Dutour Olivier

Perrin Pascale

Pálfi György

Sola Christophe

Zink Albert

Pálfi, György

Dutour, Olivier

Perrin, Pascale

Sola, Christophe

Zink, Albert

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Tuberculosis in evolution.

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György Pálfi

Olivier Dutour

Pascale Perrin

Christophe Sola

Albert Zink

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Tuberculosis

Tuberculosis in evolution

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lable at ScienceDirectTuberculosis 95 (2015) S1eS3Contents lists avaiTuberculosisjournal homepage: http : / / int l .e lsevierhealth.com/journals / tubeEDITORIALTuberculosis in evolutionGy€orgy Palﬁ a, *, Olivier Dutour b, c, Pascale Perrin d, Christophe Sola e, Albert Zink fa Department of Biological Anthropology, University of Szeged, Szeged, Hungaryb Laboratoire d'anthropologie biologique Paul Broca, Ecole Pratique des Hautes Etudes, UMR 5199 PACEA, Universite de Bordeaux, Pessac, Francec Department of Anthropology, University of Western Ontario, Canadad Unite de Recherche MIVEGEC e UR 224/IRD e UMR 5290/CNRS e UM1 e Universite Montpellier 2, Montpellier, Francee Institut de Biologie Integrative de la Cellule (I2BC), CEA-CNRS-UPS, UMR9198, Ba^t 400, F-91400 Orsay, Francef Institute for Mummies and the Iceman, EURAC Research, Bolzano, ItalyAt the beginning of the 1980s, about a hundred years afterRobert Koch had discovered the pathogen of tuberculosis (TB) in1882, many still believed that TB, like smallpox, could be eliminatedby the end of the millennium from the group of infectious diseasesafﬂicting humanity. This optimistic approach was supported by thespectacular 20th-century results in the prevention, diagnostics andtherapy of the disease. Sadly, these predictions did not come true.Instead of being eradicated, TB re-emerged at the end of the 20thcentury to become a global health threat for the new millennium.According to the latest WHO's data, TB remains one of theworld's deadliest contagious diseases despite slowly declining eachyear. In 2013, an estimated 9 million people developed TB and 1.5million died from the disease, 360,000 of whomwere HIV-positive.A global 3.5% multi-drug resistance rate was observed. Of theestimated 9 million TB cases, more than half (56%) were in theSouth-East Asia and Western Paciﬁc regions. A further one quarterwere in the African region, which also had the highest rates of casesand deaths relative to population. India and China alone accountedfor 24% and 11% of total cases respectively [2].Tuberculosis remains a major global health problemworldwide.Despite the advent of antibiotics which have widely reducedmortality, antibiotic-resistant strains have now emerged, withmulti-resistant strains raising therapeutic problems reminiscent ofpre-antibiotherapy clinical situations dating from the turn of the19th and 20th centuries. This reminder of history prompts us toincrease our knowledge both of the origin and evolutionary historyof TB and of the factors promoting the emergence and spread of TBstrains in human populations worldwide.Fifteen years after the ﬁrst multidisciplinary TB meeting ICEPT(“International Congress on The Evolution and Paleoepidemiologyof Tuberculosis”; September 1997, Budapest-Szeged, Hungarye seemore details in [1]), a further TB Evolution Meeting (ICEPT2) washeld in Szeged, Hungary between the 22nd and 25th of March 2012to gather an updated multidisciplinary synthesis of the* Corresponding author.E-mail address: palﬁgy@bio.u-szeged.hu (G. Palﬁ).http://dx.doi.org/10.1016/j.tube.2015.04.0071472-9792/Crown Copyright © 2015 Published by Elsevier Ltd. All rights reserved.evolutionary pattern of TB. The recent progresses in the knowledgeof TB evolutionary biology and the spectacular results produced bythe new interdisciplinary collaborations initiated during the ﬁrstICEPT demanded a new synthesis of these topics. Several importantquestions were addressed during ICEPT2, among them: what is theoldest evidence of this infection on human and animal remains?When did speciﬁc mutation(s) of the modern strains arise? Whatwas the relative importance of the different pathogenic species ofthe Mycobacterium genus among past populations? Can wereconstruct a consensual phylogeny of the Mycobacterium genus?How can paleopathology and paleomicrobiology contribute to theresearch on TB evolution? What are the main strategies to stop or tomoderate the re-emergence of TB? How can molecular phyloge-netics contribute to these ﬁghts? The most up-to-date answers tothese questions are providing in this Special Issue of Tuberculosis,which gathers the results of the 2012 ICEPT2 TB Evolution Meeting.When choosing the dates of the 2012 TB Evolution Meeting, itwas decided to join the Albert Szent-Gy€orgyi's Nobel Prize AwardAnniversary Conference Series (23rd-25th March 2012, Universityof Szeged, Szeged, Hungary) and the International TB day (24thMarch 2012), corresponding to the 130th anniversary of RobertKoch's discovery. This Conference Series therefore also beneﬁttedfrom the presence of nine Nobel Prize winners.The ﬁrst chapter of this special issue is dedicated to the past ofTB - and TB in the Past. It is currently usually assumed that mostmajor infectious diseases could have only emerged within the lastten thousand years, following the rise of agriculture and domesti-cation and the growth of human populations during the Neolithicperiod. Human TB could be an environmental (zoonotic) disease,e.g. derived from animal TB ormay have developed gradually by co-evolution, specialization and adaptation towards pathogenicity andvirulence of human-adapted bacteria. In this special issue, analysisof skeletons coming from the early Neolithic site of Dja'de elMughara (11th millenium BP) can now reveal that human tuber-culosis predated domestication in ancient Syria (Baker et al.),occurring at a site showing only the earliest signs of wild aurochs(Bos primigenius) domestication. Interestingly, archaeological signsof settlement during the 9th millennium BC are restricted to theEditorial / Tuberculosis 95 (2015) S1eS3S2same region. Archaeological and paleoanthropological data avail-able in this area provide adequate material to test the early pres-ence of Mtb complex pathogens. Few studies have been completedon human and animal remains, so the opportunity to test the hy-pothesis of a co-evolution rather than a direct transmission frombovines to humans is not yet possible. However, we cannot excludethat TB may also been contracted from wild or feral animals(Minnikin et al.). In that case, phylogeographical speciﬁcity ofancient wildlife and various food regimens may have played a role.With the assumption of a human Mycobacterium tuberculosisancestor, the question of TB identiﬁcation in Upper Paleolithicmodern humans if not among Neanderthals can now be asked.The vast majority of infectious diseases only affect the soft tis-sues of the body. In the case of TB, only a small proportion of pa-tients (3e5%) develops bone stigma. It is therefore a great challengeto analyze and detect speciﬁc bone lesions to target samples ofinterest. The remarkable bone changes indicative of a long-standing chronic disease (Pott's disease) would have been un-likely to develop until the infection was less virulent. Until now,paleopathology was limited to the identiﬁcation of this small pro-portion of individuals carrying such speciﬁc lesions, having suf-fered from TB for an extensive period of time. Fortunately,mycobacteria are suitable targets for paleopathological and bio-molecular studies because of their waxy, hydrophobic and lipid-rich cell wall (Daffe) that seems to help to protect DNA againstdestruction and degradation. New approaches combiningmorphological studies (minor osteological lesions, microscopicchanges) with biochemical and molecular analyses of biologicaltraces in bones (speciﬁc lipid biomarkers, proteins, DNA) providepromising results with the detection and identiﬁcation of ancientTB infection (e.g. Donoghue et al.; Hershkovitz et al.; Masson et al.;Molnar et al.; Palﬁ et al.; Santos; Schmidt-Schultz and Schultz;Schultz and Schmidt-Schultz).Paleopathological processes of TB infection can also be betterunderstood by 3D imaging (Coqueugniot et al.). Information is nowalso available on TB strains which had infected ancient humanpopulations in different geographic regions. Furthermore, newmethods can now address paleoepidemiological questions aboutthe prevalence and distribution of infection diseases in past pop-ulations (Blondiaux and Naji; Eddy; Teschler-Nicola et al.). Newstudies using themolecular analysis identiﬁcation ofM. tuberculosisin prehistoric and historic populations between 5000 BC and 1800AD give a more complete view on the infection rates in ancienttimes (Masson et al.; L€osch et al.; Posa et al.; Szikossy et al.). Theyalso provide information about the molecular evolution and thephylogenetic relationships of infectious diseases through theidentiﬁcation of possible TB strains no longer found today as well asthe comparative analysis of modern and ancient microbial se-quences (Roberts; Spigelman et al.).More than 2000 modern MTB genomes have been sequenced todate, affording a more accurate reconstruction and calibration ofthe evolutionary scheme of M. tuberculosis helping to evaluate thedistribution and prevalence of ancient strains occurring both inancient and modern populations. It must be stressed that suchstudies do not necessarily demonstrate the proportion of in-dividuals that died from TB, but rather the proportion that hadcontracted TB at some stages of their lives. Knowledge of changingprevalence in the past helps epidemiologists to understand theeffect of environmental and socio-cultural factors affecting infec-tious diseases at a time before antibiotics and other modern in-terventions (Matos and Santos; Roberts and Bernard).Ancient biomolecular analyses, including new sequencingtechnologies (next-generation sequencing), could signiﬁcantlycontribute to calibrate, improve or even change current modelsabout TB evolution and the spread of MTb complex strains.Identifying the place of origin and later spread of TBwithin humansand animals whether wild or under domestication can shed lighton its evolutionary process (Lee et al.). A genetic factor is not theonly cause for the (re-)emergence of TB, as others must also beconsidered such as international travel and trade, poor economicenvironment, demographic (human population increase) andsocio-cultural factors (urbanization), a weak health system,together with worldwide human migrations and community ofpathogens (Donoghue et al.). Several studies have provided evi-dence for a role of the host genetics in susceptibility to TB, whilenumerous candidate genes studies as well as genome-wide linkagescans have been carried out. However, some inconsistencies arenoticeable across these studies. In fact, different key elementsshould be accounted for when conducting forthcoming studies:deﬁnition of the controls is clearly questioned (are they true con-trols or latently infected with tuberculosis?), population substruc-ture (admixture) and differences in M. tuberculosis strains (Perrin).TB is caused by a group of phylogenetically closely related bac-teria, known as the M. tuberculosis complex (MTBC). What are thepotential evolutionary consequences of such long-standinghumanepathogen association? How was TB “seeded” in humanpopulations and when? These questions remain open. Whole-modern genome sequencing, systems biology and hostepathogeninteractions are generating new approaches for the understandingof the past and and ongoing evolution, as well as the pathogenicity,of M. tuberculosis. CRISPR (Clustered Regularly Interspersed ShortPalindromic Repeats), which demonstrate a historical record ofbacterial-phage struggle, have been valuable in the past. Combinedto new multi-level SNP-based identiﬁcation tools, they shouldremain useful in the future, helping to follow both the microevo-lution and macroevolution process of MTBC (Sola).Studies have shown human pathogens to have geographicstructures in terms of population genetics. Depending on a splitter/gatherer point of view, the global population structure ofM. tuberculosis complex is deﬁned by six to ten phylogeographicallineages, each associated with speciﬁc human populations (sym-patric). The links between the particular MTBC lineages and humanpopulations are maintained in cosmopolitan settings. Transmissionof allopatric strains has been associated with risk factors such asHIV-co-infection. One of the key features of co-evolution is theongoing evolutionary arms race between the pathogen and the hostimmune system. Surprisingly, the known human T-cell epitopes ofMTBC are the most conserved regions of the MTBC genome andmight contribute to the successful spread of MTb. “Ancient” and“modern” lineages can be distinguished among the six mainhuman-adapted lineages (East-African Indian, Beijing, Central-Asian, Euro-American, M. africanum, M. bovis). The three “mod-ern” lineages are more successful in terms of their geographicalspread i.e. Europe, China and India. Some studies are consistentwith the hypothesis that such strains have evolved a strategy ofhigher virulence and shorter latency (Mokrousov; Gomes et al.;Simeone et al.). The ﬁght againstM. tuberculosis also requires betterdiagnostic platforms (Somosk€ovi et al.) and new therapeutic ap-proaches (Sipos et al., Horvati et al.). Although the complexity of theco-evolutionary process is difﬁcult to understand, it is key to pre-dicting progressive genetic changes in the future and developing amore integrative view (Perrin).Questions about the origins and spread of tuberculosis in thepast are addressed, in addition to biological and genetic topics, aswell as epidemiological problems of the present. A thorough syn-thesis or concise summary of the articles from such a great numberof ﬁelds cannot be given here. The emphasis will be different for apaleopathologist and for a microbiologist, just as a clinician and amedical historian approach the evolution of TB in diverse ways.Nevertheless, we remain convinced that the study of TB through anEditorial / Tuberculosis 95 (2015) S1eS3 S3interdisciplinary approach as presented in this special issue,including ﬁndings from paleopathology to paleogenetics and frommodern diversity studies to diagnostics, offers the best potential tosigniﬁcantly improve our knowledge of TB and its continuingevolution. This special issue represents a small yet signiﬁcantcontribution to the global effort to reduce and hopefully eventuallycompletely eradicate TB infections worldwide. We sincerely believethat by reading this TB Evolution special issue, the general readerwill get a comprehensive picture of the issues related to the pastand present of Tuberculosis, while the student of its evolution willbe equipped with a reliable basis for further research.December 2014, Szeged-Bordeaux-Montpellier-Paris-BolzanoThe EditorsAcknowledgementsThe publication of this special issue titled Tuberculosis in Evo-lution, dedicated to the past and the evolution of TB, was supportedby the University of Szeged, Hungary, the Hungarian ScientiﬁcResearch Fund ‘OTKA’ (OTKA Grants No. K78555, K81230, NN78696), the TAMOP-4.2.2/B-10/1-2010-0012 project co-ﬁnanced bythe EU and Hungary, the MIVEGEC laboratory (IRD/CNRS) and theUniversity of Montpellier (UM), France, the Universite Paris-Sud,France, the Ecole Pratique des Hautes Etudes, France and theInstitute for Mummies and the Iceman, EURAC Research, Bolzano,Italy. The Guest Editors are particularly grateful for all thesesupports.References[1] Palﬁ Gy, Dutour O, Deak J, Hutas I, editors. Tuberculosis: past and present.Budapest: TB Foundation, Szeged & Golden Book Publisher; 1999. p. 608.[2] WHO. Global tuberculosis report 2014. Geneva: WHO Press, World HealthOrganization; 2014. ISBN 978 92 4 156480 9.Gy€orgy PalﬁOlivier DutourPascale PerrinChristophe SolaAlbert Zink

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