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  Review Optimized   centrifugation   preparation   of    the   platelet   rich   plasma:Literature   review B.Croise´  a,b, *,   A.Pare´  a,b ,A.Joly a ,A.Louisy a ,B.Laure a,b ,D.Goga a,b a Department    of    Maxillofacial   and   Plastic    Facial   Surgery,   Trousseau   Hospital,   CHU    Trousseau,    Avenvue   de   la   re´  publique,    37170   Chambray-le` s-Tours,   France b School   of    medicine,   University   of    Franc  ¸ ois   Rabelais,    370   Tours,   France 1.   Introduction The   Platelet   Rich   Plasma   (PRP)   is   a   plasma   rich   in   platelets,obtained   from   venous   blood.In   order   to   get   a   therapeutic   aimed   PRP,   the   concentration   mustbe   between   200      10 3 and   1000      10 3 platelets/ m L.   A   higherconcentration   would   be   unfavourable   [1].Many   studies   showed   that,   during   contact   with   collagen,   PRPreleased   growth   factors   such   as   Platelet   Derived   Growth   Factor(PDGF),   Vascular   Endothelial   Growth   Factor   (VEGF),   EpidermalGrowth   Factor   (EGF),   Platelet   Factor   4   (PF-4),   Insulin   like   GrowthFactor-1   (IGF-1)   and,   Transforming   Growth   Factor   Beta   (TGF   b )   bytheir   a -granules   [2].These   growth   factors   play   a   key   role   in   the   early   stage   of    woundhealing   by   allowing   a   stem   cell   proliferation   and,   angiogenesis.Many   medical   specialities   such   as   orthopedic,   ophthalmic   andmaxillofacial   surgery   are   looking   for   this   tissue   engineering   effect.In   our   day-to-day   practice   in   maxillo   facial   surgery,   we   use   PRPin   preimplant   surgery   during   bone   grafts,   in   order   to   get   a   goodmucosal   healing:   an   important   and   essential   step   to   avoid   the   maincomplication   linked   to   this   surgery:   infection.   Indeed,   a   badmucosal   healing   is   a   source   for   higher   infection   probability,   due   tothe   fact   that   the   graft   is   exposed   in   a   so-called   dirty   environment[3].Moreover,   PRP   use   allows   a   quicker   haemostasis   and   a   betterbone   regeneration   [4].However,   in   spite   of    PRP   substantial   use   in   our   specialities,   nocentrifugation   protocol   based   on   time,   speed   and   centrifugationnumbers   is   defined   to   obtain   a   good   quality   PRP,   leading   to   anoptimal   effect   on   healing.It   was   a   topical   issue,   since   the   first   articles   on   the   questiondating   back   to   the   seventies   disagreed.Slitcher   et   al.   [5]   drew   up   a   double   centrifugation   protocol   witha   first   centrifugation   at   1000   G   during   9   min   (min),   then   3000   Gduring   20   min,   while   Kahn   et   al.   [6],   during   the   same   year,   set   up   aprotocol   with   only   one   centrifugation   at   3800   RPM   during   4   min.Therefore,   many   questions   arise   concerning   the   PRP   prepara-tion:   Is   only   one   centrifugation   enough   to   obtain   a   clinical   effect   onthe   healing?   What   are   centrifugation   time   and   speed   to   obtain   agood   quality   PRP?The   aim   of    this   article   is   to   draw   up   a   literature   review   to   definea   simple   and   reproducible   protocol   (centrifugation   optimal   timeand   speed)   in   PRP   preparation   to   get   an   ideal   platelet   yield,   whilstavoiding   its   alteration.  J   Stomatol   Oral   Maxillofac   Surg   xxx   (2019)   xxx–xxx* Corresponding   author   at:   Department   of    Maxillofacial   and   Plastic   FacialSurgery,   Trousseau   Hospital,   CHU   Trousseau,   Avenvue   de   la   re´publique,37170   Chambray-le`s-Tours,   France. E-mail   address:   (B.   Croise´). A   R    T   I   C   L    E   I   N   F   O  Articlehistory: Received   12   April   2019Accepted   2    July   2019 Keywords: Platelet   Rich   PlasmaCentrifugationPreparationPlatelet   concentrationMaxillofacial   surgery A   B   S   T   R    A   C   T Nowadays,thePlateletRichPlasma(PRP)isfrequentlyusedforitstherapeuticeffectsonwoundhealing,andthisduetosecretionofmanygrowthfactors.However,nostandardizedprocedurehasbeensetup.Theaimofthisarticleistocheckthevariouspreparations(centrifugationtimeandspeed).Thisreviewrecordedalltheinternationalarticlespublishedbetween2007and2018,forwhichtheassessmentcriteriaweretheplateletconcentrationand/orthegrowthfactorreleaserate.Amultitudeofprotocolshasbeenlookedatwithasimpleordoublecentrifugation.Allofthemhaveshownanincreaseintheplateletconcentrationallowingatherapeuticeffect.   However,whenthecentrifugationforceisextended,plateletscanpossiblybealtered.Thediversityofmethodscanbelinkedtotheuseofvariouscentrifuges.Aprocedurewithsimplecentrifugationwouldbeagoodcompromisefortheday-to-dayuseofthePRPinsurgery.  C 2019ElsevierMassonSAS.Allrightsreserved. GModel JORMAS-715;   No.   of    Pages   5 Please   cite   this   article   in   press   as:   Croise´ B,   et   al.   Optimized   centrifugation   preparation   of    the   platelet   rich   plasma:   Literature   review.    JStomatol   Oral   Maxillofac   Surg   (2019), Available   online   at ScienceDirect  C 2019   Elsevier   Masson   SAS.   All   rights   reserved.  2.   Materials   and   Methods  2.1.   1Selection This   systematic   literature   review   looked   into   all   internationalarticles   published   between   2007   and   2018   on   Medline   (PubMed).The   used   key   words   combination   was   ‘‘Platelet   Rich   Plasma’’   and‘‘centrifugation’’   and   ‘‘platelet   concentration’’.   All   the   titles   andabstracts   of    the   identified   articles   on   the   database   have   beenanalyzed   in   order   to   evaluate   their   eligibility.   The   review   shouldstudy   a   precise   protocol   of    centrifugation   to   obtain   a   plateletconcentration.   The   sought    judging   criteria   are   the   platelet   yieldand/or   the   release   rate   of    growth   factors.   The   articles   on   studiescarried   out   on   animals   have   been   excluded   from   the   study,   as   wellas   articles   dealing   with   other   protocols   than   centrifugation.Moreover   only   the   English   and   French   articles   have   been   analyzed.Among   the   95   articles   in   the   database   searching,   21   articles   wereeligible   and   after   full-text   analysis,   14   articles   were   included   in   thissystematic   review   (Fig.   1).PRPpreparation:    whole,   non-anticoagulated   blood   collection   in   a   citrated   tube;    first   centrifugation   (soft   spin)   in   order   to   separate   the   red   bloodcells   (lower   layer   45%)   from   the   rich   in   platelets   plasma   (upperlayer   55%).   There   is   a   middle   leucocyte   layer   or   buffy   coat   ( < 1%);    sample   of    the   upper   layer;    then,   there   are   two   possible   choices:    either   we   use   this   rich   in   platelets   plasma,    or   we   carry   out   a   second   centrifugation   (hard   spin)   with   ahigher   speed   to   obtain   a   platelet   concentrated   plasma   or   purePRP,   made   of    granules,   which   is   represented   by   the   lowerlayer.   This   coat   is   homogenized   with   plasma.  2.2.   Various   centrifuges The   most   used   centrifuges   during   these   studies   are   presented   inthis   chapter: Fig.   1.   Systematic   review   study   selection   process:   flow   diagram   of    articles   identified   and   excluded   for   the   study. B.   Croise´  et    al.    /     J    Stomatol   Oral   Maxillofac    Surg     xxx   (2019)    xxx–xxx 2 GModel JORMAS-715;   No.   of    Pages   5 Please   cite   this   article   in   press   as:   Croise´ B,   et   al.   Optimized   centrifugation   preparation   of    the   platelet   rich   plasma:   Literature   review.    JStomatol   Oral   Maxillofac   Surg   (2019),  The   highest   platelet   concentration   was   found   in   the   C3   group.He   also   noticed   that,   when   the   centrifugation   time   increased,   theplatelet   concentration   became   higher.   Likewise,   when   the   centri-fugation   force   increased   at   10   min,   the   platelet   concentration   alsoincreased,   but   this   causal   link   was   not   found,   when   thecentrifugation   time   was   20   min.In   order   to   study   the   growth   factor   release,   the   various   tubeswere   centrifuged   at   172   G   for   3   min   and,   after   a   night   of    incubation,at   1552   G   for   23   min.   The   study   highlighted   that   there   was   nosignificant   difference   in   the   PDGF-AB   release.   The   TGF   B   secretionsignificantly   increased   in   all   the   groups,   except   when   time   was20   min.   The   VEGF   release   increased   in   all   the   groups,   without   anysignificant   difference   between   them.Arora   et   al.   [15]   concluded   that   the   best   protocol   was   208   G   for20   min,   because   the   increasing   centrifugation   force   leaded   to   aplatelet   aggregation   and   a   bad   release   of    growth   factors.The   aim   of    Eren’s   [16]   article   was   to   study   the   centrifugationtime   effect   on   the   growth   factors   release.   He   checked   the   plateletconcentration   and   the   growth   factors   rate   at   different   rest   times   on20   healthy   subjects   (1   h,   24   h   and   72   h),   using   2   protocols,   one   at2660   RPM   for   10   min   (Group   A)   or   12   min   (Group   B).   Thereferenced   platelet   concentration   was   235,3      52,3/ m L       10 3 ,theresult   for   the   group   A   was   218,7      50,1/ m L       10 3 and   for   the   group   B214,7      52,1/ m L       10 3 :   there   is   no   significant   difference. As   the   growth   factor   rate,   the   VEGF   rate   was   significantly   higherafter   centrifugation   during   12   min.This   study   showed   that   centrifugation   time   had   no   effect   onplatelet   concentration   and   growth   factors   other   than   VEGF.However   VEGF   being   very   important   in   the   tissue   healing   process,it   would   be   preferable   to   increase   the   centrifugation   time.Yin   et   al.   [17]   in   this   study   wanted   to   find   an   optimal   of    a   doublecentrifugation   in   80   volunteers   patients.For   the   first   centrifugation   he   studied   6   different   protocols(110   G   for   15   mn   (110      15),   130      10,   130      15,   160      10,160      15,   180      10).The   second   centrifugation   was   also   studied   by   6   variousprotocols   (180      10,   180      15,   250      10,   250      15,   450      10,450      15).The   platelet   concentration   of    PCP   obtained   using   160      10   wassignificantly   higher   than   that   of    PCP   obtained   using   110      15( P    <   0.001),   130      10   ( P    <   0.001),   160      15   ( P    <   0.001)   and180      10   ( P    <   0.001),   and   comparable   with   that   obtained   using130      15   ( P    >   0.999).   The   result   was   similar   for   leukocytes   andgrowth   factor   concentration.   Therefore,   160      10   was   designatedas   the   optimal   centrifugation   conditions   for   the   first   spin.The   second   spin   was   realized   in   the   sample   where   the   first   spinwas   160      10.   The   best   result   was   obtained   by   the   protocol250      15.   In   fact,   the   platelet   enrichment   factor   of    P-PRP   obtainedusing   250      15   was   significantly   higher   than   that   obtained   using180      10   ( P    <   0.001),   180      15   ( P    <   0.001)   and   250      10( P    <   0.001).   However,   the   platelet   enrichment   factor   did   notfurther   increase   by   preparation   using   450      10   ( P    >   0.999)   and450      15   ( P    >   0.999)   compared   with   250      15.   But250      15   allowed   to   have   a   concentration   of    growth   factor   moreimportant.   P-PRP   obtained   by   centrifugation   at   250      15   had   ahigher   level   of    PDGF-AB   compared   to   that   obtained   at   180      10( P    =   0.001),   180      15   ( P    =   0.028),   250      10   ( P    =   0.008),   450      10( P    =   0.011)   and   450      15   ( P    =   0.004)   (Table   1). 3.   Discussion Many   protocols   were   studied,   allowing   an   increase   of    the   PRPplatelet   concentration.   However,   it   is   important   to   distinguish   themethods   of    simple   and   double   centrifugation;   the   second   oneallowing   to   get   a   platelets   concentrated   plasma   with   a   longerpreparation.The   platelet   concentration   allowing   a   therapeutic   effect   isobtained   in   all   the   simple   centrifugation   protocols.Moreover   these   articles   also   show   that   the   platelets   are   fragilecells   and   whether   the   centrifugation   force   is   too   strong,   there   is   arisk   of    alteration   and   then   inefficiency.   However,   the   VEGFconcentration   increases   according   to   the   centrifugation   time.A   method   of    simple   centrifugation   would   then   be   a   goodcompromise.In   our   day-to-day   practice,   we   use   a   Sigma   centrifuge   and   aprotocol   of    simple   centrifugation   at   3000   RPM   (or   1350   G)   for3   min.A   new   method   described   by   Wu   [18]   would   allow   a   morestandardized   protocol,   with   a   shorter   preparation   time.   The   use   of ultrasounds   on   the   whole   blood   would   result   in   a   concentrationcomparable   to   that   of    centrifugation.PRP   indication   in   maxillofacial   surgery   is   also   contested.   Indeed,Betega   et   al.   [19]   shows   in   his   article   that   the   PRP   clinical   benefit   isnot   proven.   However,   in   2013,   Albanese   et   al.   [20]   studied   PRP   usein   several   maxillofacial   indications.   This   review   points   out   that   PRPuse   after   a   tooth   extraction   allows   to   improve   healing   but   does   notcontribute   to   bone   regeneration.   As   to   indication   in   periodontalsurgery,   the   results   are   heterogeneous.   The   review   also   showssatisfactory   results   in   pre-implant   and   implant   surgery,   dependingon   the   type   of    material   being   used.   This   interesting   outcome   is   alsonoted   in   osteonecrosis   mandibular   surgery.   Fornaini   et   al.   [21]states   a   case   with   PRP   treatment   in   osteonecrosis   mandibularsurgery.  Table   1 Summary   table   of    various   protocols.Study/Year   1 ST centrifugation   2 ND centrifugation   Platelet   concentrationRutkowski/2007   1350   G   for   10   min6   times   more   concentratedTamimi/2007   160   G   for   10   min400   G   for   10   min   630,2      10 3 / m L Mazzocca/2012   3200   RPM   for   15   min   873,8    207,2  10 3 / m L  Araki/2012   230   to   270   G   for   10   min   2330   G   for   10   min   7,4   higherBausset/2012   130   G   for   15   min250   G   for   15   min   3,96   times   higherOgundipe/2012   1000   RPM   for   10   min1200   RPM   for   10   min   11,8   times   higherFranco/2012   400   G   for   10   min800   G   for   10   min   8,5   times   higher Jo/2013   900   G   for   5   min1500   G   for   15   min   633,2    91,6  10 3 / m L 4,2   timeshigher Amable/2013   300G   for   5   min   700   G   for   17   min140   to   190      10 3 / m L Perez/2014   100   G   for   10   min400   G   for   10   min   5   times   higherSabarish/2015   1000   RPM   for   4   min   800   RPM   for   9   min3,5      10 8 1,6   times   higherArora/2016   208   G   for   20   min1552   G   for   23   min   87%   relative   platelet   concentrationEren/2016   2660   RPM   for   12   min   214,7    52,1/ m L   10 3 Yin/2017   160   G   for   10   min250   G   for   15   min   More   1250      10 9 /L  B.Croise´  et    al.    /     J    Stomatol   Oral   Maxillofac    Surg     xxx   (2019)    xxx–xxx 4 GModel JORMAS-715;   No.   of    Pages   5 Please   cite   this   article   in   press   as:   Croise´ B,   et   al.   Optimized   centrifugation   preparation   of    the   platelet   rich   plasma:   Literature   review.    JStomatol   Oral   Maxillofac   Surg   (2019),
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