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El movimiento dental ortodoncico en apices inmaduros. Revision sistematica.

INTRODUCCION

Diversos estudios en apices totalmente cerrados reportan la respuesta dental y de los tejidos de soporte frente al movimiento ortodoncico. (1, 2) El movimiento dental con aparatos fijos genera una fuerza constante y continua que permite un remodelado oseo sin aparentes efectos deletereos, (3) segun la teoria de presion-tension, (4) segun la cual se produce reabsorcion en la zona de presion y aposicion en la zona de tension. (3) Las celulas responsables y reguladoras de este mecanismo son los osteoclastos, osteoblastos, osteocitos y sus mediadores quimicos. (5, 6) Cuando estas fuerzas son excesivas, ocasionan mayor area de hialinizacion, (7, 8) necrosis y reabsorcion osea, lo cual genera danos en el periodonto, en la pulpa y en las raices de los dientes. (3, 9) De estos efectos, el mas atribuido al tratamiento ortodoncico es la reabsorcion radicular externa. (10, 11) Esta entidad ha sido ampliamente estudiada y se define como la perdida del componente organico e inorganico de los tejidos duros radiculares, como la dentina y el cemento, (12, 13) asociada a otros factores como edad, (13, 14) sexo, (15) trauma, (11) maloclusion, (16), 17 anatomia radicular, (18, 19) tipo de aparato, (20) mecanica utilizada, (16) caracteristicas del movimiento dental, (21, 22) tipo de fuerza (23, 24) y tiempo de tratamiento. (25) Su causa, en terminos generales, podemos decir que es multifactorial. (10)

El movimiento dental con apices abiertos que no han terminado su formacion radicular completa no ha sido estudiado suficientemente. Algunos autores (26, 27) sugieren que el movimiento dental en apices inmaduros podria ser un riesgo en la aparicion de reabsorciones radiculares o en la disminucion de la longitud radicular por cierre apical prematuro, como lo describieron Oppenheimen en 1942 y Phillips en 1955, quienes lo atribuyen a la deformacion de la Vaina de Hertwig, que altera la calcificacion del apice y por consiguiente el desarrollo radicular, impidiendo que llegue a su longitud maxima. (26, 27) En el 2001, Consolaro y colaboradores senalaron que el movimiento de los dientes con formacion radicular incompleta genera una disminucion en la longitud radicular por el cierre temprano del apice--el cual depende de la maduracion embrionaria del tejido papilar y pericoronario del foliculo dental--y no por reabsorcion radicular. (28) Por otra parte, algunos autores (25, 29) reportan que el movimiento dental no produce efectos adversos en dientes con apices inmaduros, como lo describen Sameshima y Sinclair en 2001, quienes observaron mayor resistencia a la reabsorcion radicular. (25)

El objetivo de esta revision es determinar los efectos a largo plazo del movimiento dental ortodoncico en dientes que no han terminado su formacion radicular.

MATERIALES Y METODOS

Esta revision sistematica se fundamento en los lineamientos de Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). Se utilizo el formato PICO para las revisiones sistematicas (tabla 1).

Se hizo una busqueda electronica en las siguientes bases de datos: PubMed, Cochrane, Dentistry and Oral Sciences Source, Science Direct, Google Scholar, IdeA, ProQuest, Embase, Medline, Lilacs, TRIP. Tambien se realizo una busqueda manual y de literatura gris en la biblioteca Juan Roa Vasquez de la Universidad El Bosque.

Para la seleccion de los estudios se aplicaron los siguientes criterios de inclusion: articulos publicados entre 1990 y 2014, estudios en humanos, ensayos clinicos aleatorizados, metaanalisis, estudios prospectivos y retrospectivos en todos los idiomas, estudios realizados en denticion mixta temprana con sistema 2 x 4 y que utilicen radiografias periapicales. Los criterios de exclusion fueron: estudios con pacientes con sindromes y labio paladar flsurado (LPF), antecedentes de trauma dentoalveolar, series de casos y reportes de casos (tabla 2).

Para la busqueda electronica y manual, se utilizaron las siguientes palabras clave: Orthodontic fixed appliances, orthodontic tooth movement, incomplete root formation, apical root closure, root maturation, root resorption (tabla 3).

La seleccion inicial de los articulos se baso en la lectura del titulo y luego del resumen para escoger los estudios mas relevantes segun los criterios de inclusion; posteriormente se reviso el texto completo de los articulos seleccionados.

La pregunta de investigacion fue: ?Podria el movimiento dental ortodoncico en dientes inmaduros inducir cambios en la longitud radicular, ausencia de cierre apical, reabsorcion radicular o ninguna alteracion, al ser comparados con un grupo no intervenido?

Las palabras clave, los criterios de inclusion y la seleccion de los articulos se realizaron independientemente por los cuatro investigadores, y cualquier desacuerdo se resolvio mediante la discusion.

La calificacion metodologica de los estudios se baso en la revision sistematica efectuada por Lagravere y colaboradores, (30) a la cual se le hicieron las modificaciones descritas en la tabla 4.

Todos los articulos elegidos en texto completo fueron sometidos a esta calificacion. El puntaje maximo correspondia a 20 puntos (tabla 5). Los investigadores calificaron independientemente cada uno de los articulos seleccionados, y obtuvieron una escala de evaluacion metodologica calculando un CCI (coeficiente de correlacion intraclase). Los valores fluctuaron entre 0,97 y 1, los cuales son valores adecuados de concordancia (tabla 6).

RESULTADOS

Los resultados de la busqueda se observan en el flujograma (figura 1). La busqueda electronica arrojo como resultado 5.870 articulos (PubMed 738, Cochrane 3, Dentistry and oral Sciences Source 1.414, Science Direct 2.022, Google Scholar 117, IdeA 45, ProQuest 1.478, Embase 10, Medline 27, Lilacs 11, TRIP 5).

La busqueda manual no arrojo ningun resultado. Luego de revisar los titulos y eliminar los registros y citas duplicadas, 54 articulos cumplieron con los criterios de Inclusion. Despues de leer los resumenes, se seleccionaron 14 articulos para su lectura en texto completo; se excluyeron 10 articulos por las siguientes razones: eran estudios histologicos, los dientes tratados presentaban trauma o tratamiento endodontico previo, o eran articulos de opinion de expertos o de revision de la literatura (tabla 7). Finalmente, 4 articulos se seleccionaron para llevar a cabo la evaluacion metodologica. Las caracteristicas de los articulos se encuentran en la tabla 8. Esta muestra no fue suficiente para realizar pruebas de heterogeneidad estadistica como la prueba Q de Cochran, I cuadrado o prueba H. Por lo tanto, los resultados se presentaran de forma cualitativa para responder a la siguiente pregunta de investigacion: ?Cuales son los efectos del movimiento dental ortodoncico en dientes que no han terminado su formacion radicular?

En el ano 2005, Da Silva y colaboradores (31) encontraron que 5 examinadores no hallaron imagenes de reabsorcion radicular en ninguna de las radiografias evaluadas. Solo 2 examinadores detectaron pequenos signos de reabsorcion radicular en las radiografias periapicales luego de la nivelacion. Uno de los examinadores diagnostico reabsorcion radicular en 4 incisivos, y el otro en un solo incisivo que coincidia con uno de los 4 incisivos ya identificados. Con el analisis estadistico descriptivo simple, la prevalencia de reabsorcion radicular entre los 5 examinadores en los 91 incisivos centrales permanentes correspondia al 4,4%.

Kim y Park en 2004, (32) encontraron que los 4 incisivos demostraron un aumento en la longitud radicular y que el crecimiento radicular se completo en un 70% en el grupo experimental, mientras que en el grupo control la raiz se reabsorbio en un 60%. Los cambios en la longitud radicular entre ambos grupos fueron estadisticamente significativos (p <0,001).

Mavragani y colaboradores, en 2002, (33) encontraron diferencias significativas para tres de los incisivos maxilares cuando se considera el estado pretratamiento de desarrollo radicular entre raices acortadas y alargadas. Hallaron raices mas largas cuando estas estaban poco desarrolladas antes del tratamiento (p = 0,002 para el diente 12, p = 0,030 para el 11, p = 0,356 para el 21 y p = 0,014 para el 22).

Edad al inicio del tratamiento

Mavragani y colaboradores, en 2002, (33) observaron que la edad pretratamiento fue mayor en los pacientes que demostraron acortamiento radicular de los incisivos laterales que en los que presentaron elongacion radicular (p < 0,05). Para el incisivo central, las diferencias en la edad no fueron significativas. El analisis de regresion revelo que la longitud radicular postratamiento de todos los dientes estudiados estuvo relacionada con la edad al inicio del tratamiento. El estado del desarrollo radicular demostro un coeficiente de correlacion significativo solo para el incisivo lateral. En tres de los dientes estudiados, las raices inmaduras al inicio del tratamiento alcanzaron una longitud significativamente mas larga que la de aquellas que ya estaban completamente formadas despues del tratamiento. La diferencia fue significativa para el diente 12, con longitud postratamiento promedio de 14,71 mm para raices completas y de 17,46 mm para raices incompletas (p = 0,03). Diente 21 (15,30 mm y 18,98 mm; p = 0,025); diente 22 (14,14mm y 17,79 mm; p = 0,003). Para el diente 11, la diferencia no alcanzo diferencias significativas (15,51 mm, 16,98 mm; p = 0,111).

Longitud radicular pretratamiento

Kim y Park (32) encontraron que, en el grupo experimental, la longitud radicular fue mas larga antes del tratamiento en 24 incisivos laterales derechos (85,7%), 19 incisivos centrales derechos (67,9%), 22 incisivos centrales izquierdos (78,6%) y 21 incisivos laterales izquierdos (75%). Mientras que en el grupo control la longitud radicular fue mas corta en 19 incisivos laterales derechos (61,3%), 23 incisivos centrales derechos (74,2%), 20 incisivos centrales izquierdos (64,5%) y 20 incisivos laterales izquierdos (64,5%). La relacion corono-radicular entre los dos grupos no demostro una diferencia estadisticamente significativa antes del tratamiento, pero si fue significativa despues del tratamiento, con un alto coeficiente de correlacion para el incisivo lateral izquierdo (p <0,001).

Amlani y colaboradores, en 2007, (34) encontraron que la reabsorcion radicular se observo en 4 de los 50 incisivos laterales (8%). El analisis estadistico demostro que la relacion corono-radicular de los incisivos laterales fue mas grande para los incisivos laterales que no presentaban reabsorcion radicular (p = 0,021).

Longitud radicular durante el tratamiento

Mavragani y colaboradores (33) encontraron que la evaluacion de los cambios en la longitud radicular durante el tratamiento revelo un promedio de perdida de la longitud radicular de 1,86 mm (SE 0,26; rango -3,8 a 6,54 mm) para el diente 12; 1,82 mm (SE 0,26; rango -3,82 a 8,9 mm) para el diente 11; 1,93 mm (SE 0,25; rango -5.7 a 6,27 mm) para el 21 y 1,78 mm (SE 0,33; rango -8.39 a 7,48 mm) para el 22. Se encontraron valores negativos, que indican elongacion radicular, en 50 de 280 dientes.

Longitud radicular despues del tratamiento

Kim y Park (32) encontraron diferencias estadisticamente significativas en la forma radicular, haciendo uso del sistema de medicion de Levander y Malmgren, el cual utiliza cinco grados de reabsorcion para identificar el nivel de reabsorcion radicular. El grupo experimental tenia el valor mas bajo (0,46) en el incisivo lateral derecho y el incisivo central izquierdo, y un valor de 0,50 en el incisivo lateral izquierdo y el incisivo central derecho. En contraste, todos los incisivos del grupo control se encontraron entre 0,90 y 0,97. La diferencia fue estadisticamente significativa para los cuatro incisivos, con un valor p <0,05. La relacion corono-radicular en ambos grupos no demostro diferencias antes del tratamiento, pero si se encontraron diferencias significativas despues del tratamiento, con una correlacion alta para el Incisivo lateral izquierdo (p <0,001).

Mavragani y colaboradores (33) encontraron que las raices alargadas durante el tratamiento tenian una longitud radicular similar a aquellas raices no tratadas en individuos de la misma edad. Para el diente 12, el valor promedio de aumento de la longitud radicular fue de 1,21 mm y en el grupo control el aumento fue de 0,92 mm (p = 0,65). Para el diente 11, el valor promedio de aumento de la longitud fue de 0,68 mm, y para el grupo control fue de 0,82 mm (p = 0,63). La cantidad de elongacion promedio para el diente 21 fue de 0,85 mm y para el grupo control fue de -0,08mm (p = 0,012). Para el diente 22, la elongacion fue de 1,16 mm, mientras que para el grupo control fue de 1,71 mm (p = 0,74).

Tecnica utilizada y la edad antes del tratamiento

Mavragani y colaboradores (33) no encontraron diferencias significativas entre la edad pretratamiento y la tecnica utilizada (p = 0,496). Asi mismo, no hubo diferencia significativa entre los dientes con raices completas o incompletas en relacion con la tecnica de tratamiento. (p = 0,23 para el diente 12, p = 0,17 para el diente 11, p = 0,56 para el diente 21 y p = 0,11 para el diente 22).

Duracion del tratamiento y reabsorcion radicular

Kim y Park (32) encontraron correlacion en el grupo experimental entre la duracion del tratamiento y el achatamiento radicular (p <0,05).

DISCUSION

En la presente revision sistematica se incluyeron cuatro articulos con un nivel de evidencia entre baja y moderada. De los cuatro articulos, tres fueron retrospectivos y uno prospectivo. Ninguno calculo el tamano de la muestra; tampoco reportaron aleatorizacion ni el cegamiento del investigador ni del estadistico. Asimismo, no se reporto la concordancia intraexaminador en ninguno de los estudios y no se establecieron intervalos de confianza. Solo un estudio considero los factores de confusion, determinacion del error de medicion y calibracion intraexaminador.

Existen pocos estudios acerca del comportamiento radicular en dientes con apices abiertos en donde el proceso biologico de formacion radicular aun se encuentra en proceso. Se presenta controversia sobre el riesgo biologico que tiene el movimiento ortodoncico en apices inmaduros. Por una parte, algunos autores (30, 36, 37) coinciden en que los dientes que no han completado su formacion radicular son menos propensos a presentar reabsorcion despues de inducir el movimiento con aparatos fijos. Asimismo, Linge y colaboradores (37) y Mavragani y colaboradores (33) reportan menores danos radiculares en apices con formacion radicular incompleta. Sin embargo, Hendrix y colaboradores (29) encuentran que los dientes con apices abiertos que no alcanzan la longitud normal promedio presentan raices mas largas, comparadas con dientes con apices cerrados, probablemente por el desplazamiento del apice durante el tratamiento. Hamilton y Gutmann (38) reportan que se produce un cierre apical prematuro al aplicar fuerzas ortodoncicas en apices inmaduros. En consecuencia, la principal variable evaluada en su revision sistematica fueron los cambios que se presentaron cuando se hicieron movimientos dentales en apices que no habian terminado su formacion radicular.

En cuanto a los cambios en la longitud radicular antes y despues del tratamiento, el estudio de Kim y Park (32) encuentra una diferencia estadisticamente significativa entre ambos grupos, de modo que se reporta un aumento de la longitud radicular que se completa en un 70%, mientras que en el grupo control la raiz se reabsorbe en un 60%. Dicho estudio concluye que el grado de reabsorcion es leve, debido a que los participantes en el mismo fueron tratados sin exodoncias y por lo tanto la distancia del desplazamiento y la duracion fueron cortas.

En cuanto a la proporcion corono-radicular, Kim y Park (32) no reportan diferencias significativas antes del tratamiento entre las raices con apices inmaduros y las que habian completado su desarrollo. Sin embargo, si hay diferencias significativas entre los dos grupos en el periodo posterior al tratamiento, debido a que las raices inmaduras tienden a desarrollarse, mientras que las raices con apices maduros se reabsorben y se acortan.

Kim y Park (32) encuentran diferencias significativas en cuanto a la forma de la raiz despues del tratamiento de ortodoncia en ambos grupos, utilizando el sistema de medicion descrito por Levander y Malmgren, (39) lo cual se puede explicar porque la forma final de los apices inmaduros fue similar a la forma de los apices maduros.

De igual manera, el cambio en la forma de la raiz se asocio a la duracion del tratamiento: a mayor duracion, permitio la completa formacion de la raiz, seguida por reabsorcion y acortamiento. En conclusion, a pesar de que la posibilidad de reabsorcion en apices inmaduros es reducida, y si la duracion del tratamiento es mas larga, no se deben esperar diferencias con los apices maduros.

En cuanto al cambio de longitud y forma de la raiz, Kim y Park (32) concluyen que, si el tratamiento de ortodoncia se comienza antes de la formacion completa de la raiz, sera conveniente para la reduccion de la reabsorcion radicular. Sin embargo, dicho estudio se basa en cambios observados en radiografias de apices inmaduros, excluyendo otros factores como los aspectos histologicos, la historia de trauma o los habitos.

Por otra parte, Da Silva y colaboradores (31) reportan que el riesgo de reabsorcion, o cualquier alteracion en raices en formacion durante el movimiento inducido en incisivos permanentes con apices abiertos, es practicamente nulo. De igual forma, Rudolph (35) concuerda con que el tratamiento de ortodoncia es menos perjudicial en raices en formacion, es decir, cuando se inicia tempranamente. Sin embargo, dicho resultado se debe analizar cuidadosamente, debido a la metodologia empleada (el uso de radiografias panoramicas), pues los autores tomaron como referencia la edad cronologica y no el estadio de formacion radicular, lo que provee poca informacion sobre el estadio de formacion de las raices.

Posteriormente, mediante radiografias periapicales, Linge y colaboradores (37) estudiaron la incidencia y extension de la reabsorcion radicular en incisivos superiores, y encontraron que la reabsorcion radicular fue dos veces mayor en los apices que habian completado su formacion, en comparacion con los apices inmaduros.

Da Silva y colaboradores (31) concluyen que, desde una perspectiva radiografica, no se evidencia iatrogenia en la integridad radicular durante el movimiento de ortodoncia en incisivos centrales permanentes con formacion incompleta.

Mavragani y colaboradores (33) coinciden con lo antes expuesto, dado que en su estudio encuentran que los dientes con formacion radicular parcial antes del tratamiento alcanzan mayor longitud radicular que los dientes con raices completamente formadas al inicio del tratamiento. Por lo tanto, concluyen que el tratamiento de ortodoncia no causa reabsorcion radicular en dientes con apices inmaduros.

Con base en los resultados obtenidos, se debe tener en cuenta que la mayoria de los estudios de ortodoncia fueron escasos y presentaron fallas metodologicas. Sin embargo, los hallazgos de la presente revision coinciden con los de varios autores, (30, 36, 32) quienes sugieren que el tratamiento de ortodoncia en dientes con formacion radicular incompleta no representa un riesgo biologico para su desarrollo.

CONCLUSIONES

Con base en los resultados del presente estudio, se pueden sacar las siguientes conclusiones:

1. La longitud radicular final de los incisivos que no han terminado su cierre apical, y que son movidos con ortodoncia fija, no se altera.

2. La tecnica utilizada parece no ser relevante en la longitud radicular final.

3. Estos resultados hay que tomarlos con mucha cautela porque la evidencia resultante fue baja y media.

4. Se necesitan ensayos clinicos aleatorizados a largo plazo, que nos muestren las alteraciones a nivel radicular en dientes que fueron intervenidos con fuerzas tempranamente.

CONFLICTO DE INTERESES

Esta revision sistematica no presenta conflictos de interes, no fue patrocinada por ninguna casa comercial ni por la Universidad El Bosque.

No se registro ningun protocolo en las bases de datos para revisiones sistematicas.

CORRESPONDENCIA

Isaac Wasserman

wassermanisaac@unbosque.edu.co

Universidad El Bosque

Bogota, Colombia

ISAAC WASSERMAN MILHEM [1], MAYRA LIZBETH BRAVO CASANOVA [2], FELIX ALEXANDER CARABALLO MORENO [2], DIANA ANTONIA GRANADOS PELAYO [2], CLAUDIA PATRICIA RESTREPO BOLIVAR [2]

[1] Odontologo ortodoncista, Director de la Clinica de Tratamiento Temprano, posgrado de Ortodoncia, Universidad El Bosque, Bogota, Colombia.

[2] Odontologo, residente del posgrado de Ortodoncia, Universidad El Bosque, Bogota, Colombia.

RECIBIDO: NOVIEMBRE 11/14--ACEPTADO: SEPTIEMBRE 29/15

Leyenda: Figura 1. Flujograma

Figure 1. Flowchart
Tabla 1. Formato PICO

Participantes             Ninos en denticion mixta temprana
Intervencion                        Sistema 2 x 4
Comparacion                  Grupo control no intervenido
Outcome          Cambios en la longitud radicular, ausencia de cierre
                            apical, reabsorcion radicular

Hipotesis nula     No se producen cambios en la raiz del diente con
                   apice inmaduro cuando este es movido por fuerzas
                                     ortodoncicas

Tabla 2. Criterios de inclusion y exclusion

Humanos

Ensayos clinicos aleatorizados, metaanalisis

Estudios prospectivos y retrospectivos

Todos los idiomas

1990-2014

Denticion mixta temprana con sistema 2 x 4

Estudios que utilicen Rx periapicales

Pacientes con sindromes y LPF

Antecedentes de trauma dentoalveolar

Series de casos, reportes de casos

Tabla 3. Bases de datos

Base de datos                        Numero de
                                     articulos

PubMed                                   738
Cochrane                                   3
Dentistry and Oral Sciences Source     1.414
Science Direct                         2.022
Google Scholar                           117
IdeA                                      45
ProQuest                               1.478
Embase                                    27
Medline                                   10
Lilacs                                    11
TRIP                                       5

Tabla 4. Protocolo de calificacion metodologica

Items de evaluacion                                         Puntaje *

1. Diseno del estudio                                       (/9 puntos
                                                            posibles)
A. Objetivo: El
objetivo esta
claramente formulado

B. Poblacion: se
describieron sus
caracteristicas

C. Criterios de           1. Claramente
seleccion                   descritos
                          2. Adecuados
D. Tamano de muestra      1. Adecuada
                          2. Calculada
                            antes de la
                            recoleccion
                            de los datos

E. Caracteristicas de
linea base:
Caracteristicas
similares de linea base
entre grupos de estudio

F Tiempo de medicion:
Prospectivo/
Retrospectivo

G. Aleatorizacion:
establecida o descrita

2. Medidas del estudio                                      (/5 puntos
                                                            posibles)
H. Metodo de medicion
apropiado al objetivo
del estudio

I. Mediciones a ciegas                     1. Examinador
                                           2. Estadistico
J. Confiabilidad:                          1. Descrita
calibracion de                             2. Adecuado
examinadores

3. Analisis estadistico                      nivel          (/6 puntos
                                             de acuerdo     posibles)
K. Medicion de error:
descrita

L. Analisis estadistico                    1. Apropiado
                                             para el tipo
                                             de dato
                                           2. Analisis
                                             combinando
                                             de subgrupos
M. Factores de
confusion: incluidos en
analisis

N. Nivel de                                Valor de p
significancia                                establecido
estadistica

                                           Intervalos de
                                             confianza

Tabla 5. Escala de puntuacion metodologica

Rango          Calidad

1-7 Puntos       Baja
8-13 Puntos    Moderada
14-20 Puntos     Alta

Tabla 6. Puntaje de calificacion metodologica de los articulos
seleccionados

Autor/ano      A   B     C       D     E   F   G   H       I

               1   2   3   4   5   6   7   8   9   10   11   12

Kim y Park,    1   1   1   0   1   0   0   0   0   1    0    0
2004
Da Silva et    1   1   1   0   0   0   1   1   0   1    0    0
  al., 2005
Amlani et      1   0   0   0   1   0   0   0   0   0    0    0
  al., 2007
Mavragani et   1   1   1   1   1   0   1   0   0   1    0    0
  al., 2002

Autor/ano         J      K       L         M      N    Total

               13   14   15   16   17   18   19   20

Kim y Park,    0    0    0    1    1    0    1    0      8
2004
Da Silva et    0    0    0    0    0    0    0    0      6
  al., 2005
Amlani et      0    0    0    1    0    0    1    0      4
  al., 2007
Mavragani et   0    0    0    1    1    0    1    0     10
  al., 2002

Autor/ano      Calidad

Kim y Park,    Moderada
2004
Da Silva et      Baja
  al., 2005
Amlani et        Baja
  al., 2007
Mavragani et   Moderada
  al., 2002

Tabla 7. Articulos excluidos

Articulo                       Autores                Motivo

Longitudinal clinical and   Neto Godhin De     Se realizo en dientes
radiographic evaluation     Carvalho Giro    tratados endodonticamente
of severely intruded             (42)
permanent incisors in a
pediatric population

Endodontic-orthodontic         Hamilton      Estudio in vitro. Pruebas
relationship: a review of    Gutmann (38)          histologicas
integrated treatment
planning challenges

A radiographic comparison   Blake Woodside    Realizado en pacientes
of apical root resorption    Pharoah (12)    con denticion permanente
after orthodontic
treatment with the
edgewise and speed
appliances

Quantitative digital         Sunku et al     Los pacientes comenzaron
subtraction radiography          (43)            el tratamiento de
in the assessment of                          ortodoncia en denticion
external apical toot                         mixta tardia y denticion
resorption induced by                          permanente completa.
orthodontic therapy: A
retrospective study

Treatment and orthodontic   Mendoza Solano    Los dientes presentaban
movement of a                Segura-Egea       antecedente de trauma
root-fractured maxillary         (44)
centra incisor with an
immature apex: ten-year
follow-up

Orthodontic tooth           Rudzki-Janson    Es un estudio histologico
movement in the mixed          Paschos       en un individuo con algun
dentition: Histological     Diedrich (45)     tipo de enfermedad, no
study of human specimen                      cumple con los criterios
                                                   de inclusion

Determination of working    Kim y Chandler   Realizado en dientes con
length for teeth with            (46)               endodoncia
wide or immature apices:
; review

Risk factors of root          Lopatiene        Es una revision de la
resorption after             Dumbravaite     literatura de 2002 a 2007
orthodontic treatment.           (14)

The effect of fixed           Fenn (47)       No se encontro el texto
orthodontic treatment on                             completo
developing maxillary
incisor root apices

The effects of a              Owman-Moll       Estudio realizado en
four-fold increased              (48)               premolares
orthodontic force
magnitude on toot
movement and root
resorptions. An
intra-individual study in
adolescent

Tabla 8. Descripcion de los estudios seleccionados

Autores/Ano     Muestra          Edad            Grupos empleados

Kim y Park,   59 pacientes    8 a 10 anos    Grupo experimental apices
2004                         +/- 9,8 anos      inmaduros (28) Grupo
                             11 a 15 anos     control apices maduros
                               +/- 12,9                (31)

                                               Solo grupo tratado 46
                                                     pacientes

Da Silva et   46 pacientes    Hombres +/-     79 incisivos centrales
al., 2005                      9,3 anos       superiores 12 incisivos
                                               centrales inferiores

                              Mujeres +/-
                               7,2 anos

Amlani et     26 pacientes        ND           Solo grupo tratado 26
al., 2007                                    pacientes 50 Rx incisivos
                                              laterales 50 Rx caninos

Mavragani     146 pacientes  12,7 anos +/-      Grupo tratado 80 66
et al.,                        8,0- 35,5       controles no tratados
2002

Autores/Ano       Tecnica         Tiempo de observacion

Kim y Park,      Ortodoncia          No fue descrito
2004             correctiva
                                     Hombres 7 meses
              Ortodoncia 2 x 4

Da Silva et                      Mujeres 7 meses y medio
al., 2005

Amlani et     Ortodoncia 2 x 4       No fue descrito
al., 2007

Mavragani     40 pacientes con       No fue descrito
et al.,          ortodoncia
2002          correctiva edge
                 wise y 40
               pacientes con
               estandar slot
                   0,018

Autores/Ano       Variables         Valor de p          Resultados
                  evaluadas

Kim y Park,       Longitud        Significativo p       Los cuatro
2004            radicular de       <0,001 entre         incisivos
                  incisivos        ambos grupos       demostraron un
              superiores antes                        aumento en la
                y despues del                       longitud radicular
                 tratamiento                         y el crecimiento
                                                    se completo en un
                                                    70%, mientras que
                                                       en el grupo
                                                    control la raiz se
                                                     reabsorbio en un
                                                           60%.

              Diferencias en la     Diferencia      La forma radicular
               forma radicular    significativa p       del grupo
              entre los grupos         <0,05        experimental tenia
                utilizando el                       el valor mas bajo
                 sistema de                            (0,46) en el
                 medicion de                         incisivo lateral
                 Levander y                            derecho y el
                  Malmgren                           incisivo central
                                                     izquierdo, y un
                                                     valor de 0,50 en
                                                       el incisivo
                                                    lateral izquierdo
                                                      y el incisivo
                                                     central derecho.
                                                      En contraste,
                                                        todos los
                                                      incisivos del
                                                     grupo control se
                                                    encontraron entre
                                                       0,90 y 0,97.

              Relacion corono-     Significativa       La relacion
               radicular entre          en           corono-radicular
                 los grupos       postratamiento    en ambos grupos no
                                     p <0,001            demostro
                                                    diferencias antes
                                                     del tratamiento
                                                        pero si se
                                                       encontraron
                                                       diferencias
                                                      significativas
                                                       despues del
                                                     tratamiento, con
                                                     una correlacion
                                                       alta para el
                                                     incisivo lateral
                                                        izquierdo.

                Duracion del       Significativa     Hubo correlacion
              tratamiento y el      (p <0,05).         en el grupo
                achata-miento                       experimental entre
                  radicular                            la duracion
                                                      prolongada del
                                                     tratamiento y el
                                                       achatamiento
                                                        radicular.

               Desplazamiento      Significativa       En el grupo
               del incisivo y        (p <0,05)      control, hubo una
                 reabsorcion                           correlacion
               radicular en el                        significativa
                grupo control                            entre el
                                                    desplazamiento del
                                                      incisivo y la
                                                       cantidad de
                                                       reabsorcion
                                                        radicular.

Da Silva et      Imagenes de      No se determino   Cinco examinadores
al., 2005        reabsorcion                          no encontraron
                radicular en                           imagenes de
                  incisivos                            reabsorcion
                superiores e                           radicular en
                 inferiores                           ninguna de las
                 despues del                           radiografias
                 tratamiento                        evaluadas. Uno de
                                                     los examinadores
                                                       diagnostico
                                                       reabsorcion
                                                       radicular en
                                                    cuatro incisivos.
                                                     Con el analisis
                                                       estadistico
                                                       descriptivo
                                                        simple, la
                                                      prevalencia de
                                                       reabsorcion
                                                     radicular entre
                                                        los cinco
                                                     examinadores en
                                                     los 91 incisivos
                                                        centrales
                                                       permanentes
                                                     correspondia al
                                                          4,4%.

Amlani et     Relacion corono-    Significativo p     La reabsorcion
al., 2007       radicular de          = 0,021          radicular se
                  incisivos                          observo en 4 de
              laterales despues                      los 50 incisivos
               del tratamiento                      laterales (8%). El
                                                         analisis
                                                       estadistico
                                                     demostro que la
                                                         relacion
                                                     corono-radicular
                                                     de los incisivos
                                                      laterales con
                                                       reabsorcion
                                                    radicular fue mas
                                                     grande para los
                                                        incisivos
                                                     laterales que no
                                                       presentaban
                                                       reabsorcion
                                                        radicular.

Mavragani     Relacion entre la         No               No hubo
et al.,       edad y la tecnica   significativo p      diferencias
2002              utilizada           = 0,496         significativas
                                                      entre la edad
               Relacion entre           No           pretratamiento y
                 dientes con      significativo p       la tecnica
              raices completas    = 0,23 para el    utilizada. No hubo
               o incompletas y    diente 12, p =        diferencia
                 la tecnica        0,17 para el       significativa
                  utilizada       diente 11, p =    entre los dientes
                                   0,56 para el         con raices
                                  diente 21 y p =      completas o
                                   0,11 para el       incompletas en
                                     diente 22       relacion con la
                                                        tecnica de
                                                       tratamiento.

              Relacion entre la   Significativo p        La edad
                    edad               <0,05        pretratamiento fue
              pretratamiento y                         mayor en los
                 la longitud                          pacientes que
                  radicular                            demostraron
                                                       acortamiento
                                                     radicular de los
                                                        incisivos
                                                     laterales que en
                                                         los que
                                                       presentaron
                                                        elongacion
                                                        radicular.

                  Estado de       Significativo p     Se encontraron
                 desarrollo       = 0,002 para el   raices mas largas
               radicular antes     12, p = 0,030       cuando estas
              del tratamiento y   para el 11, p =      estaban poco
               raices cortas o     0,356 para el      desarrolladas
               largas despues     21 y p = 0,014        antes del
               del tratamiento      para el 22         tratamiento.

                Alargamiento            No          Para el diente 12,
                radicular en      significativo p   el valor promedio
               relacion con el    = 0,65 para el    para el aumento de
                grupo control      diente 12 p =       la longitud
                                   0,63 para el      radicular fue de
                                   diente 11 p =     1,21 mm y en el
                                   0,012 para el     grupo control el
                                   diente 21 p =      aumento fue de
                                   0,74 para el      0,92 mm. Para el
                                     diente 22        diente 11, el
                                                      valor promedio
                                                    para el aumento de
                                                    la longitud fue de
                                                    0,68 mm y para el
                                                    grupo control fue
                                                      de 0,82 mm. La
                                                       cantidad de
                                                        elongacion
                                                     promedio para el
                                                     21 fue 0,85 mm y
                                                      para el grupo
                                                    control -0,08 mm.
                                                    Para el diente 22,
                                                    la elongacion fue
                                                       de 1,16 mm,
                                                    mientras que para
                                                     el grupo control
                                                     fue de 1,71 mm.

               Relacion entre     Significativo p     En tres de los
              raices inmaduras    = 0,03 para el         dientes
              y raices maduras     diente 12 p =     estudiados, las
                  antes del        0,025 para el     raices inmaduras
                 tratamiento       diente 21 p =      al inicio del
                                   0,003 para el       tratamiento
                                   diente 22 p =      alcanzaron una
                                   0,111 para el         longitud
                                     diente 11      significativamente
                                                      mas larga que
                                                     aquellas que ya
                                                         estaban
                                                      completamente
                                                     formadas despues
                                                     del tratamiento.
                                                    La diferencia fue
                                                    significativa para
                                                     el diente 12; la
                                                         longitud
                                                      postratamiento
                                                      promedio para
                                                     raices completas
                                                     fue de 14,71mm y
                                                     para las raices
                                                    incompletas fue de
                                                     17,46 mm. Diente
                                                      21 (15,30 mm y
                                                    18,98 mm); diente
                                                      22 (14,14 mm y
                                                    17,79 mm). Para el
                                                      diente 11, la
                                                      diferencia no
                                                         alcanzo
                                                       diferencias
                                                      significativas
                                                    (15,51 mm y 16,98
                                                           mm).


ORTHODONTIC TOOTH MOVEMENT IN IMMATURE APICES. A SYSTEMATIC REVIEW

INTRODUCTION

Several studies in fully close apices report the response of teeth and supporting tissues to orthodontic movement. (1, 2) Tooth movement with fixed appliances creates constant and continuous forces allowing bone remodeling with no apparent deleterious effects, (3) according to the theory of presion-tension, (4) which states that reabsorption occurs in the area of pressure and apposition in the tension zone. (3) The cells responsible for and regulators of this mechanism are osteoclasts, osteoblasts, osteocytes, and their chemical mediators. (5, 6) When these forces are excessive, they cause a larger area of hyalinization, (7, 8) necrosis, and bone resorption, producing damage in periodontium, pulp, and teeth roots. (3, 9) Of these effects, the most commonly attributed to orthodontic treatment is external root resorption. (10, 11) This condition has been widely studied and is defined as loss of organic and inorganic component of hard radicular tissue, such as dentin and cement, (12, 13) associated with other factors such as age, (13,14) gender, (15) trauma, (11) malocclusion, (16, 17) root anatomy, (18, 19) device type, (20) used mechanism, (16) characteristics of tooth movement, (21,22) force type, (23, 24) and treatment time. (25) We can say that its cause is in general multifactorial. (10)

Tooth movement with open apices which have not completed root formation has not been sufficiently studied. Some authors (26, 27) suggest that tooth movement in immature apices could be a risk factor for root resorption or reduced root length by premature apical closure, as described by Oppenheimen in 1942 and Phillips in 1955, who attributed it to the deformation of Hertwig sheath, which alters the calcification of apex and therefore root development preventing it from reaching maximum length. (26, 27) In 2001, Consolaro et al noted that the movement of teeth with incomplete root formation creates a decrease in root length by early apex closing--which depends on embryo maturation of papillary and pericoronal tissue of dental follicle--and not by root resorption. (28) On the other hand, some authors (25, 29) report that tooth movement does not produce adverse effects on teeth with immature apices, as described by Sameshima and Sinclair in 2001, who observed greater resistance to root resorption. (25)

The goal of this review is to determine the longterm effects of orthodontic tooth movement in teeth that have not completed root formation.

MATERIALS AND METHODS

This systematic review was based on the guidelines of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). It used the PICO format for systematic reviews (table 1).

An electronic search was conducted in the following databases: PubMed, Cochrane, Dentistry and Oral Sciences Source, Science Direct, Google Scholar, IdeA, ProQuest, Embase, Medline, Lilacs, TRIP. A manual search was also conducted for grey literature in Universidad El Bosque Juan Roa Vasquez Library.

The following inclusion criteria were used for article selection: articles published since 1990 to 2014, studies in humans, clinical randomized trials, meta-analysis, prospective and retrospective studies in all languages, studies in early mixed dentition with 2x4 system using periapical radiographs. The exclusion criteria were: studies on patients with syndromes and cleft lip and palate (CLP), history of dentoalveolar trauma, case series, and case reports (table 2).

The following key words were used for both the electronic and manual search: orthodontic fixed appliances, orthodontic tooth movement, incomplete root formation, apical root closure, root maturation, root resorption (table 3).

The initial selection of articles involved reading titles and abstracts to choose the most relevant studies according to the inclusion criteria; the full texts of selected articles were then reviewed.

The research question was: ?Can orthodontic tooth movement in immature teeth induce changes in root length, absence of apical closure, root resorption, or no alteration at all, compared with a group that has not been intervened?

Key words, inclusion criteria and article selection were carried out by four independent researchers, and all disagreements were resolved by discussion.

The methodological qualification of studies was based on the systematic review by Lagravere et al, (30) which was modified as described in table 4. All selected full-text articles were subjected to this qualification. The maximum score was 20 points (table 5). The researchers independently scored each of the selected articles, obtaining a methodological assessment scale by calculating ITC (intraclass correlation coefficient). The values ranged from 0.97 to 1, which are appropriate concordance values (table 6).

RESULTS

The search results are described in the flow diagram (Figure 1). The electronic search yielded 5,870 articles (PubMed 738, Cochrane 3, Dentistry and oral Sciences Source 1,414, Science Direct 2,022, Google Scholar 117, IdeA 45, ProQuest 1,478, Embase 10, Medline 27, Lilacs 11, TRIP 5).

The manual search did not yield any results. After reviewing titles and eliminating duplicate records and quotations, 54 articles met the inclusion criteria. After reading the abstracts, 14 articles were selected for reading in full-text; 10 articles were excluded for the following reasons: they were histological studies, the treated teeth showed trauma or previous endodontic treatment, or were opinion articles by experts or literature reviews (table 7). Finally, 4 articles were selected and the methodological evaluation was conducted. The characteristics of articles are listed in table 8. This sample was not sufficient to run tests of statistical heterogeneity such as the Cochran's Q test, I2 or H test. Therefore, the results will be presented in a qualitative manner to answer the following research question: What are the effects of orthodontic tooth movement in teeth that have not completed root formation?

In 2005, Da Silva et al (31) found out that 5 examiners found no root resorption images in any of the evaluated radiographs. Only 2 examiners detected small signs of root resorption in periapical radiographs after leveling. One of the examiners diagnosed root resorption in 4 incisors, and the other in a single incisor that coincided with one of the 4 incisors already identified. Simple descriptive statistical analysis showed that the prevalence of root resorption among 5 examiners in 91 permanent central incisors was 4.4%.

In 2004, Kim & Park (32) found out that 4 incisors showed increased root length and that root growth was completed by 70% in the experimental group, while in the control group the root was reabsorbed by 60%. Changes in root length between the two groups were statistically significant (p < 0.001).

In 2002, Mavragani et al (33) found significant differences for three of the maxillary incisors when considering the pretreatment state of root development between shortened and elongated roots. They found longer roots when they were poorly developed prior to treatment (p = 0.002 for tooth 12, p = 0.030 for 11, p = 0.356 for 21 and p = 0.014 for 22).

Age of treatment start up

In 2002, Mavragani et al (33) observed that pretreatment age was higher in patients with root shortening of lateral incisors compared with patients with root elongation (p < 0,05). For the central incisor, age differences were not significant. Regression analysis showed that post-treatment root length in all studied teeth was related to age at baseline. The state of root development showed significance of correlation coefficient for lateral incisors only. In three of the studied teeth, immature roots at baseline reached a significantly longer length than the ones that were already fully formed after treatment. The difference was significant for tooth 12, with an average posttreatment length of 14,71 mm for complete roots and 17.46 mm for incomplete roots (p = 0.03). Tooth 21 (15.30 mm and 18,98 mm; p = 0.025); tooth 22 (14.14 mm and 17.79 mm; p = 0.003). For tooth 11, the difference did not reach significant differences (15.51 mm, 16.98 mm; p = 0.111).

Pre-treatment root length

Kim & Park (32) found out that, in the experimental group, root length was longer before treatment in 24 right lateral incisors (85.7%), 19 right central incisors (67.9%), 22 left central incisors (78.6%), and 21 left lateral incisors (75%). While in the control group root length was shorter in 19 right lateral incisors (61.3%), 23 right central incisors (74.2%), 20 left central incisors (64.5%) and 20 left lateral incisors (64.5%). Crown-root ratio between the two groups did not show statistically significant differences before treatment, but differences were significant after treatment, with a high coefficient of correlation for left lateral incisors (p < 0.001).

In 2007, Amlani et al (34) found root resorption in 4 of 50 lateral incisors (8%). Statistical analysis showed that crown-root ratio in lateral incisor was larger for the lateral incisors with no root resorption (p = 0.021).

Root length during treatment

Mavragani et al (33) found that evaluation of changes in root length during treatment showed an average of root length loss of 1.86 mm for tooth 12 (0.26 SE, -3.8 to 6.54 mm range); 1.82 mm for tooth 11 (0.26 SE, -3.82 to 8.9 mm range); 1.93 mm for tooth 21 (0.25 SE, -5.7 to 6.27 mm range) and 1.78 mm for tooth 22 (0.33 SE, -8.39 to 7.48 mm range). Negative values were found in 50 of 280 teeth, suggesting root canal elongation.

Post-treatment root length

Kim & Park (32) found statistically significant differences in root shape by means of the Levander & Malmgren measuring system, which uses five resorption degrees to identify levels of root resorption. The experimental group had the lowest value (0.46) in the right lateral and left central incisors, and a value of 0.50 in the left lateral and right central incisors. In contrast, all of the incisors in the control group were found between 0.90 and 0.97. The difference was statistically significant for the four incisors, with <0.05 p value. Crown-root ratio in both groups showed no pre-treatment differences, but there were significant post-treatment differences, with a high correlation for the left lateral incisor (p < 0.001).

Mavragani et al (33) found out that roots which elongated during treatment had a root length similar to that of un-treated roots in individuals of the same age. For tooth 12, the average value of root length increase was 1.21 mm and in the control group the increase was 0.92 mm (p= 0.65). For tooth 11, the average value of length increase was 0.68 mm, and for the control group was 0.82 mm (p = 0.63). The amount of average elongation for tooth 21 was 0.85 mm and for the control group was -0.08 mm (p = 0.012). For tooth 22, elongation was 1.16 mm, while for the control group was 1.71 mm (p = 0.74).

Technique used and pre-treatment age

Mavragani et al (33) found no significant differences between pretreatment age and technique used (p = 0.496). Similarly, there was no significant differencebetween teethwith incompleteor complete roots in relation to treatment technique (p = 0.23 for tooth 12, p = 0.17 for tooth 11, p = 0.56 for tooth 21 and p = 0.11 for tooth 22).

Duration of treatment and root resorption

Kim & Park (32) found correlation between treatment duration and root flattening (p < 0.05) in the experimental group.

DISCUSSION

This systematic review included four articles with low to moderate levels of evidence. Of the four articles, three were retrospective and one was prospective. None of them calculated sample size, and they did not report randomization nor researcher or statistician blinding. Also, none of them reported intra-examiner concordance and none established confidence intervals. Only one study considered confounders, measurement error, or intra-examiner calibration.

There are few studies on root behavior in teeth with open apices where the biological process of root formation is still in process. There is controversy over the biological risk of orthodontic movement in immature apices. On the one hand, some authors (30, 36, 37) agree that teeth that have not completed root formation are less prone to resorption after inducing movement with fixed appliances. In addition, Linge et al (37) and Mavragani et al (33) report lower root damage in apices with incomplete root formation. However, Hendrix et al (29) found out that teeth with open apices which do not achieve the average standard length usually have longer roots compared to teeth with closed apices, probably due to apex displacement during treatment. Hamilton & Gutmann (38) reported that premature apical closure occurs when applying orthodontic forces on immature apices. In consequence, the main variable evaluated in their systematic review was the changes occurring when tooth movements were applied on apices that had not completed root formation.

Concerning changes in root length before and after treatment, the study by Kim & Park (32) found statistically significant differences between both groups, reporting increased root length that is complete by 70%, while in the control group the root reabsorbed by 60%. Their study concludes that the resorption degree was low because participants were treated without extractions and therefore both displacement distance and duration were short.

Concerning crown-root ratio, Kim & Park (32) reported no significant differences before treatment between roots with immature apices and those that had completed their development. However, there were significant post-treatment differences between the two groups, since immature roots tend to grow while roots with mature apices are reabsorbed and shorten.

Kim & Park (32) found significant differences in terms of root shape after orthodontic treatment in both groups, using the measuring system described by Levander and Malmgren, (39) which can be explained because the final shape of immature apices was similar to the shape of mature apices.

Similarly, the change in root shape was associated with treatment duration: longer treatment periods allowed complete root formation, followed by reabsorption and shortening. In conclusion, while the possibility of reabsorption in immature apices is low, in longer treatments one should not expect differences with mature apices.

Concerning changes in root length and shape, Kim & Park (32) concluded that starting orthodontic treatment before full root formation is convenient for reducing root resorption. However, their study is based on changes observed in x-rays of immature apices, excluding other factors such as histological aspects, history of trauma, or habits.

On the other hand, Da Silva et al (31) reported that the risk of resorption or any other alteration in roots in formation during induced movement in permanent incisors with open apices is practically non-existent. In the same way, Rudolph (35) agrees that orthodontic treatment is less damaging in roots in formation, i.e., when it is started early. However, this result should be taken carefully because of the methodology used (panoramic radiographs), since the authors took chronological age as a reference instead of the stage of root formation, thus providing little information on the stage of root formation.

Subsequently, by means of periapical radiographs, Linge et al (37) studied the incidence and extent of root resorption in maxillary incisors, finding out that root resorption was two times higher in apices which had completed their formation, compared with immature apices.

Da Silva et al (31) concluded that, from a radiographic perspective, there is no evidence of iatrogenesis in root integrity during orthodontic movement in permanent central incisors with incomplete formation.

Mavragani et al (33) agree, as in their study they found out that teeth with partial root formation prior to treatment reach longer root length than teeth with fully formed roots when treatment starts. Therefore, they conclude that orthodontic treatment does not cause root resorption in teeth with immature apices.

Based on the obtained results, we must bear in mind that most orthodontic studies were scarce and had methodological weaknesses. However, the findings of the present review agree with those of several authors, (30, 36, 32) who suggest that orthodontic treatment in teeth with incomplete root formation does not represent a biological risk for its development.

CONCLUSIONS

Based on the results of the present study, the following conclusions can be drawn:

1. There are no alterations in the final root length of incisors that have not completed apical closure and which are moved with fixed orthodontics.

2. The technique used does not seem to be relevant in final root length.

3. These results should be taken cautiously because the resultant evidence was low to moderate.

4. Long-term randomized clinical trials are needed in order to show root alterations in teeth that have received early treatment with forces.

CONFLICT OF INTEREST

This systematic review does not have any conflicts of interest; it was not sponsored by any company or by Universidad El Bosque.

No protocol for systematic reviews was found in the databases.

CORRESPONDING AUTHOR

Isaac Wasserman

wassermanisaac@unbosque.edu.co

Universidad El Bosque

Bogota, Colombia

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(27.) Phillips, J. Apical Root Resorption Under Orthodontic Therapy. Angle Orthod 1955; 25(1): 1-22.

(28.) Consolaro A, Ortiz M, Velloso, T, Dentes com rizogenese incompleta e movimento ortodontico: bases biologicas. R Dental Press Ortodon Ortop Facial 2001; 6(2): 25-30.

(29.) Hendrix I, Carels C, Kuijpelrs-Jagtman AM, Van'T-Hof M. A radiographic study of posterior apical root resorption in orthodontic patients. Am J Orthod Dentofacial Orthop 1994; 105(4): 345-349.

(30.) Lagravere M, Majorb P, Flores C. Long-term skeletal changes with rapid maxillary expansion: a systematic review. Angle Orthod 2005; 75(6): 1046-1052.

(31.) Da Silva Filho O, Mendez Ode F, Ozawa TO, Ferrari Junior FM, Correa TM. Behavior of partially formed roots of teeth submitted to orthodontic movement. J Clin Pediatr Dent 2005; 28 (2): 147-154

(32.) Kim H, Park S. The changes of root length and form in immature teeth after orthodontic treatment. Korean J Orthod 2004; 3 (3): 241-251.

(33.) Mavragani M, Egil O, Wisth B, Selvig K. Changes in root length during orthodontic treatment: advantages for immature teeth. Eur J Orthod 2002; 24(1): 91-97.

(34.) Amlani MS, Inocencio F, Hatibovic-Kofman S. Lateral incisor root resorption and active orthodontic treatment in the early mixed dentition. Eur J Paediatr Dent 2007; 8(4): 188-192.

(35.) Rudolph CE. An evaluation of root resorption occurring during orthodontic treatment. J Dent Res 1940; 19(4): 367371.

(36.) Reitan K. Initial tissue behavior during apical root resorption. Angle Orthod 1974; 44(1): 68-82.

(37.) Linge B. Ohm, Linge L. Apical root resorption in upper anterior teeth. Eur J Orthod 1983; 5(3): 173-183.

(38.) Hamilton RS, Gutmann JL. Endodontic-orthodontic relationships: a review of integrated treatment planning challenges. Int Endod J 1999; 32(5): 343-360.

(39.) Levander E, Malmgren O. Evaluation of the risk of root resorption during orthodontic treatment: a study of upper incisors. Eur J Orthod 1988; 10(1): 30-38.

(40.) Rosenberg M. An evaluation of the incidence and amount of apical root resorption and dilaceration occurring in orthodontically treated teeth having incompletely formed roots at the beginning of Begg treatment. Am J Orthod 1972; 61(5): 524-525.

(41.) Stenvik A, Ivar A. The effect of experimental tooth intrusion on pulp and dentine. Oral Surg Oral Med Oral Pathol 1971; 32(4): 639-648.

(42.) Neto JJ, Gondim JO, de-Carvalho FM, Giro EM. Longitudinal clinical and radiographic evaluation of severely intruded permanent incisors in a pediatric population. Dent Traumatol 2009; 25(5): 510-514.

(43.) Sunku R, Roopesh R, Kancherla P, Perumalla KK, Yudhistar PV, Reddy VS. Quantitative digital subtraction radiography in the assessment of external apical toot resorption induced by orthodontic therapy: A retrospective study. J Contemp Dent Pract 2011; 12(6): 422-428.

(44.) Mendoza A, Solano E, Segura-Egea J. Treatment and orthodontic movement of a root-fractured maxillary central incisor with an immature apex: 10-year follow-up. Int Endod J 2010; 43(12): 1162-1170.

(45.) Rudzki-Janson E, Paschos E, Diedrich P. Orthodontic tooth movement in the mixed dentition: Histological study of a human specimen. J Orofac Orthop 2001; 62(3): 177190.

(46.) Kim YJ, Chandler NP. Determination of working length for teeth with wide or immature apices: a review. Int Endod J 2013; 46(6): 483-491.

(47.) Fenn KM. The effect of fixed orthodontic treatment on developing maxillary incisor root apices. Am J Orthod Dentofacial Orthop 1998; 114(5): A1.

(48.) Owman-Moll P. The effects of a four-fold increased orthodontic force magnitude on tooth movement and root resorptions. An intra-individual study in adolescents. Eur J Orthod 1996; 18 (3): 287-294.

ISAAC WASSERMAN MILHEM [1], MAYRA LIZBETH BRAVO CASANOVA [2], FELIX ALEXANDER CARABALLO MORENO [2], DIANA ANTONIA GRANADOS PELAYO [2], CLAUDIA PATRICIA RESTREPO BOLIVAR [2]

[1] Orthodontist, Head of Clinica de Tratamiento Temprano, Graduate Program in Orthodontics, Universidad El Bosque, Bogota, Colombia.

[2] DMD, Intern in the Graduate Program in Orthodontics, Universidad El Bosque, Bogota, Colombia.

SUBMITTED: NOVEMBER 11/14--ACCEPTED: SEPTEMBER 29/15
Table 1. PICO Format

Participants              Children in early mixed dentition
Intervention                         System 2 x 4
Comparison                  Non-intervention control group
Outcome           Changes in root length, absence of apical closure,
                                   root resorption

Null hypothesis   No changes in the root of teeth with immature apex
                           when moved by orthodontic forces

Table 2. Inclusion and exclusion criteria

Human beings

Clinical randomized trials, meta-analysis

Prospective and retrospective studies

All languages

1990-2014

Early mixed dentition with 2 x 4 system

Studies using periapical Rx

Patients with syndromes and CLP

History of dentoalveolar trauma

Case series, case reports

Table 3. Databases

Database                             Number of
                                     articles

PubMed                                   738
Cochrane                                   3
Dentistry and Oral Sciences Source     1.414
Science Direct                         2.022
Google Scholar                           117
IdeA                                      45
ProQuest                               1.478
Embase                                    27
Medline                                   10
Lilacs                                    11
TRIP                                       5

Table 4. Protocol of methodological qualification

Evaluated items                                               Score *

1 Study design                                                (/9
                                                              possible
A. Objective: the objective                                   points)
is clearly formulated

B. Population:
Characteristics were
described

C. Selection criteria         1. Clearly
                                described
                              2. Accurate
D. Sample size                1. Accurate
                              2. Calculated
                                before data
                                collection
E. Baseline
characteristics: Similar
baseline characteristics
among study groups

F Measurement time:
Prospective/Retrospective

G. Randomization:
established or described

2 Measures of the study                                       (/5
                                                              possible
                                                              points
H. Method of measurement is
appropriate to the study's
objective

I. Blind measurements                         1 Examiner
                                              2 Statistics

J. Reliability: calibration                   1 Described
of examiners                                  2. Adequate
                                                level of
                                                agreement
3. Statistical analysis                                       (/6
                                                              possible
                                                              points)
K. Error measurement:
described

L. Statistical analysis                       1. Accurate
                                                for data
                                                type
                                              2. Combined
                                                analysis of
                                                subgroups
M. Confounding factors:
included in analysis

N. Level of statistical                       Established
significance                                    p-value
                                              Confidence
                                                intervals

Table 5. Methodological scoring scale

Range          Quality

1-7 points       Low
8-13 points    Moderate
14-20 points     High

Table 6. Methodological rating score of selected articles

Author/year             A   B   C         D     E   F   G   H

                        1   2   3   4   5   6   7   8   9   10

Kim and Park, 2004      1   1   1   0   1   0   0   0   0   1
Da Silva et al, 2005    1   1   1   0   0   0   1   1   0   1
Amlani et al, 2007      1   0   0   0   1   0   0   0   0   0
Mavragani et al, 2002   1   1   1   1   1   0   1   0   0   1

Author/year                I         J      K       L         M

                        11   12   13   14   15   16   17   18   19

Kim and Park, 2004      0    0    0    0    0    1    1    0    1
Da Silva et al, 2005    0    0    0    0    0    0    0    0    0
Amlani et al, 2007      0    0    0    0    0    1    0    0    1
Mavragani et al, 2002   0    0    0    0    0    1    1    0    1

Author/year             N    Total   Quality

                        20

Kim and Park, 2004      0      8     Moderate
Da Silva et al, 2005    0      6       Low
Amlani et al, 2007      0      4       Low
Mavragani et al, 2002   0     10     Moderada

Table 7. Excluded articles

Article                        Authors                Reason

Longitudinal clinical and   Neto Godhin De      It was conducted in
radiographic evaluation     Carvalho Giro     endodontically treated
of severely intruded             (42)                  teeth
permanent incisors in a
pediatric population

Endodontic-orthodontic         Hamilton           In vitro study.
relationship: a review of    Gutmann (38)       Histological tests
integrated treatment
planning challenges

A radiographic comparison   Blake Woodside       In patients with
of apical root resorption    Pharoah (12)       permanent dentition
after orthodontic
treatment with the
edgewise and speed
appliances

Quantitative digital         Sunku et al         Patients started
subtraction radiography          (43)        orthodontic treatment in
in the assessment of                         mixed dentition and full
external apical toot                           permanent dentition.
resorption induced by
orthodontic therapy: A
retrospective study

Treatment and orthodontic   Mendoza Solano   Because teeth had history
movement of a                Segura-Egea             of trauma
root-fractured maxillary         (44)
central incisor with an
immature apex: ten-year
follow-up

Orthodontic tooth           Rudzki-Janson      It is a histological
movement in the mixed          Paschos        study in an individual
dentition: Histoogical      Diedrich (45)        with some type of
study of a human specimen                    disease; it does not meet
                                              the inclusion criteria

Determination of working     Kim Chandler    It is in teeth with root
length for teeth with            (46)             canal treatment
wide or immature apices:
a review

Risk factors of root          Lopatiene      It is a literature review
resorption after             Dumbravaite         from 2002 to 2007
orthodontic treatment.           (14)

The effect of fixed           Fenn (47)       Full text was not found
orthodontic treatment on
developing maxillary
incisor root apices

The effects of a four-        Owman-Moll        Study conducted in
fold increased                   (48)                premolars
orthodontic force
magnitude on tooth
movement and root
resorptions. An intra-
individual study in
adolescents

Table 8. Description of selected studies

Authors/         Sample           Age              Groups used
year

Kim &         59 patients    8 to 10 years      Experimental group
Park, 2004                    +/-9.8 years     immature apices (28)

                              11-15 years      Control group mature
                                +/- 12.9           apices (31)
                                 Males
                              +/-9.3 years    Only group treated 46
                                                     patients

Da Silva et   46 patients       Females          79 upper central
al, 2005                      +/-7.2 years      incisors 12 lower
                                                 central incisors

Amlani et     26 patients          NA         Only group treated 26
al, 2007                                        patients 50 Rx of
                                              lateral incisors 50 Rx
                                                    of canines

Mavragani     146 patients   12.7 years +/-    Group treated: 80 66
et al, 2002                     8,0-35.5        untreated controls

Authors/               Technique                Time of
year                                          observation

Kim &           Corrective orthodontics      Not described
Park, 2004

                  Orthodontics 2 x 4         Males 7 months

Da Silva et                                 Females 7 months
al, 2005                                       and a half

Amlani et         Orthodontics 2 x 4         Not described
al, 2007

Mavragani     40 patients with edge wise     Not described
et al, 2002   corrective orthodontics and
               40 patients with standard
                      slot 0.018

Authors/      Evaluated variables     p value            Results
year

Kim & Park,    Root length of      Significant p    The four incisors
2004           upper incisors     <0.001 between     showed increased
              before and after      both groups      root length and
                  treatment                             growth was
                                                    completed in 70%,
                                                       while in the
                                                    control group the
                                                         root was
                                                    reabsorbed by 60%.

               Differences in       Significant       Root shape of
              root shape among     difference p     experimental group
              groups using the         <0.05          had the lowest
                  system of                          values (0.46) in
               measurement by                       the right lateral
                Levander and                         and left central
                  Malmgren                           incisors, and a
                                                     value of 0.50 in
                                                     the left lateral
                                                    and right central
                                                       incisors. In
                                                     contrast, all of
                                                     the incisors of
                                                    the control group
                                                    were found between
                                                      0.90 and 0.97.

              Crown-root ratio    Significant in     Crown-root ratio
                inter-groups      post-treatment      in both groups
                                     p <0.001           showed no
                                                    differences before
                                                      treatment, but
                                                        there were
                                                       significant
                                                    differences after
                                                    treatment, with a
                                                     high correlation
                                                     for left lateral
                                                        incisors.

                 Duration of      Significant (p        There was
                treatment and        < 0.05).       correlation in the
               root flattening                      experimental group
                                                     between duration
                                                       of extended
                                                    treatment and root
                                                       flattening.

               Displacement of    Significant (p      In the control
              incisor and root        < 0.05)        group, there was
                resorption in                          significant
                control group                          correlation
                                                     between movement
                                                      of incisor and
                                                      amount of root
                                                       resorption.

Da Silva et    Images of root       Not defined       Five examiners
al, 2005        resorption in                         found no root
               upper and lower                      resorption images
                  incisors                            in any of the
               post-treatment                           evaluated
                                                     radiographs. One
                                                     of the examiners
                                                      diagnosed root
                                                    resorption in four
                                                      incisors. The
                                                    simple descriptive
                                                       statistical
                                                     analysis showed
                                                    that prevalence of
                                                     root resorption
                                                        among five
                                                     examiners in 91
                                                    permanent central
                                                    incisors was 4.4%.

Amlani et     Crown-root ratio    Significant p =    Root resorption
al, 2007         of lateral            0.021         occurred in 4 of
                  incisors                              50 lateral
               post-treatment                       incisors (8%). The
                                                       statistical
                                                     analysis showed
                                                     that crown-root
                                                     ratio in lateral
                                                    incisors with root
                                                      resorption was
                                                      larger for the
                                                     lateral incisors
                                                       with no root
                                                       resorption.

Mavragani       Relationship      Non-significant     There were no
et al, 2002    between age and       p = 0.496         significant
               technique used                          differences
                                                         between
                                                     pretreatment age
                                                      and technique.

                Relationship      Non-significant      There was no
                between teeth      p = 0.23 for        significant
              with complete or     tooth 12, p =    difference between
              incomplete roots    0.17 for tooth        teeth with
                and technique      11, p = 0.56        complete or
                    used           for tooth 21,     incomplete roots
                                   and p = 0.11       in relation to
                                   for tooth 22         treatment
                                                        technique.

                Relationship      Significant p <    Pretreatment age
                   between             0.05           was higher in
              pretreatment age                      patients with root
               and root length                        shortening of
                                                     lateral incisors
                                                     than those with
                                                     root elongation.

                State of root     Significant p =   Longer roots were
                 development      0.002 for 12, p    found when they
              pre-treatment and   = 0.030 for 11,      were poorly
                short or long      p = 0.356 for    developed prior to
                    roots           21 and p =          treatment.
               post-treatment      0.014 for 22

              Root lengthening    Non-significant   For tooth 12, the
               in relation to      p = 0.65 for      average value of
                control group      tooth 12 p =        root length
                                  0.63 for tooth    increase was 1.21
                                   11 p = 0.012       mm while this
                                  for tooth 21 p    value was 0.92 mm
                                    = 0.74 for        in the control
                                     tooth 22        group. For tooth
                                                     11, the average
                                                     value for length
                                                    increase was 0.68
                                                      mm and for the
                                                    control group was
                                                       0.82 mm. The
                                                    average elongation
                                                     amount for tooth
                                                    21 was 0.85 mm and
                                                     for the control
                                                    group 0.08 mm. For
                                                        tooth 22,
                                                      elongation was
                                                    1.16 mm, while for
                                                    the control group
                                                       was 1.71 mm

                Relationship      Significant p =    In three of the
              between immature    0.03 for tooth      studied teeth,
              and mature roots     12 p = 0.025     immature roots at
                pre-treatment     for tooth 21 p    baseline reached a
                                    = 0.003 for       significantly
                                   tooth 22 p =     longer length than
                                  0,111 for tooth    those that were
                                        11            already fully
                                                       formed after
                                                      treatment. The
                                                      difference was
                                                     significant for
                                                    tooth 12; average
                                                      post-treatment
                                                     length for full
                                                    roots was 14.71 mm
                                                    and for incomplete
                                                     roots 17.46 mm.
                                                    Tooth 21 (15.30 mm
                                                      and 18.98 mm);
                                                    tooth 22 (14,14 mm
                                                    and 17,79 mm). For
                                                      tooth 11, the
                                                    difference did not
                                                    reach significant
                                                    differences (15,51
                                                    mm and 16,98 mm).
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