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: davidnormando@hotmail.com1Department 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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