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Dental malocclusion and upper airway obstruction, an otolaryngologist's perspective
International Journal of Pediatric Otorhinolaryngology (2003) 67, 323 /331
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Dental malocclusion and upper airway obstruction, an otolaryngologist’s perspective Dudley J. Weidera,*, Greg L. Bakerb, Fred W. Salvatorielloc a
Dartmouth-Hitchcock Clinic, Department of Surgery/Division of Otolaryngology, Hanover, NH 03756, USA Private practice of Orthodontia, Rt 10 West Lebanon, NH 03756, USA c Private practice of Orthodontia, 3 Summer Street, Hanover, NH 03755, USA b
Received 9 June 2002; received in revised form 13 November 2002; accepted 13 November 2002
KEYWORDS Adenoidectomy; Polaroid; Tonsillectomy
Summary Introduction: This paper, through the presentation of eight case reports and a limited literature review, attempts to illustrate the negative effect that upper airway obstruction can have on developing dental occlusion and the positive effect that upper airway relief can have on the ‘normalization’ of various malocclusion patterns believed to be related to chronic obligate mouth breathing. Objective: To study the effect of airway relief (usually through tonsillectomy and/or adenoidectomy) on various patterns of dental malocclusion. Methods: Children coming to the office of the lead author (D.J.W.) found to be obligate mouth breathers and who also had dental malocclusion had Polaroid ‘bite’ pictures taken at the time of their initial visit. One year or more after their surgery for upper airway relief (tonsillectomy and adenoidectomy in these cases) a second ‘bite’ photograph was taken and compared to the first. Results: In all cases selected in this study there was observed improvement in their dental occlusion within a year following surgery to improve their breathing. Conclusion: It is the opinion of the authors of this paper that upper airway obstruction may have a negative effect on the developing transitional dental occlusion and that eliminating the cause of upper airway obstruction can lead to ‘normalization’ of occlusion in such children. Further orthodontic corrective modalities may be required for optimal occlusal results. – 2002 Elsevier Science Ireland Ltd. All rights reserved.
1. Introduction and personal involvement When I (D.J.W.) began to practice otolaryngology at the Dartmouth Hitchcock Medical Center in April of 1974 I began receiving referrals from orthodon-
*Corresponding author. Present Address: DartmouthHitchcock Clinic, Division of Otolaryngology, Lebanon, NH 03756, USA. E-mail address: [email protected] (D.J. Weider).
tic colleagues in the local area. These referrals were to see if I could ascertain what might be the cause of their obligate mouth breathing. They also wanted me to perform surgery to correct the problem if possible. It was their feeling that upper airway obstruction lead to, or at-least contributed to, dental malocclusion of various types. They supported their views with papers and book chapters from the orthodontic literature, many of which appear footnoted in this article. Most patients referred to me had tonsil and/or adenoid hypertrophy. A few had purely nasal obstruction second-
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D.J. Weider et al.
Table 1 Conditions associated with tonsil and adeniod hypertrophy and naso-pharyngeal obstruction Case
Post. x-bite
Ant. open bite
Rec. tonsilitis (strep throat)*
Rec. OME
(1) (2) (3) (4) (5) (6) (7) (8)
x x x x x x x x
x x x x x
x
x
5 yo F 7 yo F+ 9 yo M++ 8 yo M ffl 3 yo F+ 5 yo M 13 yo F 7 yo F
x
Enuresis
x x x x
x
x
T **
A ** (%)
Touching Touching Touching Touching Touching Almost touching Small** Touching
90 90 55 85 60 80 85 98
Key: F, female; M, male; post. x-bite, posterior cross-bite; ant. open-bite, anterior open-bite; rec. OME, recurrent otitis media with effusion; (+ ) frequent URIs; (++ ) Allergy; (*) more than 3 strep rhtoats/year for 3 years; (**) not removed; (ffl ) nocturnal drooling; T, tonsil size at time of surgery (relaxed and asleep); A, estimated percentage of adenoidal obstruction at the time of surgery (relaxed and asleep). Note: Cases 2, 3, 4, 5 did not have touching tonsils when observed in the office but did when relaxed and asleep at the time of surgery.
ary to septal deviation, vasomotor rhinitis or rarely, polyps. The great majority of patients referred to me were in deed obstructed and often had related otolaryngologic problems as those enumerated in Table 1. In most cases removal of tonsils and/or adenoids did succeed in their conversion to normal nasal breathing resulting in happy parents, patients and orthodontic colleagues. In December of 1981 a 3-year-old girl (Fig. 1a) presented to me with a 3 month history of otitis media with effusion. Additionally, her tonsils were touching and her adenoids were completely obstructive on her lateral soft tissue X-ray. She had a bilateral cross-bite and an anterior open-bite. I (D.J.W.) decided to take a Polaroid picture of her bite and see if it would change over the coming year. I suggested that a tonsillectomy and adenoidectomy be done in addition to bilateral myringotomies and ventillation tubes. Her parents agreed. A year later her bite demonstrated considerable improvement as shown in Fig. 1b. I then went on and continued to take similar ‘before and after shots’ in similar situations. Co-authors (G.L.B. and F.W.S.) joined me by suggesting we follow a number of such cases delaying orthodontic intervention for 2 years.
2. Literature review Perhaps the most intriguing paper to this author (D.J.W.) is the one written by Harvold [1] in 1979. Ten chimpanzees were converted to obligate mouth breathers by placing silastic plugs in their noses for a period of one year. All developed a strategy for breathing, which consisted of making a ‘V shaped’ passage with their tongues, which
protruded slightly from their mouths. This put subtle but constant pressure on their mandibular incisors and created an anterior cross-bite with some open-bite in all subjects. After one year the plugs were removed and in each case the anterior cross-bites tended to revert toward a more normal occlusal pattern. Linder-Anronson’s [2] work with children who had adenoid hyperplasia showed convincingly that nasal obstruction could alter facial growth. He found that children with large adenoids tended to have longer and narrower faces, lower tongue placement, narrower upper jaws, steeper mandibles and more open anterior bites commonly called ‘adenoid facies’ than those with small adenoids. One year after these children had undergone adenoidectomies, he observed a tendency toward ‘normalization’ of their dentofacial measurements. The ‘negative effect’ on facial growth of pharyngeal flap surgery is discussed and documented by Long and McNamara [3]. A secondary effect of reduction in velopharyngeal port size (to improve the quality of speech in the hypernasal cleft palate patient) is a simultaneous increase in nasal airway resistance, thus raising the possibility of compensatory alteration in oropharyngeal muscle function. These may contribute to some of the dentofacial growth changes seen in the cleft palate population. Such surgery simulates, perhaps to a lessor extent, what Harvold was doing with monkeys and LinderAronson found in children with large adenoids. Adenoidal enlargement has long been considered the primary cause of chronic upper airway obstruction in children. The literature uses the term ‘adenoid facies’ or ‘long face syndrome’ to describe the facial expression often seen in these
Dental malocclusion and upper airway obstruction
Fig. 1 (a) Three-year-old girl photographed on 22 December 1981. T and A performed on 14 January 1982. (b) Follow up photograph taken 7 January 1983, 1 year later.
individuals. Characteristic features are open mouth posture, nostrils that are small and poorly developed, short upper lip with a thick pouting lower lip. Dental and skeletal features include maxillary vertical excess with associated gummy smile, narrow V-shaped dental arches described by Tomes [4], anterior open-bite, posterior cross-bites, lower positioning of the tongue to accommodate and oral airway leading to an increased opening of the jaw angle (gonial angle). The environmental theory of abnormal dentofacial growth was recorded as early as 1868 when Dr William Meyer [5] a Danish physician stated that patients with reduced nasal respiration often suffered from poor general health and hearing loss. Tomes [4] postulated that adenoids were the principal cause of mouth breathing
325
which contributed the V-shaped contracted maxilla. This viewpoint was supported by Angle [6] claiming that ‘of all the various cases of malocclusion, mouth breathing is the most potent, constant and varied in its results’. The Functional Matrix Theory proposed by Van der Klaauw and elaborated on by Moss [7] further supports environmental influences on dentofacial development by suggesting that the skeletal system responds to the influences of the adjoining soft tissues which explain the narrow palate and the long face often seen in chronic mouth breathers. The pendulum began to swing toward a genetically determined facial growth pattern in the early 30s and 40s with the serial studies of Broadbent [8] and Brodie [9]. They observed a ‘constancy’ of the facial growth pattern which is established during the first year or two of life. The work of Lundstrom [10] and Goldstein [11] further supported this theory. In the 50s Subtelny [12] re-evaluated the subject and concluded that blockage of normal naso-respiratory function resulted in mouth breathing which had a detrimental effect on the developing denture. Ricketts [13] postulated that the oral and nasal compartments are interdependent. What affects one affects the other. Therefore, normal nasal function is conducive to normal growth of the maxilla and dentition. One of the most frequently sighted papers dealing with nasal airway obstruction and a dentofacial morphology is by Linder-Aronson [2]. This study consisted of 162 pre-pubital children divided into two groups. The control population consisted of 81 children who were grouped into three categories according to the size of the adenoidal mass as assessed on lateral cephalometric films. The experimental population consisted of 81 children who had undergone adenoidectomy for either otitis media or nasal obstruction. Multiple dentitional variables were assessed in this study with the author concluding that enlarged adenoids affect the mode of breathing which can influence dentofacial development. Current articles pertain to the relationship between airway obstruction and the development of the stomatognathic system. McNamara [14], Bresolin et al. [15], Long and McNamara [16], and Quin [17] strongly support the environmental theory. Our own experience at DHMC and community tends to support the environmental theory as we will attempt to show in the case report section of this paper. The orthodontic literature sites many examples of normal occlusal patterns being negatively altered by doing such things as posterior pharyngeal
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flaps [16] to aid a cleft palate child’s speech. In aiding the speech pattern a certain percentage of these children become nocturnal mouth breathers and develop an increase in their gonial angles and some will ‘drift’ into a posterior cross-bite. There are, like wise, plenty of examples of occlusion improving with appropriate surgery to improve the airways of children [2,6,13]. In addition to orthodontic considerations it would be remiss not to mention the importance of establishing a clear upper airway in respect to the establishment of a healthy sleep pattern and it’s secondary benefits which include reduction in nocturnal enuresis [18 /20], sleep disordered breathing [21] and sleep apnea and its related issues and improvement in otologic issues.
3. Method As stated above, in the early 1980s the I (D.J.W.) decided to follow a group of children who came to him in routine course for various otolaryngologic problems who incidentally happened to have obvious malocclusion. These children came to me for various reasons (Table 1), which included recurrent otitis media, sleep apnea, snoring, recurrent sinusitis, recurrent streptococcal sore throats and related (Table 1) problems. In the course of examining the mouth and hypopharynx the dental occlusal pattern would be inspected. If obvious malocclusion existed then a Polaroid photograph would be taken. If the family decided to proceed with the suggested surgery (generally and tonsillectomy and/or adenoidectomy) the surgery would be performed and a year or more later a follow-up photograph would be taken and compared with the original. These comparison photographs form the essence of this paper. During the course of this study an attempt was made to study some of these children in our pulmonary physiology laboratory to see if nasal resistance in the ‘awake patient’ could be used as a guide as to which patients should be considered for surgery. A number of children were studied preoperatively. Even when the tonsils and/or adenoids were obviously anatomically large and seemingly obstructive none of these children seemed to fulfill the criteria for surgery (i.e. demonstrate significant obstruction). Though this aspect of the study was well-intended many of these children when awake and ‘stimulated’ by the discomfort of the apparatus seemed to breath normally during their testing but were obviously ‘obstructed’ when they slept. All snored and most if not all would have met
D.J. Weider et al.
the criteria to what we now term sleep disordered breathing [21].
4. Case reports 4.1. Case 1 A 3-year-old female presented on 22 December 1981 with a 3-month history of hearing loss. She had several documented cases of otitis media with effusion. She was a very heavy ‘open mouth’ breather at night. She had frequent colds and was always stuffy generally being worse in the winter. On physical exam both tympanic membranes were hypervascular and fixed. She had a fairly severe right posterior cross-bite and an anterior open-bite deformity (Fig. 1a). Her tonsils were huge and within 2 mm of touching. Her lateral soft tissue film demonstrated adenoids to be nearly totally obstructive. A tonsillectomy and adenoidectomy was performed on 14 January 1982. Tonsils touched (D.J.W. has found that when children are asleep and relaxed that tonsils frequently will be found to touch each other when during the office examination they may have as much as 1 /1.5 cm between them). Adenoids were occupying about 80% of the choana. On 7 January 1983 (1 year after surgery) she was no longer a nocturnal mouth breather and her bite had improved to the extent that her right posterior cross-bite was nearly gone and her anterior openbite had completely reverted to normal. She did go on to have further orthodontic correction.
4.2. Case 2 A 5-year-old male presented to DHMC on 29 January 1982 referred to D.J.W. by F.W.S. He was mouth breathing all of the time. He snored at night and had nocturnal enuresis [18 /20]. He was also a ‘finger sucker’. His tonsils touched on office exam and his naso-pharyngeal lateral soft tissue film demonstrated only 1 mm of air space between the adenoid pad and his soft palate. He was found to have bilateral otitis media with effusion. He presented with a bilateral cross-bite (Fig. 2a). On 1 March 1982 he had a tonsillectomy and adenoidectomy with bilateral myringotomies and tubes. Photos taken on 2 February 1984 (about 2 years after surgery) demonstrate that his bilateral crossbite was much less apparent (Fig. 2b). He did proceed to have further orthodontic correction. His enuresis completely stopped by his 1-month post-
Dental malocclusion and upper airway obstruction
327
Fig. 2 (a) Five-year-old boy photograph on 29 January 1982. T and A performed on 1 March 1982. (b) Follow up photograph taken 2 February 1984, about 2 years later.
Fig. 3 (a) Five-year-old girl photographed on 2 March 1983. Adenoidectomy performed on 21 March 1983. (b) Follow up photograph taken on 5 May 1984, 10 months later.
operative visit. The relationship between upper airway obstruction and enuresis has been discussed by D.J.W. et al. in other articles [18 /20].
4.3. Case 3 A 5-year-old female was referred to D.J.W. by F.W.S. on 2 March 1983. She was a day and nighttime mouth breather demonstrating a ‘long face’ and a narrow maxillary arch with bilateral posterior cross-bite (Fig. 3a). An adenoidectomy was performed on 21 March 1983 (adenoids 90% obstructing). Within 10 months she had stopped mouth breathing and snoring and her bilateral cross-bite was nearly totally corrected (Fig. 3b). She did go on to have further orthodontic correction.
4.4. Case 4 A 7-year-old female presented to DHMC with a history of recurrent streptococcal sore throats. She was a chronic day and nighttime mouth breather demonstrating light snoring. She also experienced
frequent winter colds. Tonsils were nearly touching and her turbinates were swollen. She had a left posterior cross-bite (Fig. 4a). On 30 July 1985 she had a tonsillectomy and adenoidectomy. Her tonsils not only touched but ‘over lapped’ and her adenoids were more than 90% obstructing. By 15 December 1987 (29 months later) her posterior cross-bite was nearly gone with an anterior openbite remaining. She went on to further orthodontic correction.
4.5. Case 5 A 5-year-old female presented to DHMC on 5 December 1983 with a history of more than 4 streptococcal sore throats for 3 consecutive years. She had a chronic stuffy nose and was a constant day and nighttime mouth breather and snored. On 22 December 1983 she had a tonsillectomy and adenoidectomy. Her tonsils were touching and her adenoids were 90% obstructing. Pre-operatively she had a right posterior cross-bite (Fig. 5a). Breathing
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Fig. 4 (a) Seven-year-old girl photographed on 5 June 1985. T and A performed on 30 July 1985. (b) Follow up photograph taken 15 December 1989, about 4.5 years later.
immediately reverted to normal and sore throats stopped. On 4 October 1990 (7 years later) she returned to my office for post-operative photography demonstrating near normal occlusion (Fig. 5b). She has had no orthodontia.
4.6. Case 6 A 9-year-old male was referred to D.J.W. on 3 May 1988 with a history of chronic day and nighttime mouth breathing, severe snoring and secondary nocturnal enuresis (a dry period of 6 months between ages 3 and 6 years). The nocturnal enuresis re-commenced at age 6, about the same time that his upper airway obstruction became severe. He had ‘4 plus’ tonsilar enlargement, a tendency to left posterior cross-bite and an anterior open-bite (Fig. 6a). On 16 June 1988 he had a tonsillectomy and adenoidectomy. Thirteen months later on 11 July 1989 his anterior open-bite was closed and his cross-bite had improved becoming
D.J. Weider et al.
Fig. 5 (a) Five-year-old girl photographed on 16 October 1983. T and A performed on 22 December 1983. (b) Follow up photograph taken on 4 October 1990, about 12 years later.
less obvious (Fig. 6b). Enuresis stopped almost immediately post-operatively.
4.7. Case 7 An 8-year-old male was referred to D.J.W. on 13 September 1984. Presenting symptoms were chronic nighttime mouth breathing, intermittent daytime mouth breathing, nocturnal drooling and snoring. He also lacked physical stamina. On physical exam his tonsils were almost touching and adenoids were enlarged on his lateral soft tissue films. His pre-operative photographs demonstrate narrow maxillary and mandibular arches with a marked anterior open-bite (Fig. 7A). On 6 November 1984 he underwent tonsillectomy and adenoidectomy. When relaxed and asleep his tonsils touched and the adenoids were found to be 85% obstructing. Post-operatively nocturnal drooling and snoring immediately stopped. Physical stamina returned. Eleven months later on 10 October 1985 his anterior open-bite had resolved
Dental malocclusion and upper airway obstruction
329
Fig. 6 (a) Nine-year-old boy photographed on 3 May 1988. T and A performed on 16 June 1988. (b) Follow up photograph taken on 11 July 1989, about 1 year later.
Fig. 7 (a) Eight-year-old boy photographed on 13 September 1984. T and A performed on 6 November 1984. (b) Follow up photograph taken on 10 October 1989, about 5 years later.
and there is less inward tilt to the mandibular and maxillary cuspids and bicuspids (Fig. 7b).
4.8. Case 8 A 7-year-old female was referred to D.J.W. on 15 September 1988 with a posterior cross-bite and an anterior open-bite (Fig. 8a). She was an occasional snorer but a constant day and nighttime mouth breather. Additionally she averaged about 3 streptococcal sore throats per year and had occasional bouts of otitis media. On physical exam her tonsils were near touching and her lateral soft tissue films demonstrated moderate adenoid hypertrophy. At surgery (18 July 1990) her tonsils were touching and her adenoids were found to be almost completely obstructing the choana (bigger than anticipated on the pre-operative lateral naso-pharyngeal X-rays). Eight months later (4 March 1991) her cross-bite was no longer evident and her open-bite was only very slightly evident (Fig. 8b). Streptococcal sore
throats no longer occurred and she had no further attacks of otitis media.
5. Results Only cases 2, 3 and 8 were referred to D.J.W. by orthodontists. Cases 5 and 8 never had any postoperative orthodontic treatment. With the exception of cases 5 and 8 all eventually underwent orthodontic treatment to further improve an already improving occlusion. All of the orthodontists that D.J.W. works with feel that correcting the chronic mouth-breathing problem greatly facilitates their orthodontic treatment. All of the 8 cases presented demonstrated a definite trend toward improvement in their occlusion.
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D.J. Weider et al.
beginning to experience drift out of occlusion (usually toward a posterior cross-bite). Appropriate interventional surgery will usually arrest the drift. This could be a subject for another paper. I also frequently see adult patients who have never been able to breathe comfortably through their nose with severe uncorrected malocclusion, a major component usually being unilateral or bilateral posterior cross-bite. Though we have only reported on 8 cases we have continued to collect other cases which generally demonstrate the same trend. We challenge other otolaryngologists and pediatricians to continue to make such observations and prove or disprove us. The literature sited and much more not sited generally supports our observations. Likewise, when surgery is performed to convert a normal nasal breather into an obligate mouth breather malocclusion usually results [1,16]. Finally, this material is not presented as ‘new knowledge’ but rather as an attempt to put forth to the ‘non-dental’ and ‘non-orthodontic’ world a subject seldom covered in many otolaryngologic and pediatric training programs.
7. Conclusion Fig. 8 (a) Seven-year-old girl photographed on 15 September 1988. T and A performed on 18 July 1990. (b) Follow up photograph taken on 4 March 1991, only 8 months later.
6. Discussion Admittedly there are some deficiencies in this study. The quality of the photography is amateurish and could have been better. Despite the reduced quality of some of the pictures the authors feel that they still tell the story we are trying to present. Secondly this study has no matched controls. What would have happened to a similar group of children had they not had interventional surgery? We do not know. On the other hand it was my (D.J.W.) feeling that the primary reason that these patients were referred to me was to offer them the best therapy that I could for the conditions for which they were referred (Table 1). That is what I did. I followed their bites as a completely separate issue. I see on a yearly basis from one to three teenagers who have completed their orthodontia despite having uncorrected upper airway obstruction. They tend to present about 3 /6 months after their braces have been removed and they are
It is the feeling of the authors of this paper that the cases presented in this manuscript tend to support the observations of many of the authors sited in the bibliography. Upper airway relief, most commonly by performing an adenoidectomy or tonsillectomy and adenoidectomy, seemingly allows cross- and open-bites and the development of the maxilla and mandible to ‘transition’ to more normal occusal patterns.
Acknowledgements Dr Dudley J. Weider would like to thank Dr Donald J. Neely, DMD for introducing him to this subject.
References [1] E.P. Harvold, Neuromuscular and morphological adaptations in experimentally induced oral respiration. In: J.A. McNamara, (Ed.), Naso-Respiratory Function and Craniofacial Growth. Monograph No. 9. Ann. Arbor., The University of Michigan, 1979. [2] S. Linder-Aronson, Effects of adenoidectomy on dentition and nasopharynx, Am. J. Orthod. 65 (1974) 1 /15. [3] R.E. Long, J.A. McNamara, Facial growth following pharyngeal flap surgery: skeletal assessment on serial lateral
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331
cephalometric radiographs, Am. J. Orthod. 87 (1985) 187 / 196. C.S. Tomes, On the developmental origin of the V-shaped contracted maxilla, Mon. Rev. Dent. Surg. 1 (1872) 2 /5. W. Meyer, On adenoidal vegetation in the nasopharyngeal cavity, their pathology, diagnosis and treatment, Med. Chir. Trans 53 (1991) 191. E.H. Angle, Treatment of Malocclusion of the Teeth, seventh ed., The SS White Dental Manufacturing Co, Philadelphia, 1907. M.L. Moss, in: B.S. Kraus, R. Rei del (Eds.), The Functional Matrix: Functional Cranial Components, in Vistus in Orthodontics, Lea and Febiger, Philadelphia, 1962, pp. 85 /90. B.H. Broadbent, The face of the normal child: Bolton standards and technique, Angle Orthod. 7 (1973) 183 /208. A.G. Brodie, On the growth pattern of the human head from the third month to the eighth year of life, Am. J. Anat. 194 (68) (1941) 209. A. Lundstrom, The significance of genetic and non-genetic factors in the profile of the facial skeleton, Am. J. Orthod. 41 (1955) 819 /826. A. Goldstein, The dominance of the morphological pattern: implications for treatment, Angle Orthod. 23 (1953) 187 / 195. J.D. Subtelny, The significance of adenoid tissue in orthodontia, Angle Orthod. 24 (1954) 59 /69. R.M. Ricketts, The interdependence of the nasal and oral capsules. In: Nasorespiratory function and craniofacial
growth. J.S. McNamara Jr., Monograph No. 9, Craniofacial growth series, Center for Human Growth and Development, The University of Michigan, Ann. Arbor., 1979. J.A. McNamara, Jr., Influence of respiratory pattern on craniofacial growth, Angle Orthod. 51 (1981) 269 /300. D. Bresolin, P.A. Shapiro, G. Shapiro, M.K. Chapko, S. Dassel, Mouth breathing in allergic children: its relationship to dentofacial development, Am. J. Orthod. 8 (1983) 334 / 340. R.E. Long, Jr., J.A. McNamara, Jr., Facial growth following pharyngeal flap surgery: skeletal assessment on serial lateral cephalometric radiographs, Am. J. Orthod. 87 (1985) 187 /196. G.W. Quin, Are dentofacial deformities a preventable disease?, NC Dent. J. 61 (1978) 5 /6. D.J. Weider, P.J. Hauri, Nocturnal enuresis in children with upper airway obstruction, Int. J. Pediatr. Otolaryngol. 9 (1985) 173 /182. D.J. Weider, M.J. Sateia, R.P. West, Nocturnal enuresis in children with upper airway obstruction, Otolaryngol. Head Neck Surg. 105 (1991) 427 /432. K.C. Nowak, D.J. Weider, Pediatric nocturnal enuresis secondary to airway obstruction from cleft palate repair, Clin. Pediatr. 37 (1998) 653 /658. J.P.L. Tang, C.L. Rosen, E.K. Larkin, J.M. DiFiore, J.L. Arnold, S.A. Surovec, J.M. Youngblut, S. Redline, Identification of sleep-disordered breathing in children: variation with event definition, Sleep 25 (2002) 72 /97.
[4] [5]
[6]
[7]
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[10]
[11]
[12] [13]
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[16]
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[19]
[20]
[21]
www.elsevier.com/locate/ijporl
Dental malocclusion and upper airway obstruction, an otolaryngologist’s perspective Dudley J. Weidera,*, Greg L. Bakerb, Fred W. Salvatorielloc a
Dartmouth-Hitchcock Clinic, Department of Surgery/Division of Otolaryngology, Hanover, NH 03756, USA Private practice of Orthodontia, Rt 10 West Lebanon, NH 03756, USA c Private practice of Orthodontia, 3 Summer Street, Hanover, NH 03755, USA b
Received 9 June 2002; received in revised form 13 November 2002; accepted 13 November 2002
KEYWORDS Adenoidectomy; Polaroid; Tonsillectomy
Summary Introduction: This paper, through the presentation of eight case reports and a limited literature review, attempts to illustrate the negative effect that upper airway obstruction can have on developing dental occlusion and the positive effect that upper airway relief can have on the ‘normalization’ of various malocclusion patterns believed to be related to chronic obligate mouth breathing. Objective: To study the effect of airway relief (usually through tonsillectomy and/or adenoidectomy) on various patterns of dental malocclusion. Methods: Children coming to the office of the lead author (D.J.W.) found to be obligate mouth breathers and who also had dental malocclusion had Polaroid ‘bite’ pictures taken at the time of their initial visit. One year or more after their surgery for upper airway relief (tonsillectomy and adenoidectomy in these cases) a second ‘bite’ photograph was taken and compared to the first. Results: In all cases selected in this study there was observed improvement in their dental occlusion within a year following surgery to improve their breathing. Conclusion: It is the opinion of the authors of this paper that upper airway obstruction may have a negative effect on the developing transitional dental occlusion and that eliminating the cause of upper airway obstruction can lead to ‘normalization’ of occlusion in such children. Further orthodontic corrective modalities may be required for optimal occlusal results. – 2002 Elsevier Science Ireland Ltd. All rights reserved.
1. Introduction and personal involvement When I (D.J.W.) began to practice otolaryngology at the Dartmouth Hitchcock Medical Center in April of 1974 I began receiving referrals from orthodon-
*Corresponding author. Present Address: DartmouthHitchcock Clinic, Division of Otolaryngology, Lebanon, NH 03756, USA. E-mail address: [email protected] (D.J. Weider).
tic colleagues in the local area. These referrals were to see if I could ascertain what might be the cause of their obligate mouth breathing. They also wanted me to perform surgery to correct the problem if possible. It was their feeling that upper airway obstruction lead to, or at-least contributed to, dental malocclusion of various types. They supported their views with papers and book chapters from the orthodontic literature, many of which appear footnoted in this article. Most patients referred to me had tonsil and/or adenoid hypertrophy. A few had purely nasal obstruction second-
0165-5876/03/$ - see front matter – 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 1 6 5 - 5 8 7 6 ( 0 2 ) 0 0 3 9 4 - 4
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D.J. Weider et al.
Table 1 Conditions associated with tonsil and adeniod hypertrophy and naso-pharyngeal obstruction Case
Post. x-bite
Ant. open bite
Rec. tonsilitis (strep throat)*
Rec. OME
(1) (2) (3) (4) (5) (6) (7) (8)
x x x x x x x x
x x x x x
x
x
5 yo F 7 yo F+ 9 yo M++ 8 yo M ffl 3 yo F+ 5 yo M 13 yo F 7 yo F
x
Enuresis
x x x x
x
x
T **
A ** (%)
Touching Touching Touching Touching Touching Almost touching Small** Touching
90 90 55 85 60 80 85 98
Key: F, female; M, male; post. x-bite, posterior cross-bite; ant. open-bite, anterior open-bite; rec. OME, recurrent otitis media with effusion; (+ ) frequent URIs; (++ ) Allergy; (*) more than 3 strep rhtoats/year for 3 years; (**) not removed; (ffl ) nocturnal drooling; T, tonsil size at time of surgery (relaxed and asleep); A, estimated percentage of adenoidal obstruction at the time of surgery (relaxed and asleep). Note: Cases 2, 3, 4, 5 did not have touching tonsils when observed in the office but did when relaxed and asleep at the time of surgery.
ary to septal deviation, vasomotor rhinitis or rarely, polyps. The great majority of patients referred to me were in deed obstructed and often had related otolaryngologic problems as those enumerated in Table 1. In most cases removal of tonsils and/or adenoids did succeed in their conversion to normal nasal breathing resulting in happy parents, patients and orthodontic colleagues. In December of 1981 a 3-year-old girl (Fig. 1a) presented to me with a 3 month history of otitis media with effusion. Additionally, her tonsils were touching and her adenoids were completely obstructive on her lateral soft tissue X-ray. She had a bilateral cross-bite and an anterior open-bite. I (D.J.W.) decided to take a Polaroid picture of her bite and see if it would change over the coming year. I suggested that a tonsillectomy and adenoidectomy be done in addition to bilateral myringotomies and ventillation tubes. Her parents agreed. A year later her bite demonstrated considerable improvement as shown in Fig. 1b. I then went on and continued to take similar ‘before and after shots’ in similar situations. Co-authors (G.L.B. and F.W.S.) joined me by suggesting we follow a number of such cases delaying orthodontic intervention for 2 years.
2. Literature review Perhaps the most intriguing paper to this author (D.J.W.) is the one written by Harvold [1] in 1979. Ten chimpanzees were converted to obligate mouth breathers by placing silastic plugs in their noses for a period of one year. All developed a strategy for breathing, which consisted of making a ‘V shaped’ passage with their tongues, which
protruded slightly from their mouths. This put subtle but constant pressure on their mandibular incisors and created an anterior cross-bite with some open-bite in all subjects. After one year the plugs were removed and in each case the anterior cross-bites tended to revert toward a more normal occlusal pattern. Linder-Anronson’s [2] work with children who had adenoid hyperplasia showed convincingly that nasal obstruction could alter facial growth. He found that children with large adenoids tended to have longer and narrower faces, lower tongue placement, narrower upper jaws, steeper mandibles and more open anterior bites commonly called ‘adenoid facies’ than those with small adenoids. One year after these children had undergone adenoidectomies, he observed a tendency toward ‘normalization’ of their dentofacial measurements. The ‘negative effect’ on facial growth of pharyngeal flap surgery is discussed and documented by Long and McNamara [3]. A secondary effect of reduction in velopharyngeal port size (to improve the quality of speech in the hypernasal cleft palate patient) is a simultaneous increase in nasal airway resistance, thus raising the possibility of compensatory alteration in oropharyngeal muscle function. These may contribute to some of the dentofacial growth changes seen in the cleft palate population. Such surgery simulates, perhaps to a lessor extent, what Harvold was doing with monkeys and LinderAronson found in children with large adenoids. Adenoidal enlargement has long been considered the primary cause of chronic upper airway obstruction in children. The literature uses the term ‘adenoid facies’ or ‘long face syndrome’ to describe the facial expression often seen in these
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Fig. 1 (a) Three-year-old girl photographed on 22 December 1981. T and A performed on 14 January 1982. (b) Follow up photograph taken 7 January 1983, 1 year later.
individuals. Characteristic features are open mouth posture, nostrils that are small and poorly developed, short upper lip with a thick pouting lower lip. Dental and skeletal features include maxillary vertical excess with associated gummy smile, narrow V-shaped dental arches described by Tomes [4], anterior open-bite, posterior cross-bites, lower positioning of the tongue to accommodate and oral airway leading to an increased opening of the jaw angle (gonial angle). The environmental theory of abnormal dentofacial growth was recorded as early as 1868 when Dr William Meyer [5] a Danish physician stated that patients with reduced nasal respiration often suffered from poor general health and hearing loss. Tomes [4] postulated that adenoids were the principal cause of mouth breathing
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which contributed the V-shaped contracted maxilla. This viewpoint was supported by Angle [6] claiming that ‘of all the various cases of malocclusion, mouth breathing is the most potent, constant and varied in its results’. The Functional Matrix Theory proposed by Van der Klaauw and elaborated on by Moss [7] further supports environmental influences on dentofacial development by suggesting that the skeletal system responds to the influences of the adjoining soft tissues which explain the narrow palate and the long face often seen in chronic mouth breathers. The pendulum began to swing toward a genetically determined facial growth pattern in the early 30s and 40s with the serial studies of Broadbent [8] and Brodie [9]. They observed a ‘constancy’ of the facial growth pattern which is established during the first year or two of life. The work of Lundstrom [10] and Goldstein [11] further supported this theory. In the 50s Subtelny [12] re-evaluated the subject and concluded that blockage of normal naso-respiratory function resulted in mouth breathing which had a detrimental effect on the developing denture. Ricketts [13] postulated that the oral and nasal compartments are interdependent. What affects one affects the other. Therefore, normal nasal function is conducive to normal growth of the maxilla and dentition. One of the most frequently sighted papers dealing with nasal airway obstruction and a dentofacial morphology is by Linder-Aronson [2]. This study consisted of 162 pre-pubital children divided into two groups. The control population consisted of 81 children who were grouped into three categories according to the size of the adenoidal mass as assessed on lateral cephalometric films. The experimental population consisted of 81 children who had undergone adenoidectomy for either otitis media or nasal obstruction. Multiple dentitional variables were assessed in this study with the author concluding that enlarged adenoids affect the mode of breathing which can influence dentofacial development. Current articles pertain to the relationship between airway obstruction and the development of the stomatognathic system. McNamara [14], Bresolin et al. [15], Long and McNamara [16], and Quin [17] strongly support the environmental theory. Our own experience at DHMC and community tends to support the environmental theory as we will attempt to show in the case report section of this paper. The orthodontic literature sites many examples of normal occlusal patterns being negatively altered by doing such things as posterior pharyngeal
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flaps [16] to aid a cleft palate child’s speech. In aiding the speech pattern a certain percentage of these children become nocturnal mouth breathers and develop an increase in their gonial angles and some will ‘drift’ into a posterior cross-bite. There are, like wise, plenty of examples of occlusion improving with appropriate surgery to improve the airways of children [2,6,13]. In addition to orthodontic considerations it would be remiss not to mention the importance of establishing a clear upper airway in respect to the establishment of a healthy sleep pattern and it’s secondary benefits which include reduction in nocturnal enuresis [18 /20], sleep disordered breathing [21] and sleep apnea and its related issues and improvement in otologic issues.
3. Method As stated above, in the early 1980s the I (D.J.W.) decided to follow a group of children who came to him in routine course for various otolaryngologic problems who incidentally happened to have obvious malocclusion. These children came to me for various reasons (Table 1), which included recurrent otitis media, sleep apnea, snoring, recurrent sinusitis, recurrent streptococcal sore throats and related (Table 1) problems. In the course of examining the mouth and hypopharynx the dental occlusal pattern would be inspected. If obvious malocclusion existed then a Polaroid photograph would be taken. If the family decided to proceed with the suggested surgery (generally and tonsillectomy and/or adenoidectomy) the surgery would be performed and a year or more later a follow-up photograph would be taken and compared with the original. These comparison photographs form the essence of this paper. During the course of this study an attempt was made to study some of these children in our pulmonary physiology laboratory to see if nasal resistance in the ‘awake patient’ could be used as a guide as to which patients should be considered for surgery. A number of children were studied preoperatively. Even when the tonsils and/or adenoids were obviously anatomically large and seemingly obstructive none of these children seemed to fulfill the criteria for surgery (i.e. demonstrate significant obstruction). Though this aspect of the study was well-intended many of these children when awake and ‘stimulated’ by the discomfort of the apparatus seemed to breath normally during their testing but were obviously ‘obstructed’ when they slept. All snored and most if not all would have met
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the criteria to what we now term sleep disordered breathing [21].
4. Case reports 4.1. Case 1 A 3-year-old female presented on 22 December 1981 with a 3-month history of hearing loss. She had several documented cases of otitis media with effusion. She was a very heavy ‘open mouth’ breather at night. She had frequent colds and was always stuffy generally being worse in the winter. On physical exam both tympanic membranes were hypervascular and fixed. She had a fairly severe right posterior cross-bite and an anterior open-bite deformity (Fig. 1a). Her tonsils were huge and within 2 mm of touching. Her lateral soft tissue film demonstrated adenoids to be nearly totally obstructive. A tonsillectomy and adenoidectomy was performed on 14 January 1982. Tonsils touched (D.J.W. has found that when children are asleep and relaxed that tonsils frequently will be found to touch each other when during the office examination they may have as much as 1 /1.5 cm between them). Adenoids were occupying about 80% of the choana. On 7 January 1983 (1 year after surgery) she was no longer a nocturnal mouth breather and her bite had improved to the extent that her right posterior cross-bite was nearly gone and her anterior openbite had completely reverted to normal. She did go on to have further orthodontic correction.
4.2. Case 2 A 5-year-old male presented to DHMC on 29 January 1982 referred to D.J.W. by F.W.S. He was mouth breathing all of the time. He snored at night and had nocturnal enuresis [18 /20]. He was also a ‘finger sucker’. His tonsils touched on office exam and his naso-pharyngeal lateral soft tissue film demonstrated only 1 mm of air space between the adenoid pad and his soft palate. He was found to have bilateral otitis media with effusion. He presented with a bilateral cross-bite (Fig. 2a). On 1 March 1982 he had a tonsillectomy and adenoidectomy with bilateral myringotomies and tubes. Photos taken on 2 February 1984 (about 2 years after surgery) demonstrate that his bilateral crossbite was much less apparent (Fig. 2b). He did proceed to have further orthodontic correction. His enuresis completely stopped by his 1-month post-
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Fig. 2 (a) Five-year-old boy photograph on 29 January 1982. T and A performed on 1 March 1982. (b) Follow up photograph taken 2 February 1984, about 2 years later.
Fig. 3 (a) Five-year-old girl photographed on 2 March 1983. Adenoidectomy performed on 21 March 1983. (b) Follow up photograph taken on 5 May 1984, 10 months later.
operative visit. The relationship between upper airway obstruction and enuresis has been discussed by D.J.W. et al. in other articles [18 /20].
4.3. Case 3 A 5-year-old female was referred to D.J.W. by F.W.S. on 2 March 1983. She was a day and nighttime mouth breather demonstrating a ‘long face’ and a narrow maxillary arch with bilateral posterior cross-bite (Fig. 3a). An adenoidectomy was performed on 21 March 1983 (adenoids 90% obstructing). Within 10 months she had stopped mouth breathing and snoring and her bilateral cross-bite was nearly totally corrected (Fig. 3b). She did go on to have further orthodontic correction.
4.4. Case 4 A 7-year-old female presented to DHMC with a history of recurrent streptococcal sore throats. She was a chronic day and nighttime mouth breather demonstrating light snoring. She also experienced
frequent winter colds. Tonsils were nearly touching and her turbinates were swollen. She had a left posterior cross-bite (Fig. 4a). On 30 July 1985 she had a tonsillectomy and adenoidectomy. Her tonsils not only touched but ‘over lapped’ and her adenoids were more than 90% obstructing. By 15 December 1987 (29 months later) her posterior cross-bite was nearly gone with an anterior openbite remaining. She went on to further orthodontic correction.
4.5. Case 5 A 5-year-old female presented to DHMC on 5 December 1983 with a history of more than 4 streptococcal sore throats for 3 consecutive years. She had a chronic stuffy nose and was a constant day and nighttime mouth breather and snored. On 22 December 1983 she had a tonsillectomy and adenoidectomy. Her tonsils were touching and her adenoids were 90% obstructing. Pre-operatively she had a right posterior cross-bite (Fig. 5a). Breathing
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Fig. 4 (a) Seven-year-old girl photographed on 5 June 1985. T and A performed on 30 July 1985. (b) Follow up photograph taken 15 December 1989, about 4.5 years later.
immediately reverted to normal and sore throats stopped. On 4 October 1990 (7 years later) she returned to my office for post-operative photography demonstrating near normal occlusion (Fig. 5b). She has had no orthodontia.
4.6. Case 6 A 9-year-old male was referred to D.J.W. on 3 May 1988 with a history of chronic day and nighttime mouth breathing, severe snoring and secondary nocturnal enuresis (a dry period of 6 months between ages 3 and 6 years). The nocturnal enuresis re-commenced at age 6, about the same time that his upper airway obstruction became severe. He had ‘4 plus’ tonsilar enlargement, a tendency to left posterior cross-bite and an anterior open-bite (Fig. 6a). On 16 June 1988 he had a tonsillectomy and adenoidectomy. Thirteen months later on 11 July 1989 his anterior open-bite was closed and his cross-bite had improved becoming
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Fig. 5 (a) Five-year-old girl photographed on 16 October 1983. T and A performed on 22 December 1983. (b) Follow up photograph taken on 4 October 1990, about 12 years later.
less obvious (Fig. 6b). Enuresis stopped almost immediately post-operatively.
4.7. Case 7 An 8-year-old male was referred to D.J.W. on 13 September 1984. Presenting symptoms were chronic nighttime mouth breathing, intermittent daytime mouth breathing, nocturnal drooling and snoring. He also lacked physical stamina. On physical exam his tonsils were almost touching and adenoids were enlarged on his lateral soft tissue films. His pre-operative photographs demonstrate narrow maxillary and mandibular arches with a marked anterior open-bite (Fig. 7A). On 6 November 1984 he underwent tonsillectomy and adenoidectomy. When relaxed and asleep his tonsils touched and the adenoids were found to be 85% obstructing. Post-operatively nocturnal drooling and snoring immediately stopped. Physical stamina returned. Eleven months later on 10 October 1985 his anterior open-bite had resolved
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Fig. 6 (a) Nine-year-old boy photographed on 3 May 1988. T and A performed on 16 June 1988. (b) Follow up photograph taken on 11 July 1989, about 1 year later.
Fig. 7 (a) Eight-year-old boy photographed on 13 September 1984. T and A performed on 6 November 1984. (b) Follow up photograph taken on 10 October 1989, about 5 years later.
and there is less inward tilt to the mandibular and maxillary cuspids and bicuspids (Fig. 7b).
4.8. Case 8 A 7-year-old female was referred to D.J.W. on 15 September 1988 with a posterior cross-bite and an anterior open-bite (Fig. 8a). She was an occasional snorer but a constant day and nighttime mouth breather. Additionally she averaged about 3 streptococcal sore throats per year and had occasional bouts of otitis media. On physical exam her tonsils were near touching and her lateral soft tissue films demonstrated moderate adenoid hypertrophy. At surgery (18 July 1990) her tonsils were touching and her adenoids were found to be almost completely obstructing the choana (bigger than anticipated on the pre-operative lateral naso-pharyngeal X-rays). Eight months later (4 March 1991) her cross-bite was no longer evident and her open-bite was only very slightly evident (Fig. 8b). Streptococcal sore
throats no longer occurred and she had no further attacks of otitis media.
5. Results Only cases 2, 3 and 8 were referred to D.J.W. by orthodontists. Cases 5 and 8 never had any postoperative orthodontic treatment. With the exception of cases 5 and 8 all eventually underwent orthodontic treatment to further improve an already improving occlusion. All of the orthodontists that D.J.W. works with feel that correcting the chronic mouth-breathing problem greatly facilitates their orthodontic treatment. All of the 8 cases presented demonstrated a definite trend toward improvement in their occlusion.
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beginning to experience drift out of occlusion (usually toward a posterior cross-bite). Appropriate interventional surgery will usually arrest the drift. This could be a subject for another paper. I also frequently see adult patients who have never been able to breathe comfortably through their nose with severe uncorrected malocclusion, a major component usually being unilateral or bilateral posterior cross-bite. Though we have only reported on 8 cases we have continued to collect other cases which generally demonstrate the same trend. We challenge other otolaryngologists and pediatricians to continue to make such observations and prove or disprove us. The literature sited and much more not sited generally supports our observations. Likewise, when surgery is performed to convert a normal nasal breather into an obligate mouth breather malocclusion usually results [1,16]. Finally, this material is not presented as ‘new knowledge’ but rather as an attempt to put forth to the ‘non-dental’ and ‘non-orthodontic’ world a subject seldom covered in many otolaryngologic and pediatric training programs.
7. Conclusion Fig. 8 (a) Seven-year-old girl photographed on 15 September 1988. T and A performed on 18 July 1990. (b) Follow up photograph taken on 4 March 1991, only 8 months later.
6. Discussion Admittedly there are some deficiencies in this study. The quality of the photography is amateurish and could have been better. Despite the reduced quality of some of the pictures the authors feel that they still tell the story we are trying to present. Secondly this study has no matched controls. What would have happened to a similar group of children had they not had interventional surgery? We do not know. On the other hand it was my (D.J.W.) feeling that the primary reason that these patients were referred to me was to offer them the best therapy that I could for the conditions for which they were referred (Table 1). That is what I did. I followed their bites as a completely separate issue. I see on a yearly basis from one to three teenagers who have completed their orthodontia despite having uncorrected upper airway obstruction. They tend to present about 3 /6 months after their braces have been removed and they are
It is the feeling of the authors of this paper that the cases presented in this manuscript tend to support the observations of many of the authors sited in the bibliography. Upper airway relief, most commonly by performing an adenoidectomy or tonsillectomy and adenoidectomy, seemingly allows cross- and open-bites and the development of the maxilla and mandible to ‘transition’ to more normal occusal patterns.
Acknowledgements Dr Dudley J. Weider would like to thank Dr Donald J. Neely, DMD for introducing him to this subject.
References [1] E.P. Harvold, Neuromuscular and morphological adaptations in experimentally induced oral respiration. In: J.A. McNamara, (Ed.), Naso-Respiratory Function and Craniofacial Growth. Monograph No. 9. Ann. Arbor., The University of Michigan, 1979. [2] S. Linder-Aronson, Effects of adenoidectomy on dentition and nasopharynx, Am. J. Orthod. 65 (1974) 1 /15. [3] R.E. Long, J.A. McNamara, Facial growth following pharyngeal flap surgery: skeletal assessment on serial lateral
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cephalometric radiographs, Am. J. Orthod. 87 (1985) 187 / 196. C.S. Tomes, On the developmental origin of the V-shaped contracted maxilla, Mon. Rev. Dent. Surg. 1 (1872) 2 /5. W. Meyer, On adenoidal vegetation in the nasopharyngeal cavity, their pathology, diagnosis and treatment, Med. Chir. Trans 53 (1991) 191. E.H. Angle, Treatment of Malocclusion of the Teeth, seventh ed., The SS White Dental Manufacturing Co, Philadelphia, 1907. M.L. Moss, in: B.S. Kraus, R. Rei del (Eds.), The Functional Matrix: Functional Cranial Components, in Vistus in Orthodontics, Lea and Febiger, Philadelphia, 1962, pp. 85 /90. B.H. Broadbent, The face of the normal child: Bolton standards and technique, Angle Orthod. 7 (1973) 183 /208. A.G. Brodie, On the growth pattern of the human head from the third month to the eighth year of life, Am. J. Anat. 194 (68) (1941) 209. A. Lundstrom, The significance of genetic and non-genetic factors in the profile of the facial skeleton, Am. J. Orthod. 41 (1955) 819 /826. A. Goldstein, The dominance of the morphological pattern: implications for treatment, Angle Orthod. 23 (1953) 187 / 195. J.D. Subtelny, The significance of adenoid tissue in orthodontia, Angle Orthod. 24 (1954) 59 /69. R.M. Ricketts, The interdependence of the nasal and oral capsules. In: Nasorespiratory function and craniofacial
growth. J.S. McNamara Jr., Monograph No. 9, Craniofacial growth series, Center for Human Growth and Development, The University of Michigan, Ann. Arbor., 1979. J.A. McNamara, Jr., Influence of respiratory pattern on craniofacial growth, Angle Orthod. 51 (1981) 269 /300. D. Bresolin, P.A. Shapiro, G. Shapiro, M.K. Chapko, S. Dassel, Mouth breathing in allergic children: its relationship to dentofacial development, Am. J. Orthod. 8 (1983) 334 / 340. R.E. Long, Jr., J.A. McNamara, Jr., Facial growth following pharyngeal flap surgery: skeletal assessment on serial lateral cephalometric radiographs, Am. J. Orthod. 87 (1985) 187 /196. G.W. Quin, Are dentofacial deformities a preventable disease?, NC Dent. J. 61 (1978) 5 /6. D.J. Weider, P.J. Hauri, Nocturnal enuresis in children with upper airway obstruction, Int. J. Pediatr. Otolaryngol. 9 (1985) 173 /182. D.J. Weider, M.J. Sateia, R.P. West, Nocturnal enuresis in children with upper airway obstruction, Otolaryngol. Head Neck Surg. 105 (1991) 427 /432. K.C. Nowak, D.J. Weider, Pediatric nocturnal enuresis secondary to airway obstruction from cleft palate repair, Clin. Pediatr. 37 (1998) 653 /658. J.P.L. Tang, C.L. Rosen, E.K. Larkin, J.M. DiFiore, J.L. Arnold, S.A. Surovec, J.M. Youngblut, S. Redline, Identification of sleep-disordered breathing in children: variation with event definition, Sleep 25 (2002) 72 /97.
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