EDITOR’S NOTE:From time to time, the JOURNAL receives manuscripts that are well-written and scholarly reviews of important subjects in otolaryngology which challenge us to expand existing information. In most cases, the reviews do not go beyond the obselvations of previous authors, so they do not qualify as original articles.
Upper airway obstruction and craniofaciaI rnorphology JEROLD J. PRINCIPATO, MD, Bethesda, Maryland
Otolaryngologists are being asked with increasing frequency to assess adequacy of the upper airway and to treat upper airway obstructive problems in orthodontic patients. The incentive has been provided by recent studies that purport to relate upper airway obstruction to dental and craniomorphologic changes. It is hypothesized that prolonged oral respiration during critical growth periods in children initiates a sequence of events that commonly results in dental and skeletal changes. In the chronic mouth-breather excessive molar tooth eruption is almost a constant feature, causing a clockwise rotation of the growing mandible, with a disproportional increase in anterior lower vertical face height. Such increases in anterior lower vertical face height are often associated with retrognathia and open bites. Low tongue posture seen with oral respiration impedes the lateral expansion and anterior development of the maxilla. Otolaryngologists have the ability to objectively and accurately assess upper airway patency. Rhinometric assessment before and after application of topical nasal decongestant, in conjunction with clinical examination, provides valuable information regarding upper airway patency and the cause of any existing obstructive pathologic condition. Studies should be designed carefully to control the numerous variables that have an impact on the growing face of a young child so that meaningful data can be obtained in our own field regarding this challenging topic. (OTOWNGOL HEAD NECK SURG 1991;104:881.]
craniofacial morphology and occlusal patterns are influenced by a variety of factors. The issue of upper airway obstruction and its impact on craniofacial development and dental patterns has been considered since the turn of the century. Findings in numerous clinical studies have suggested a relationship between mouth breathing and the development of skeletal and dental abnormalities. The anecdotal nature of some of these reports, poor study designs of others, and the paucity of adequate statistical analysis has prevented general
From the Section of Otolaryngology, George Washington University School of Medicine and Health Services. Presented at the Annual Meeting of the American Academy of Otolaryngology-Head and Neck Surgery, New Orleans, La., Sept. 24-28, 1989. Received for publication March 5 , 1990; accepted Nov. 16, 1990. Reprint requests: Jerold J. Principato, MD, 10401 Old Goergetown Rd., Suite 409, Bethesda, MD 20814. 2311127133
acceptance of the relationship. Adequate investigation of an alleged relationship between the obstructed airway and craniofacial patterns was further thwarted by the use of the commonly used descriptive phrase “adenoid facies. ” This terminology prompted the erroneous notion that the familiar elongated facial pattern, with an open mouth and dull expression, was exclusively related to only or primarily an obstructing adenoid mass. The occurrence of craniofacial changes and abnormal dental patterns in the absence of enlarged adenoids led to skepticism regarding the hypothesis that associated upper airway obstruction with abnormal facial growth and development. The simplistic notion that related only enlarged adenoids to abnormal craniofacial morphology failed to take into account that the pathologic condition causing the obstruction is more often related to disease of the turbinates, septum, and external nasal architecture (Table 1). In addition, an obstructing adenoid mass in a younger child producing abnormal skeletal and dental patterns may well have resolved by the time an
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Table 1. Common causes of upper airway obstruction Cause
%
Allergic rhinitis Adenoid hypertrophy Nonallergic rhinitis Seotal deforrnitv Architectural deformity
43 35 33 13 5
upper airway assessment is performed. Acceptance of the relationship was further hindered by the tonsil and adenoid controversy, which prompted a dramatic decrease in the number of tonsillectomies and adenoidectomies being considered and performed. A report by Linder-Aronson’ in 1970 provided the incentive for a renewed interest in this complex relationship between impaired nasal breathing and facial growth and development. Although he was aware of other common pathologic conditions causing obstruction in the nasal airway, Linder-Aronson’ attempted to relate adenoid size, assessed by means of lateral cephalometric x-ray films, to craniofacial morphology.””” This study and others were meticulously designed and used stringent statistical analysis. Results of the investigations demonstrated a statistically significant relationship between obstructing adenoid tissue and certain skeletal and dental patterns. These changes included rotation of the mandible in a clockwise manner so that the growth of the mandible was in a more vertical and backward direction, often causing elongation of the lower anterior vertical face height, open bite, and retrognathia. The change in the mandibular growth pattern accounted for a very obtuse gonial angle and a steep mandibular plane. Other findings included shallow nasopharyngeal space, narrowing and elevation of the palate, a tendency toward posterior and anterior crossbite, and crowding of the maxillary and mandibular teeth. Subsequent studies demonstrated that the direction of mandibular growth nornialized in a more horizontal or less vertical manner after adenoidectomy and change to nasal respiration. This accelerated growth of the mandible in a more horizontal direction was more apparent in girls and caused diminished lower anterior vertical face height and improvement of the retrognathia. Kerr et al.23 studied mandibular growth patterns in 26 children, treated for nasal obstruction by adenoidectomy, who exhibited a changed mode of breathing postoperatively. These authors concluded that a change from oral to nasal respiration after adenoidectomy resulted in a more anterior direction of growth in the body of the mandible and some reversal of the initial tendency
Fig. I . Child with nasal obstruction.
toward a posterior or clockwise rotation of the mandible. Experiments in primates by Harvold et a1.”-2‘’ demonstrated a variety of skeletal, dental, and muscular alterations in animals with artificially obstructed nasal airways. The magnitude and nature of the changes appeared to be related to the manner in which mouth breathing was accomplished. Consistent elongation of the face with crossbite developed in the animals that maintained oral respiration by persistent protrusion and lowering of the mandible. DentaI, muscular, and skeletal impact on the obstructed primates was less severe and more variable in animals that rhythmically opened and closed their mouths to achieve adequate respiration. These studies suggested that a change to oral respiration was critical in the process leading to craniofacial and dental alterations. The duration of the oral respiration and the age of the obstructed primate were important variables. When the function of the oral cavity became primarily that of respiration for an extended period of time in young growing primates, the form of the skeleton and associated muscles was always altered. Harvold et al.”-”’ concluded that skeletal and dental form in obstructed animals was related to alterations in neuromuscular activity required to maintain the function of adequate respiration through the oral cavity. Postural and anatomic similarities are striking in children and primates with nasal obstruction (Figs. 1 and 2). In recent years, many studies have been published that suggest the degree of impact caused by oral respiration on facial growth and development varies with
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Fig. 2. Primote with nasal obstruction (Photograph, courtesy of E. Horvold)
Table 2. Hypothetical sequence relating upper airway obstruction and orthodontic deformity Sequence
Increased nasal resistance Oral respiration and low tongue posture Excessive molar eruption Molar fulcruming Mandibular rotation Increased ALVFH ~
~
ALVFH, Anterior lower vertical face height
W Fig. 3. Lower anterior vertical face height. Anterior facial height Is direct measurement from anterior nasal spine to menton.
different facial types.”’ Persons with a brachycephalic or broad-faced facial pattern with strong facial musculature, low mandibular plane. and deep bite appear to be less severely affected than those with a disposition toward a more dolichocephalic elongated narrow facial pattern with weaker musculature.
Cheng et al.” recently studied craniofacial niorphology and occlusal patterns in 71 persons with impaired breathing. All of the subjects in the study were assessed by otolaryngologists and underwent rhinometric evaluation of the nasal airway. The researchers concluded that the group with impaired nasal airway had characteristic combinations of skeletal deformities and malocclusions. They concluded that craniofacial morphology and occlusal patterns in persons with obstructed breathing were statistically and significantly different from those of persons with normal nasal airway breathing. The most profound change appeared to be related to the vertical skeletal measurements associated with a longer face and increased dentoalveolar and palatal heights. Because younger subjects with impaired nasal airways had fewer of these craniofacial morphologic and occlusal changes, the authors advocated a multidisciplinary approach involving the oto-
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Fig. 4. Over-erupted posterior teeth often present in children with chronic oral respiration.
Fig. 5. Excessive eruption of posterior teeth causes lower jaw to rotate down and backward.
laryngologist, the pediatrician, and the orthodontist in early recognition of specific combinations of craniofacial features, so that early intervention and correction of pathologic conditions causing nasal obstruction could be offered. Principato et al." compared lower anterior vertical face heights, as determined from lateral cephalometrir x-ray films (Fig. 3), and nasal airway resistance in 60 children. This investigation demonstrated a statistically significant correlation between elevations in nasal airway resistance as determined by active anterior rhinometry and increases in lower anterior vertical face height. From numerous studies over the decades regarding the relationship between nasal obstruction and orthodontic deformity,-'"" a plausible sequence of events be-
gins to emerge. Some of the steps in this extremely variable process cry out for further investigation and remain hypothetical or anecdotal. Nevertheless, a clinical model (Table 2) can be pieced together from the investigative studies. Craniofacial morphology and dental patterns appear to be consequentially affected by long-standing oral respiration during periods of rapid facial growth in susceptible persons.'" A change to oral respiration occurs when nasal resistance reaches some two to three times that of normal. This does not mean that a person with an impaired nasal airway cannot sustain nasal respiration for short periods of time. Nevertheless, the effort is of such magnitude that the oral airway is preferred and more often used. It should be kept in mind that when a person is in reclining position, normal airway resistance is elevated even further.
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Fig. 6. Anterior open bite.
Fig. 8. Lateral forces exerted by tongue positioned in roof of mouth normally influence expansion and growth of maxilla.
Fig. 7. Increased lower vertical face height often associated with strained lip posture and chin pad displacement.
Therefore. borderline obstructive resistances in the upright position frequently are converted to resistances that prompt oral respiration throughout sleep. During oral respiration, the mandible rotates open to a more
downward position. the teeth are naturally apart, and the tongue must assume a low position in the mouth to allow adequate air How. The tongue is no longer in contact with the hard palate and assumes a low posture in the floor of the mouth. Extended durations of mouth breathing at critical times of facial growth and development in children with predisposition to development of a long face are at particular risk for development of the following sequential changes in skeleton and den-
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tition. In the absence of tooth contact over an extended period of time, there often occurs excessive eruption of the posterior molar teeth. This is not seen only during oral respiration in children, but occurs in adults who are missing opposing molar tooth contact as a result of extraction, trauma, or both. Overerupted posterior teeth (Fig. 4), a common finding on lateral cephalometric x-ray films in children undergoing orthodontic management, exert a downward vector of force on the forward-growing mandible, causing the lower jaw to rotate down and back in a clockwise manner (Fig. 5). Although quite variable with different facial types, our dental colleagues frequently associate 1 mm of excessive posterior molar eruption with a 3-mm elongation of the lower anterior vertical face height. Because of the lower jaw rotation, retrognathia is almost always present and anterior open bites are common (Fig. 6). The increase in lower vertical face height often produces lip incompetence and chin pad displacement (Fig. 7). The overall facial pattern can be characterized as an “upper airway obstructed facies.” Some of these rotational skeletal changes, along with open bite, can be reversed partially or completely in young children by therapy directed at intrusion of the molar teeth. Repelling magnets on the contact surfaces of the molar teeth, and external devices such as the wearing of reverse cervical collars, can encourage intrusion of the posterior teeth and closure of the open bite, with diminution of lower anterior vertical face heights. Natural growth and expansion of the maxilla is influenced by tongue forces exerted both at rest and during ~ w a l l o w i n g .Complete ~~ maxillary expansion appears to be dependent on lateral forces exerted by the tongue (Fig. 8). It follows that low tongue posture, as seen in mouth breathers with upper airway obstruction, frequently diminishes or eliminates these lateral expansive forces on the upper jaw (Fig. 9). The diminished force exerted by the tongue on the growth of the maxilla is compounded by the relatively unopposed lingually directed constricting forces exerted on the buccal segment by the taut buccinator and masseter muscles in the open mouth position. One of the goals of the commonly used Frankel orthodontic appliance is to diminish these constricting muscular forces. In the absence of adequate expansion, there often occurs a narrow high maxilla with posterior teeth in crossbite in which the upper maxillary teeth are situated in a more lingual position than the opposing mandibular teeth. This incomplete lateral expansion of the maxilla can result in either a unilateral (Fig. 10) or bilateral crossbite (Fig. 11) pattern. Low tongue posture with limited lateral expansive forces of the tongue is exaggerated when short lingual frenula (Fig. 12) provide additional restriction to tongue motion and posi-
i
Fig. 9. Low tongue posture, as seen during oral respiration, diminishes lateral expansive forces on maxilla.
tioning in the roof of the mouth. It would appear that upper airway obstruction, whether related to adenoid enlargement, chronic rhinitis, or nasal septa1 deformity, can be associated with elongation of the lower anterior face and development of certain abnormal dental patterns. Narrow nasal architecture and wide columellae (Fig. 13) can also create formidable obstructions. Children with predisposition to longer faces are more severely affected by long-standing oral respiration. Early detection and treatment of pediatric nasal obstructive disorder, particularly in children with evidence of early craniofacial and I or dentoalveolar changes would seem justified. The data presented in recent literature supporting the relationship are not without controversy. Vig et al.5’-53 assert that current study conclusions are frequently supported only by circumstantial evidence, and there is little adherence to the Scientific Method. Even if the hypothesis is correct, justifiable concern is raised regarding accurate means of identifying patients at risk. Furthermore, it must be demonstrated with good study designs that there is a tangible benefit on the orthodontic outcome provided by a given medical or surgical intervention. The relative risks/costs of any treatment must be considered. If upper airway obstruction is indeed an important variable initiating dental and skeletal alterations, early recognition and treatment of pathologic conditions causing obstructed airway are in order. Suspicion on the part of the clinicians could be prompted by any or all
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Fig. 10. Unilateral molar crossbite.
Fig. 11. Bilateral molar crossbite.
deleterious impact of consequential obstruction on craof the following: chronic nasal stuffiness. excessive niofacial development is virtually complete by puberty. snoring, open mouth posture and oral respiration, low Hence the opportunity for successful intervention is tongue position (especially with short lingual frenubrief. lum), elongation of the lower anterior face height (parThe necessity for surgery should be carefully conticularly in families with tendency toward doliochosidered. and the procedure and timing should be decephalic facial patterns), posterior tooth crossbite, and termined by the age of the child and the magnitude of overt orthodontic changes. Some of these tendencies the skeletal and dental problem. Delay or absence of are apparent in a child as young as 3 years of age, but appropriate intervention niay result in unsuccessful they are more commonly detected Downloaded after age 5. The from oto.sagepub.com at PENNSYLVANIA STATE UNIV on May 28, 2015
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Fig. 12. Short lingual frenulum restricting tongue mobility.
Fig. 13. Wide nasal columella.
orthodontic treatment, with recurrence in late adolescence and the necessity for orthognathic surgical intervention with osteotomies of either or both the maxilla or mandible. Referral at an early age might include otolaryngologic and orthodontic examination, cephalometric radiology. and rhinometry to determine nasal airway resistance (Table 3). Simultaneous X-y display
of both nasal pressure and air flow, with resistance determinations made at 100 pascals, provides an objective means of assessing the airway. Such devices are readily available and suitable for the clinical setting. In addition to obtaining definitive data with regard to the patency of the upper airway, rhinometry performed before and after nasal lining decongesting allows local-
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-
Rhinitis
vative, but effective. Such a goal is aided by objective evaluation of the airway by means of rhinometric measurements. The timing of the intervention would seem critical. Above all-and in spite of some comments to the contrary-the “quality of life” deformities and disabilities associated with long-standing nasal obstruction do indeed justify serious consideration on the part of pediatricians, dentists, and otolaryngologists.
Enlargement
Septa1 Deformity
Fig. 14. Rhinometry. performed before and after nasal lining decongesting, helps identify site of obstructing pathologic condition.
Table 3. Standard evaluation of children with suspected upper airway obstruction Assessment
Clinical examination Cephalometric x-ray films Rhinomanometry
ization (Fig. 14) of the pathologic condition, causing the obstruction to either the lateral wall of the nose, the adenoids, or the nasal septum and helps in the selection of the appropriate treatment modality.54 Every effort should be made to provide the safest and simplest surgical corrective measure. When indicated, adenoidectomy is very beneficial, as is the selective use of cryosurgery in the management of chronic r h i n i t i ~ . ~ ~Conservative .~’ and judicious use of submucous resection of the inferior turbinate?’ in young children, as well as conservative correction of nasal deformity, can provide substantial relief of the ill effects of nasal obstruction. In conclusion, much more investigation is necessary to completely understand the sequential craniofacial, muscular, and dental changes that appear to result from nasal airway obstruction and oral respiration. The variables are numerous and must be placed in appropriate scientific perspective. The assessment of children at risk should be multidisciplinary, timely, and exhaustive. The selection of surgical modalities should be conser-
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maxilla. Monthly Rev Dent Surg 1872;1:2-5. 2. Tomes CS. The bearing of the development of the jaws on irregularities. Dent Cosmos 1873;15:292-6. 3. Angle EH. Treatment of malocclusion of the teeth. 7th ed. Philadelphia: S S White Dental Manufacturing Co., 1907. 4. Howard AJ. Obstructed nasal respiration and its relation to dental abnormalities. Dent Cosmos 1908;50:453-8. 5. Ketcham AH. Treatment by the orthodontists supplementing that by the rhinologist. Laryngoscope 1912;22:1286-99. 6. Whitaker RHR. The relationship of nasal obstruction to contracted arches and dental irregularities. Dent Rec 191 1;3l: 425. 7. Linder-Aronson S . Adenoids: their effect on the mode of breathing and nasal airflow, and their relationship to characteristics of the facial skeleton and the dentition. Acta Otolaryngol 1970; 265(suppl). 8. Linder-Aronson S , Aschan G. Nasal resistance to breathing and palatal height before and after expansion of the median palatine suture. Odontologist Revy 1963;14:254-70. 9. Linder-Aronson S , Woodside D. The channelization of upper and lower anterior face heights compared to population standards in males between ages 6 to 20 years. Eur J Orthod 1979;1:2540. 10. Linder-Aronson S . Adenoid obstruction of the nasopharynx. In: McNamara JA Jr ed. Nasorespiratory function and craniofacial growth. Monograph 9. Craniofacial growth series. Ann Arbor: University of Michigan, 1979:121-47. 11. Linder-Aronson S . Effects of adenoidectomy on dentition and facial skeleton over a period of five years. In: Cook JT, ed. Transactions of the Third International Orthodontic Congress. London: Crosby Lockwood Staples, 1975:85-100. 12. Linder-Aronson S . Effects of adenoidectomy on dentition and nasopharynx. Am J Orthod 1974;65:1-15. 13. Linder-Aronson S . Respiratory function in relation to facial morphology and the dentition. Br J Orthod 1979;6:59-71. 14. Linder-Aronson S. Nasal resistance to breathing and palatal height before and after expansion of the media palatine suture. Odontologist Revy 1963;14:254-70. ’, 15. Linder-Aronson S . Nasorespiratory function and craniofacial growth. In: McNamara JA Jr, ed. Nasorespiratory function and craniofacial growth. Monograph No. 9. Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor: University of Michigan, 1979:121-47. 16. Linder-Aronson S , Backstrom A. Comparison between mouth and nose breathers with respect to occlusion and facial dimensions. A biometric study. Odontologist Revy 1961;11:343-76. 17. Linder-Aronson S , Leighton BC. A longitudinal study of the development of the posterior nasopharyngeal wall between 3 and 16 years of age. Eur J Orthod 1983;5:47-58.
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18. Linder-Aronson S, Woodside DG, Lundstrom A. Mandibular growth direction following adenoidectomy. Am J Orthod 1986; 89:273-84. 19. Linder-Aronson S, Woodside DG. Some craniofacial variables related to small or diminishing lower anterior facial height. Swed Dent J 1982;15(suppl):131-46. 20. Linder-Aronson S. Nasorespiratory considerations in orthodontics. In: Lee W, ed. Orthodontics state of the art, essence of the science. Chicago: Graber, 1984: 1 16-21. 21. Linder-Aronson S, Holmberg H. Cephalometric radiographs as a means of evaluating the capacity of the nasal and nasopharyngeal airway. Am J Orthod Dentofacial Orthop 1979;76:479-90. 22. Linder-Aronson S , Woodside DG. The growth in the sagittal depth of the bony nasopharynx in relation to some other facial variables. In: McNamara JA Jr, ed. Nasorespiratory function and craniofacial growth. Monograph No. 9. Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor: University of Michigan, 1979:27-40. 23. Kerr WJ, McWilliams JS, et al. Mandibular form and position related to changed mode of breathing-a five year longitudinal study. Angle Orthod 1987;59:91-6. 24. Harvold EP. Neuromuscular and morphological adaptations in experimentally induced oral respiration. In: McNamara JA Jr, ed. Nasorespiratory function and cranial growth. 3rd ed. Ann Arbor: University of Michigan Press, 1978:149-64. 25. Harvold EP, Tomer B, Vargervik K, et al. Primate experiments in oral respiration. Am J Orthod 1981;79;359-72. 26. Harvold EP, Chierici G, Vargevik K. Experiments on the development of dental malocclusions. Am J Orthod 1972;61:3844. 27. Harvold EP, Vargevik K , Chierici G. Primate experiments on oral sensation and dental malocclusions. Am J Orthod 1973; 63:494-508. 28. Harvold EP. The role of function in the etiology and treatment of malocclusions. Am J Orthod 1968;54:883-98. 29. Harvold EP. Experiments on mandibular morphogenesis. In: McNamara JA Jr, ed. Determinants of mandibular form and growth. Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor: The University of Michigan, 1965:155-77. 30. Cheng MC. Evaluation of craniofacial morphology and occlusion in patients with nasal obstruction [Thesis]. Cleveland, Ohio: Case Western Reserve University, 1988. 31. Cheng MC, Enlow DH, et al. Developmental effects of impaired breathing in the face of the growing child. Angle Orthod 1988;58:309-19. 32. Principato JJ, Kenigan JP, Wolf P. Pediatric Nasal Resistance HEAD and lower anterior vertical face height. OTOLARYNGOL NECKSURG 1986;95:226-9. 33. Bushey RS. Alterations in certain anatomical relations accompanying the change from oral to nasal breathing [Thesis]. Chicago: University of Illinois, 1965. 34. Bushey RS. Adenoid obstruction of the nasopharynx. In: McNamara JA Jr, ed. Nasorespiratory function and craniofacial growth. Monograph 9. Craniofacial Growth Series. Ann Arbor: University of Michigan, 1979:199-232. 35. Bushey RS. Diagnosis and treatment planning of nasopharyngeal obstructions. Nasorespiratory function and craniofacial growth. Center for Human Growth and Development. Ann Arbor: University of Michigan, 1979. 36. Enlow DH, Kuroda T, Lewis AG. The morphological and mor-
phogenic basis of craniofacial form and pattern. Angle Orthod 1971;41: 161-88. 37. Enlow DH. Handbook of facial growth. 2nd ed. Philadelphia: WB Saunders Company, 1982. 38. McNamara JA Jr. Influence of respiratory pattern on craniofacial growth. Angle Orthod 1981;51:269-99. 39. McNamara JA Jr. Nasorespiratory function and craniofacial growth. Proceedings of a symposium at the Center for Human Growth and Development. Ann Arbor: The University of Michigan, 1979. 40. Melsen B, Attina L, Santiuari M, Attina A. Relationships between swallowing pattern, mode of respiration and development of malocclusion. Angle Orthod 1987;57: 1 13-20. 41. Quinn GW. Deformity of the face, jaws and dentition-a preventable disease-nasal obstruction. N C Dent J 1978;61:14-5. 42. Quinn GW. Airway interference and its effect upon the growth and development of the face, jaws, dentition and associated parts. N C Dent J 1978;60:28-31. 43. Ricketts RM. Respiratory obstruction syndrome (in forum on the tonsil and adenoid problems in orthodontics). Am J Orthod 1968;54:495-5 14. 44. Rubin RM. Mode of respiration and facial growth. Am J Orthod 1980;78:504-10. 45. Subtelny JD. The significance of adenoid tissue in orthodontia. Angle Orthod 1954;24:59-69. 46. Subtelny JD. Oral respiration: facial maldevelopment and corrective dentofacial orthopedics. Angle Orthod 1980;50: 147-64. 47. Vargervik K, Miller AJ, Cherici G, et al. Primate experiments on oral respiration. Am J Orthod 1981;79:359-72. 48. Vaergervik K, Miller AJ, Chierici G, et al. Morphologic response to changes in neuromuscular patterns experimentally induced by altered modes of respiration. Am J Orthod 1984;85:115-24. 49. Warren DW. Aerodynamic studies of upper airway: implications for growth, breathing and speech. In: McNamara JA, ed. Nasorespiratory function and craniofacial growth. Ann Arbor: University of Michigan, 1979:41-86. 50. Principato JJ. Crossbite and increased anterior vertical face height secondary to oral respiration. Proceedings of the International College of Cranio-Mandibular Orthopedics. Florence, Italy, April, 1989. 51. Vig PS, Sarver DM, Hall DJ, et al. Quantitative evaluation of nasal air flow in relation to facial morphology. Am J Orthod 1981;79:263-72. 52. Vig PS. Respiratory mode and morphological types: some thoughts and preliminary conclusions. In: McNamara JA, ed. Nasorespiratory function and craniofacial growth. Monograph 9. Craniofacial Growth Series, Center for Human Growth and Development. Ann Arbor: University of Michigan, 1979:233-50. 53. Vig PS. Personal communication. September 8, 1989. 54. Principato JJ. A 15-year retrospective of chronic rhinitis and cryosurgery. Ear Nose Throat J 1986;65:22-8. 55. Ozenberger JM, Principato JJ. Cryosurgery in chronic rhinitis: a preliminary report. International Congress of Otolaryngology, Mexico, 1969. 56. Preston CB. Preliterate environment and the nasopharynx. Am J Orthod 1979;76:646-55. 57. Principato JJ. Pediatric nasal resistance. Laryngoscope 1985; 1067-9. 58. Principato JJ. Current techniques and management of nonallergic rhinitis. American Academy of Otolaryngology-Head and Neck Surgery, Instructional Course Textbook, 1988.
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Upper airway obstruction and craniofaciaI rnorphology JEROLD J. PRINCIPATO, MD, Bethesda, Maryland
Otolaryngologists are being asked with increasing frequency to assess adequacy of the upper airway and to treat upper airway obstructive problems in orthodontic patients. The incentive has been provided by recent studies that purport to relate upper airway obstruction to dental and craniomorphologic changes. It is hypothesized that prolonged oral respiration during critical growth periods in children initiates a sequence of events that commonly results in dental and skeletal changes. In the chronic mouth-breather excessive molar tooth eruption is almost a constant feature, causing a clockwise rotation of the growing mandible, with a disproportional increase in anterior lower vertical face height. Such increases in anterior lower vertical face height are often associated with retrognathia and open bites. Low tongue posture seen with oral respiration impedes the lateral expansion and anterior development of the maxilla. Otolaryngologists have the ability to objectively and accurately assess upper airway patency. Rhinometric assessment before and after application of topical nasal decongestant, in conjunction with clinical examination, provides valuable information regarding upper airway patency and the cause of any existing obstructive pathologic condition. Studies should be designed carefully to control the numerous variables that have an impact on the growing face of a young child so that meaningful data can be obtained in our own field regarding this challenging topic. (OTOWNGOL HEAD NECK SURG 1991;104:881.]
craniofacial morphology and occlusal patterns are influenced by a variety of factors. The issue of upper airway obstruction and its impact on craniofacial development and dental patterns has been considered since the turn of the century. Findings in numerous clinical studies have suggested a relationship between mouth breathing and the development of skeletal and dental abnormalities. The anecdotal nature of some of these reports, poor study designs of others, and the paucity of adequate statistical analysis has prevented general
From the Section of Otolaryngology, George Washington University School of Medicine and Health Services. Presented at the Annual Meeting of the American Academy of Otolaryngology-Head and Neck Surgery, New Orleans, La., Sept. 24-28, 1989. Received for publication March 5 , 1990; accepted Nov. 16, 1990. Reprint requests: Jerold J. Principato, MD, 10401 Old Goergetown Rd., Suite 409, Bethesda, MD 20814. 2311127133
acceptance of the relationship. Adequate investigation of an alleged relationship between the obstructed airway and craniofacial patterns was further thwarted by the use of the commonly used descriptive phrase “adenoid facies. ” This terminology prompted the erroneous notion that the familiar elongated facial pattern, with an open mouth and dull expression, was exclusively related to only or primarily an obstructing adenoid mass. The occurrence of craniofacial changes and abnormal dental patterns in the absence of enlarged adenoids led to skepticism regarding the hypothesis that associated upper airway obstruction with abnormal facial growth and development. The simplistic notion that related only enlarged adenoids to abnormal craniofacial morphology failed to take into account that the pathologic condition causing the obstruction is more often related to disease of the turbinates, septum, and external nasal architecture (Table 1). In addition, an obstructing adenoid mass in a younger child producing abnormal skeletal and dental patterns may well have resolved by the time an
Downloaded from oto.sagepub.com at PENNSYLVANIA STATE UNIV on May 28, 2015
881
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882 Review Article
Table 1. Common causes of upper airway obstruction Cause
%
Allergic rhinitis Adenoid hypertrophy Nonallergic rhinitis Seotal deforrnitv Architectural deformity
43 35 33 13 5
upper airway assessment is performed. Acceptance of the relationship was further hindered by the tonsil and adenoid controversy, which prompted a dramatic decrease in the number of tonsillectomies and adenoidectomies being considered and performed. A report by Linder-Aronson’ in 1970 provided the incentive for a renewed interest in this complex relationship between impaired nasal breathing and facial growth and development. Although he was aware of other common pathologic conditions causing obstruction in the nasal airway, Linder-Aronson’ attempted to relate adenoid size, assessed by means of lateral cephalometric x-ray films, to craniofacial morphology.””” This study and others were meticulously designed and used stringent statistical analysis. Results of the investigations demonstrated a statistically significant relationship between obstructing adenoid tissue and certain skeletal and dental patterns. These changes included rotation of the mandible in a clockwise manner so that the growth of the mandible was in a more vertical and backward direction, often causing elongation of the lower anterior vertical face height, open bite, and retrognathia. The change in the mandibular growth pattern accounted for a very obtuse gonial angle and a steep mandibular plane. Other findings included shallow nasopharyngeal space, narrowing and elevation of the palate, a tendency toward posterior and anterior crossbite, and crowding of the maxillary and mandibular teeth. Subsequent studies demonstrated that the direction of mandibular growth nornialized in a more horizontal or less vertical manner after adenoidectomy and change to nasal respiration. This accelerated growth of the mandible in a more horizontal direction was more apparent in girls and caused diminished lower anterior vertical face height and improvement of the retrognathia. Kerr et al.23 studied mandibular growth patterns in 26 children, treated for nasal obstruction by adenoidectomy, who exhibited a changed mode of breathing postoperatively. These authors concluded that a change from oral to nasal respiration after adenoidectomy resulted in a more anterior direction of growth in the body of the mandible and some reversal of the initial tendency
Fig. I . Child with nasal obstruction.
toward a posterior or clockwise rotation of the mandible. Experiments in primates by Harvold et a1.”-2‘’ demonstrated a variety of skeletal, dental, and muscular alterations in animals with artificially obstructed nasal airways. The magnitude and nature of the changes appeared to be related to the manner in which mouth breathing was accomplished. Consistent elongation of the face with crossbite developed in the animals that maintained oral respiration by persistent protrusion and lowering of the mandible. DentaI, muscular, and skeletal impact on the obstructed primates was less severe and more variable in animals that rhythmically opened and closed their mouths to achieve adequate respiration. These studies suggested that a change to oral respiration was critical in the process leading to craniofacial and dental alterations. The duration of the oral respiration and the age of the obstructed primate were important variables. When the function of the oral cavity became primarily that of respiration for an extended period of time in young growing primates, the form of the skeleton and associated muscles was always altered. Harvold et al.”-”’ concluded that skeletal and dental form in obstructed animals was related to alterations in neuromuscular activity required to maintain the function of adequate respiration through the oral cavity. Postural and anatomic similarities are striking in children and primates with nasal obstruction (Figs. 1 and 2). In recent years, many studies have been published that suggest the degree of impact caused by oral respiration on facial growth and development varies with
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Fig. 2. Primote with nasal obstruction (Photograph, courtesy of E. Horvold)
Table 2. Hypothetical sequence relating upper airway obstruction and orthodontic deformity Sequence
Increased nasal resistance Oral respiration and low tongue posture Excessive molar eruption Molar fulcruming Mandibular rotation Increased ALVFH ~
~
ALVFH, Anterior lower vertical face height
W Fig. 3. Lower anterior vertical face height. Anterior facial height Is direct measurement from anterior nasal spine to menton.
different facial types.”’ Persons with a brachycephalic or broad-faced facial pattern with strong facial musculature, low mandibular plane. and deep bite appear to be less severely affected than those with a disposition toward a more dolichocephalic elongated narrow facial pattern with weaker musculature.
Cheng et al.” recently studied craniofacial niorphology and occlusal patterns in 71 persons with impaired breathing. All of the subjects in the study were assessed by otolaryngologists and underwent rhinometric evaluation of the nasal airway. The researchers concluded that the group with impaired nasal airway had characteristic combinations of skeletal deformities and malocclusions. They concluded that craniofacial morphology and occlusal patterns in persons with obstructed breathing were statistically and significantly different from those of persons with normal nasal airway breathing. The most profound change appeared to be related to the vertical skeletal measurements associated with a longer face and increased dentoalveolar and palatal heights. Because younger subjects with impaired nasal airways had fewer of these craniofacial morphologic and occlusal changes, the authors advocated a multidisciplinary approach involving the oto-
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Fig. 4. Over-erupted posterior teeth often present in children with chronic oral respiration.
Fig. 5. Excessive eruption of posterior teeth causes lower jaw to rotate down and backward.
laryngologist, the pediatrician, and the orthodontist in early recognition of specific combinations of craniofacial features, so that early intervention and correction of pathologic conditions causing nasal obstruction could be offered. Principato et al." compared lower anterior vertical face heights, as determined from lateral cephalometrir x-ray films (Fig. 3), and nasal airway resistance in 60 children. This investigation demonstrated a statistically significant correlation between elevations in nasal airway resistance as determined by active anterior rhinometry and increases in lower anterior vertical face height. From numerous studies over the decades regarding the relationship between nasal obstruction and orthodontic deformity,-'"" a plausible sequence of events be-
gins to emerge. Some of the steps in this extremely variable process cry out for further investigation and remain hypothetical or anecdotal. Nevertheless, a clinical model (Table 2) can be pieced together from the investigative studies. Craniofacial morphology and dental patterns appear to be consequentially affected by long-standing oral respiration during periods of rapid facial growth in susceptible persons.'" A change to oral respiration occurs when nasal resistance reaches some two to three times that of normal. This does not mean that a person with an impaired nasal airway cannot sustain nasal respiration for short periods of time. Nevertheless, the effort is of such magnitude that the oral airway is preferred and more often used. It should be kept in mind that when a person is in reclining position, normal airway resistance is elevated even further.
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Fig. 6. Anterior open bite.
Fig. 8. Lateral forces exerted by tongue positioned in roof of mouth normally influence expansion and growth of maxilla.
Fig. 7. Increased lower vertical face height often associated with strained lip posture and chin pad displacement.
Therefore. borderline obstructive resistances in the upright position frequently are converted to resistances that prompt oral respiration throughout sleep. During oral respiration, the mandible rotates open to a more
downward position. the teeth are naturally apart, and the tongue must assume a low position in the mouth to allow adequate air How. The tongue is no longer in contact with the hard palate and assumes a low posture in the floor of the mouth. Extended durations of mouth breathing at critical times of facial growth and development in children with predisposition to development of a long face are at particular risk for development of the following sequential changes in skeleton and den-
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tition. In the absence of tooth contact over an extended period of time, there often occurs excessive eruption of the posterior molar teeth. This is not seen only during oral respiration in children, but occurs in adults who are missing opposing molar tooth contact as a result of extraction, trauma, or both. Overerupted posterior teeth (Fig. 4), a common finding on lateral cephalometric x-ray films in children undergoing orthodontic management, exert a downward vector of force on the forward-growing mandible, causing the lower jaw to rotate down and back in a clockwise manner (Fig. 5). Although quite variable with different facial types, our dental colleagues frequently associate 1 mm of excessive posterior molar eruption with a 3-mm elongation of the lower anterior vertical face height. Because of the lower jaw rotation, retrognathia is almost always present and anterior open bites are common (Fig. 6). The increase in lower vertical face height often produces lip incompetence and chin pad displacement (Fig. 7). The overall facial pattern can be characterized as an “upper airway obstructed facies.” Some of these rotational skeletal changes, along with open bite, can be reversed partially or completely in young children by therapy directed at intrusion of the molar teeth. Repelling magnets on the contact surfaces of the molar teeth, and external devices such as the wearing of reverse cervical collars, can encourage intrusion of the posterior teeth and closure of the open bite, with diminution of lower anterior vertical face heights. Natural growth and expansion of the maxilla is influenced by tongue forces exerted both at rest and during ~ w a l l o w i n g .Complete ~~ maxillary expansion appears to be dependent on lateral forces exerted by the tongue (Fig. 8). It follows that low tongue posture, as seen in mouth breathers with upper airway obstruction, frequently diminishes or eliminates these lateral expansive forces on the upper jaw (Fig. 9). The diminished force exerted by the tongue on the growth of the maxilla is compounded by the relatively unopposed lingually directed constricting forces exerted on the buccal segment by the taut buccinator and masseter muscles in the open mouth position. One of the goals of the commonly used Frankel orthodontic appliance is to diminish these constricting muscular forces. In the absence of adequate expansion, there often occurs a narrow high maxilla with posterior teeth in crossbite in which the upper maxillary teeth are situated in a more lingual position than the opposing mandibular teeth. This incomplete lateral expansion of the maxilla can result in either a unilateral (Fig. 10) or bilateral crossbite (Fig. 11) pattern. Low tongue posture with limited lateral expansive forces of the tongue is exaggerated when short lingual frenula (Fig. 12) provide additional restriction to tongue motion and posi-
i
Fig. 9. Low tongue posture, as seen during oral respiration, diminishes lateral expansive forces on maxilla.
tioning in the roof of the mouth. It would appear that upper airway obstruction, whether related to adenoid enlargement, chronic rhinitis, or nasal septa1 deformity, can be associated with elongation of the lower anterior face and development of certain abnormal dental patterns. Narrow nasal architecture and wide columellae (Fig. 13) can also create formidable obstructions. Children with predisposition to longer faces are more severely affected by long-standing oral respiration. Early detection and treatment of pediatric nasal obstructive disorder, particularly in children with evidence of early craniofacial and I or dentoalveolar changes would seem justified. The data presented in recent literature supporting the relationship are not without controversy. Vig et al.5’-53 assert that current study conclusions are frequently supported only by circumstantial evidence, and there is little adherence to the Scientific Method. Even if the hypothesis is correct, justifiable concern is raised regarding accurate means of identifying patients at risk. Furthermore, it must be demonstrated with good study designs that there is a tangible benefit on the orthodontic outcome provided by a given medical or surgical intervention. The relative risks/costs of any treatment must be considered. If upper airway obstruction is indeed an important variable initiating dental and skeletal alterations, early recognition and treatment of pathologic conditions causing obstructed airway are in order. Suspicion on the part of the clinicians could be prompted by any or all
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Fig. 10. Unilateral molar crossbite.
Fig. 11. Bilateral molar crossbite.
deleterious impact of consequential obstruction on craof the following: chronic nasal stuffiness. excessive niofacial development is virtually complete by puberty. snoring, open mouth posture and oral respiration, low Hence the opportunity for successful intervention is tongue position (especially with short lingual frenubrief. lum), elongation of the lower anterior face height (parThe necessity for surgery should be carefully conticularly in families with tendency toward doliochosidered. and the procedure and timing should be decephalic facial patterns), posterior tooth crossbite, and termined by the age of the child and the magnitude of overt orthodontic changes. Some of these tendencies the skeletal and dental problem. Delay or absence of are apparent in a child as young as 3 years of age, but appropriate intervention niay result in unsuccessful they are more commonly detected Downloaded after age 5. The from oto.sagepub.com at PENNSYLVANIA STATE UNIV on May 28, 2015
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Fig. 12. Short lingual frenulum restricting tongue mobility.
Fig. 13. Wide nasal columella.
orthodontic treatment, with recurrence in late adolescence and the necessity for orthognathic surgical intervention with osteotomies of either or both the maxilla or mandible. Referral at an early age might include otolaryngologic and orthodontic examination, cephalometric radiology. and rhinometry to determine nasal airway resistance (Table 3). Simultaneous X-y display
of both nasal pressure and air flow, with resistance determinations made at 100 pascals, provides an objective means of assessing the airway. Such devices are readily available and suitable for the clinical setting. In addition to obtaining definitive data with regard to the patency of the upper airway, rhinometry performed before and after nasal lining decongesting allows local-
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-
Rhinitis
vative, but effective. Such a goal is aided by objective evaluation of the airway by means of rhinometric measurements. The timing of the intervention would seem critical. Above all-and in spite of some comments to the contrary-the “quality of life” deformities and disabilities associated with long-standing nasal obstruction do indeed justify serious consideration on the part of pediatricians, dentists, and otolaryngologists.
Enlargement
Septa1 Deformity
Fig. 14. Rhinometry. performed before and after nasal lining decongesting, helps identify site of obstructing pathologic condition.
Table 3. Standard evaluation of children with suspected upper airway obstruction Assessment
Clinical examination Cephalometric x-ray films Rhinomanometry
ization (Fig. 14) of the pathologic condition, causing the obstruction to either the lateral wall of the nose, the adenoids, or the nasal septum and helps in the selection of the appropriate treatment modality.54 Every effort should be made to provide the safest and simplest surgical corrective measure. When indicated, adenoidectomy is very beneficial, as is the selective use of cryosurgery in the management of chronic r h i n i t i ~ . ~ ~Conservative .~’ and judicious use of submucous resection of the inferior turbinate?’ in young children, as well as conservative correction of nasal deformity, can provide substantial relief of the ill effects of nasal obstruction. In conclusion, much more investigation is necessary to completely understand the sequential craniofacial, muscular, and dental changes that appear to result from nasal airway obstruction and oral respiration. The variables are numerous and must be placed in appropriate scientific perspective. The assessment of children at risk should be multidisciplinary, timely, and exhaustive. The selection of surgical modalities should be conser-
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