- Email: [email protected]
Mucociliary clearance impairment after zygomaticomaxillary-orbital fractures
Vol. 115 No. 6 June 2013
Mucociliary clearance impairment after zygomaticomaxillaryorbital fractures Tomasz Janic, DDS, PhD, and Iwona Niedzielska, DDS, MD, PhD Objective. The purpose of this study was to examine the influence of zygomaticomaxillo-orbitalis (ZMO) fracture and its symptoms on mucociliary transport (MCT). Study Design. The study encompassed 144 patients who sustained ZMO fracture. A saccharine test was conducted in every patient both on the side of fracture and on the unaffected side. The results were analyzed in connection with the patients’ age, sex, degree of injury, method of treatment, time since fracture, and duration of surgery. Results. It was shown that MCT was considerably impaired on the affected side compared with the control side. However, the degree of impairment did not vary significantly in the patients regardless of the analyzed parameters. Conclusions. ZMO fracture induces the disorder of MCT. Balloon Foley catheter in the open reduction of ZMO fracture impairs MCT. The analyzed parameters do not affect the disorders of MCT. (Oral Surg Oral Med Oral Pathol Oral Radiol 2013;115:e6-e12)
Mucociliary clearance (MCC) is one of the most important airway defense mechanisms. It occurs due to continuous ciliary motion resulting in the flow of the overlying mucus. The thickness of the periciliary fluid layer is controlled by the respiratory epithelium via changes in the activity of ion channels and transmembrane conductors.1 Mucus production in the nasal passages and sinus cavities is regulated by the seromucous glands found in the submucosal layer and epithelial goblet cells.2 Mucus is composed mainly of water (95%) but also includes glycoproteins, immunoglobulins (IgA, IgG), lysozyme, and lactoferrin.3,4 The mucous layer also contains T lymphocytes, NK cells, macrophages, basophils, and neutrophils.5 The most fundamental mucus properties in terms of MCC are its viscosity and elasticity. A mucus layer of 0.5-2 m in thickness also protects the respiratory epithelium against mechanical and chemical damage as well as against dryness and pathogen entry.6 Mucociliary clearance is most frequently assessed using the saccharine test of Rutland and Cole.7 Nasal MCC time ranges from 3.17 to 20.9 minutes.8,9 MCC ⬎30 minutes indicates its compromise, i.e., mucus stasis. Because it is noninvasive and comparable to other measurement methods, the saccharine test is recommended for screening to detect abnormal MCC7-10. MCC is affected by numerous factors. Genetic ciliary motility disorders cause multiorgan abnormalities not only in the respiratory tract but also in those organs Department of Craniomaxillofacial Surgery and Dental Surgery, Katowice, Poland. Received for publication Jul 23, 2011; returned for revision Sep 28, 2011; accepted for publication Oct 17, 2011. © 2013 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2011.10.035
e6
which contain ciliated epithelial cells (reproductive organs, ear). MCC is accelerated by mucolytic agents (bromhexine, ambroxol, acetylcysteine, carbocysteine), adenosinotriphosphate, aminophylline, -sympathicomimetics, and acetylocholine. The rate of mucociliary clearance is reduced by inhalation anesthetics (halothane, isoflurane) and intravenous anesthetics (temazepam, diazepam). Ciliary actions are also influenced by biologic (viral and bacterial infections, allergies, astma, anatomic anomalies) and physicochemical factors (temperature, humidity, ionizing radiation, air pollution, cigarette smoke). There are a few research reports about the effect of upper respiratory tract injury on MCC; however, in the case of craniofacial trauma the issue of MCC impairment has been considered only for maxillary fractures. It has been demonstrated that surgical management of maxillary fractures resulted in greater impairment of MCC than less invasive techniques, such as maxillomandibular fixation thereof.11 The effect of damage to nasal structures on MCC is well established; however the role of maxillary sinuses in the process remains puzzling. Therefore, it seemed essential to investigate MCC in patients who had sustained zygomaticomaxillary-orbital fractures (ZMOF),
Statement of Clinical Relevance The results of this study show complications after zygomaticomaxillary-orbital fractures (ZMOF), which have not been previously described. The awareness of possible and frequent complications will allow taking appropriate preventive measures and treating the disorders caused by ZMOF more effectively.
OOOO Volume 115, Number 6
and the more so because both the affected and contralateral (control) side of the face could be assessed. The aim of the study was to assess: 1) the effect of the severity of SMOF and accompanying symptoms on mucociliary clearance; and 2) MCC impairment depending on time elapsed from injury to presentation, management type, and duration of surgery.
MATERIALS AND METHODS A total of 144 patients treated for ZMOF in the Craniomaxillofacial Surgery Department, Medical University of Silesia in Katowice, in the years 2004-2010 were enrolled. The prospective part of the study comprised 15 patients (3 women and 12 men, ages 21-56 years) with a diagnosis of displaced ZMOF; the patients had no history of any other craniofacial injuries and had been qualified for surgical management. Exclusion criteria were systemic disease, cigarette smoking, alcohol and drug use, and nasal septum deviation. The saccharine test was carried out twice, i.e., after injury and after surgery (at the latest on day 5 after the operative procedure), and on both the affected and the control sides of the face. The retrospective part included 129 patients (21 female and 108 male, aged 12-76 years) with displaced/ nondisplaced ZMOF regardless of their treatment; the patients had no history of any other craniofacial injuries; exclusion criteria were the same as in the prospective subgroup. The patients in the retrospective study were assessed in terms of MCC rate at the following time intervals: 1-3 months (18 patients); 3-6 months (16 patients); 6-12 months (15 patients); 12-36 months (47 patients), and ⬎36 months (32 patients) after injury and ZMOF management. Detailed analyses of case histories, including X-rays and operative reports were carried out in order to identify the type of fracture (displaced or nondisplaced ZMOF), the time elapsed between injury and surgical management, the type of treatment, the duration of surgery, and symptoms accompanying the fracture and concomitant diseases. At each follow-up time point, the patient’s history was taken and clinical examination performed, including for bone irregularities, nasal septum deviation, facial asymmetry, occlusion defects, and sensation in the area supplied by the infraorbital nerve. MCC assessment In the prospective group, the saccharine test was carried out twice, i.e., within 5 days of injury and surgical procedure; a saccharine crystal was inserted into each nasal passage to assess MCC both on the affected and
ORIGINAL ARTICLE Janic and Niedzielska e7
control sides of the face. In the retrospective group, bilateral MCC assessment was also carried out at 1-3, 3-6, 6-12, 12-36, and ⬎36 months after injury and treatment. Saccharine test Before the test, the patients were instructed to blow their nose (except the prospective group owing to the risk of developing subcutaneous emphysema) and restrict their physical activity. The test was carried out with the patient in sitting position with head on the headrest, after a 15-minute adaptation to test conditions (the same for all patients). Test room temperature was 18-27°C, and humidity 40%-70%. Using a moistened pipette and Hartmann nasal speculum, a small saccharine crystal (1 mm) was placed ⬃1 cm from the anterior edge of the inferior turbinate. In case of sneezing or nasal discharge, the test was discontinued and repeated after a couple of minutes. Time to first feeling of sweetness was measured in seconds and expressed as decimal fraction of a minute. If, during 30 minutes (time ⬎30 min was considered to be mucus stasis), the patient did not report the taste of sweetness, the measurement was continued for another 10 minutes not exceeding 40 minutes for the affected and control sides of the face. In both prospective and retrospective groups, the test was carried out starting on the right side regardless of what part of the face had been injured. MCC rate was analyzed in relation to age, gender, injury severity (displaced or nondisplaced ZMOF), type of treatment (closed reduction, open reduction and osteosynthesis with/without Foley catheter placement), time between injury and treatment (⬍48 h, ⬎48 h), and surgery duration (⬍1 h, ⬎1 h). Statistical analysis Statistical analyses were carried out using Statistica 9.0 (Windows), the Wilcoxon test, Mann-Whitney U test (to compare 2 categoric outcomes), and Spearman rank correlation coefficients. Statistical significance was set at P ⬍ .05, and high statistical significance at P ⬍ .01. Differences between saccharine test results regarding the affected and control sides of the face for the same patient were calculated according to the following formula: difference [min] ⫽ (MCC rate on the affected side) ⫺ (MCC rate on the control side) Percentage difference was calculated as follows: difference [%] ⫽ (difference ⫻ 100%)/MCC rate on the control side Based on the results of the above, mean values of intrapersonal differences between MCC rates on the affected and control sides were calculated as well as
ORAL AND MAXILLOFACIAL SURGERY e8 Janic and Niedzielska
OOOO June 2013
Table I. Results of the prospective part of the study (control side)
Postinjury Postsurgery Difference (min) Percent difference (%)
Meam
Median
Minimum
Maximum
Lower quartile
Upper quartile
SD
12.09 12.30 0.21 5.19
10.83 12.60 0.13 1.29
6.73 7.48 ⫺5.80 ⫺28.78
20.15 19.62 8.79 81.16
8.23 9.12 ⫺0.60 ⫺4.55
15.17 15.22 0.75 11.14
4.24 3.69 2.94 23.79
Table II. Results of the retrospective part of the study
Control side (min) Affected side (min) Difference (min) Difference (%)
Mean
Median
Minimum
Maximum
Lower quartile
Upper quartile
SD
10.55 15.03 4.47 50.62
10.33 13.67 2.71 27.57
5.13 5.92 ⫺8.82 ⫺50.70
24.72 40.00 34.28 599.30
7.66 10.52 0.41 3.75
12.33 17.75 7.03 69.29
3.52 6.87 6.70 78.88
mean differences between the affected and control sides of groups and subgroups under analysis. IRB approval The research was approved by the Bioethics Committee of the Medical University of Silesia (L.dz.KNW-0022/ KB1/125/08). The authors have read the Helsinki Declaration and have followed its guidelines in this investigation.
RESULTS The prospective part of the study comprised 15 patients (3 women and 12 men, aged 21-56 years, mean age 36.2 years). Assault and battery was the most frequent cause of ZMOF in this group. Within 5 days of injury and surgical intervention, all patients demonstrated mucus stasis on the affected side (Table I). Mean postinjury and postsurgery MCC rates on the control side were 12.09 minutes (SD 4.24 min) and 12.3 minutes (SD 3.69 min), respectively. The retrospective part ultimately included 128 patients (21 female and 107 male, aged 12-76 years, mean age 33.47 years, SD 14.34). ZMOF was most frequently sustained by patients in their third decade of life (53 patients, 41.4%). The most common cause of the trauma was assault and battery (73 patients, 57%). Differences between mean MCC rates on the affected and control sides in this group were statistically significant (P ⬍ .001). Five patients had mucus stasis on the affected side of the face (Table II). The highest MCC rates (15.24-15.71 min) were noted on the affected side between months 3 and 36 after treatment. The longer the observation time, the more mean MMC rates on the control side exceeded the value of 9.34 minutes (SD 2.82 min) seen in the subgroup followed within the first 3 months. The rate increased to 11.4 minutes (SD 3.30 min) in the subgroup examined at 36 months after treatment (Figure 1).
Mean MCC rates on the affected and control sides decreased and increased with age, respectively. The subgroup below the age of 20 years (17 patients) had the highest mean MCC rates on the affected side (18.58 min, SD 11.42 min), and the lowest on the control side (9.98 min, SD 2.46 min) compared with the other age subgroups. Mean MCC rate in the subgroup aged 20-50 years was between the rates calculated for the youngest and oldest patients (range 14.28-14.8 min). The retrospective part included 21 (16.4%) female and 107 (83.6%) male subjects. MCC rates were lower for female subjects on both affected (14.28 min, SD 7.66 min) and control sides (9.42 min, SD 2.90 min). Differences in MCC rates between the affected and control sides were highly statistically significant for both male (P ⬍ .0001) and female (P ⫽ .0013) subjects. Nondisplaced and displaced ZMOF were diagnosed in 13 and 115 patients, respectively. Mean MCC rates were slightly higher on the affected side with displacement (15.10 min, SD 7.03 min) compared with nondisplaced injury (14.41 min, SD 3.55 min). Saccharine test results differed significantly between the affected and control sides both in the case of displaced (P ⬍ .0001) and nondisplaced fractures (P ⫽ .0037). Open reduction and osteosynthesis was performed in 93 patients, 14 of whom also had a Foley catheter placed. Closed reduction with a single-toothed hook but no osteosynthesis was carried out in 22 patients. The highest MCC rates on the affected side (15.18 min, SD 7.13 min) were seen in the group with open reduction and osteosynthesis. Saccharine test results on the affected and control sides were significantly different for all treatment modalities (P ⬍ .01). In the case of open reduction, mean MCC rate on the affected side was higher in patients with a Foley catheter (17.5 min, SD 6.06 min; Figure 2). Mean difference between intrapersonal MCC rates in this group of patients was 6.44
OOOO Volume 115, Number 6
ORIGINAL ARTICLE Janic and Niedzielska e9
Fig. 1. Mucociliary transport (MCC) rates on the affected and control sides depending on time after termination of treatment.
Fig. 2. Mucociliary transport (MCC) rates on the affected and control sides depending on Foley catheter placement during open reduction.
minutes (SD 4.83 min), i.e., higher than in patients with no maxillary sinus roof support (4.45 min, SD 6.92 min). Saccharine test results differed significantly between the affected and control sides in individual patients with open reduction and Foley catheter (P ⫽ .0012) and those without catheter placement (P ⬍ .0001). Catheter use significantly increased the MCC rate on the affected side (P ⫽ .0451) but seemed to have no effect on the saccharine test parameters on the control side (P ⫽ .8299; Figure 2). Forty-six patients were operated on within 48 hours, whereas 69 underwent surgery beyond 48 hours of injury.
Mean MCC rate in the latter subgroup was higher than in the former, on both the control (10.75 min, SD 2.93 min) and the affected (15.71 min, SD 7.83 min) sides. Those operated on beyond 48 hours of injury also had a higher difference between MCC rates on the affected and control sides (4.95 min, SD 7.66 min) compared with the respective value in the group who had undergone surgery within 48 hours (3.8 min, SD 5.52 min). Saccharine test results were significantly different between both sides of the face in patients operated on within and beyond 48 hours of injury (P ⬍ .0001). Sixty-eight interventions lasted ⬍60 minutes, whereas 42 surgical procedures were longer. Mean MCC rates were
ORAL AND MAXILLOFACIAL SURGERY e10 Janic and Niedzielska
higher in the subgroup with short-lasting surgery and on both affected and control sides (i.e., 15.29 min, SD 7.47; and 11.06 min, SD 3.48 min; respectively). Saccharine test results differed significantly between the affected and control sides of individual patients operated on within or beyond 48 hours of injury (P ⬍ .0001). A comparison of mean intrapersonal MCC rates on the affected and control sides did not reveal significant differences regarding age, gender, observation time, injury severity, treatment modality, surgery delay, and surgery duration in both absolute and percentage values. Significant differences were seen only between subgroups with and without Foley catheter use and between the affected and control sides.
DISCUSSION Epidemiologic analysis of our results is consistent with that of other authors suggesting that the most common cause of ZMOF is assault and battery of men in their third decade of life.12-16 Eighty-five percent of our ZMOF patients showed MCC impairment; however, this can not be verified through comparison with other reports, owing to the lack of similar investigations. It may only be suspected that chronic sinusitis commonly reported after injury might contribute to MCC impairment. There are no literature reviews concerning the effect of ZMOF on mucociliary clearance. The only publication possibly available for results comparison deals with MCC assessment after LeFort maxillary fractures.11 Mean MCC rates in Le Fort I, II, and III fractures were 17, 19, and 30 minutes, respectively. Less invasive techniques, such as maxillomandibular fixation, impaired the rate of MCC to less extent than surgical interventions.11 Subjective examination revealed a significant effect of ZMOF on MCC impairment both directly after injury (mucus stasis) and in the later period. Slightly lower mean saccharine test results, i.e., more efficient MCC during ZMOF compared with maxillary fractures, might be related to the extent of the damage to the ciliary epithelium. Le Fort fractures involve not only maxillary sinus walls but also, among others, the lateral wall of the nasal cavity. The saccharine test is simple, noninvasive, inexpensive, and reproducible.7,8,10 Its main disadvantage is the time frame: up to 80 minutes for a patient (up to 40 min on each side). Literature-reported MCC reference range for healthy patients is 3.17-20.9 minutes, which is similar to our results (5.13-24.72 min). However, it should be emphasized that the comparison made in our study was not between trauma patients and healthy control subjects, but between the affected and control sides of the same individuals.8,9
OOOO June 2013
Our analysis included saccharine test results obtained on the affected and control sides of the face of each individual patient. We intended to analyze not only mean MCC rates on each side, but also intrapersonal differences (i.e., the differences between bilateral MCC rates of the same individual) so as not to disregard changes in environmental conditions or individual parameters, e.g., body temperature. Mean MCC rates differed between both sides in the same patients, evidencing impairment on the affected side. Intrapersonal differences are not found during MCC rate measurements under physiologic conditions,17-20 but are observed in patients with unilateral nasolacrimal stenosis.21 Individuals with no systemic disease and external confounders have shown age-related compromise of mucociliary clearance under physiologic conditions— without gender predilection.22-25 However, lack of age effect has also been reported.26,27 Our results did not indicate significant correlations between age and MCC rate on both affected and control sides of the face. However, this could be associated with a small number of patients at developmental age (⬍15 y). Despite some suggestions regarding more efficient MCC in female subjects, the majority of authors have not observed significant differences between female and male groups.28,29 Literature reports seem to suggest a tendency to minimize surgical interventions, surgery duration, and number of incisions.30-33 Analyses of complications related to surgery delay do not include data on MCC impairment. Our analysis did not reveal statistically significant differences between saccharine test results associated with surgery duration and time elapsed between injury and surgery. The results of the study of Niedzielska et al.11 urged us to investigate ZMOF-related MCC impairment in the context of treatment modalities used. In patients with Le Fort maxilliary fractures, less invasive techniques, such as maxillomandibular fixation, seemed to impair the rate of MCC to less extent than surgical interventions.11 However, our analysis did not show differences between the results of the saccharine test performed in patients who had received different ZMOF treatments. A subgroup of patients was treated by open reduction and osteosynthesis with Foley catheter placement. This was done because, although the proponents of catheter placement claim it allows postoperative sinus lavage, improves sinus drainage, and prevents bleeding, it has also been argued that compression of sinus mucous membrane by a catheter might result in necrosis.34-36 Our studies indicate significant MCC impairment associated with catheter placement. There are also other reasons to abandon the procedure of temporary bone segment support with Foley catheter or antral packing
OOOO Volume 115, Number 6
of the maxillary sinus; instead, recently developed materials for orbital floor reconstruction are used.37,38 Craniofacial fractures are among those factors affecting mucociliary clearance that remain insufficiently investigated and understood. Mucociliary clearance impairment is one of potential complications of ZMOF. Further investigations are indispensable to develop treatment algorithms for ZMOF to minimize negative injury outcomes, including MCC impairment.
CONCLUSIONS 1. ZMOF result in MCC impairment. 2. Foley catheter placement during open reduction of ZMOF decreases MCC clearance rates. 3. MCC impairment is not related to injury severity, time elapsed between injury and treatment, the majority of treatment modalities, or surgery duration.
ORIGINAL ARTICLE Janic and Niedzielska e11
15. 16.
17.
18.
19.
20. 21.
REFERENCES 1. Boucher RC. Human airway ion transport. Part one. Am J Respir Crit Care Med 1994;150:271-81. 2. Jeffery PK, Gaillard D, Moret S. Human airway secretory cells during development and in mature airway epithelium. Eur Respir J 1992;5:93-104. 3. Joo NS, Lee DJ, Winges KM, Rustagi A, Wine JJ. Regulation of antiprotease and antimicrobial protein secretion by airway submucosal gland serous cells. J Biol Chem 2004;279: 38854-60. 4. Houtmeyers E, Gosselink R, Gayan-Ramirez G, Decramer M. Regulation of mucociliary clearance in health and disease. Eur Respir J 1999;13:1177-88. 5. Beisswenger C, Bals R. Antimicrobial peptides in lung inflammation. Chem Immunol Allergy 2005;86:55-71. 6. Girod S, Zahm JM, Plotkowski C, Beck G, Puchelle E. Role of the physicochemical properties of mucus in the protection of the respiratory epithelium. Eur Respir J 1992;5:477-87. 7. Rutland J, Cole PJ. Nasal mucociliary clearance and ciliary beat frequency in cystic fibrosis compared with sinusitis and bronchiectasis. Thorax 1981;36:654-8. 8. Pietrasiak A. Test sacharynowy—stałym elementem badania laryngologicznego. Nowa Pediatr 2005;3:87-90. 9. 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 Otorhinolaryngol 1995;252:340-3. 10. Plaza Valía P, Carrión Valero F, Marín Pardo J, Bautista Rentero D, González Monte C. Saccharin test for the study of mucociliary clearance: reference values for a Spanish population. Arch Bronconeumol 2008;44:540-5. 11. Niedzielska IA, Wróbel K, Wziatek W, Bazarnik Z, Drugacz J. Mucociliary clearance and sense of smell following management of le fort maxilla fractures. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:287-91. 12. Samolczyk-Wanyura D. Epidemiologiczna oraz kliniczno-radiologiczna ocena chorych leczonych z powodu złaman´ jarzmowoszczekowo-oczodołowych-obserwacje własne. Czas Stomatol 2004;9:590-7. 13. Obuekwe O, Owotade F, Osaiyuwu O. Etiology and pattern of zygomatic complex fractures: a retrospective study. J Natl Med Assoc 2005;97:992-6. 14. Chowdhury R, Menon S. Etiology and management of zygoma-
22.
23.
24.
25. 26.
27. 28.
29.
30.
31.
32.
33.
ticomaxillary complex fractures in the armed Forces. Med J Armed Forces India 2005;61:238-40. Maturo S, Lopez MA. Zygomatico-orbito-maxillary complex fractures. Operat Techn Otolaryngol 2008;19:86-9. Dziadek H, Cies´lik T. Leczenie złaman´ jarzmowo-oczodołowych i jarzmowo-szczekowo-oczodołowych z zastosowaniem repozycji otwartej i bezpos´redniej osteosyntezy minipłytkowej. Wiad Lek 2005;58:270-4. Sun SS, Hsieh JF, Tsai SC, Ho YJ, Kao CH. Evaluation of nasal mucociliary clearance function in allergic rhinitis patients with technetium 99m-labeled macroaggregated albumin rhinoscintigraphy. Ann Otol Rhinol Laryngol 2002;111:77-9. Kao CH, Jiang RS, Wang SJ, Yeh SH. Influence of age, gender, and ethnicity on nasal mucociliary clearance function. Clin Nucl Med 1994;19:813-6. Littlejohn MC, Stiernberg CM, Hokanson JA, Quinn FB Jr, Bailey BJ.The relationship between the nasal cycle and mucociliary clearance. Laryngoscope 1992;102:117-20. Doyle WJ, van Cauwenberge PB. Relationship between nasal patency and clearance. Rhinology 1987;25:167-79. Naiboglu B, Deveci I, Kalaycik C, Daylan A, Habesoglu TE, Toros SZ, et al. Effect of nasolacrimal duct obstruction on nasal mucociliary transport. J Laryngol Otol 2010;124: 166-70. Hüttenbrink KB, Wrede H, Lagemann S, Schleicher E, Hummel T, Lokalisierte,endonasal emessung der mukoziliaren Transportgeschwindigkeit als neues verfahren für die nasale. Laryngorhinootologie 2006;85:24-31. Ho JC, Chan KN, Hu WH, Lam WK, Zheng L, Tipoe GL, et al. The effect of aging on nasal mucociliary clearance, beat frequency, and ultrastructure of respiratory cilia. Am J Respir Crit Care Med 2001;163:983-8. Armengot M, Barona R, Garín L, Basterra J. The influence of age, sex and circadian rhythms on the nasal mucosal in the mucociliary clearance. An Otorrinolaringol Ibero Am 1993; 20:581-8. Puchelle E, Zahm JM, Bertrand A. Influence of age on bronchial mucociliary transport. Scand J Respir Dis 1979;60:307-13. Jorissen M, Willems T, van der Schueren B. Nasal ciliary beat frequency is age independent. Laryngoscope 1998;108: 1042-7. Mortensen J, Lange P, Jorgen N, Groth S. Lung mucociliary clearance. Eur J Nucl Med 1994;21:953-61. Armengot M, Basterra J, Marco J. Nasal mucociliary function during the menstrual cycle in healthy women. Rev Laryngol Otol Rhinol (Bord) 1990;111:107-9. Hasani A, Vora H, Pavia D, Agnew JE, Clarke SW. No effect of gender on lung mucociliary clearance in young healthy adults. Respir Med 1994;88:697-700. Lee PK, Lee JH, Choi YS, Oh DY, Rhie JW, Han KT, Ahn ST. Single transconjunctival incision and two-point fixation for the treatment of noncomminuted zygomatic complex fracture. J Korean Med Sci 2006;21:1080-5. Folkestad L, Granström G. A prospective study of orbital fracture sequelae after change of surgical routines. J Oral Maxillofac Surg 2003;61:1038-44. Kayikçiog˘lu A, Erk Y, Mavili E, Vargel I, Ozgür F. Botulinum toxin in the treatment of zygomatic fractures. Plast Reconstr Surg 2003;111:341-6. Bezuhly M, Lalonde J, Alqahtani M, Sparkes G, Lalonde DH. Gillies elevation and percutaneous Kirschner wire fixation in the treatment of simple zygoma fractures: long-term quantitative outcomes. Plast Reconstr Surg 2008;121:948-55.
ORAL AND MAXILLOFACIAL SURGERY e12 Janic and Niedzielska 34. Celiköz B, Duman H, Selmanpakog˘lu N. Reconstruction of the orbital floor with lyophilized tensor fascia lata. J Oral Maxillofac Surg 1997;55:240-4. 35. Miki T, Wada J, Haraoka J, Inaba I. Endoscopic transmaxillary reduction and balloon technique for blowout fractures of the orbital floor. Minim Invasive Neurosurg 2004;47:359-64. 36. Rath EZ, Goldfeld M, Samet A, Rehany U, Rumelt S. Entrapment of inferior rectus muscle as a complication of sinus balloon expansion for maxillary sinus fracture. Eye (Lond) 2007;21:97-9. 37. Paludetti G, Almadori G, Corina L, Parrilla C, Rigante M, Ottaviani F. Midfacial fractures: our experience. Acta Otorhinolaryngol Ital 2003;23:265-73.
OOOO June 2013 38. Folkestad L, Granström G. A prospective study of orbital fracture sequelae after change of surgical routines. J Oral Maxillofac Surg 2003;61:1038-44.
Reprint requests: Tomasz Janic, DDS 13 ul. Szymanowskiego 441-219 Sosnowiec Poland [email protected]
Mucociliary clearance impairment after zygomaticomaxillaryorbital fractures Tomasz Janic, DDS, PhD, and Iwona Niedzielska, DDS, MD, PhD Objective. The purpose of this study was to examine the influence of zygomaticomaxillo-orbitalis (ZMO) fracture and its symptoms on mucociliary transport (MCT). Study Design. The study encompassed 144 patients who sustained ZMO fracture. A saccharine test was conducted in every patient both on the side of fracture and on the unaffected side. The results were analyzed in connection with the patients’ age, sex, degree of injury, method of treatment, time since fracture, and duration of surgery. Results. It was shown that MCT was considerably impaired on the affected side compared with the control side. However, the degree of impairment did not vary significantly in the patients regardless of the analyzed parameters. Conclusions. ZMO fracture induces the disorder of MCT. Balloon Foley catheter in the open reduction of ZMO fracture impairs MCT. The analyzed parameters do not affect the disorders of MCT. (Oral Surg Oral Med Oral Pathol Oral Radiol 2013;115:e6-e12)
Mucociliary clearance (MCC) is one of the most important airway defense mechanisms. It occurs due to continuous ciliary motion resulting in the flow of the overlying mucus. The thickness of the periciliary fluid layer is controlled by the respiratory epithelium via changes in the activity of ion channels and transmembrane conductors.1 Mucus production in the nasal passages and sinus cavities is regulated by the seromucous glands found in the submucosal layer and epithelial goblet cells.2 Mucus is composed mainly of water (95%) but also includes glycoproteins, immunoglobulins (IgA, IgG), lysozyme, and lactoferrin.3,4 The mucous layer also contains T lymphocytes, NK cells, macrophages, basophils, and neutrophils.5 The most fundamental mucus properties in terms of MCC are its viscosity and elasticity. A mucus layer of 0.5-2 m in thickness also protects the respiratory epithelium against mechanical and chemical damage as well as against dryness and pathogen entry.6 Mucociliary clearance is most frequently assessed using the saccharine test of Rutland and Cole.7 Nasal MCC time ranges from 3.17 to 20.9 minutes.8,9 MCC ⬎30 minutes indicates its compromise, i.e., mucus stasis. Because it is noninvasive and comparable to other measurement methods, the saccharine test is recommended for screening to detect abnormal MCC7-10. MCC is affected by numerous factors. Genetic ciliary motility disorders cause multiorgan abnormalities not only in the respiratory tract but also in those organs Department of Craniomaxillofacial Surgery and Dental Surgery, Katowice, Poland. Received for publication Jul 23, 2011; returned for revision Sep 28, 2011; accepted for publication Oct 17, 2011. © 2013 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2011.10.035
e6
which contain ciliated epithelial cells (reproductive organs, ear). MCC is accelerated by mucolytic agents (bromhexine, ambroxol, acetylcysteine, carbocysteine), adenosinotriphosphate, aminophylline, -sympathicomimetics, and acetylocholine. The rate of mucociliary clearance is reduced by inhalation anesthetics (halothane, isoflurane) and intravenous anesthetics (temazepam, diazepam). Ciliary actions are also influenced by biologic (viral and bacterial infections, allergies, astma, anatomic anomalies) and physicochemical factors (temperature, humidity, ionizing radiation, air pollution, cigarette smoke). There are a few research reports about the effect of upper respiratory tract injury on MCC; however, in the case of craniofacial trauma the issue of MCC impairment has been considered only for maxillary fractures. It has been demonstrated that surgical management of maxillary fractures resulted in greater impairment of MCC than less invasive techniques, such as maxillomandibular fixation thereof.11 The effect of damage to nasal structures on MCC is well established; however the role of maxillary sinuses in the process remains puzzling. Therefore, it seemed essential to investigate MCC in patients who had sustained zygomaticomaxillary-orbital fractures (ZMOF),
Statement of Clinical Relevance The results of this study show complications after zygomaticomaxillary-orbital fractures (ZMOF), which have not been previously described. The awareness of possible and frequent complications will allow taking appropriate preventive measures and treating the disorders caused by ZMOF more effectively.
OOOO Volume 115, Number 6
and the more so because both the affected and contralateral (control) side of the face could be assessed. The aim of the study was to assess: 1) the effect of the severity of SMOF and accompanying symptoms on mucociliary clearance; and 2) MCC impairment depending on time elapsed from injury to presentation, management type, and duration of surgery.
MATERIALS AND METHODS A total of 144 patients treated for ZMOF in the Craniomaxillofacial Surgery Department, Medical University of Silesia in Katowice, in the years 2004-2010 were enrolled. The prospective part of the study comprised 15 patients (3 women and 12 men, ages 21-56 years) with a diagnosis of displaced ZMOF; the patients had no history of any other craniofacial injuries and had been qualified for surgical management. Exclusion criteria were systemic disease, cigarette smoking, alcohol and drug use, and nasal septum deviation. The saccharine test was carried out twice, i.e., after injury and after surgery (at the latest on day 5 after the operative procedure), and on both the affected and the control sides of the face. The retrospective part included 129 patients (21 female and 108 male, aged 12-76 years) with displaced/ nondisplaced ZMOF regardless of their treatment; the patients had no history of any other craniofacial injuries; exclusion criteria were the same as in the prospective subgroup. The patients in the retrospective study were assessed in terms of MCC rate at the following time intervals: 1-3 months (18 patients); 3-6 months (16 patients); 6-12 months (15 patients); 12-36 months (47 patients), and ⬎36 months (32 patients) after injury and ZMOF management. Detailed analyses of case histories, including X-rays and operative reports were carried out in order to identify the type of fracture (displaced or nondisplaced ZMOF), the time elapsed between injury and surgical management, the type of treatment, the duration of surgery, and symptoms accompanying the fracture and concomitant diseases. At each follow-up time point, the patient’s history was taken and clinical examination performed, including for bone irregularities, nasal septum deviation, facial asymmetry, occlusion defects, and sensation in the area supplied by the infraorbital nerve. MCC assessment In the prospective group, the saccharine test was carried out twice, i.e., within 5 days of injury and surgical procedure; a saccharine crystal was inserted into each nasal passage to assess MCC both on the affected and
ORIGINAL ARTICLE Janic and Niedzielska e7
control sides of the face. In the retrospective group, bilateral MCC assessment was also carried out at 1-3, 3-6, 6-12, 12-36, and ⬎36 months after injury and treatment. Saccharine test Before the test, the patients were instructed to blow their nose (except the prospective group owing to the risk of developing subcutaneous emphysema) and restrict their physical activity. The test was carried out with the patient in sitting position with head on the headrest, after a 15-minute adaptation to test conditions (the same for all patients). Test room temperature was 18-27°C, and humidity 40%-70%. Using a moistened pipette and Hartmann nasal speculum, a small saccharine crystal (1 mm) was placed ⬃1 cm from the anterior edge of the inferior turbinate. In case of sneezing or nasal discharge, the test was discontinued and repeated after a couple of minutes. Time to first feeling of sweetness was measured in seconds and expressed as decimal fraction of a minute. If, during 30 minutes (time ⬎30 min was considered to be mucus stasis), the patient did not report the taste of sweetness, the measurement was continued for another 10 minutes not exceeding 40 minutes for the affected and control sides of the face. In both prospective and retrospective groups, the test was carried out starting on the right side regardless of what part of the face had been injured. MCC rate was analyzed in relation to age, gender, injury severity (displaced or nondisplaced ZMOF), type of treatment (closed reduction, open reduction and osteosynthesis with/without Foley catheter placement), time between injury and treatment (⬍48 h, ⬎48 h), and surgery duration (⬍1 h, ⬎1 h). Statistical analysis Statistical analyses were carried out using Statistica 9.0 (Windows), the Wilcoxon test, Mann-Whitney U test (to compare 2 categoric outcomes), and Spearman rank correlation coefficients. Statistical significance was set at P ⬍ .05, and high statistical significance at P ⬍ .01. Differences between saccharine test results regarding the affected and control sides of the face for the same patient were calculated according to the following formula: difference [min] ⫽ (MCC rate on the affected side) ⫺ (MCC rate on the control side) Percentage difference was calculated as follows: difference [%] ⫽ (difference ⫻ 100%)/MCC rate on the control side Based on the results of the above, mean values of intrapersonal differences between MCC rates on the affected and control sides were calculated as well as
ORAL AND MAXILLOFACIAL SURGERY e8 Janic and Niedzielska
OOOO June 2013
Table I. Results of the prospective part of the study (control side)
Postinjury Postsurgery Difference (min) Percent difference (%)
Meam
Median
Minimum
Maximum
Lower quartile
Upper quartile
SD
12.09 12.30 0.21 5.19
10.83 12.60 0.13 1.29
6.73 7.48 ⫺5.80 ⫺28.78
20.15 19.62 8.79 81.16
8.23 9.12 ⫺0.60 ⫺4.55
15.17 15.22 0.75 11.14
4.24 3.69 2.94 23.79
Table II. Results of the retrospective part of the study
Control side (min) Affected side (min) Difference (min) Difference (%)
Mean
Median
Minimum
Maximum
Lower quartile
Upper quartile
SD
10.55 15.03 4.47 50.62
10.33 13.67 2.71 27.57
5.13 5.92 ⫺8.82 ⫺50.70
24.72 40.00 34.28 599.30
7.66 10.52 0.41 3.75
12.33 17.75 7.03 69.29
3.52 6.87 6.70 78.88
mean differences between the affected and control sides of groups and subgroups under analysis. IRB approval The research was approved by the Bioethics Committee of the Medical University of Silesia (L.dz.KNW-0022/ KB1/125/08). The authors have read the Helsinki Declaration and have followed its guidelines in this investigation.
RESULTS The prospective part of the study comprised 15 patients (3 women and 12 men, aged 21-56 years, mean age 36.2 years). Assault and battery was the most frequent cause of ZMOF in this group. Within 5 days of injury and surgical intervention, all patients demonstrated mucus stasis on the affected side (Table I). Mean postinjury and postsurgery MCC rates on the control side were 12.09 minutes (SD 4.24 min) and 12.3 minutes (SD 3.69 min), respectively. The retrospective part ultimately included 128 patients (21 female and 107 male, aged 12-76 years, mean age 33.47 years, SD 14.34). ZMOF was most frequently sustained by patients in their third decade of life (53 patients, 41.4%). The most common cause of the trauma was assault and battery (73 patients, 57%). Differences between mean MCC rates on the affected and control sides in this group were statistically significant (P ⬍ .001). Five patients had mucus stasis on the affected side of the face (Table II). The highest MCC rates (15.24-15.71 min) were noted on the affected side between months 3 and 36 after treatment. The longer the observation time, the more mean MMC rates on the control side exceeded the value of 9.34 minutes (SD 2.82 min) seen in the subgroup followed within the first 3 months. The rate increased to 11.4 minutes (SD 3.30 min) in the subgroup examined at 36 months after treatment (Figure 1).
Mean MCC rates on the affected and control sides decreased and increased with age, respectively. The subgroup below the age of 20 years (17 patients) had the highest mean MCC rates on the affected side (18.58 min, SD 11.42 min), and the lowest on the control side (9.98 min, SD 2.46 min) compared with the other age subgroups. Mean MCC rate in the subgroup aged 20-50 years was between the rates calculated for the youngest and oldest patients (range 14.28-14.8 min). The retrospective part included 21 (16.4%) female and 107 (83.6%) male subjects. MCC rates were lower for female subjects on both affected (14.28 min, SD 7.66 min) and control sides (9.42 min, SD 2.90 min). Differences in MCC rates between the affected and control sides were highly statistically significant for both male (P ⬍ .0001) and female (P ⫽ .0013) subjects. Nondisplaced and displaced ZMOF were diagnosed in 13 and 115 patients, respectively. Mean MCC rates were slightly higher on the affected side with displacement (15.10 min, SD 7.03 min) compared with nondisplaced injury (14.41 min, SD 3.55 min). Saccharine test results differed significantly between the affected and control sides both in the case of displaced (P ⬍ .0001) and nondisplaced fractures (P ⫽ .0037). Open reduction and osteosynthesis was performed in 93 patients, 14 of whom also had a Foley catheter placed. Closed reduction with a single-toothed hook but no osteosynthesis was carried out in 22 patients. The highest MCC rates on the affected side (15.18 min, SD 7.13 min) were seen in the group with open reduction and osteosynthesis. Saccharine test results on the affected and control sides were significantly different for all treatment modalities (P ⬍ .01). In the case of open reduction, mean MCC rate on the affected side was higher in patients with a Foley catheter (17.5 min, SD 6.06 min; Figure 2). Mean difference between intrapersonal MCC rates in this group of patients was 6.44
OOOO Volume 115, Number 6
ORIGINAL ARTICLE Janic and Niedzielska e9
Fig. 1. Mucociliary transport (MCC) rates on the affected and control sides depending on time after termination of treatment.
Fig. 2. Mucociliary transport (MCC) rates on the affected and control sides depending on Foley catheter placement during open reduction.
minutes (SD 4.83 min), i.e., higher than in patients with no maxillary sinus roof support (4.45 min, SD 6.92 min). Saccharine test results differed significantly between the affected and control sides in individual patients with open reduction and Foley catheter (P ⫽ .0012) and those without catheter placement (P ⬍ .0001). Catheter use significantly increased the MCC rate on the affected side (P ⫽ .0451) but seemed to have no effect on the saccharine test parameters on the control side (P ⫽ .8299; Figure 2). Forty-six patients were operated on within 48 hours, whereas 69 underwent surgery beyond 48 hours of injury.
Mean MCC rate in the latter subgroup was higher than in the former, on both the control (10.75 min, SD 2.93 min) and the affected (15.71 min, SD 7.83 min) sides. Those operated on beyond 48 hours of injury also had a higher difference between MCC rates on the affected and control sides (4.95 min, SD 7.66 min) compared with the respective value in the group who had undergone surgery within 48 hours (3.8 min, SD 5.52 min). Saccharine test results were significantly different between both sides of the face in patients operated on within and beyond 48 hours of injury (P ⬍ .0001). Sixty-eight interventions lasted ⬍60 minutes, whereas 42 surgical procedures were longer. Mean MCC rates were
ORAL AND MAXILLOFACIAL SURGERY e10 Janic and Niedzielska
higher in the subgroup with short-lasting surgery and on both affected and control sides (i.e., 15.29 min, SD 7.47; and 11.06 min, SD 3.48 min; respectively). Saccharine test results differed significantly between the affected and control sides of individual patients operated on within or beyond 48 hours of injury (P ⬍ .0001). A comparison of mean intrapersonal MCC rates on the affected and control sides did not reveal significant differences regarding age, gender, observation time, injury severity, treatment modality, surgery delay, and surgery duration in both absolute and percentage values. Significant differences were seen only between subgroups with and without Foley catheter use and between the affected and control sides.
DISCUSSION Epidemiologic analysis of our results is consistent with that of other authors suggesting that the most common cause of ZMOF is assault and battery of men in their third decade of life.12-16 Eighty-five percent of our ZMOF patients showed MCC impairment; however, this can not be verified through comparison with other reports, owing to the lack of similar investigations. It may only be suspected that chronic sinusitis commonly reported after injury might contribute to MCC impairment. There are no literature reviews concerning the effect of ZMOF on mucociliary clearance. The only publication possibly available for results comparison deals with MCC assessment after LeFort maxillary fractures.11 Mean MCC rates in Le Fort I, II, and III fractures were 17, 19, and 30 minutes, respectively. Less invasive techniques, such as maxillomandibular fixation, impaired the rate of MCC to less extent than surgical interventions.11 Subjective examination revealed a significant effect of ZMOF on MCC impairment both directly after injury (mucus stasis) and in the later period. Slightly lower mean saccharine test results, i.e., more efficient MCC during ZMOF compared with maxillary fractures, might be related to the extent of the damage to the ciliary epithelium. Le Fort fractures involve not only maxillary sinus walls but also, among others, the lateral wall of the nasal cavity. The saccharine test is simple, noninvasive, inexpensive, and reproducible.7,8,10 Its main disadvantage is the time frame: up to 80 minutes for a patient (up to 40 min on each side). Literature-reported MCC reference range for healthy patients is 3.17-20.9 minutes, which is similar to our results (5.13-24.72 min). However, it should be emphasized that the comparison made in our study was not between trauma patients and healthy control subjects, but between the affected and control sides of the same individuals.8,9
OOOO June 2013
Our analysis included saccharine test results obtained on the affected and control sides of the face of each individual patient. We intended to analyze not only mean MCC rates on each side, but also intrapersonal differences (i.e., the differences between bilateral MCC rates of the same individual) so as not to disregard changes in environmental conditions or individual parameters, e.g., body temperature. Mean MCC rates differed between both sides in the same patients, evidencing impairment on the affected side. Intrapersonal differences are not found during MCC rate measurements under physiologic conditions,17-20 but are observed in patients with unilateral nasolacrimal stenosis.21 Individuals with no systemic disease and external confounders have shown age-related compromise of mucociliary clearance under physiologic conditions— without gender predilection.22-25 However, lack of age effect has also been reported.26,27 Our results did not indicate significant correlations between age and MCC rate on both affected and control sides of the face. However, this could be associated with a small number of patients at developmental age (⬍15 y). Despite some suggestions regarding more efficient MCC in female subjects, the majority of authors have not observed significant differences between female and male groups.28,29 Literature reports seem to suggest a tendency to minimize surgical interventions, surgery duration, and number of incisions.30-33 Analyses of complications related to surgery delay do not include data on MCC impairment. Our analysis did not reveal statistically significant differences between saccharine test results associated with surgery duration and time elapsed between injury and surgery. The results of the study of Niedzielska et al.11 urged us to investigate ZMOF-related MCC impairment in the context of treatment modalities used. In patients with Le Fort maxilliary fractures, less invasive techniques, such as maxillomandibular fixation, seemed to impair the rate of MCC to less extent than surgical interventions.11 However, our analysis did not show differences between the results of the saccharine test performed in patients who had received different ZMOF treatments. A subgroup of patients was treated by open reduction and osteosynthesis with Foley catheter placement. This was done because, although the proponents of catheter placement claim it allows postoperative sinus lavage, improves sinus drainage, and prevents bleeding, it has also been argued that compression of sinus mucous membrane by a catheter might result in necrosis.34-36 Our studies indicate significant MCC impairment associated with catheter placement. There are also other reasons to abandon the procedure of temporary bone segment support with Foley catheter or antral packing
OOOO Volume 115, Number 6
of the maxillary sinus; instead, recently developed materials for orbital floor reconstruction are used.37,38 Craniofacial fractures are among those factors affecting mucociliary clearance that remain insufficiently investigated and understood. Mucociliary clearance impairment is one of potential complications of ZMOF. Further investigations are indispensable to develop treatment algorithms for ZMOF to minimize negative injury outcomes, including MCC impairment.
CONCLUSIONS 1. ZMOF result in MCC impairment. 2. Foley catheter placement during open reduction of ZMOF decreases MCC clearance rates. 3. MCC impairment is not related to injury severity, time elapsed between injury and treatment, the majority of treatment modalities, or surgery duration.
ORIGINAL ARTICLE Janic and Niedzielska e11
15. 16.
17.
18.
19.
20. 21.
REFERENCES 1. Boucher RC. Human airway ion transport. Part one. Am J Respir Crit Care Med 1994;150:271-81. 2. Jeffery PK, Gaillard D, Moret S. Human airway secretory cells during development and in mature airway epithelium. Eur Respir J 1992;5:93-104. 3. Joo NS, Lee DJ, Winges KM, Rustagi A, Wine JJ. Regulation of antiprotease and antimicrobial protein secretion by airway submucosal gland serous cells. J Biol Chem 2004;279: 38854-60. 4. Houtmeyers E, Gosselink R, Gayan-Ramirez G, Decramer M. Regulation of mucociliary clearance in health and disease. Eur Respir J 1999;13:1177-88. 5. Beisswenger C, Bals R. Antimicrobial peptides in lung inflammation. Chem Immunol Allergy 2005;86:55-71. 6. Girod S, Zahm JM, Plotkowski C, Beck G, Puchelle E. Role of the physicochemical properties of mucus in the protection of the respiratory epithelium. Eur Respir J 1992;5:477-87. 7. Rutland J, Cole PJ. Nasal mucociliary clearance and ciliary beat frequency in cystic fibrosis compared with sinusitis and bronchiectasis. Thorax 1981;36:654-8. 8. Pietrasiak A. Test sacharynowy—stałym elementem badania laryngologicznego. Nowa Pediatr 2005;3:87-90. 9. 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 Otorhinolaryngol 1995;252:340-3. 10. Plaza Valía P, Carrión Valero F, Marín Pardo J, Bautista Rentero D, González Monte C. Saccharin test for the study of mucociliary clearance: reference values for a Spanish population. Arch Bronconeumol 2008;44:540-5. 11. Niedzielska IA, Wróbel K, Wziatek W, Bazarnik Z, Drugacz J. Mucociliary clearance and sense of smell following management of le fort maxilla fractures. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:287-91. 12. Samolczyk-Wanyura D. Epidemiologiczna oraz kliniczno-radiologiczna ocena chorych leczonych z powodu złaman´ jarzmowoszczekowo-oczodołowych-obserwacje własne. Czas Stomatol 2004;9:590-7. 13. Obuekwe O, Owotade F, Osaiyuwu O. Etiology and pattern of zygomatic complex fractures: a retrospective study. J Natl Med Assoc 2005;97:992-6. 14. Chowdhury R, Menon S. Etiology and management of zygoma-
22.
23.
24.
25. 26.
27. 28.
29.
30.
31.
32.
33.
ticomaxillary complex fractures in the armed Forces. Med J Armed Forces India 2005;61:238-40. Maturo S, Lopez MA. Zygomatico-orbito-maxillary complex fractures. Operat Techn Otolaryngol 2008;19:86-9. Dziadek H, Cies´lik T. Leczenie złaman´ jarzmowo-oczodołowych i jarzmowo-szczekowo-oczodołowych z zastosowaniem repozycji otwartej i bezpos´redniej osteosyntezy minipłytkowej. Wiad Lek 2005;58:270-4. Sun SS, Hsieh JF, Tsai SC, Ho YJ, Kao CH. Evaluation of nasal mucociliary clearance function in allergic rhinitis patients with technetium 99m-labeled macroaggregated albumin rhinoscintigraphy. Ann Otol Rhinol Laryngol 2002;111:77-9. Kao CH, Jiang RS, Wang SJ, Yeh SH. Influence of age, gender, and ethnicity on nasal mucociliary clearance function. Clin Nucl Med 1994;19:813-6. Littlejohn MC, Stiernberg CM, Hokanson JA, Quinn FB Jr, Bailey BJ.The relationship between the nasal cycle and mucociliary clearance. Laryngoscope 1992;102:117-20. Doyle WJ, van Cauwenberge PB. Relationship between nasal patency and clearance. Rhinology 1987;25:167-79. Naiboglu B, Deveci I, Kalaycik C, Daylan A, Habesoglu TE, Toros SZ, et al. Effect of nasolacrimal duct obstruction on nasal mucociliary transport. J Laryngol Otol 2010;124: 166-70. Hüttenbrink KB, Wrede H, Lagemann S, Schleicher E, Hummel T, Lokalisierte,endonasal emessung der mukoziliaren Transportgeschwindigkeit als neues verfahren für die nasale. Laryngorhinootologie 2006;85:24-31. Ho JC, Chan KN, Hu WH, Lam WK, Zheng L, Tipoe GL, et al. The effect of aging on nasal mucociliary clearance, beat frequency, and ultrastructure of respiratory cilia. Am J Respir Crit Care Med 2001;163:983-8. Armengot M, Barona R, Garín L, Basterra J. The influence of age, sex and circadian rhythms on the nasal mucosal in the mucociliary clearance. An Otorrinolaringol Ibero Am 1993; 20:581-8. Puchelle E, Zahm JM, Bertrand A. Influence of age on bronchial mucociliary transport. Scand J Respir Dis 1979;60:307-13. Jorissen M, Willems T, van der Schueren B. Nasal ciliary beat frequency is age independent. Laryngoscope 1998;108: 1042-7. Mortensen J, Lange P, Jorgen N, Groth S. Lung mucociliary clearance. Eur J Nucl Med 1994;21:953-61. Armengot M, Basterra J, Marco J. Nasal mucociliary function during the menstrual cycle in healthy women. Rev Laryngol Otol Rhinol (Bord) 1990;111:107-9. Hasani A, Vora H, Pavia D, Agnew JE, Clarke SW. No effect of gender on lung mucociliary clearance in young healthy adults. Respir Med 1994;88:697-700. Lee PK, Lee JH, Choi YS, Oh DY, Rhie JW, Han KT, Ahn ST. Single transconjunctival incision and two-point fixation for the treatment of noncomminuted zygomatic complex fracture. J Korean Med Sci 2006;21:1080-5. Folkestad L, Granström G. A prospective study of orbital fracture sequelae after change of surgical routines. J Oral Maxillofac Surg 2003;61:1038-44. Kayikçiog˘lu A, Erk Y, Mavili E, Vargel I, Ozgür F. Botulinum toxin in the treatment of zygomatic fractures. Plast Reconstr Surg 2003;111:341-6. Bezuhly M, Lalonde J, Alqahtani M, Sparkes G, Lalonde DH. Gillies elevation and percutaneous Kirschner wire fixation in the treatment of simple zygoma fractures: long-term quantitative outcomes. Plast Reconstr Surg 2008;121:948-55.
ORAL AND MAXILLOFACIAL SURGERY e12 Janic and Niedzielska 34. Celiköz B, Duman H, Selmanpakog˘lu N. Reconstruction of the orbital floor with lyophilized tensor fascia lata. J Oral Maxillofac Surg 1997;55:240-4. 35. Miki T, Wada J, Haraoka J, Inaba I. Endoscopic transmaxillary reduction and balloon technique for blowout fractures of the orbital floor. Minim Invasive Neurosurg 2004;47:359-64. 36. Rath EZ, Goldfeld M, Samet A, Rehany U, Rumelt S. Entrapment of inferior rectus muscle as a complication of sinus balloon expansion for maxillary sinus fracture. Eye (Lond) 2007;21:97-9. 37. Paludetti G, Almadori G, Corina L, Parrilla C, Rigante M, Ottaviani F. Midfacial fractures: our experience. Acta Otorhinolaryngol Ital 2003;23:265-73.
OOOO June 2013 38. Folkestad L, Granström G. A prospective study of orbital fracture sequelae after change of surgical routines. J Oral Maxillofac Surg 2003;61:1038-44.
Reprint requests: Tomasz Janic, DDS 13 ul. Szymanowskiego 441-219 Sosnowiec Poland [email protected]