-wide scan with nearly 700 000 SNPs in two Sardinian sub-populations suggests some regions as candidate targets for positive selection , 2012, European Journal of Human Genetics.

[67]  Alessandra Mereu,et al.  Population Based Study of 12 Autoimmune Diseases in Sardinia, Italy: Prevalence and Comorbidity , 2012, PloS one.

[68]  M. Poulain,et al.  Height and Survival at Older Ages among Men Born in an Inland Village in Sardinia (Italy), 1866–2006 , 2012, Biodemography and social biology.

[69]  I. Ludwig‐Portugall,et al.  TLRs, Treg, and B Cells, an Interplay of Regulation during Helminth Infection , 2011, Front. Immun..

[70]  M. Poulain,et al.  A Population Where Men Live As Long As Women: Villagrande Strisaili, Sardinia , 2011, Journal of aging research.

[71]  E. Tognotti Program to Eradicate Malaria in Sardinia, 1946–1950 , 2009, Emerging infectious diseases.

[72]  P. Craig,et al.  Control of cystic echinococcosis/hydatidosis: 1863-2002. , 2006, Advances in parasitology.

[73]  S. Sabbatani [The fight against tuberculosis and developments in public health from 1890 to 1930 in Italy]. , 2005, Le infezioni in medicina : rivista periodica di eziologia, epidemiologia, diagnostica, clinica e terapia delle patologie infettive.

[74]  L. Ferrucci,et al.  Identification of a geographic area characterized by extreme longevity in the Sardinia island: the AKEA study , 2004, Experimental Gerontology.

[75]  D. Graham,et al.  High Prevalence of Helicobacter pylori Infection in Shepherds , 1999, Digestive Diseases and Sciences.

[76]  C. Palmas,et al.  Causality or coincidence: may the slow disappearance of helminths be responsible for the imbalances in immune control mechanisms? , 2003, Journal of Helminthology.

[77]  S. Kaufmann,et al.  Protection against tuberculosis: cytokines, T cells, and macrophages , 2002, Annals of the rheumatic diseases.

[78]  D. Graham,et al.  Isolation of helicobacter pylori from sheep—implications for transmission to humans , 2001, American Journal of Gastroenterology.

[79]  D. Graham,et al.  Helicobacter pylori in sheep milk , 1999, The Lancet.

[80]  G. Ferretti,et al.  Hydatidosis in Sardinia: review and recommendations. , 1985, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[81]  E. Rolandi,et al.  [Clinical and epidemiologic aspects of typhoid fever in northern Sardinia]. , 1968, Giornale di clinica medica.