Vol. 102 No. 3 September 2006
ORAL AND MAXILLOFACIAL SURGERY
Editor: James R. Hupp
Mucociliary clearance and sense of smell following management of Le Fort maxilla fractures Iwona Anna Niedzielska, PhD,a Karolina Wróbelusb zaq;2?,b Wojciech Wziatek,b Zbigniew Bazarnik,b and Jan Drugacz,a Tychy, Poland SILESIAN MEDICAL ACADEMY
Objective. To assess mucociliary transport and olfaction in patients after Le Fort fractures. Study design. Forty-one patients were enrolled who had sustained a Le Fort fracture during the preceding five years. Control group consisted of students. Olfaction and mucociliary transport were examined in all subjects. A capillary with saccharine was placed on the inferior nasal concha, and time was recorded in which the subject tasted sweetness in the mouth. Results were subject to statistical analysis. Patients with allergy, sinus disease and smokers were excluded from the examination. Results. Disturbance of mucociliary transport and olfaction turned out to be statistically dependent on the type of fracture and management. Conclusions. Le Fort fracture might be complicated by compromised mucociliary clearance and olfactory disturbances. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:287-91)
Mucociliary transport serves as one of the most important defense mechanisms in the human respiratory tract. Its important components are the cilia and two-layered mucus secreted by goblet cells and seromucous glands.1 The transport occurs within the upper and lower respiratory tracts.2 Its mechanism has been best described in the nasal cavities.3,4 The route of mucus transport within the sinuses was observed in cadaveric studies as the ciliary activity continues for 24 and 48 hours after death.1 Sharpey was one of the first do describe mucociliary clearance mechanism and emphasized the role of the ciliated epithelium.5 Ciliary kinetics was studied using scanning electron microscopy (SEM) and transmission electron miroscopy (TEM).5,6 At present, research has been done on the processes of cilia formation and molecular mechanisms of ciliary motility.7 In the case of inherited and acquired a
Professor, Department of Maxillofacial Surgery, Silesian Medical Academy. b Student, Department of Maxillofacial Surgery, Silesian Medical Academy. Received for publication May 29, 2005; returned for revision Aug 1, 2005; accepted for publication Sep 6, 2005. 1079-2104/$ - see front matter © 2006 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2005.09.001
disease of the cilia, mucociliary clearance tends to be compromised. Many physicochemical properties and biological factors, as well as different substances, may affect the activity of the cilia. Mucus also plays an important part in the transport.1 Experimental studies revealed that mucus might have varying chemical structure, but in order for mucociliary transport to progress smoothly, its characteristic viscosity and elasticity must be maintained.7 Several methods have been described to evaluate the efficacy of mucociliary transport.8,9 The most frequently applied is the Andersen saccharin test, first used in 1973.10 The method has been subsequently modified through introduction of better measurement techniques (isotope, radiographic, and endoscopic), and various substances (aqueous saccharin solution, barium sulphate, blue-stained saccharin, etc).11-14 Mucociliary transport time ranges, according to different authors, between 5 and 20 min.8,9 When the time exceeds 30 min, the transport is considered severly hindered—the condition has been referred to as mucus stasis, and might result from inflammatory response to infections, allergies, noxious effects of air-conditioning, fumes, chemical and physical pollution, and contamination; menstruation also decreases mucociliary clearance.15,16 Literature describes mucociliary transport 287
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288 Niedzielska et al. impairment in the course of various upper and lower respiratory disorders, systemic diseases, and developmental anomalies.9,11,17-20 The effects of endoscopic procedures, pharmacotherapy, alcohol, coffee, and so on, were also studied.20,21 To our best knowledge, however, there have been no reports on the changes in mucociliary function associated with trauma to facial skeleton, including maxilla fractures. The roof of the nasal cavity, which sustains injury in the case of Le Fort II and III fractures, is lined with the olfactory epithelium. Hence, not only mucociliary transport might be impaired, but olfactory loss or smell disturbance can be experienced. Post-traumatic anosmia, associated with cranial and facial skeleton injury (including maxilla fractures), was described by Renzi et al.22 and Gatot et al.23 The aim of the present study was to evaluate mucociliary transport rate and olfactory disturbances following Le Fort I, II, and III fractures, and in healthy controls. MATERIAL AND METHODS Patients were examined who had sustained Le Fort I, II, or III fractures in the years 1995 to 2002, and were otherwise in good general condition, non-smokers, with no history of allergic disease and paranasal sinusitis. Those with nose structure abnormalities, nasal septum deviation, and a history of other fractures of the facial skeleton were excluded from investigations. Three women and 38 men (41 participants) were selected out of 86 individuals. All had been previously hospitalized in the Department of Maxillofacial Surgery in Katowice. There were 9, 20, and 12 patients with Le Fort I, II, and III fractures, respectively. Treatment had been undertaken depending on fracture type, the patient’s general condition, and indications. Orthopedic management was implemented in 70% (6/9 Le Fort I; 14/20 Le Fort II; 9/12 Le Fort III), and surgery was performed in 30% (3/9 Le Fort I; 6/20 Le Fort II; 3/12 Le Fort III) of the cases. Orthopedic treatment consisted of intermaxillary fixation on dental splints and extramaxillary fixation (closed reduction). When teeth were missing, rigid fixation was obtained by acrylic prosthesis, and in the case of inveterate fracture traction was used. Operative management with miniplate osteosynthesis was recommended in patients with open and penetrating wounds or considerable bone displacement (open reduction). Mean age in the patient group was 43 years. The control group consisted of 20 healthy volunteers, students of the Department of Dentistry; mean age was 25 years. All patients underwent the Rutland-Cole24 saccharin transport test to determine the efficacy of mucociliary transport. Saccharin was applied with a capillary on the inferior nasal concha, and time elapse was measured until the subject reported perception of a sweet taste (up to 45
30 25 20 15 10
30 17
19 12
5 0
Le Fort I
Le Fort II
Le Fort III
Control group
Fig. 1. Mucociliary transport time in trauma subjects and control group.
min). A six-grade scale was used to register possible olfactory deficits while the subjects were assessing the intensity of coffee, lavender, garlic, and vinegar smell. Nasal dimensions were measured with slide callipers: length, width, and the base of the nose. Mann-Whitney and Kruskal-Willis tests were used in statistical analysis of the relationship between mucociliary transport impairment, olfactory deficit, and the following parameters: study groups, type of maxilla fracture, type of management, nose dimensions. RESULTS The most significant impairment of mucociliary transport were noted following Le Fort III fractures when compared to those resulting from Le Fort II and I (P ⬍ .05). In Le Fort III patients the average period of saccharin test was 30 min, whereas it was 12 minutes in healthy controls. The distribution of mucociliary transport rate in Le Fort I, II, and III fracture patients and in the control group is presented in Fig. 1. Similar results were obtained for olfactory disturbances, the most profound being observed after Le Fort III fracture (Fig. 2). Surgery tended to cause greater impairment to mucociliary transport and the sense of smell than orthopedic management (P ⬍ .05) (Fig. 3). There were no statistically significant differences in mucociliary transport rate and the sense of smell dependent on nose dimensions (Fig. 3). DISCUSSION Mucociliary transport impairment results when the structure of the cilia is defective or their function is disabled; or when mucous secretion is hindered.25 This mostly happens in the course of pathologic processes within the paranasal sinuses, allergic and systemic disease, and Kartagener’s syndrome.18,19,25-28 Nicotine, pharmacotherapy, and ambient temperature also affect
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Niedzielska et al. 289
24 20
35
p<0,01
p<0,001
p<0,001
30 25
16
Mean range
Mean range
20 12 8 4
15 10 5
0
0
coffee
lavender garlic
vinegar
coffee
Control group
Le Fort- I
lavender garlic
Le Fort- II
vinegar
Control group
32 28
Mean range
24 20 16 12 8 4 0
coffee
lavender
Le Fort - III
garlic
vinegar
Control group
Fig. 2. Sense of smell in trauma subjects and control group (Mann-Whitney test).
p>0.05
p>0.05
p>0.05
p>0.05
Mann-Whitney- Test 25
20
20 clearance
Mean range
25
15 10
15
Mucociliary
10 5 0 coffee
lavender
Surgical management
garlic
vinegar
5 0
Orthopaedic management
Fig. 3. Mucociliary transport impairment and olfactory deficit depending on the management (surgical vs. orthopedic).
mucociliary transport.21,29 Anatomical anomalies increase mucociliary transport time.9,17 Therefore, only patients treated for uncomplicated Le Fort I, II, or III fractures were included; all were non-smokers, and with no concomitant disease and associated pharmacotherapy. The subjects were examined under optimum and comparable conditions.
Possible effects of iatrogenic injury on mucociliary transport have already been discussed by Inanli et al.20 and Stringer et al.30 Literature lacks reports referring to mucociliary transport impairment and Le Fort fractures of the maxilla. For years now, most fractures of the facial skeleton have been subject to surgical treatment.32,33 Prior to this,
290 Niedzielska et al. orthopedic management had been used.31 Both methods have been widely discussed, and their outcomes compared. Our investigations seem to suggest that surgical protocol causes more noticeable impairment to mucociliary transport than does orthopedic intervention. It might be because surgery itself can be considered a type of iatrogenic trauma, which disables the transport efficacy.20 During surgical management, a closed system becomes open, which can be deleterious to cilia function. The most considerable abnormalities of mucociliary clearance were associated with Le Fort III fractures. This could be accounted for by damage to larger surfaces participating in the transport. Olfactory deficit results, as might be expected following the injury to olfactory nerves. Some authors observed sense of smell disturbances in patients who had sustained head trauma (including facial skeleton injury); however, possible associations between the deficit and maxilla fractures have not been investigated so far. In the present study, measurements of the nose were taken into consideration because we hypothesized that mucociliary transport might, to some extent, depend on the parameters (and, more precisely, on the number of surface cilia). The investigation results did not confirm the hypothesis. We have not found any literature reports on mucociliary transport in patients who had sustained maxilla fracture; hence, the article does not present any comparison between the literature and the data reported here. CONCLUSIONS Our results imply that Le Fort fracture might be complicated by compromised mucociliary clearance and olfactory disturbances. Further, orthopedic management of Le Fort maxilla fractures causes less impairment to mucociliary clearance and olfaction than results from surgical intervention.30 REFERENCES 1. Manasterski J. [Mucociliary transport in the upper respiratory tract]. Otolaryngologia 1992;66:305-12. 2. Paul A, Marelli D, Shennib H, et al. Mucociliary function in autotransplanted, allotransplanted, and sleeve resected lungs. Thorac Cardiovasc Surg 1989;98:523-8. 3. Kelly J, Prasada, Wexler A. Detailed flow patterns in the nasal cavity. J Appl Physiol 2000;89:323-37. 4. Rehorek S, Firth B, Hutchinson M. The structure of the nasal chemosensory system in squamate reptiles. 1. The olfactory organ, with special reference to olfaction in geckos. J Biosci 2000;25:173-9. 5. Sharpey W. On a peculiar motion excited in fluids by the surfaces of certain animals. Edinburg Med J 1830;34:113-9. 6. Sleigh MA. Ciliary function in transport of mucus. Eur J Respir Dis Suppl 1983;128:287-92. 7. Deitmer T. Physiology and pathology of the mucociliary system. Special regards to mucociliary transport in malignant lesions of the human larynx. Adv Otorhinolaryngol 1989;43:1-136.
OOOOE September 2006 8. Duchateau GS, Graamans K, Zuidema J, Merkus FW. Correlation between nasal ciliary beat frequency and mucus transport rate in volunteers. Laryngoscope 1985;95:854-9. 9. Ginzel A, Illum P. Nasal mucociliary clearance in patients with septal deviation. Rhinology 1980;18:177-81. 10. Andersen I, Cammer P, Jensen PL, Philipson K, Proctor DF. A comparison of nasal and tracheobronchial clearance. Arch Environ Health 1974;29:290-3. 11. Hady MR, Shehata O, Hassan R. Nasal mucociliary function in different diseases of the nose. J Laryngol Otol 1983;97:497-502. 12. Lindberg S, Runer T. Method for in vivo measurement of mucociliary activity in the human nose. Ann Otol Rhinol Laryngol1994;103(7):558-66. 13. Ingels K, Van Hoorn V, Obrie E, Osmanagaoglu K. A modified technetium-99m isotope test to measure nasal mucociliary transport: comparison with the saccharine-dye test. Eur Arch Otorhinolaryngo. 1995;252(6):340-3. 14. Kleinschmidt E.G, Witt G.: Evaluation of nasal mucociliary clearance with a modified saccharin test. Laryngorhinootologie 1995;74:286-8. 15. Armengot M, Basterra J, Marco J. Nasal mucociliary function during the menstrual cycle in healthy women. Rev Laryngol Otol Rhinol 1990;111:107-9. 16. Quinlan MF, Salman SD, Swift DL, Wagner HH, Proctor DF. Measurement of mucociliary function in man. Am Rev Respir Dis 1969;99:13-23. 17. Slater A, Smallman LA, Logan ACM, Drake-Lee AB. Mucociliary function in patients with nasal polyps. Clin Otolaryngol 1996;21:34-37. 18. Karnitzki G, Mlynski G, Mlynski B. Nasal mucociliary transport time and ciliary beat frequency in healthy probands and patients with sinusitis. Laryngorhinootologie 1993;72:595-8. 19. Emeryk A, Górnicka G. [Saccharose transport time in with bronchial asthma and allergic rhinitis]. Pediatria Polska 1993;68:19-21. 20. Inanli S, Tutkun A, Batman C, Okar I, Uneri C, Sehitoglu MA. The effect of endoscopic sinus surgery on mucociliary activity and healing of maxillary sinus mucosa. Rhinology 2000;38(3):120-3. 21. Van de Donk HJ, van den Heuvel AG, Zuidema J, Merkus FW. The effect of nasal drops and their additives on human nasal mucociliary clearance. Rhinology 1982;20:127-37. 22. Renzi G, Carboni A, Gasparini G, Perugini M, Becelli R. Taste and olfactory disturbances after upper and middle third facial fractures: a preliminary study. Ann Plast Surg 2002;48(4):355-8. 23. Gatot A, Fliss DM, Zucker G, et al. The subcranial approach to the anterior skull base. Retrospective study of 75 cases. Ann Otolaryngol Chir Cervicofac 2000;117(6):367-73. 24. Rutland J, Cole PJ. Nasal mucocilliary clearance and ciliary beat frequency in cystic fibrosis compared with sinusitis and bronchiectasis. Thorax 1981;36:654-8. 25. Bush A. Primary ciliary dyskinesia. Acta Otorhinolaryngol Belg 2000;54(3):317-24. 26. Morr A, Rhodius U, Ahrens P, Hofmann D. Aspects of mucociliary clearance in mucoviscidosis. Pneumologie 1991;45:790-3. 27. Teknos TN, Metson R, Chasse T, Balercia G, Dickersin GR. New developments in the diagnosis of Kartagener’s syndrome. Otolaryngol Head Neck Surg 1997;116(1):68-74. 28. Corbo GM, Foresi A, Bonfitto P, Mugnano A, Agabiti N, Cole PJ. Measurements of nasal mucociliary clearance. Arch Dis Child 1989;64:546-50. 29. Green A, Smallman LM, Logan AC, Drake-Lee AB. The effect of temperature on nasal ciliary beat frequency. Clin Otolaryngol 1995;20:178-80.
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