allergies/asthma and root resorption: a systematic review
TRANSCRIPT
REVIEW Open Access
Allergies/asthma and root resorption: asystematic reviewCibelle Cristina Oliveira dos Santos1, Silvio Augusto Bellini-Pereira2, Melany Clarissa Gamez Medina1 andDavid Normando1*
Abstract
Background: This review synthesizes the available evidence about the predisposition of individuals with asthma orallergies to orthodontically induced inflammatory root resorption (OIIRR) and possible factors related to rootresorption that were investigated in the included studies, such as the type of malocclusion, duration of orthodontictreatment, and tooth units.
Material and methods: Six electronic databases and partial gray literature were searched without date or languagerestrictions until September 2020. Prospective and retrospective observational cohort and case-control studies wereincluded. The risk of bias (RoB) was assessed using the checklists from the Joanna Briggs Institute and the certaintyof the evidence using the GRADE tool. To complement the case-control studies, the odds ratio (OR) of theindividuals with allergies/asthma to develop root resorption was calculated.
Results: Six studies were included. One study with low RoB, one with moderate, and one with high RoB stated thatallergic patients did not report a greater chance of developing OIIRR (OR = 1.17 to 2.10, p = 0.1 to 1), while onlyone study with low RoB reported that individuals with allergies tend to develop root resorption (OR = 2.4, 95% CI =1.08-5.37). Three studies with low RoB and one with moderate showed no significant association between asthmaand OIIRR (OR = 1.05 to 3.42, p = 0.12 to 0.94). No association was identified between the type of malocclusion andthe degree of OIIRR. Uniradicular dental units and a prolonged treatment time seem to be associated with anincreased risk of resorption. The certainty of the evidence was considered low for both exposure factors.
Conclusion: Evidence with a low level of certainty indicates that individuals with allergies or asthma are not morepredisposed to OIIRR. Uniradicular teeth and long-term orthodontic treatments are associated with a higher risk ofOIIRR.
Systematic review registration: PROSPERO CRD42020188463
Keywords: Allergy, Asthma, Root resorption, Orthodontics
© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you giveappropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate ifchanges were made. The images or other third party material in this article are included in the article's Creative Commonslicence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commonslicence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtainpermission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
* Correspondence: [email protected] of Orthodontics, Dental School, Federal University of Pará,Belém, Pará, BrazilFull list of author information is available at the end of the article
Santos et al. Progress in Orthodontics (2021) 22:8 https://doi.org/10.1186/s40510-021-00351-x
IntroductionOrthodontically induced inflammatory root resorption(OIIRR) affects the apical third and promotes a re-duction of approximately 1 mm from the root [1]. Itis considered an undesirable and inevitable side effectin approximately 80% of orthodontic patients [2].However, severe resorption can cause mobility andtooth loss [3]. External factors related to orthodonticmechanics such as the type of appliance [4], intensityand direction of the applied force [4], duration oforthodontic treatment [5], and dental extractions [5]can be associated with OIIRR. Additionally, individualfactors such as genetics [6], sex [7], age [8], rootmorphology [9], bone density [10], and systemic fac-tors related to the immune system [11] were also de-scribed as potential factors for OIIRR.The inflammatory mechanism promoted by immune
cells that precede tooth movement can influence themagnitude of root resorption. In patients with asthma,the action of T-helper lymphocytes synthesizes inflam-matory mediators that reach the blood circulation andthe periodontal ligament interacting with bone remodel-ing cells and tooth movement [12]. The presence of pri-mary leukocytes in the bloodstream caused by lungdiseases supports a possible association between exces-sive root resorption and pathological conditions thataffect the immune system [11]. There is a hypothesisthat individuals with allergies or asthma may have agreater chance of developing root resorption after ortho-dontic treatment [13]. Many of the inflammatory media-tors stimulated in an allergic condition, such as asthma,circulate via blood vessels and possibly penetrate theextravascular space of the periodontal ligament, espe-cially during orthodontic tooth movement [14]. A cohortstudy reported the highest incidence of root resorptionin individuals with asthma and concluded that asthma isa risk factor for OIIRR [14]. However, the literature haspointed out divergent results [11, 15]. A retrospectivecase-control study observed that the prevalence of theallergy risk factor was higher in the group of individualswith root resorption [11]. In contrast, some studiesfound no association between the presence of the allergyrisk factor and a higher level of OIIRR [16, 17].Orthodontic patients with allergies or asthma are iden-
tified before treatment if they have a greater predispos-ition to the development of root resorption. Consideringthe inconsistency in the literature on the association be-tween immune diseases and orthodontically inducedroot resorption, the primary objective of this review wasto synthesize the available evidence about the predispos-ition of individuals with asthma or allergies to orthodon-tically induced root resorption. The secondary aim wasto investigate possible factors related to root resorptionthat were investigated in the included studies, such as
the type of malocclusion, duration of orthodontic treat-ment, and tooth units.
Material and methodsProtocol and registrationThis systematic review was submitted to the PROS-PERO database (https://www.crd.york.ac.uk/prospero/),under protocol ID CRD42020188463 and carried outaccording to the PRISMA guidelines (https://Prisma-statement.org/).
Eligibility criteriaThe eligibility criteria were adopted according to the PE-COS strategy:• P: Individuals treated orthodontically.• E: Allergies or asthma.• C: Orthodontically treated individuals without aller-
gies or asthma.• O: Predisposition of individuals with asthma or aller-
gies to root resorption induced by orthodontic treat-ment. As a secondary outcome, the type ofmalocclusion, time of orthodontic treatment, and theevaluated dental elements were considered.• S: Prospective and retrospective observational cohort
and case-control studies.The exclusion criteria included patients with root frac-
tures; dental anomalies regarding number or form, agen-esis, incomplete rhizogenesis, microdontia, andtaurodontism; previous orthodontic treatment; and othersystemic diseases.
Information sourcesSearches were conducted in the databases: PubMed, Sco-pus, Web of Science, LILACS, Embase, LIVIVO, GoogleScholar, and OpenGrey. The search strategies are shownin Table 1 and were carried out until September 26,2020, without restrictions regarding the date or languageof publication. The reference lists of the included studieswere searched manually. An alert was created for newstudies compatible with the search strategy in thedatabases.
Search strategy and study selectionTwo independent examiners (C.S and S.B) screened thetitles and/or abstracts of studies retrieved from thesearches to identify the inclusion criteria. In cases of dis-agreement, a third examiner was consulted (D.N). Thesearch strategy was developed from a combination ofMeSH, entry-terms, and keywords related to the PECOSstrategy using Boolean operators. The selected articleswere exported to a reference manager (EndNote®, Clari-vate Analytics, Philadelphia, USA) for the removal of du-plicates and to exclude those that did not meet the pre-established inclusion criteria. Finally, the relevant articles
Santos et al. Progress in Orthodontics (2021) 22:8 Page 2 of 12
Table
1Search
strategies
inthedatabase
Datab
ase
Key
words
Results
Pubm
ed((((((((((((“asthm
a”[M
eSHTerm
s]OR“asthm
a”[AllFields])OR“asthm
as”[A
llFields])OR“asthm
as”[AllFields])OR(((“asthm
a”[M
eSHTerm
s]OR“asthm
a”[AllFields])OR
(“bronchial”[A
llFields]A
ND“asthm
a”[AllFields]))
OR“bronchialasthma”[AllFields]))
OR((“respiratory
tractdiseases”[M
eSHTerm
s]OR((“Respiratory”[A
llFields]A
ND“tract”[A
llFields])AND“diseases”[AllFields]))
OR“respiratory
tractdiseases”[A
llFields]))
OR((“rhinitis”[M
eSHTerm
s]OR“rhinitis”[A
llFields])OR“rhinitid
es”[A
llFields]))
OR((((“rhinitis,
allergic”[M
eSHTerm
s]OR(“rhinitis”[A
llFields]A
ND“allergic”[A
llFields]))
OR“allergicrhinitis”[AllFields])OR(“rhinitis”[A
llFields]AND“allergic”[AllFields]))
OR“rhinitis
allergic”[A
llFields]))
OR((“respiratio
ndisorders”[M
eSHTerm
s]OR(“respiratio
n”[AllFields]AND“disorde
rs”[A
llFields]))
OR“respiratio
ndisorders”[AllFields]))
OR(((((((“allergie”[A
llFields]O
R“hypersensitivity”[M
eSHTerm
s])OR“hypersensitivity”[A
llFields])OR“allergies”[AllFields])OR“allergy”[AllFields])OR“allergyandim
mun
olog
y”[M
eSHTerm
s])OR(“allergy”[All
Fields]A
ND“im
mun
olog
y”[AllFields]))
OR“allergyandim
mun
olog
y”[AllFields]))
OR((((“respiratory
tractinfections”[M
eSHTerm
s]OR((“Respiratory”[A
llFields]A
ND“tract”[A
llFields])AND“in
fections”[A
llFields]))
OR“respiratory
tractinfections”[A
llFields])OR(“R
espiratory”[A
llFields]AND“in
fection”[AllFields]))
OR“respiratory
infection”[AllFields]))
OR
((((“respiratory
tractinfections”[M
eSHTerm
s]OR((“Respiratory”[A
llFields]AND“tract”[A
llFields])AND“in
fections”[A
llFields]))
OR“respiratory
tractinfections”[A
llFields])OR
(“Respiratory”[A
llFields]A
ND“in
fections”[A
llFields]))
OR“respiratory
infections”[A
llFields]))
OR(“R
espiratory”[A
llFields]AND((((“chang
e”[AllFields]OR“chang
ed”[A
llFields])OR
“chang
es”[AllFields])OR“chang
ing”[AllFields])OR“chang
ings”[A
llFields])))AND((((((((“plantroots”[M
eSHTerm
s]OR(“p
lant”[A
llFields]A
ND“roo
ts”[A
llFields]))
OR“plant
roots”[AllFields])OR“roo
t”[AllFields])AND“resorp*”[A
llFields])OR((((“p
lant
roots”[M
eSHTerm
s]OR(“p
lant”[A
llFields]AND“roo
ts”[A
llFields]))
OR“plant
roots”[AllFields])OR
“roo
t”[AllFields])AND((((“sho
rten
”[AllFields]OR“sho
rten
ed”[A
llFields])OR“sho
rten
ing”[AllFields])OR“sho
rten
ings”[A
llFields])OR“sho
rten
s”[AllFields])))OR((((“apical”[All
Fields]O
R“apically”[A
llFields])OR“apicals”[A
llFields])OR“apices”[AllFields])AND((((“resorption”[AllFields]OR“resorptional”[AllFields])OR“resorptions”[A
llFields])OR
“resorptive”[AllFields])OR“resorptives”[A
llFields])))OR“OIRR”[AllFields])OR((“toothresorptio
n”[M
eSHTerm
s]OR(“too
th”[A
llFields]AND“resorption”[AllFields]))
OR“too
thresorptio
n”[AllFields]))
120
Scop
us((A
LL(asthm
aOR“Respiratory
tractdisease”
OR“Allergicrhinitis”ORrhinitisOR“Rhinitis,A
llergic”OR“Respiratio
nDisorde
rs”OR“Respiratory
diseases”OR“Respiratory
change
s”OR“Respiratory
infection”
OR“Respiratory
infections”ORallergyORallergicOR“Allergyasthma”
OR“BronchialAsthm
a”))AND(TITLE-ABS-KEY
(“Roo
tresorptio
n”OR
“Resorption,root”OR“Too
thresorptio
n”OR“Roo
tResorp*”OR“Roo
tShortening
”OR“ApicalR
esorption”
ORoirr)))
109
Web
ofScience
ALL=(asthm
aORRespiratory
tractdiseaseORAllergicrhinitisORrhinitisORRh
initis,AllergicORRespiratio
nDisorde
rsORRespiratory
diseases
ORRespiratory
change
sOR
Respiratory
infectionORRespiratory
infections
ORallergyORallergicORAllergyasthmaORBron
chialA
sthm
a)ANDALL=(Roo
tresorptio
nORResorptio
n,root
ORTooth
resorptio
nORRo
otResorp*ORRo
otShortening
ORApicalR
esorptionORoirr)
56
LILA
CS
(mh:(asthm
a))OR(m
h:(asm
a))OR(m
h:(asthm
a,bron
quial))
OR(m
h:(re
spiratory
tractdiseases))OR(m
h:(asm
abron
quial))
OR(m
h:(re
spiratory
tractdisease))O
R(tw:
(enfermed
ades
tracto
respiratório
))OR(m
h:(rh
initis))OR(tw:(rinitis))OR(m
h:(rh
initisallergic))OR(m
h:(re
spiratio
ndisorders))OR(tw:(desórde
nesrespiratório
s))OR(tw:(allergy))
AND(m
h:(Roo
tresorptio
n))OR(m
h:(Reabsorción
radicular))
OR(tw:(Roo
tshortening
))OR(tw:(A
cortam
ientode
laraiz))OR(tw:(O
IRR))OR(tw:(A
picalresorption))OR(tw:(Too
thresorptio
n))OR(tw:(Reabsorción
dental))
119
Embase
(“asthm
a”/exp
OR“asthm
aticstate”/exp
OR“respiratory
tractdisease”/exp
OR“rhinitis”/expOR“allergicrhinitis”/exp
OR“breathing
disorder”/expOR“allergy”/exp
OR
“respiratory
infections”/exp)
AND(“roo
tresorptio
n”OR“roo
tshortening
or”OR“apicalresorptionor
toothresorptio
n”)
19
LIVIVO
(Asthm
aORBron
chialA
sthm
aORRespiratory
TractDiseasesORRh
initisORRh
initisAllergicORRespiratio
nDisorde
rsORAllergyORRespiratory
InfectionORRespiratory
Infections
ORRespiratory
Chang
es)AND(Roo
tResorp*ORRo
otShortening
OROIRRORApicalR
esorptionORToothResorptio
n)82
Goo
gle
Scho
lar
(Asthm
aORRh
initisORAllergyANDRo
otResorptio
nORRo
otShortening
OROIRR)
200
Ope
nGrey
Root
resorptio
n9
Santos et al. Progress in Orthodontics (2021) 22:8 Page 3 of 12
were read for the final selection and a third examinerwas consulted (D.N) to resolve discrepancies.
Data collection process and summary measuresThe same reviewers performed data extraction inde-pendently. Data were collected based on the followingitems: authorship, including author names, year of publi-cation and study design; sample characteristics, samplesize, distribution by sex, and average age; characteristicsof malocclusion, orthodontic appliance, and duration oforthodontic treatment; exposure to the allergy or asthmarisk factor; methodology including teeth evaluated andevaluation method; results, including the amount of rootresorption and the prevalence of risk factors, in additionto the odds ratio of individuals with allergies or asthmato develop root resorption; and study conclusions.
Risk of bias in individual studiesThe analysis of the risk of bias (RoB) of the selectedstudies was carried out through the checklists for criticalevaluation from the Joanna Briggs Institute for cohortand case-control studies (https://joannabriggs.org/). Thegoal of critical appraisal (assessment of the risk of bias)is to assess the methodological quality of a study and todetermine the extent to which a study has excluded orminimized the possibility of bias in its design, conduct,and analysis. The critical analysis corresponds to thecompletion of checklists with 10 questions with answers“Yes,” “No,” “Not clear,” and “Not applicable.” The eval-uators agreed on the scoring criteria prior to conductingthe critical analysis. Thus, the studies were characterizedas high RoB when up to 49% of the answers were “YES,”moderate risk when between 50 and 69% of the answerswere “YES,” and low when more than 70% of the an-swers were “YES,” regardless of the question asked. Twoexaminers independently evaluated the RoB of the se-lected studies (C.S and S.B) and in the case of discrepan-cies, a third examiner was consulted (D.N).
Level of evidenceThe outcomes evaluated using the GRADE tool wereclassified based on the predisposition of patients withasthma or allergies to OIIRR. The studies were evaluatedbased on the study design, RoB, inconsistency, indirectevidence, and imprecision.
ResultsStudy selectionThe database searches found 505 references: PubMed (n= 120), Scopus (n = 109), Web of Science (n = 56), Lilacs(n = 119), Embase (n = 19), and Livivo (n = 82). Afterthe removal of duplicate references using EndNote®manager, 376 articles remained. After reading titles andabstracts, five potentially selectable studies remained.
The search in the gray literature found 209 references:Google scholar (n = 200) and OpenGrey (n = 9). Fromthe gray literature, three studies were selected after read-ing titles and abstracts. Thus, eight studies were selectedfor reading the texts in full and applying the eligibilitycriteria, which resulted in the exclusion of two caseseries studies [4, 18]. Six studies were selected for quali-tative analysis [11, 14–17, 19]. The process of identifica-tion, selection, and exclusion of studies is shown in thePRISMA flow diagram of article retrieval (Fig. 1).
Study characteristicsThe six included studies were observational and retro-spective of which one was a cohort type [14] and aimedto determine whether individuals with asthma had ahigher incidence of root resorption. Five were case-control studies [11, 15–17, 19], among which, one studyobserved the influence of asthma on the degree of rootresorption [15], two evaluated the association betweenthe allergy risk factor and root resorption [17, 19]; oneassessed the association between root resorption andrisk factors for allergies and asthma [11]; and the otherverified the prevalence of immune diseases in individualswho underwent orthodontic treatment and expressedroot resorption [16].Thus, four studies evaluated patients with allergies [11,
16, 17, 19] and four studies included individuals withasthma in their samples [11, 14–17, 19]. The mean aver-age age ranged between 13.9 (± 1.8) [14] and 17.7 (±5.1) years [11]. The average time of orthodontic treat-ment ranged from 1.8 (± 0.4) to 3.1 (± 1.19) years [11,14]. The cohort study [14] showed a sample of 141 indi-viduals. The sample sizes of the case-control studies var-ied between 50 [17] and 683 [15] individuals. Twostudies did not report the classification of their samplesbased on malocclusion [14, 17]. All studies were per-formed on individuals with fixed appliances in botharches. Concerning the teeth evaluated for the level ofroot resorption, two studies included maxillary premo-lars [13, 19], two—the maxillary and mandibular incisors[15, 19], one—the mesial- and distal roots of the maxil-lary 1st molars [14], and two studies evaluated all teeth[11, 16].There was great methodological heterogeneity among
the included studies regarding the methods of evaluationand diagnosis of root resorption. The evaluation was car-ried out through panoramic radiography in three studies[11, 14, 16], periapical radiographs in two [15, 19], andhistological sections in one study [17]. Two studies usedthe Levander and Malmgren [20] method to measureroot resorption [15, 19], one [14] used the Sharpe Scale[21] method, one used a digital caliper to measure thedistance from the cementum-enamel junction to theroot apex [11], one carried out the histological analysis
Santos et al. Progress in Orthodontics (2021) 22:8 Page 4 of 12
of the resorption areas measuring the length and depthof the resorbed area [17], and one study measured theroot length using panoramic radiographs and deter-mined that individuals with up to 25% of resorption didnot have root resorption [16]. The summary of datafrom the included studies is available in Table 2.
Results of individuals studiesOf the four studies [11, 16, 17, 19] that evaluated pa-tients with allergies, three [16, 17, 19] reported that al-though the prevalence of allergies is higher amongindividuals with root resorption, individuals with aller-gies have the same chance of developing OIIRR as indi-viduals with no allergies. Only one study consideredallergies as a risk factor for the development of root re-sorption after orthodontic treatment [11]. Likewise, thefour studies [11, 14–16] in asthmatic individuals statethat they have the same chance of OIIRR as non-
asthmatics, although the prevalence of asthma washigher in groups of individuals with considerable rootresorption. The cohort study [14] reported that whilethere is an association between root resorption and aller-gies (p = 0.019), the level of severe resorption was simi-lar between individuals with and without asthma.
Synthesis of resultA meta-analysis was not performed due to the con-siderable methodological differences between thestudies regarding the teeth evaluated, the sampleunits, and the methods of diagnosis and measurementof root resorption. To complement the findings of thecase-control studies, the odds ratio of the individualswith allergies/asthma was calculated. The results canbe seen in Table 2.Only one study [11] reported a greater chance of
individuals with allergies developing OIIRR, OR =
Fig. 1 PRISMA flow diagram of article retrieval
Santos et al. Progress in Orthodontics (2021) 22:8 Page 5 of 12
Table
2Summaryof
thedata
from
includ
edstud
ies
1. Autho
rship
2.Material
3. Exposure
4.Metho
dolog
y5.
Results
6.Con
clusions
Autho
r,ye
arStud
ydesign
Risk
factor/outco
me
M/F
(n)
Mea
nag
e±SD
(yea
rs)
Maloc
clusion(M
ocl)
Ortho
don
ticdev
ice
Mea
ntrea
tmen
ttime
oforthod
ontictrea
tmen
t±SD
(yea
rs)
Asthm
aor
allergies
Evalua
tedteeth
Evalua
tion
metho
dInciden
ceof
root
resorption
(%)/prevalenc
eof
risk
factors(%
)
Oddsratio
(OR)
(IC95
%)
pvalue
Con
trol
Exposed
Con
trol
Exposed
Con
trol
Exposed
McN
abet
al.
[14],1999
Retrospe
ctive
coho
rt
Patients
with
out
asthma
38M/59F
13.9±
1.8years
Patients
with
asthma
18M/26F
14.5±3.2
years
Mocl:N.I
Fixed
appliance,
with
orwith
out
headge
ar1.9±0.5
years
Mocl:NI
Fixed
appliance,
with
orwith
out
headge
ar1.8±0.4
years
Asthm
aPM
’s,mesio-buccaland
disto-
buccalrootsof
theup
per1stM,
mesialand
distalrootsof
the
lower
1stM
Pano
ramicradiog
raph
ySharpe
scale
T0:
Severe
OIIRR:
0.93%
T1:
Severe
OIIRR:
15.27%
N.I
T0:
Severe
OIIRR:
2.3%
T.1:
Severe
OIIRR:
13.15%
N.I
OR=
N.A
Multivariate
analysis:p=
0.019
-Alth
ough
thereisan
associationbe
tween
root
resorptio
nandtheasthmariskfactor
(p=0.019),asthm
aticandno
n-asthmatic
individu
alsexhibitedsimilarvalues
ofsevere
OIIRR.
Meloet
al.
[15],2018
Case-control
Patients
with
initial
OIIRR
300M
/314F
14.37±
2.76
years
Patients
with
severe
OIIRR
32M/37F
15.09±
3.44
years
Mocl:
ClI=266
ClII=319
ClIII=
29Fixed
appliance
2.07
±0.93
years
Mocl:
ClI=24
ClII=43
ClIII=
2Fixed
appliance
2.72
±1.07
years
Asthm
aUpp
erandlower
incisors
Periapicalradiography
Levand
erandMalmgren
metho
d
N.I
With
asthma=
35%
With
out
asthma=
65%
N.I
With
asthma=
36.2%
With
out
asthma=
63.7%
OR=
1.05
(0.62-1.77)
p=0.94
-The
prevalen
ceof
individu
alswith
asthma
was
likethetw
ogrou
ps.
-The
rewas
noassociationbe
tweentherisk
factor
asthmaandOIIRR(p
=0.841)
-Asthm
aticandno
n-asthmaticindividu
als
have
thesamechance
ofde
veloping
OIIRR
(OR=
1.05,95%
CI=0.62-1.77).
Nishiokaet
al.
[11],2006
Case-control
Patients
with
out
OIIRR
18M/42F
M:15.9±
4.5years
F:18.5±
5.2years
17.7±
5.1years
Patients
with
OIIRR
18M/42F
M:17.7±
5.7years
F:16.4±
6.0years
16.8±5.9
years
Mocl:
ClI=10
ClII=29
ClIII=
21Fixed
appliance
2.96
±0.56
years
Mocl:
ClI=10
ClII=29
ClIII=
21Fixed
appliance
3.10
±1.19
years
Allergies
and
asthma
Allteeth
Pano
ramicradiog
raph
y,measuredwith
adigital
pachym
eter
N.I
With
allergies:
21%
With
asthma:
5%
N.I
With
allergies:
40%
With
asthma:
15%
Alle
rgyrisk
factor:
OR=
2.41
(1.08-5.37)
p=0.04
Asthm
arisk
factor:
OR=
3.35
(0.86-13.06)
p=0.12
-The
prevalen
ceof
riskfactorswas
high
erin
individu
alswith
OIIRR.
-Allergicindividu
alsaremorelikelyto
developOIIRRthan
non-allergicindividu
als
(OR=2.41,95%
CI=
1.08-5.37).
-How
ever,asthm
atic,and
non-asthmatic
individu
alshave
thesamechance
ofde
veloping
OIIRR(OR=
3.35,95%
CI=0.86-13.06).
Owman-M
oll
etal.[17],
2000
Case-control
Patients
with
initial
OIIRR
25(N.I.)
13.4a±
N.I
Patients
with
severe
OIIRR
25(N.I.)
13.4a±N.
I
Mocl:
N.I.
Fixed
appliance
andlower
lingu
alarch
N.I
Mocl:
N.I.
Fixed
appliance
andlower
lingu
alarch
N.I
Allergy
Upp
erPM
’sHistologicalanalysis
N.I
With
allergies:
13.3%
N.I
With
allergies:
26.6%
OR=
1.17
(0.38-3.75)
p=1
-Theprevalen
ceof
allergieswas
high
erin
individu
alswith
severe
OIIRR.
-How
ever,allergic,and
non-allergic
individu
alshave
thesamechance
ofde
veloping
OIIRR(OR=
1.17,95%
CI=0.38-3.75).
Pastro
etal.
[19],2018
Case-control
Patients
with
initial
OIIRR
252M
/
Patients
with
severe
OIIRR
40M/53F
Mocl:
ClI=220
ClII=269
ClIII=
18Fixed
Mocl:
ClI=38
ClII=52
ClIII=
3Fixed
Allergy
Upp
erandlower
incisors
Periapicalradiography
Levand
erandMalmgren
metho
d
N.I
With
allergies:
42%
With
out
N.I
With
allergies:
49.46%
With
out
OR=
1.35
(0.86-2.1)
p=0.22
-The
prevalen
ceof
allergieswas
high
erin
individu
alswith
severe
OIIRR.
-The
rewas
noassociationbe
tweenthe
allergyriskfactor
andOIIRR(p
=0.182).
-Allergicandno
n-allergicindividu
alshave
Santos et al. Progress in Orthodontics (2021) 22:8 Page 6 of 12
Table
2Summaryof
thedata
from
includ
edstud
ies(Con
tinued)
1. Autho
rship
2.Material
3. Exposure
4.Metho
dolog
y5.
Results
6.Con
clusions
Autho
r,ye
arStud
ydesign
Risk
factor/outco
me
M/F
(n)
Mea
nag
e±SD
(yea
rs)
Maloc
clusion(M
ocl)
Ortho
don
ticdev
ice
Mea
ntrea
tmen
ttime
oforthod
ontictrea
tmen
t±SD
(yea
rs)
Asthm
aor
allergies
Evalua
tedteeth
Evalua
tion
metho
dInciden
ceof
root
resorption
(%)/prevalenc
eof
risk
factors(%
)
Oddsratio
(OR)
(IC95
%)
pvalue
Con
trol
Exposed
Con
trol
Exposed
Con
trol
Exposed
255F
14.21±
2.45
years
14.57±
2.67
years
appliance
1.81
±0.83
years
appliance
2.41
±0.99
years
allergy:
58%
allergy:
50.53%
thesamechance
ofde
veloping
OIIRR
(OR=
1.35,95%
CI=0.86-2.1).
Shim
etal.
[16],2003
Case-control
Patients
with
out
OIIRR
25M/26F
15.40±
4.10
years
Patients
with
OIIRR
25M/26F
16.10±
3.30
years
Mocl:
ClI=15
ClII=13
ClIII=
23Fixed
appliance
2.31
±0.77
years
Mocl:
ClI=15
ClII=14
ClIII=
22Fixed
appliance
2.13
±0.73
years
Allergy
and
asthma
Allteeth
Pano
ramicradiog
raph
yMeasuremen
tof
root
leng
thon
pano
ramicradiog
raph
y
N.I
With
allergies:
31%
With
asthma:
5.88%
N.I
With
allergies:
49%
With
asthma:
17.64%
Alle
rgyrisk
factor:
OR=
2.10
(0.93-4.71)
p=0.1
Asthm
arisk
factor:
OR=
3.42
(0.87-13.5)
p=0.12
-The
prevalen
ceof
allergieswas
high
erin
individu
alswith
OIIRR,bu
twith
out
statisticalsign
ificance(OR=
2.1,
95%CI=
0.93-4.71).
-The
prevalen
ceof
asthmawas
statistically
high
erin
individu
alswith
OIIRR(p
=0.01).
-How
ever,asthm
aticindividu
alshave
the
samechance
ofde
veloping
OIIRRas
non-asthmaticindividu
als(OR=3.42,
95%CI=
0.87-13.5).
T0be
fore
orthod
ontic
treatm
ent;T1
afterorthod
ontic
treatm
ent;M
molar;P
Mprem
olar,N
Inot
inform
ed;N
.Ano
tap
plied;
SDstan
dard
deviation;
Mmale;
Ffemale;
OIIRRorthod
ontically
indu
cedinflammatory
root
resorptio
n
Santos et al. Progress in Orthodontics (2021) 22:8 Page 7 of 12
2.41, p = 0.04. Three studies [11, 15, 16] demon-strated that individuals with asthma have a similarchance compared to non-asthmatic individuals of de-veloping OIIRR, OR = 1.05 to 3.42, p = 0.12 to 0.94.The odds ratio for one study was not calculated be-cause it is a cohort study [14].
Risk of bias within studiesOf the four studies that evaluated patients with allergies[11, 16, 17, 19], two were classified with low RoB [11,19], one with high [17], and one with a moderate RoB[16]. Three studies evaluating individuals with asthmapresented low RoB [11, 14, 15], and one moderate [16].The RoB was related to unreported [8, 15] and uncon-trolled [11, 15, 17] confounding factors, to the use of im-precise methods of measuring root resorption [11, 14,16], and to the absence of an appropriate statistical ana-lysis including regression models to adjust for confound-ing factors [16, 17]. Tables 3 and 4 show the evaluationof the RoB of the included studies.
Assessment of the certainty of evidenceThe certainty of evidence that individuals with allergieshave the same predisposition to OIIRR as individualswith no allergies was low. Among the four includedstudies, one had a high RoB [17], one moderate [16],and two low RoB [11, 19]. In addition to the fact thatthey are observational studies, which reduces the level ofcertainty of the evidence, they have limitations in theidentification [16, 17, 19] and control of confoundingfactors [11, 16, 17] and in the accuracy of the method ofevaluation of root resorption [11, 16]. Similarly, the evi-dence that asthmatic individuals have the same predis-position to OIIRR as non-asthmatic was judged as low.
Among the four studies evaluated, one had moderateRoB [16] and the other low RoB [11, 14, 15]. The lowlevel of certainty of evidence was justified by the meth-odological differences between the studies related to thestudy designs, where one study was a cohort [14] andthe others were case-control studies [11, 15, 16], associ-ated with the lack of control of confounding variables[11, 15, 16] and the use of panoramic radiographs forthe diagnosis of root resorption in three studies [11, 14,16]. The assessment of the certainty of evidence accord-ing to GRADE is described in Table 5.
DiscussionSummary of evidenceAlthough it was shown that individuals with allergies orasthma have the same predisposition to OIIRR as indi-viduals without allergies or asthma, the level of certaintyof the evidence was low. However, it is important forclinical applicability since these patients are part of theorthodontist’s clinical routine.Among two studies with low RoB [11, 19], one with
moderate [16] and one with high RoB [17], the preva-lence of the allergy was higher in individuals with ahigher level of root resorption, varying from 26.6% [17]to 49.46% [19]. However, only one of these studies [11]with an estimated allergy prevalence of 40% in the groupof individuals with resorption stated that these patientshave a greater chance of developing root resorption,where OR = 2.41, 95% CI 1.08-5.37. This fact may be as-sociated with cellular changes in the immune system ofallergic or asthmatic individuals since the chemical me-diators produced by allergies or asthma can stimulatethe cells that trigger the process of root resorption [14].
Table 3 RoB of case control studies in the qualitative synthesis based on the Joanna Briggs Institute Critical Appraisal Checklist
Questions—analytical case control studies Meloet al. [15]
Nishiokaet al. [11]
Owman-Mollet al. [17]
Pastroet al. [19]
Shimet al. [16]
1—Were the groups comparable other than the presence of disease in casesor the absence of disease in controls?
Y Y U Y Y
2—Were cases and control matched appropriately? Y Y U Y Y
3—Were the same criteria used for identification of cases and controls? Y Y Y Y Y
4—Was exposure measured in a standard, valid, and reliable way? Y Y Y Y Y
5—Was exposure measured in the same way for cases and controls? Y U Y Y Y
6—Were confounding factors identified? U Y U U U
7—Were strategies to deal with confounding factors stated? N N N N U
8—Were outcomes assessed in a standard, valid, and reliable way for casesand controls?
Y N Y Y N
9—Was the exposure period of interest long enough to be meaningful? Y Y U Y Y
10—Was appropriate statistical analysis used? Y Y U Y U
%Yes/risk 80.0 70.0 40.0 80.0 60.0
Overall Low Low High Low Moderate
Y yes, N no, U unclear, N.A not applicable
Santos et al. Progress in Orthodontics (2021) 22:8 Page 8 of 12
Regarding the ethnicity of the evaluated population,the only study in this review [11] that associated thepresence of allergies with a higher level of root resorp-tion was carried out in a Japanese sample. The literaturepoints to a study carried out in Thailand that reportedallergies as a factor associated with OIIRR (p = 0.003),but it was not included in the assessment because it wasa case series [5]. Contrarily, a previous study [22]showed that Asians have less root resorption than His-panic or white individuals. Considering that ethnic dif-ferences can affect the shape and size of teeth [22], it isplausible that initial root resorption, without clinical sig-nificance in teeth with normal dimensions, can result inmajor damage to teeth with reduced size. The predispos-ition of Asian individuals to OIIRR can be elucidatedwith new studies with samples that contain a balancednumber of individuals from different ethnicities con-trolled as a confounding factor.The diagnosis of allergies based on clinical records can
be inaccurate. Also, the studies did not report whichtypes of allergy or allergenic factors were evaluated,which is considered a confounding factor when inter-preting the results. There is no homogeneity related tothe criteria for the diagnosis of immune diseases be-tween the evaluated studies, which increases the RoB as-sociated with the interpretation of the results. However,even in a study [17] with moderate RoB where the aller-gic condition was verified with medications taken ormedical consultation, no association was observed be-tween allergies and OIIRR.Three studies [11, 14, 15] with low RoB and one with
moderate RoB [16] evaluated the predisposition of indi-viduals with asthma to OIIRR. The three case-controlstudies [11, 15, 16] demonstrated that there is no greaterchance of developing OIIRR associated with the asthma
risk factor. The cohort study [14] corroborates this find-ing because although there is an association betweenroot resorption and asthma (p = 0.019), the level of re-sorption was similar between asthmatic and non-asthmatic individuals. In all studies evaluating individ-uals with asthma [11, 14, 16], the prevalence of asthmawas higher in groups of patients with a higher level ofroot resorption, ranging from 15% [11] to 36.2% [15].However, the odds ratio values for each study did notshow significant differences between the individuals withasthma compared to the individuals without asthma todevelop root resorption (Table 2).Regarding the duration of orthodontic treatment, in
two case-control studies with low RoB [15, 19], wherethe sample was initially classified based on the levelof root resorption in patients with mild and severeresorption, the treatment time was approximately 6months longer in the group with severe resorption.These results corroborate with the literature and indi-cate that there is a positive association betweenOIIRR and treatment time [5].Class II malocclusion had the highest prevalence in
three [11, 15, 19] of the six [11, 14, 17] studies evaluated,ranging from 48.3% [11] to 53.5% [19]. The literaturedoes not indicate an association between the type ofmalocclusion and the severity of root resorption [4, 19].However, individuals with class I or II malocclusion andvertical growth have decreased pharyngeal air spacecompared to individuals who have a normal growth pat-tern [23], confirming the fact that the width of the airspace can be influenced by the craniofacial growth pat-tern [24]. It is important to emphasize the prevalence ofmouth breathing in individuals with nasopharyngeal air-way obstruction and class II malocclusion [25]. This isbecause individuals with asthma or allergies may develop
Table 4 RoB of cohort study in the qualitative synthesis based on the Joanna Briggs Institute Critical Appraisal Checklist
Questions—analytical cohort study McNab et al. [14]
1—Were the two groups similar and recruited from the same population? Y
2—Were the exposures measured similarly to assign people to both exposed and unexposed groups? Y
3—Was the exposure measured in a valid and reliable way? Y
4—Were confounding factors identified? Y
5—Were strategies to deal with confounding factors stated? Y
6—Were groups/participant free of the outcome at the start of the study (or at the moment of exposure)? Y
7—Were the outcomes measured in a valid and a reliable way? N
8—Was the follow-up time reported and sufficient to be long enough for outcomes to occur? U
9—Was follow-up complete, and if not, were the reasons for loss to follow up described and explored? Y
10—Were strategies to address incomplete follow-up utilized? U
11—Was appropriate statistical analysis used? Y
%Yes/risk 72.7
Overall Low
Y yes, N no, U unclear, N.A not applicable
Santos et al. Progress in Orthodontics (2021) 22:8 Page 9 of 12
Table
5Evaluatio
nof
thelevelo
fcertaintyof
theeviden
ceby
theGRA
DEPROtool
Certainty
assessmen
tIm
pact
Certainty
Importanc
e
№of
stud
ies
Stud
ydesign
Risk
ofbias
Inco
nsistenc
yIndirectness
Imprecision
Other
considerations
Pred
ispositionof
allergicpatientsto
orthod
ontically
induc
edroot
resorption
4Observatio
nal
stud
ies
Serio
usa
Not
serio
usNot
serio
usNot
serio
usAllplausibleresidu
alconfou
ndingwou
ldsugg
est
spurious
effect,w
hileno
effect
was
observed
.
Ofthe4stud
iesinclud
ed,one
hasahigh
RoB[17]
and
oneamod
eraterisk[16].Studies
have
limitatio
nsin
the
iden
tificationandcontrolo
fconfou
ndingfactors.Three
stud
iesstatethat
allergyisno
tariskfactor
forroot
resorptio
n[16,17],whileastud
ywith
alow
RoBstates
that
allergyisariskfactor
fororthod
onticallyindu
ced
root
resorptio
n[11]
⨁⨁◯◯
LOW
IMPO
RTANT
Pred
ispositionof
asthmaticpatientsto
orthod
ontically
induc
edroot
resorption
3Observatio
nal
stud
ies
Serio
usb
Serio
usc
Not
serio
usNot
serio
usStrong
association.Allplausible
residu
alconfou
ndingwou
ldsugg
estspurious
effect,w
hile
noeffect
was
observed
Amon
gthe3stud
iesevaluated,
onehasamod
erateRo
B[16]
andtheothe
rshave
alow
RoB[11,15].In
additio
nto
thelack
ofcontrolo
fconfou
ndingvariables,the
reis
inconsistencybe
tweentheresults
demon
stratedby
the
valueof
themetho
dologicalh
eterog
eneity
betw
eenthe
stud
ies.Allstud
iesconclude
that
asthmaisno
tarisk
factor
forroot
resorptio
n.
⨁⨁◯◯
LOW
IMPO
RTANT
a One
stud
yha
shigh
RoB[17],o
neha
smod
erate[16],w
hile
theothe
rsha
velow
[11,
19].Allstud
iesarede
ficient
intheiden
tificationan
dcontrolo
fconfou
ndingfactors
bTw
ostud
iesha
velow
RoB[11,
15],while
onestud
yha
smod
erateRo
B[16].A
llarede
ficient
intheiden
tificationan
dcontrolo
fconfou
ndingfactors
c The
reisconsiderab
lemetho
dologicalh
eterog
eneity
betw
eenthestud
ies,concerning
theteethevalua
tedforroot
resorptio
n,thesampleun
it,an
dthemetho
dsof
diag
nosisof
resorptio
n
Santos et al. Progress in Orthodontics (2021) 22:8 Page 10 of 12
mouth breathing because of breathing difficulties causedby increased airflow resistance due to inflammatory re-sponse characteristic of these systemic changes [26].Still, asthmatic individuals may have a higher prevalenceof malocclusion, especially related to a crossbite, over-bite, overjet, and crowding [27]; in addition to the de-crease in air space, which can change the mandibularposition and lip sealing, causing esthetic, functionalchanges, and malocclusion [28]. Children with allergicrhinitis have increased anterior facial height, increasedoverjet, deep palate, and decreased intermolar width inthe upper arch [29]. Orthodontic treatment in individ-uals with vertical growth pattern potentially associatedwith mouth breathing [26], atresic jaws, crossbites, in-creased overbite or overjet, may require a longer time toperform orthodontic mechanics, and consequently leadto a greater incidence of root resorption. These vari-ables, which can confuse the interpretation of the re-sults, were not identified, or controlled by the evaluatedstudies. Thus, it is recommended that further studies becarried out to control the variables related to malocclu-sion and the craniofacial growth pattern of individualswith asthma or allergies.Two studies with low RoB and larger sample sizes [15,
19] evaluated maxillary and mandibular incisors in morethan 500 individuals diagnosed with mild root resorptionusing periapical radiographs. The results corroborate thatincisors are the elements most affected by root resorption[30]. The assessment of the root region is more accuratewhen performed by periapical radiographs compared topanoramic radiographs, which can overestimate resorp-tion by approximately 20% [3]. The evaluation of root re-sorption using panoramic radiographs was considered amethodological limitation present in three studies [11, 14,16]. The methods of evaluation by Levander and Mal-mgren [20] and Sharpe [21] are methods of qualitativeand subjective analysis and there is no one method super-ior to the other. A study reported that individuals with al-lergies have a greater chance of developing OIIRR thanones without allergies [11] evaluated all dental elementsthrough panoramic radiographs and measurement in mil-limeters corresponding to the longitudinal axis of theenamel-cement junction to the root apex. Although thismeasurement is quantitative, and therefore less subjectivethan the assessments by predetermined visual scales,panoramic radiographs have limitations in accuratelyidentifying the enamel-cement junction [31]. Finally, thestudy with high RoB [17] evaluated premolars from longi-tudinal histological sections where the amount of the ex-tent and depth of the total root resorption area wasmeasured, which seems to be a more accurate assessmentthan the qualitative measurement methods. Thus, we ob-serve the great methodological differences between thestudies regarding the measurement of root resorption,
compromising the level of certainty of the evidence gener-ated. This signals the need for further studies with stan-dardized methods of measurement and diagnosis of bothroot resorption and systemic conditions.Using the GRADE tool, the certainty of the evidence
generated states that patients with asthma or allergies donot have a greater predisposition to OIIRR was classifiedas low. However, even though it has a low level of cer-tainty, the evidence is considered important for clinicalapplicability because it addresses immunological condi-tions that can be manifested by the general population,and consequently, by individuals undergoing orthodontictreatment. Also, the patient should be informed that rootresorption can occur because of orthodontic mechanicsregardless of the systemic conditions inherent to the indi-viduals. Considering that the magnitude of these ortho-dontically induced resorptions has an average value of 1mm [2], they are not contraindications to orthodontictreatment. They can be identified from periodic radio-graphic examinations, and if necessary, attenuated frominterruptions in the activation of orthodontic force [5].
LimitationsQuantitative synthesis was not possible because of thegreat methodological heterogeneity among the includedstudies and resulted in a low level of certainty. New pro-spective studies with adequate methodological designfrom a multiple regression model controlling confound-ing factors may increase the certainty of the evidence re-garding the predisposition of patients with asthma orallergies to OIIRR. Also, it is important to establish aprevious protocol for the diagnosis of immune changes,which will reduce the RoB associated with the interpret-ation of the results. Measurements made with panoramicradiographs may have overestimated the amount of rootresorption found. Thereby, it is recommended that newassessments should be made with periapical radiographsor, if possible, with cone-beam computed tomography.
Conclusions• Scientific evidence with a low level of certainty statesthat individuals with asthma or allergies do not have adifferent predisposition to orthodontically induced rootresorption when compared to individuals with noasthma or allergies.• There was no association between the type of mal-
occlusion and the degree of root resorption. However,uniradicular teeth and patients undergoing longer treat-ment times are more prone to root resorption.
AbbreviationsOIIRR: Orthodontically induced inflammatory root resorption; RoB: Risk ofbias; GRADE: Grading of Recommendations Assessment, Development andEvaluation; OR: Odds ratio; T0: Before orthodontic treatment; T1: After
Santos et al. Progress in Orthodontics (2021) 22:8 Page 11 of 12
orthodontic treatment; M: Molar; PM: Premolar; NI: Not informed; N.A: Notapplied; SD: Standard deviation; M: Male; F: Female
AcknowledgementsNot applicable
Authors’ contributionsC.S realized the research and was the major contributor in writing themanuscript. S.B also realized the research and all the stages of this article.M.G helped with research and writing. D.N corrected all the steps of thissystematic review and the writing. All authors read and approved the finalmanuscript.
FundingThere is no funding support.
Availability of data and materialsThe authors declare that all data generated or analyzed during this study areincluded in this published article and its supplementary information files.
Ethics approval and consent to participateNot applicable
Consent for publicationNot applicable
Competing interestsThere are no competing interests.
Author details1Department of Orthodontics, Dental School, Federal University of Pará,Belém, Pará, Brazil. 2Department of Orthodontics, Bauru Dental School,University of São Paulo, São Paulo, Brazil.
Received: 6 January 2021 Accepted: 10 February 2021
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