Abst ract
Submitted: September 2, 2016
0RGL¿HG)HEUXDU\
Accepted: March 11, 2017
Fact or s affect ing t he per iapical healing
pr ocess of endodont ically t r eat ed
t eet h
Tissue r epair is an essent ial pr ocess t hat r eest ablishes t issue int egr it y
and r egular funct ion. Never t heless, differ ent t herapeut ic fact or s and clinical
condit ions m ay int er fer e in t his pr ocess of per iapical healing. This r eview
aim s t o discuss t he im por t ant t herapeut ic fact or s associat ed w it h t he clinical
pr ot ocol used dur ing r oot canal t r eat m ent and t o highlight t he syst em ic
condit ions associat ed w it h t he per iapical healing pr ocess of endodont ically
t r eat ed t eet h. The ant ibact er ial st rat egies indicat ed in t he convent ional
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host ’s im m une r esponse m ay assist in t issue r epair, if w ound healing has
been hinder ed by infect ion. Syst em ic condit ions, such as diabet es m ellit us
and hy per t ension, can also inhibit w ound healing. The success of r oot
canal t r eat m ent is affect ed by t he cor r ect choice of clinical pr ot ocol. These
fact or s ar e dependent on t he sanit izat ion pr ocess ( inst r um ent at ion, ir r igant
solut ion, ir r igat ing st rat egies, and int racanal dr essing) , t he apical lim it of
t he r oot canal pr eparat ion and obt urat ion, and t he qualit y of t he sealer.
The challenges affect ing t he healing pr ocess of endodont ically t r eat ed t eet h
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sim ult aneous neut ralizat ion of unpr edict able pr ovocat ions t o t he per iapical
t issue. Along w it h t hese fact or s, one m ust under st and t he local and general
clinical condit ions ( syst em ic healt h of t he pat ient ) t hat affect t he out com e
of r oot canal t r eat m ent pr edict ion.
Ke y w or ds: Root canal t herapy. Per iapical per iodont it is. Endodont ics.
Clinical pr ot ocols.
Roberto HOLLAND1
João Eduardo GOMES FILHO1
Luciano Tavares Angelo CINTRA1
Índia Olinta de Azevedo QUEIROZ1
Carlos ESTRELA2
http://dx.doi.org/10.1590/1678-7757-2016-0464
1Universidade Estadual Paulista, Faculdade de Odontologia de Araçatuba, Departamento de Odontologia Restauradora, Araçatuba, SP, Brasil.
2Universidade Federal de Goiás, Faculdade de Odontologia, Departamento de Ciências Estomatológicas, Goiânia, GO, Brasil.
Corresponding address: João Eduardo Gomes Filho Departamento de Odontologia Restauradora. Faculdade de Odontologia de Araçatuba. Univ. Estadual Paulista R. José Bonifácio, 1193 - Vila Mendonça - 16015-050
I nt r oduct ion
The pr ocess of healing depends on t he st r uct ural
an d f u n ct ion al r eplacem en t of t h e ar eas af f ect ed
by int r insic or ex t r insic fact or s. I t can involve t he
r e p a i r a n d r e g e n e r a t i o n o f t h e a f f e ct e d si t e1 8.
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t hat occur s in vascular ized t issue. Connect ive t issue
inv olv es a pr ocess of r epair v ia t h e f or m at ion of
granulat ion t issue, w her eas non- connect ive t issue,
such as t hat of t he glandular organs, sm oot h m uscles,
skelet al m uscles and per ipheral ner ves, involves t he
p r olif er at ion , an d t h er ef or e, r eg en er at ion , of t h e
rem aining t issue18. These t wo processes are dependent
upon t he r egenerat ive capacit y of t he affect ed cells,
t he ex t ent of t he affect ed sit e, and t he pr oliferat ive
act iv it y of t he st r om al t issue. Regenerat ion involves a
pr ocess of t issue r enewal w it h cells t hat have sim ilar
charact er ist ics t o t hose t hat w er e pr ev iously lost ; it is
t he m orphological and funct ional rest orat ion of t issue.
Conver sely, r epair is charact er ized by t he for m at ion
of connect ive t issue at t he sit e of t he lesion, and t he
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of t he im m unogen t hat induces t he t issue r esponse10.
Com plet e r epair only occur s once t he ant igen has
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Du r in g p u lp in f ect ion , t h e occlu d ed b lood su p p ly
of t h e r oot can al becom es con du civ e t o bact er ial
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per iapical r egion is elicit ed t o neut ralize t he ant igen.
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im m une cells, w hich ar e t hen or ganized int o a bar r ier
t o sequest er t he infect ion.
Bone r esor pt ion and bone for m at ion ar e pr ocesses
involv ing t he act iv it y of ost eoclast s, ost eoblast s, and
ost eocyt es; t hey are affect ed by t he syst em ic and local
condit ions66. How ever, bone hom eost asis is disr upt ed
dur ing apical per iodont it is, w hich pr om ot es incr eased
rat es of bone r esor pt ion.
I deally, cases of apical per iodon t it is sh ou ld be
charact erized by a repair process t hat is asym pt om at ic
in nat ur e, an absence of radiographic abnor m alit ies
in t he per iradicular t issues, and ev idence of biological
sealin g ( cem en t sealin g t h e f or am in a) , or by t h e
SUHVHQFHRID¿EURXVFDSVXOHZLWKWKHLQ¿OWUDWLRQRIIHZ LQÀDPPDWRU\FHOOV54. Thus, t he applicat ion of clinical p r ot ocols sh ou ld con sid er t h e local an d sy st em ic
condit ions t hat cont ribut e t owards t he healing process.
Th i s r e v i e w a i m s t o d i s c u s s t h e i m p o r t a n t
t herapeut ic fact or s under ly ing t he clinical pr ot ocols
used dur ing a r oot canal t r eat m ent . Addit ionally, w e
w ill analy ze local and sy st em ic condit ions associat ed
w it h t he per iapical healing pr ocess of endodont ically
t r eat ed t eet h.
Th er ap eu t ic f act or s t h at af f ect t h e r ep air
pr ocess
Biochem ical pr epar at ion
Ro o t ca n a l sh a p i n g i s a n i m p o r t a n t st e p i n
endodont ic t herapy t o achieve t he apical healing and
t he cleaning and m odeling of t he r oot canal sy st em .
How ever, t he com plex r oot canal anat om y, associat ed
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t he shape, and t he posit ion of t he apical foram ina,
can int er fer e and hinder t he r oot canal shaping and
cleaning79.
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t he developm ent of new inst r um ent s m ade of
nickel-t inickel-t an iu m ( NiTi) alloy s ( r onickel-t anickel-t or y an d r ecip r ocanickel-t in g
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cleaning and shaping of r oot canals by r educing t he
inst rum ent at ion t im e and by keeping t he original canal
shape5,35,88. Besides, r educt ion of t he occur r ence of
zips, ledges, perforat ions, and t ransport ing of t he root
canals, especially in nar r ow and cur ved canals35,88,
w er e also obser ved aft er using t hose inst r um ent s.
Despit e all t hese im pr ov em ent s, t he possibilit y of
fract ur e of NiTi inst r um ent s, m ainly in r oot canals
w it h sever e cur vat ur es, has been found76,82. Mor eover,
Panit v isai, et al.75 ( 2010) show ed no r educt ion on t he
pr ognost ic of endodont ic t r eat m ent w hen a fract ur ed
inst r um ent fragm ent is left w it hin a r oot .
I nvest igat ions com par ing t he m anual, r ot ar y, and
r ecipr ocat ing sy st em s and t he associat ion bet w een
t hem hav e been ex t ensiv ely per for m ed5 , 3 5 , 8 8. Azar,
et al.4 ( 2 0 1 2 ) r ep or t ed n o sig n if ican t d if f er en ces
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inst rum ent s. Besides, evaluat ion of t he apical bact erial
ex t r u si on p r om ot ed b y r eci p r ocat i n g an d r ot ar y
inst r um ent at ion show ed t hat bot h sy st em s ex t r uded
b act er ia b ey on d t h e f or am en ; n ev er t h eless, t h e
r ecipr ocat ing show ed lesser ex t r usion t han t he r ot ar y
sy st em107$GGLWLRQDOO\QRGLIIHUHQFHVLQWKHHI¿FDF\ of r ot ar y an d r ecipr ocat in g sy st em s for r em ov in g
sy st em s in associat ion w er e able t o r em ove a lar ge
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cur ved canals84.
Subram aniam , et al.97 ( 2013) show ed t hat bot h
m an u al an d r o t at o r y i n st r u m en t at i o n w er e ab l e
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r oot canals of pr im ar y m olar s. Meanw hile, bact er ia
w er e det ect ed in r oot can als of t eet h w it h apical
per iodont it is befor e and aft er t he use of hand and
r ot ar y NiTi in st r u m en t at ion an d n o d if f er en ce in
bact er ial r educt ion in infect ed canals aft er using bot h
inst r um ent s was obser ved83. Fur t her m or e, Pinheir o,
et al.80 ( 2012) com par ed t he cleaning effect iveness of
m anual, hybrid, and rot ary inst rum ent at ion t o rem ove
Ent er ococcus faecalis fr om pr im ar y m olar t eet h. The
aut hor s found t hat all t echniques w er e able t o r educe
t he num ber of Ent er ococcus faecalis; t hus, hy br id
in st r u m en t at ion sh ow ed t o bet t er r edu ct ion w h en
com par ed w it h m anual.
Th er ew it h , ev en w it h t h e im pr ov em en t on t h e
biom echanical pr eparat ion of r oot canal sy st em using
NiTi in st r u m en t s, b act er ia can su r v iv e an d g r ow
LQVLGHURRWFDQDOV\VWHPVRURQDSLFDOELR¿OP47,83,105, com pr om ising t he per iapical t issue r epair. Ther efor e,
t he com plet e r epair depends on t he associat ion of an
effect ive ir r igat ing solut ion, int racanal dr essing, and
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I r r igat ing solut ions
Root canal t r eat m ent ( RCT) r equir es t he use of
ir r igat ing solut ions t o pr ov ide an ant im icr obial effect ,
r em ove debr is, and neut ralize t he pr esence of or ganic
com pounds. Because of t he risk of periapical ext rusion
v ia t he apical foram en, ir r igat ing solut ions should
be biocom pat ible and non- ir r it at ing t o t he per iapical
t issue37,58,94.
Th e per sist en ce of bact er ial in fect ion follow in g
r oot canal pr eparat ion r eveals t he lim it at ions of t he
ir r ig at in g solu t ion s, su ch as sod iu m h y p och lor it e
( NaOCl) and chlorhexidine ( CHX) . These solut ions can
only r educe t he m icr obial populat ion and, t her efor e,
cannot ent ir ely elim inat e it . The sanit izat ion pr ocess
consist s of t he disinfect ion and enlar gem ent of t he
r oot canal v ia t he act ion of sodium hy pochlor it e and
t h e in st r u m en t at ion t ech n iqu es of t h e r oot can al,
r espect ively. Fur t her m or e, t hese pr ot ocols r educe t he
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t he int racanal dr essing and incr eases t he success rat e
of t he endodont ic t r eat m ent22.
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of Ent er ococcus faecalis infect ion was discussed in
a sy st em at ic r ev iew an d m et a- an aly sis2 3. Sodiu m
hy pochlor it e is a com m only used endodont ic ir r igant
because of it s ant ibact er ial pr oper t ies and it s abilit y
t o dissolve or ganic t issue21,50,103.
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b ased on it s p h y sicoch em ical p r op er t ies an d it s
r eact ion w it h or ganic t issue21,50. Sodium hy pochlor it e
act s as a solvent for or ganic com pounds and lipids;
it degrades fat t y acids int o t he pr oduct s of fat t y acid
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r eact ion . Th is r edu ces t h e su r f ace t en sion of t h e
r em aining solut ion. Fur t her m or e, NaOCl is able t o
cause am ino acids t o undergo a neut ralizat ion react ion
t o for m wat er and salt . Sim ilar ly, hy pochlor ous acid
( HOCl) act s as solv ent in t he pr esence of or ganic
t issue, and r eleases chlor ine; t his com bines w it h t he
am ine gr oup of t he pr ot ein and for m s chloram ines,
in a ch lor in at ion r eact ion . Hy poch lor ou s acid an d
h y p och lor it e can u n d er g o a r eact ion w it h am in o
acids, w hich w ould r esult in t heir degradat ion and
hydrolysis. The chlorinat ion react ion bet w een chlorine
and t he am ine gr oup ( - NH2) r esult s in t he pr oduct of
chloram ines, w hich int er fer e w it h cell m et abolism .
Ch lor in e is a st r on g ox idan t ; it h as an t im icr obial
pr oper t ies, and is able t o inhibit bact er ial enzy m es.
This r esult s in t he ir r ever sible ox idat ion of sulfhydr y l
( - SH) gr oup, w hich is essent ial for t he funct ion of
bact er ial enzy m es21,50.
Fr ou gh - Rey h an i, et al.2 6 ( 2 0 1 6 ) ev alu at ed t h e
ant im icr obial act iv it y of 1% , 2.5% , and 5% NaOCl
solut ion in t he t r eat m ent of Ent er ococcus faecalis
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t hat 2.5% and 5% NaOCl com plet ely elim inat ed t he
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r esist ant t o 1% NaOCl. I n an in vit r o st udy, Siqueira,
et al.95 IRXQGQRGLIIHUHQFHLQWKHHI¿FDF\RI
t he ant ibact er ial act iv it y of 1% , 2.5% , and 5% NaOCl
solut ion. Mor eover, r egar dless of t he concent rat ion,
NaOCl w as also in ef f ect iv e in t h e r em ov al of t h e
sm ear layer for m ed dur ing r oot canal pr eparat ion;
t h e sm ear lay er im pair s t h e clean in g of t h e r oot
canal sy st em59. Reinfect ion of t he r oot canal sy st em
af t er in st r u m en t at ion h as b een r ep or t ed8 3. Teet h
w it h per iapical lesions and a higher concent rat ion
of en dot ox in s h av e also been det ect ed3 6. Sodiu m
hy pochlor it e solut ions can inhibit t he act ion of cer t ain
t hem74.
The sm ear layer is t he m at er ial t hat is at t ached
t o t he canal walls dur ing r oot canal pr eparat ion. I t is
com posed of dent in, r em nant s of pulp t issue ( or ganic
and inor ganic com ponent s) , chem ical r esidues, and
m icroorganism s. The use of EDTA and NaOCl solut ions
has been show n t o be m or e effect ive t o r em ove t he
sm ear layer104.
Ner y, et al .7 3 ( 2 0 1 1 ) r ep o r t ed si m i l ar r esu l t s
follow ing t he use of 1% and 2.5% NaOCl solut ion
dur ing t he endodont ic ir r igat ion of canine t eet h. The
incidence of pulp necr osis and apical per iodont it is was
report ed and t reat ed in one session. Therefore, t he use
of 1% and 2.5% NaOCl solut ion had sim ilar t r eat m ent
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is pr efer r ed for clinical pur poses because of it s m or e
st able nat ur e.
Re c e n t l y, n e w a n t i m i c r o b i a l a p p r o a c h e s t o
disinfect ion of root canals have been proposed, such as
phot odynam ic t herapy ( PDT) , a t herapy t hat com bines
t he associat ion bet w een a phot osensit izer dye and a
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st im ulat ed em ission of radiat ion) or Led ( light em it t ing
diode) . The singlet oxygen, which is responsible for t he
disr upt ion of t he bact er ial m em brane and inact ivat ion
of en d ot ox in s, p r om ot es an t im icr ob ial act ion6 7 , 9 2.
Several invest igat ions have been r epor t ing t hat PDT
r educes t he num ber of bact er ia fr om r oot canal30,61,108
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solu t ion t o elim in at e En t er ococcu s f aecalis1 1 4 , 1 1 5.
I n addit ion , Vazir i, et al.1 1 0 ( 2 0 1 2 ) fou n d t h at t h e
com binat ion of PDT and 2.5% NaOCl solut ion was m ore
ef f ect iv e again st En t er ococcu s f aecalis. Mor eov er,
Bor sat t o, et al.7 ( 2016) evaluat ed t he r esponse of
t he apical and per iapical t issues of canine t eet h w it h
apical per iodont it is aft er one session w it h and w it hout
an t i m i cr ob i al p h ot od y n am i c t h er ap y ( aPDT) an d
com pared it wit h t wo sessions using calcium hydroxide
as int racanal dr essing. They show ed t hat t he bet t er
repair and sm all periapical lesions were associat ed wit h
t he t w o sessions using calcium hydr ox ide.
Th u s, d esp i t e a l l o f t h ese n ew a n t i m i cr o b i a l
m et h o d s, NaOCl so l u t i o n s ar e st i l l t h e g r eat est
choice for clinical pr ocedur e due t o t heir effect iv e
an t im icr obial pot en t ial. Mor eov er, becau se of t h e
inst abilit y of t hese solut ions, especially during st orage
and t ranspor t at ion t im e, t he 1% NaOCl solut ion m ay
not be effect ive; t hus, t he 2.5% NaOCl solut ion is t he
m ost r ecom m ended.
I nt racanal dr essing
Several t y pes of m edicat ion have been developed
an d u sed as in t r acan al d r essin g5 1. How ev er, t h e
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t his has cont ribut ed t owards t he increasing preference
am on g p r of ession als t o p er f or m RCT in a sin g le
session34, 68, 77, 81. Addit ionally, t he pract ice of
single-appoint m ent endodont ics, as opposed t o m ult
iple-appoint m ent endodont ics, has been encouraged by
t he negligible differ ences in t he t r eat m ent out com es
b et w een t h e t w o, w h i ch i n cl u d e a n a b sen ce o f
post operat ive pain and t he clinical and radiographic
repair77,78 of t eet h. Conversely, st udies assessing canine
t eet h have r epor t ed super ior r esult s w it h t he pract ice
of m ult iple- appoint m ent endodont ic t r eat m ent54,64.
I n an at t em pt t o fur t her clar ify t his issue, Holland,
et al.54 ( 2003) conduct ed a st udy using canine t eet h
as a m odel. These specim ens w er e charact er ized by
a necr ot ic pulp and had per iapical lesions t hat w er e
t r eat ed in eit her one or t w o appoint m ent s. The t eet h
t hat w er e t r eat ed in t w o appoint m ent s r eceived a
course of calcium hydroxide int racanal dressing for 7 or
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were evaluat ed for six m ont hs aft er t he t reat m ent . The
aut hors observed t hat t he use of calcium hydroxide for
7 or 14 day s obt ained bet t er r esult s t han t he
single-appoint m ent endodont ic t reat m ent . Furt herm ore, t hey
at t r ibut ed t he r epair pr ocess obser ved aft er t he single
appoint m ent t o t he alk aline pH of Sealapex ; once t he
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r esult s t han t he ot her sealer s t hat w er e used in t eet h
w it h apical per iodont it is63,64.
Geor gopoulou, et al.33 ( 1993) r epor t ed t hat t he
calciu m h y d r ox id e in t r acan al d r essin g w as m or e
effect ive against anaer obic bact er ia t han t he use of
cam phorat ed param onochlor ophenol. The high pH of
calcium hydr ox ide, due t o t he r elease of hydr ox ide
ions, is capable of alt er ing t he st r uct ural int egr it y of
t he cy t oplasm ic m em brane of bact er ia24. Addit ionally,
t he calcium hydr ox ide had an indir ect effect on t he
anaer obic m icr oor ganism s of t he r oot canal because
of t he r eact ion bet w een calcium ion and aqueous
car bon diox ide24. Calcium hydr ox ide also r esult s in
t he degradat ion of bact er ial lipopoly sacchar ides1,24.
The biological and ant im icr obial act ion of calcium
hydr oxide is based on it s dissociat ion int o calcium and
hydr ox ide ions, and on t he act ion of t hese ions on
t issues and bact er ia24. Calcium hydr ox ide induces t he
periodont al connect ive t issue54. I t s act ion on connect ive
t issu e ( pu lpal an d per iodon t al t issu es) st im u lat es
PLQHUDOL]DWLRQ IURP WKH VLJQL¿FDQW LQYROYHPHQW RI DONDOLQHSKRVSKDWDVHDQG¿EURQHFWLQ54,71.
Nair, et al.7 2 ( 2 0 0 5 ) ev alu at ed t h e in t r acan al
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pr im ar y apical per iodon t it is, in h u m an s, follow in g
single- appoint m ent endodont ic t reat m ent . The result s
show ed t he anat om ical com plex it y of t he r oot canal
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t he ineffect iveness of cont em porar y inst r um ent s and
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only one appoint m ent . This was m ost ly at t r ibut able
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of t he canal sy st em . Ther efor e, t o achieve a highly
favorable long- t erm prognosis of t he RCT, t he st ringent
applicat ion of all nonant ibiot ic and chem om echanical
m easur es m ust be t aken t o t r eat t eet h w it h infect ed
and necr ot ic r oot canals; addit ionally, t hese m easur es
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t o m inim ize t he int raradicular m icr obial load.
The challenges affect ing a successful r oot canal
pr eparat ion include t he follow ing fact or s: com plex
anat om y ; num ber of canals; cur vat ur es; r oot canal
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w hich com plicat es cleaning22,79. Ther ew it h, t o achieve
a com plet e r oot canal cleaning, an int racanal dr essing
m u st b e u sed . Th u s, t h e b iolog ical p r op er t ies of
calcium hydroxide, as well as it s ant im icrobial capacit y
t o induce t he deposit ion of a har d t issue, pr om ot ing
a bet t er r epair, m ak e it t he int racanal m edicat ion
r ecom m ended dur ing t he RCT.
5RRWFDQDO¿OOLQJ
Th e goal of r oot can al obt u r at ion is t o obt ain
com plet e sealing in order t o hinder t he com m unicat ion
bet w een t he r oot canal and t he per iapical t issue. This
favor s t he pr ocess of apical and per iapical r epair aft er
endodont ic t herapy53.
An ideal r oot canal sealer m ust have adequat e
p h y sical, ch em ical, an d b iolog ical p r op er t ies3 1 , 8 6.
Several fact ors can affect t he success of RCT, including
t he t y pe and com posit ion of sealer ut ilized31,57,86. The
pr esence and r elease of subst ances fr om t he sealer s
can cause differ ent r eact ions w hen in cont act w it h
t issue86.
7KHUHDFWLRQEHWZHHQFDOFLXPR[LGHDQGWLVVXHÀXLG
w as pr ev iously descr ibed55. This r eact ion pr oduces
calciu m hy dr ox ide, w h ich dissociat es in t o calciu m
and hydr ox ide ions in t he pr esence of wat er. Calcium
ions t hen r eact w it h aqueous car bon diox ide w it hin
t h e t issu e t o f or m cr y st als of calciu m car bon at e,
w hich subsequent ly st im ulat e t he deposit ion of har d
t issue ( Figur e 1) . Ther efor e, r oot canal sealer s t hat
cont ain calcium hydr oxide or calcium oxide have been
clinically used.
Th e t issu e r espon se t o Sealapex , CPM Sealer,
and MTA Fillapex , w hich cont ain in t heir com posit ion
calcium hydr oxide or calcium oxide, w er e evaluat ed in
t he subcut aneous t issue of rat s. The r esult s show ed
WKDW DOO VHDOHUV LQGXFHG D PRGHUDWH LQÀDPPDWRU\
r esponse at 7 and 15 day s, w hich r esolved over t im e.
I n addit ion, all sealer s w er e capable of st im ulat ing t he
deposit ion of m ineralized t issue42,44. Anot her st udy43
HYDOXDWHGWKHHI¿FDF\RI5&7XVLQJWKHDIRUHPHQWLRQHG
sealer s, in canine t eet h, follow ing a single session of
endodont ic t r eat m ent . I ncom plet e per iapical t issue
r epair was r epor t ed, and t he sealer s w er e capable of
cont r olling t he r oot canal infect ion r egar dless of t he
differ ences in t heir ant im icr obial act iv it y20,101. The use
of Sealapex and MTA Fillapex r esult ed in a sim ilar seal
and had a bet t er r esponse t han t he use of CPM Sealer.
This was pr obably due t o t he fact t hat bot h sealer s
SURGXFHGOHVVRIDQLQÀDPPDWRU\UHDFWLRQWKHUHIRUH
Figure 1-$3UHVHQFHRIG\VWURSKLFFDOFL¿FDWLRQRQWKHWXEHRSHQLQJ%3UHVHQFHRIELUHIULQJHQWVWUXFWXUHVH[SRVHGE\SRODUL]HGOLJKW
they have been formed by the reaction between the calcium ions derived from the material and the carbonic gas released from the tissues
show ing t heir biocom pat ible nat ur e40.
Fur t her m or e, even w it h t he use of biocom pat ible
sealer s, w hich ar e capable of inducing m ineralizat ion,
com plet e repair is only possible wit h t he disinfect ion of
t he r oot canal sy st em . Ther efor e, an im pr oved r epair
pr ocess follow ing RCT is pr om ot ed by t he com plet e
cleaning of t he r oot canal, as w ell as by t he use of an
int racanal dr essing, such as calcium hydr ox ide.
Apical lim it of obt urat ion
Sy st em at ic r ev iew s have show n t hat r oot canal
preparat ion and obt urat ion inferior t o t he radiographic
apex ( r oot canal obt urat ion at 1- 2 m m infer ior t o t he
apex) w er e associat ed w it h a bet t er pr ognosis ( higher
success rat es)87.
St udies evaluat ing t he success of endodont ically
t r eat ed t eet h sh o w ed t h at ov er f i l l s d el ay ed t h e
a p i ca l r e p a i r p r o ce ss5 2 , 9 9 , 1 0 0; t h e a p i ca l l i m i t o f
REWXUDWLRQFDQDIIHFWWKH¿QDORXWFRPHRIHQGRGRQWLF
t r eat m ent100 ,Q DGGLWLRQ WKH ¿QGLQJV REVHUYHG LQ hist ological invest igat ions cor r oborat e t hese clinical
and radiographic st udies52 ( Figur e 2 and Figur e 3) .
Evidence has show n t hat t he t ype of sealer applied
can also affect t he r epair pr ocess. Suzuk i, et al.99
( 2011) invest igat ed t he effect s of endom et hasone as
D¿OOLQJPDWHULDOLQFDQLQHWHHWKDQGIRXQGWKDWQRQHRI WKH¿OOLQJOLPLWVLQIHULRURUDERYHWKHDSLFDOIRUDPHQ
pr om ot ed t he com plet e r epair of t he per iapical t issue.
)XUWKHUPRUHWKHSUHVHQFHRIDQLQWHQVHLQÀDPPDWRU\ LQ¿OWUDWHZDVDOVRREVHUYHGLQWKHFDVHVRIRYHU¿OOLQJ
Sim ilar r esult s w er e also obt ained w it h EndoRez w hen
HYDOXDWHG DV D ¿OOLQJ PDWHULDO LQ FDQLQH WHHWK1 0 0, t her efor e cor r oborat ing t he st udies t hat show ed high
t ox icit y8 an d t h e pr esen ce of m oder at e t o sev er e
LQÀDPPDWRU\UHDFWLRQVLQLQWUDRVVHRXVLPSODQWV96. How ever, even t he use of biocom pat ible m at er ials,
VXFKDV07$ZKHQXVHGDV¿OOLQJEH\RQGWKHOLPLWRI
t he apical foram en, show ed unsat isfact or y r esult s52;
WKLVVXJJHVWHGWKDWRYHU¿OOLQJVKRXOGEHDYRLGHG
Expansion of t he apical foram en
5RRWFDQDOFOHDQLQJZLWKWKHXVHRIÀH[LEOH¿OHV
is r ecom m en ded f or t h e en dodon t ic t r eat m en t of
necr ot ic t eet h; addit ionally, t he apical const r ict ion is
m aint ained. This procedure, which is also referred t o as
apical pat ency, is com m on; it prevent s t he com pact ion
of dent in chips int o t he foram en and helps t he local
elim inat ion of m icr oor ganism s t hat inhibit t he pr ocess
of r epair follow ing endodont ic t r eat m ent . How ever,
st udies on canine t eet h w it h per iapical lesions show ed
t hat opt im al r esult s w er e obt ained w hen t he apical
foram en was ex panded t o a gr eat er ex t ent t han t he
pat ency inst r um ent6.
The enlar gem ent of t he apical foram en affect s
t he healing of chr onic per iapical lesions6. Accor ding
t o som e aut hor s, t he com pact ion of debr is int o t he
apical t h ir d of t h e r oot can al sh ou ld be r em ov ed
m echanically106, w hile ot her s believe t hat it can be
r em oved w it h t he use of abundant ir r igat ion52,and
t hat t he infect ion could be addit ionally elim inat ed
w it h t he use of an int racanal dr essing54. Mor eover,
t he enlar gem ent of t he foram en appear ed t o hinder
Figure 2-3URFHVVRIREWXUDWLRQIURPWKHDSLFDOOLPLWDQHZFHPHQWVHDOLQJWHFKQLTXHLQWKHDSLFDOIRUDPHQLQFORVHFRQWDFWZLWK6HDODSH[
t he apical seal39.
Apical pat ency is an im por t ant fact or det er m ining
t he success of endodont ic t r eat m ent ; nonet heless,
fur t her r esear ch concer ning t he enlar gem ent of t he
foram en is r equir ed.
Syst em ic fact or s t hat int er fer e in t he r epair
pr ocess
The r epair of apical per iodont it is in endodont ically
t r eat ed t eet h depends on differ ent t herapeut ic fact or s
and clinical condit ions19,65,89. Selt zer90 ( 1988)correlat es
t he local and syst em ic fact ors affect ing t he endodont ic
r epair pr ocess, and suggest s t hat t he failur e of t he
endodont ic t r eat m ent m ay be beyond t he dent ist ’s
cont r ol. Local fact or s include: infect ion; hem or r hage,
t issu e in j u r y ; occlu sion of t h e blood su pply ; an d
pr esence of for eign bodies. Sy st em ic fact or s include:
n u t r i t i o n ; st r e ss; st a t e o f ch r o n i c d e b i l i t a t i o n ;
h or m on es; v it am in in t ak e; dehy dr at ion ; an d age.
Th er ew it h , t h is r ev iew also aim s t o d iscu ss t h e
associat ion bet w een som e sy st em ic condit ions, such
as diabet es m ellit us, hy per t ension, and ost eopor osis,
and t he per iapical healing pr ocess of endodont ically
t r eat ed t eet h.
Chr onic condit ions
Diabet es
Diabet es m ellit us ( DM) is a m et abolic disor der
charact erized by hyperglycem ia result ing from a defect
in t h e secr et ion of in su lin an d/ or t h e im pair m en t
of it s act ion3. St udies hav e been em phasizing t he
r elat ionship bet w een DM and oral diseases29, 48, 65, 89.
Fouad25 ( 2003) show ed t hat DM m ay be a m odulat ing
f act or of en d od on t ic in f ect ion s, an d t h at it m ay
com pr om ise t he healing pr ocess of per iapical t issues.
Th e asso ci at i o n b et w een p er i o d o n t al d i sease
and t he incidence of DM has been r epor t ed in som e
st udies48; however, few st udies have suggest ed t hat t he
incidence of DM was com orbid wit h endodont ic disease.
Cint ra, et al.12VWXGLHGWKHLQÀXHQFHRIDSLFDO periodont it is and periodont al disease by exam ining t he
concent rat ion of glycosy lat ed hem oglobin ( HbA1c) in
norm oglycem ic and hyperglycem ic rat s. They observed
t hat t he incidence of endodont ic infect ions t hat w er e
eit her isolat ed or associat ed w it h per iodont al disease
had affect ed t he glycem ic cont rol, especially in diabet ic
rat s. This result ed in an increase in bot h blood glucose
and HbA1c levels.
I n anot her st udy14, t he r elat ionship bet w een t he
EORRGSUR¿OHDQGWKHKLVWRORJLFDO¿QGLQJVRIWKHFDVHV
involv ing apical per iodont it is and per iodont al disease
asso ci at ed w i t h d i ab et es w as ex am i n ed . I n t h e
pr esence of oral infect ion, t he aut hor s obser ved an
incr ease in t he num ber of neut r ophils, ly m phocy t es,
an d leu k ocy t es, as w ell as sig n if ican t st at ist ical
differ ence bet w een t he diabet ics and t he diabet ics
wit h endodont ic and periodont al infect ion. Hist ological
¿QGLQJV VKRZHG DQ H[DFHUEDWLRQ RI LQÀDPPDWLRQ ZLWK WKH FRQVHTXHQW LQFUHDVH LQ LQÀDPPDWRU\ FHOO LQ¿OWUDWLRQDQGERQHUHVRUSWLRQLQGLDEHWLFUDWV
The r elat ionship bet w een endodont ic infect ions
an d t h e in t er act ion w it h sy st em ic diseases is n ot
Figure 3- Obturation over the apical limit showing the absence of new cement sealing the apical foramen in close contact with Sealapex.
clear. Hy per glycem ia elevat es t he levels of sy st em ic
LQÀDPPDWRU\PDUNHUV48 and alt ers t he various funct ions of t he im m une sy st em91,102, including t he r elease of
i n f l am m at o r y m ed i at o r s. Ci n t r a, et al .1 3 ( 2 0 1 4 )
cor r elat ed t he ser um levels of int er leuk in- 17 ( I L- 17)
DQG WKH LQ¿OWUDWLRQ RI QHXWURSKLOV LQ WKH SUHVHQFH
of apical per iodon t it is an d/ or per iodon t al disease
in diabet ic rat s. They found t hat t he com or bidit y of
bot h diseases incr eased t he ser um levels of I L- 17
r egar dless of t he diabet ic condit ion. Fur t her m or e, an
incr ease in t he neut r ophil populat ion was obser ved in
diabet ic rat s.
Hy p e r g l y ce m i a r e su l t i n g f r o m D M p r o m o t e d
m olecular and cellular effect s t hat can pr edispose
i n d i v i d u a l s t o sy st e m i c co m p l i ca t i o n s, su ch a s
t h e d y sf u n ct i o n a n d f a i l u r e o f v a r i o u s o r g a n s3.
Nephr opat hy is one of t he chr onic com plicat ions of
DM, and a possible r elat ionship t o per iodont al disease
has been r epor t ed49.
Ba se d o n a p r e v i o u s st u d y1 5, a r e l a t i o n sh i p
bet w een t he per iapical lesions and/ or t he pr esence
of p er iod on t al d isease an d t h e ser u m cr eat in in e
levels in diabet es was also suggest ed. An incr ease
in cr eat inine lev els w as obser v ed in diabet ic rat s;
t h e lev els w er e elev at ed in t h e p r esen ce of or al
infect ion. This suggest ed t hat a high glycem ic increase
m ay pr edispose indiv iduals t o r enal disor der s. An
addit ional invest igat ion was perform ed t o evaluat e t he
t r iglycer ide and cholest er ol levels in diabet ic rat s. The
r elat ionship bet w een t hese fact or s and t he incidence
of pulpal and periodont al diseases was t hen exam ined;
it was obser ved t hat t he isolat ed cases of per iodont al
infect ion, or it s associat ion w it h endodont ic infect ions,
led t o an incr ease in t he t r iglycer ide levels of diabet ic
rat s. How ever, t he differ ence in t he cholest er ol levels
ZDVQRWVLJQL¿FDQW16.
Alt erat ions in t he healt h of t he skelet al sy st em
w er e also associat ed w it h diabet es113. The cont r ol of
LQÀDPPDWLRQLVHVVHQWLDOLQWKHERQHUHSDLUSURFHVV4.
6\VWHPLF LQÀDPPDWLRQ ZKLFK LV SURPRWHG E\ '0
can lead t o a pr olon ged h ealin g t im e in t h e case
of f r act u r es1 7. Pr ev iou s st u d ies3 8 , 4 1 ev alu at ed t h e
m ineralizat ion capacit y and t issue r esponse of MTA
cem ent and t w o endodont ic sealer s, MTA Fillapex and
Sealapex, using a diabet ic m odel. The t issue r esponse
of t hese sealer s was unaffect ed by t he incidence of
DM ( Figur e 4) .
Hyper t ension
H y p e r t e n s i o n i s a c h r o n i c d i s o r d e r t h a t i s
ch ar act er ized by an in cr eased per iph er al vascu lar
UHVLVWDQFHWREORRGÀRZ,WLVDWWULEXWDEOHWRYDVFXODU
rem odeling, and elevat es blood pressure in art eries111.
Th e r e l a t i o n sh i p b e t w e e n h y p e r t e n si o n a n d
calcium loss in bones has been show n in clinical and
ex per im ent al st udies32,109. Likew ise, t he alt erat ion in
t he act iv it y and differ ent iat ion of bone cells obser ved
in p at ien t s h as b een r elat ed t o t h e in cid en ce of
hy per t ension60. I t has been cor r elat ed w it h elevat ed
blood pr essur e, incidence of dent al pr oblem s ( such
as per iodont al disease56,62) , high rat e of im plant loss
due t o defect s in t he pr ocess of osseoint egrat ion2,and
GLI¿FXOWLHVLQERQHKHDOLQJIROORZLQJWRRWKH[WUDFWLRQV69. Periodont al disease and chronic apical periodont it is
VKRZHGVLPLODULQÀDPPDWRU\SURFHVVHV)XUWKHUPRUH
pat ient s w it h sy st em ic diseases m ay have a r educed
r esist ance t o bact er ial infect ion and t issue r epair85.
Figure 4- Tissue response of the subcutaneous tissue on the 30th day under normal (A, B, C) and diabetic (D, E, F) conditions. Use of Gray MTA Angelus® (A) and MTA Fillapex®%LQERWKPDWHULDOVDPLOGLQÀDPPDWRU\UHVSRQVHZLWKWKHLQ¿OWUDWLRQRIPDFURSKDJHV
DQGO\PSKRF\WHVZDVHYLGHQWKHPDWR[\OLQHRVLQîPDJQL¿FDWLRQ6HDODSH[®&WKLFN¿EURXVFDSVXOHIRUPDWLRQDQGDPRGHUDWH
LQÀDPPDWRU\ FHOO LQ¿OWUDWLRQ KHPDWR[\OLQHRVLQ î PDJQL¿FDWLRQ *UD\ 07$ $QJHOXV® ' SUHVHQFH RI D PRGHUDWH LQÀDPPDWRU\
LQ¿OWUDWLRQRIPDFURSKDJHVDQGO\PSKRF\WHVKHPDWR[\OLQHRVLQîPDJQL¿FDWLRQ07$)LOODSH[®(SUHVHQFHRIDPLOGLQÀDPPDWRU\
LQ¿OWUDWLRQRIPDFURSKDJHVDQGO\PSKRF\WHVDIWHUGD\VKHPDWR[\OLQHRVLQîPDJQL¿FDWLRQ6HDODSH[®)WKLFN¿EURXVFDSVXOH
3HULDSLFDOOHVLRQVRFFXUDVDQLQÀDPPDWRU\UHVSRQVH
t o infect ion and, along w it h hy per t ension, can lead t o
YDVFXODULQMXU\DQGLQÀDPPDWLRQ70.
Mar t i n s, et al .7 0 ( 2 0 1 6 ) ev al u at ed t h e t i ssu e
r esponse and m ineralizat ion capacit y of MTA cem ent
i n h y p e r t e n si v e r a t s. Th e r e su l t s sh o w e d t h a t
h y p er t en si v e r a t s h a d a n i n t en se i n f l a m m a t o r y
r eact ion an d w er e ch ar act er ized b y a d ecr eased
m ineralizat ion rat e com par ed t o nor m ot ensive rat s;
t his suggest ed t hat t he com or bidit y of hy per t ension
w as ab le t o im p air t h e t issu e r esp on se an d t h e
m ineralizat ion abilit y of MTA.
The hy per t ensive st at e can be a r isk fact or for
per iodont it is and per iapical lesions. How ever, fur t her
r esear ch link ing hy per t ension and per iapical lesion
healing is r equir ed.
Menopause/ Ost eopor osis
The longer life ex pect ancy of elder ly indiv iduals
raises a concer n for bot h t he qualit y of life and t he
prevent ion of age- relat ed diseases. I n t his cont ext , an
incr ease in t he pr evalence of bone fract ur e because
of advanced age has been obser ved11, par t icular ly
in post - m enopausal w om en; t his is a r esult of t he
decr eased concent rat ion of est r ogen.
Ost eop or osis an d ap ical p er iod on t it is ar e t w o
diseases t hat involve bone r esor pt ion. St udies have
VKRZQ D VLJQL¿FDQW FRUUHODWLRQ EHWZHHQ WKHVH WZR
diseases98,112. Xiong, et al.112 ( 2007) show ed t hat t he
condit ion of apical per iodont it is is aggravat ed by an
HVWURJHQGH¿FLHQF\/RZHVWURJHQFRQFHQWUDWLRQDOVR
pr om ot ed an incr ease in t he r esor pt ive act iv it y of t he
alveolar pr ocess in rat s46,112.
Hor m one r eplacem ent t herapies ( or t he use of
st abilizing subst ances for t he pr ocess of r esor pt ion)
aim t o r ed u ce t h e f r eq u en cy of f r act u r es an d t o
pr event fur t her loss of m at ur e bone9. This includes
t he use of bisphosphonat e9,28. Ralox ifene, w hich is an
ex am ple of bisphosphonat e, is used in t he t r eat m ent
and pr event ion of ost eopor osis in post m enopausal
w om en27. I nv est igat ions using ovar iect om ized rat s
show ed t hat t his t r eat m ent also pr event ed bone loss
and suppressed it s form at ion. This result ed in reduced
bone r em odeling45,46.
I n addit ion, t he r elat ionship bet w een t he incidence
of apical per iodont it is in ovar iect om ized rat s, w it h or
w it hout t he t r eat m ent of Ralox ifene, suggest ed t hat
DGH¿FLHQF\LQHVWURJHQFRQFHQWUDWLRQVHQKDQFHGWKH
pr ogr ession of per iapical lesions45,46.
Conclusion
I n sum m ar y, t he r epair pr ocess of endodont ically
t r eat ed t eet h depends not only on t he adopt ion of
t he cor r ect clinical appr oaches t o pr om ot e a bet t er
RCT ( such as use of good ir r igant solut ion, int racanal
GUHVVLQJDQGURRWFDQDO¿OOLQJEXWDOVRRQV\VWHPLF
fact or s ( such as chr onic diseases, hor m ones, and
age) t hat can change t he host ’s im m une defenses and
int er fer e in t he out com e of r oot canal t r eat m ent and
in t he healing pr ocess.
Acknow ledgem ent
Th e au t h o r s d ecl ar e n o co n f l i ct s o f i n t er est .
Th is st u dy w as su ppor t ed, in par t , by t h e gr an t s
r eceiv ed f r om t h e Nat ion al Cou n cil f or Scien t if ic
an d Tech n olog ical Dev elop m en t ( CNPq g r an t s n .
3 0 1 1 2 3 / 2 0 1 3 - 6 t o J. E. G. F., n . 3 0 5 9 6 9 / 2 0 1 5 - 3 t o
L. T. A. C., n. 306394/ 2011- 1 t o C. E. ) and fr om t he
São Paulo Resear ch Foundat ion ( FAPESP grant s n.
2 0 1 2 / 0 6 9 4 3 - 1 , 2 0 1 2 / 0 6 7 8 5 - 7 an d 2 0 1 2 / 0 1 1 5 3 - 2
t o J.E.G.F., n. 2012/ 09987- 0 and 2012/ 02083- 8 t o
L.T.A.C.)
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Ral ox i f en e, est r o g en , an d al en d r o n at e af f ect t h e p r o cesses o f fract ur e r epair differ ent ly in ovar iect om ized rat s. J Bone Miner Res.
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