|Year : 2018 | Volume
| Issue : 1 | Page : 254-261
Evaluation of nasal mucosal changes of tracheastomized patients
Mohammad El-Sharnouby, Yaser Khalil, Ibrahim A El-Shafy, Mervat Khalil
Department of Otorhinolaryngology, Faculty of Medicine, Menoufia University, Menoufia; Otorhinolaryngology Department, Faculty of Medicine, Menoufia University, Shebin Elkom, Egypt
|Date of Submission||18-Jan-2017|
|Date of Acceptance||07-May-2017|
|Date of Web Publication||14-Jun-2018|
Otorhinolaryngology Department, Faculty of Medicine, Menoufia University, Shebin Elkom
Source of Support: None, Conflict of Interest: None
The aim of this study was to evaluate the changes in the nasal mucosa of tracheostomized patients as a result of decreased nasal airflow.
The effect of tracheostomy on the chest is well established, but the effect on the nasal mucosa and the upper respiratory tract has not been extensively investigated.
Patients and methods
Thirty-one participants who underwent total laryngectomy or tracheostomy for prolonged intubation were enrolled in the study. Patients were evaluated at 2 and 6 months after tracheostomy endoscopically as regards the color, discharge, crustations, and atrophy of nasal mucosa. The Saccharine test and the methylene blue test were used to assess the mucociliary clearance. Nasal biopsy and histopathological examination with hematoxylin and eosin staining was performed to confirm our findings.
There was a significant increase in nasal discharge with histopathological increase in mucous-secreting glands by 2 months after tracheostomy and a significant decrease at 6 months postoperatively. The color of the nasal mucosa became more pink 2 months after tracheostomy with no significance, but at 6 months it became more pale with significance. There was a significant improvement in the saccharine times and methylene blue movement toward the nasopharyn × 2 months postoperatively, whereas there was a significant delay in the saccharine times and methylene blue movement at 6 months. On histopathological examination, there was a significant incidence of nasal mucosal atrophy at 6 months.
There was an increase in the number of mucous glands with their secretion along with an increase in mucociliary clearance of the nose early after tracheostomy or total laryngectomy. However, with time the reverse occurs due to the long-term effect of airflow deprivation on the nasal mucosa with increased incidence of nasal mucosal atrophy as shown by histopathological examination.
Keywords: airflow deprivation, mucociliary clearance, nasal mucosa
|How to cite this article:|
El-Sharnouby M, Khalil Y, El-Shafy IA, Khalil M. Evaluation of nasal mucosal changes of tracheastomized patients. Menoufia Med J 2018;31:254-61
|How to cite this URL:|
El-Sharnouby M, Khalil Y, El-Shafy IA, Khalil M. Evaluation of nasal mucosal changes of tracheastomized patients. Menoufia Med J [serial online] 2018 [cited 2020 Aug 7];31:254-61. Available from: http://www.mmj.eg.net/text.asp?2018/31/1/254/234204
| Introduction|| |
Tracheostomy is a relatively common operation used to maintain a patient's airway, reduce ventilatory dead space, and facilitate access to the lower respiratory tract, bypassing the upper respiratory tract. The effect of this operation on the chest is well established, but the effect on the nasal mucosa and the upper respiratory tract has not been extensively investigated .
Turbulent nasal airflow (e.g., relating to a septal deviation) is thought to lead to a localized drying of the epithelium, with changes in mucociliary transport, nasal crusting, and microbiological flora leading to atrophic rhinitis . It is also suggested that some airflow is necessary for normal mucosal function , and hence inadequate flow may be equally likely to cause pathology. Much of the understanding of the effect of nasal airflow on the mucosal epithelium comes from animal experiments in which one side of the nose has been surgically occluded , and in humans from laryngectomy patients. In recent studies, Shin and Heo  concluded that 'inadequate airflow is an important causative factor in nasal and sinus infection'.
Few and sometimes contradictory studies on the effect of nasal airflow on nasal mucosa are present for now. For instance, a recent systematic review attempted to determine whether nasal airflow is essential for a healthy nasal epithelium, and concluded that there is no convincing evidence that a reduction in nasal airflow (complete or partial) is a causative factor for rhinitis and sinusitis . The aim of this study was to evaluate the changes in the nasal mucosa of tracheostomized patients as a result of decreased nasal airflow.
| Patients and Methods|| |
Patients were enrolled in this observational cohort study during the period from December 2014 to September 2016 at the Department of Otolaryngology – Head and Neck Surgery and Intensive Care Unit, Menoufia University Hospital, after approval of the ethical committee of the hospital. Written consent was taken from all patients and they were informed with the results of the study.
Patients who underwent total laryngectomy or tracheostomy (e.g., for prolonged endotracheal intubation) with age over 15 years were included in the study. Patients with previous nasal operation, previous atrophic nasal disease such as rhinoscleroma, autoimmune diseases, exposure to previous head and neck radiotherapy, temporary preoperative tracheostomy, or significant anatomical or pathological variations were excluded from the study. The study included 31 patients [five patients who underwent total laryngectomy and 26 patients who underwent tracheostomy (e.g., for prolonged endotracheal intubation)].
All patients were evaluated with a preliminary nasal examination at the onset of tracheostomy to rule out patients with exclusion criteria and to provide baseline data as regards the condition of nasal cavity and nasal mucosa. The patients were revaluated at 2 and 6 months after tracheostomy to assess the changes in the nasal mucosa as a result of decreased nasal airflow. Endoscopic nasal examination included color of nasal mucosa, nasal discharge, and nasal crustations. Color of the nasal mucosa was described as pink or pale (which indicates nasal atrophy). According to the Lund–Kennedy grading system, nasal discharge was graded as thin or thick and nasal crustations were graded as absent, mild, or severe.
For assessment of the mucociliary clearance of the nasal mucosa, the methylene blue and saccharine tests were used on the day of tracheostomy and at 2 and 6 months after tracheostomy to assess the possible changes in mucociliary activity.
Methylene blue test
A volume of 0.5 ml of methylene blue dye was instilled into the antrum of the nose taking care not to soil the nasal mucosa. We waited 10–15 min and then we looked endoscopically for movement of the dye along the nasal mucosa toward the nasopharynx. We deduced the following three conclusions from this test: normal movement of the dye indicated by movement of the dye as blue streaks along the walls of the nasal cavity toward the nasopharynx in patients with a normally functioning nasal mucosa. Delayed movement of the dye: the movement could be observed within minutes of instilling the dye as a few pockets but not quite reaching the nasopharynx, in patients with defective mucociliary clearance. No movement of the dye: no movement of the dye at all could be seen in patients with no mucociliary clearance.
A particle of sodium saccharine measuring 1 mm across was placed on the surface of the inferior nasal concha, 1 cm behind its head to avoid the area of squamous epithelium. The patients were seated with their head tipped slightly forward, without sneezing or blowing their nose, and without taking any substances that might interfere with the test. The patients were told to indicate when they noted any particular taste. The time elapsed was recorded to the nearest minute and the test was considered complete (normal: 6–36 min). If the participant did not detect any taste after 60 min, a saccharine particle would be placed on the tongue to ensure that he or she did not suffer any taste abnormalities. The most patent nostril with least resistance to physiological airflow was chosen.
For assessment of the histopathological changes in the nasal mucosa, tissue biopsies were taken during endoscopic examination at onset of tracheostomy to provide baseline description of nasal mucosa. Follow-up biopsies at 2 and 6 months after tracheostomy were performed to assess histopathological changes.
Samples were taken from the anterior end of the inferior turbinate and the nasal septal mucosa. The biopsy was performed under local anesthesia (pantocaine 5% and adrenaline 1/1000) using a nasal forceps (Blakesley-Wilde nasal forceps, 45° upturned).
Preparation of tissue block
All tissue specimens were fixed in 10% neutral-buffered formalin and sent to the Pathology Department, Faculty of Medicine, Menoufia University. The specimens were subjected to routine tissue processing, followed by sectioning of paraffin-embedded blocks for hematoxylin and eosin staining. Routine histopathological assessment was carried out for the following parameters with the pathologist blinded to the onset of sampling: epithelium as normal or atrophic, mucous-secreting glands as few or increased, and inflammatory infiltrate as mild or dense.
Data were collected, tabulated, and statistically analyzed using an IBM personal computer with statistical package of the social science (SPSS, version 20, SPSS Inc., Chicago, Illinois, USA) and Epi Info 2000 programs. Descriptive statistics included quantitative data presented as mean and SD and qualitative data presented as numbers and percentages. McNemar's test is a statistical test used on paired qualitative nominal data. It is applied to 2 × 2 contingency tables. For comparing the same group on different times the paired t-test was used for parametric quantitative variables. The χ2 was used to study the association between two qualitative variables. A P value of less than or equal to 0.05 was considered statistically significant.
| Results|| |
The current study included 31 patients (five with total laryngectomy and 26 with tracheostomy). Among the cases, there were 25 male and six female patients with their ages ranging from 23 to 72 years with a median of 47 years.
On endoscopic examination, we found that nasal discharge significantly changed from thin to thick at 2 months after tracheostomy (P = 0.008) and significantly changed from thick to thin at 6 months postoperatively (P = 0.02) [Figure 1] and [Table 1]). For nasal crustations there was a decrease at 2 months postoperatively showing no significance (P = 0.73), whereas at 6 months postoperatively there was a significant increase when compared with that observed preoperatively (P = 0.01) [Table 2]). The color of the nasal mucosa became more pink 2 months after tracheostomy with no significance (P = 0.07), but at 6 months it became more pale with significance than that preoperatively (P = 0.002) [Figure 2] and [Table 3]).
|Figure 1: Endoscopic view of the left nasal cavity of a patient with total laryngectomy 6 months after operation showing thin nasal discharge.|
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|Figure 2: Endoscopic view of the right nasal cavity of a patient with tracheostomy 6 months after operation showing pale nasal mucosa.|
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On mucociliary assessment, there was a significant shortening of the saccharine time and increase in methylene blue movement toward the nasopharynx 2 months postoperatively (P = 0.01 and 0.02, respectively) [Figure 3]. However, there was a significant delay in the saccharine times and decrease in methylene blue movement at 6 months when compared with that observed preoperatively (P = 0.00 and 0.013, respectively) [Table 4] and [Table 5].
|Figure 3: Endoscopic view of the left nasal cavity of a patient with total laryngectomy 2 months after operation showing methylene blue test: (a) Application of a drop of methylene blue at the anterior end of inferior turbinate, (b) The methylene blue dye reaching the nasopharynx.|
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On histopathological examination, there was no change in the epithelium of the nasal mucosa 2 months after tracheostomy, whereas there was highly significant atrophy 6 months after tracheostomy when compared with that observed preoperatively (P = 0.00) [Figure 4] and [Table 6].
|Figure 4: Section of nasal mucosal biopsy taken two months postoperative showing proliferating submucosal mucous secreting glands with dense fibrosis ( H and E, x40).|
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There was a highly significant increase in the number of mucous-secreting glands 2 months after tracheostomy (P = 0.00) [Figure 5], whereas there was a decrease in the number of mucous-secreting glands 6 months after tracheostomy when compared with that observed preoperatively, showing no significance (P1 = 0.18) [Table 7].
|Figure 5: Section of nasal mucosal biopsy taken 6 months postoperative showing destructed nasal epithelium with focal atrophy ( H and E, x100).|
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There was a significant increase in the number of the inflammatory cells 2 months after tracheostomy (P = 0.016) [Figure 6] and more significant increase 6 months after tracheostomy (P2 = 0.008) when compared with that observed preoperatively [Table 8].
|Figure 6: Section of nasal mucosal biopsy taken two months postoperative showing dense infiltration of subepithelium with lymphocytes together with fibrosis (H and E, x100).|
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| Discussion|| |
The laryngectomy patient provides a convenient model for the study of total airflow deprivation in man and has been the patients of several studies ,. In patients undergoing total laryngectomy, the nasal cavity is excluded from the respiration. Thus, the nasal cavity loses its physiological function. Generally, the structural changes are usually reflected by functional changes and vice versa.
In the current study, there was a significant shortening of the saccharine time and increase in methylene blue movement toward the nasopharynx at 2 months postoperatively. These findings match the finding of Maurizi et al. , who found that the mean value of saccharine test decreased at 2 months after total laryngectomy reaching statistical significance. They attributed the increase in the value of saccharine test to the increase in the mucociliary activity, which results from an increase in the endonasal temperature  and humidity , the mucous modifications arising in the absence of evaporation of the watery component , the disappearance of the nasal cycle , and the reduction in the endonasal blood flow . Other reports showed that laryngectomy patients have faster clearance with less variability  and that they have no slow clearance as judged by the saccharin test . In addition, Sakakura et al.  reported such increase in the speed of clearance in the early months following laryngectomy.
However, our findings are contradictory to the finding of Fisher et al. , who found that the saccharin times were not significantly different in the laryngectomy and control groups. However, they found that the ciliary beat frequency values were raised in the postoperative laryngectomy group compared with the control group. Moreover, Quinlan et al. , using a radioactive tracer, found that the mean transport rates were similar in laryngectomy cases and controls.
Fisher et al.  attributed their findings to the variability of the transition zone at the anterior end of the inferior turbinate. This makes the placement of the saccharin particle crucial, as too anterior placement will result in values that simply reflect structural changes in the anterior turbinate epithelium (which are known to change radically after airflow change, rather than any overall change in transport rate). Thus, their posterior placement circumvented this problem.
In the current study, there was a significant delay in the saccharine times and a decrease in methylene blue movement at 6 months when compared with that observed preoperatively. These findings match the finding of Maurizi et al. , who found that at later stages there was impairment of nasal mucociliary function, which could be attributed to secondary infections due to saprophytic bacteria. The consequent inflammatory process tends to become chronic and to cause marked epithelial alterations, which affect the mucociliary interaction, [19,.
In the current study there was more hyperemia of the nasal mucosa but showing no statistical significance at 2 months when compared with that observed that preoperatively (P = 0.07). This finding matched the finding of Ozgursoy and Dursun  who found that at the end of first month postoperatively. The endoscopic examinations of the nasal cavities revealed that 28 of the 42 (66.7%) patients had hyperemic nasal mucosa. However, there was a significant change in the color of the nasal mucosa to pallor at 6 months when compared with that observed at 2 months and reaching high significance when compared with that observed preoperatively. This change matches the finding of Ozgursoy and Dursun, who found thatthe endoscopic examination demonstrated pale and grayish nasal mucosa in all patients after total laryngectomy. Moreover, Ozgursoy and Dursun reported thatduring long-term follow-up, the overall change in the color of the nasal mucosa was mild –from pink to a pale purple.
In the current study we found that nasal discharge changed from thin to thick significantly at 2 months postoperatively. This finding matches the finding of Sesterhenn et al. , whoreported an increased nasal discharge that is not related to common colds and acute or chronic sinusitis . The reason for the increased mucous production in laryngectomized patients could be the increase in goblet cells, which starts in the second week after the laryngectomy . In addition, Deniz et al. reported a hypersecretory phase in an early periodafter the laryngectomy. However, someauthors reported decreased mucus productionduring the first 12 postoperative months . Our finding was confirmed by our histopathological finding of increased number of mucous-secreting glands at 2 months postoperatively reaching high statistical significance.
However, our study showed a significant decrease in nasal discharge at 6 months when compared with that observed at 2 months and reaching high significance when compared with that observed preoperatively. This corresponds to the decreased number of mucous-secreting glands 6 months postoperatively by histopathological examination. This finding matches the findings of Karaca et al. , who found that goblet cell destruction and stromal fibrosis were the most common findings (81%), followed by focal epithelial atrophy and subepithelial seromusinous gland destruction (45%) when studying late histologic changes after total laryngectomy. They reported that these findings increase with increasing interval between total laryngectomy and examination from less than 12 months in one group to more than 36 months in another group.
In the current study, histopathological examination revealed that epithelial atrophy affected 51.6% of patients (16/31) at 6 months postoperatively, reaching high statistical significance (P = 0.00) when compared with that observed preoperatively and 2 months postoperatively (P = 0.00). Our finding matches the findings of Ozgursoy and Dursun , who studied the effect of nasal airflow deprivation on nasal dimensions after total laryngectomy using endoscopic nasal examinations and answered questionnaires preoperatively and postoperatively. Acoustic rhinometry at both 1-year and 2-year follow-ups showed the dimensions of the nasal cavity appear to be significantly and permanently reduced 1 year after total laryngectomy.
Karaca et al.  found that atrophy in cilindric epithelium (focal or total), destruction of goblet cells, subepithelial glands and cilia, fibrosis of stroma, neovascularization, congestion, and myxoid degeneration of the stroma were detected. The most frequently observed findings were goblet cell and stroma destruction (81%), whereas focal atrophy affected 45% of patients.
In our study we found that the number of inflammatory cells was increased, reaching statistical significance at 2 months postoperatively, and it continued to increase at 6 months postoperatively when compared with that observed preoperatively. This finding was against the finding of Skoloudik et al., who found that the inflammatory changes in nasal mucosa were found rarely in patients after total laryngectomy. This difference can be attributed to the different follow-up periods being 3 years in their study compared with 6 months in our study. Mild signs of inflammation (grade 1) were found in only three (10%) patients. Marked inflammatory changes (grade 2) were absent.
The limitations of our study include the lack of age-matched and sex-matched control group to increase the significance of our findings. In addition, longer follow-up periods may be more helpful in future studies to confirm our findings. In addition, all methods used in our study are subjective to further need for future objective measures for assessment such as electron microscopy, measurement of the transport of markers placed on the mucosa such as 99m Tc-labeled particles – rhinoscintigraphy,99m Tc-labeled resin particle.
| Conclusion|| |
In our study we found that there was an increase in the number of mucous glands with their secretion along with an increase in mucociliary clearance of the nose early after tracheostomy or total laryngectomy. However, with time the reverse occurs due to long-term effect of airflow deprivation on the nasal mucosa with increased incidence of nasal mucosal atrophy as shown by histopathological examination.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Tsikoudas A, Barnes ML, White P. The impact of tracheostomy on the nose. Eur Arch Otorhinolaryngol 2011; 268
Tos M, Mogensen C. Experimental surgery on the nose. Changes of the epithelium in the vestibular region at altered airflow. Acta Otolaryngol 1979; 87
Cvetnic V, Batistic B, Sankovic F. Cytological and histological alterations in the nasal mucous membrane during experimental obstruction of nasal openings. Rhinology 1987; 25
Shin SH, Heo WW. Effects of unilateral naris closure on the nasal & maxillary sinus mucosa in the rabbit. Auris Nasus Larynx 2006; 32
Boyce J, Eccles R. Do chronic changes in nasal airflow have any physiological effect on the nose and paranasal sinuses? A systematic review. Clin Otolaryngol 2006; 31
Fisher EW, Lund VJ, Rutman A. The human nasal mucosa after deprivation of air flow. A study of laryngectomy patients. Rhinology l992; 30
Cveinic V, Skrlin J, Rak I. Bacterial flora of the nasal cavity in laryngectomized patients. Infection 1996; 24
Maurizi M, Paludetti G, Almadori G, Ottaviani, F, Todisco T. Mucociliary clearance and mucosal surface characteristics before and after total laryngectomy. Acta Otolaryngol 1986; 102
Blot F, Similowski T, Trouillet JL, Chardon P, Korach JM, Costa MA, et al.
Early tracheotomy versus prolonged endotracheal intubation in unselected severely ill ICU patients. Intensive Care Med 2008; 34
Ciaglia P, Firsching R, Syniec C. Elective percutaneous dilatational tracheostomy. A new simple bedside procedure; preliminary report. Chest 1985; 87
Grundling M, Uhn SO, Nees J, Westphal K, Pavlovic D, Wendt M, Feyerherd F. Percu. Twist-dilatations tracheostomy prospective evaluation an 54 patients. Anaesthesist 2004; 53
Byhahn C, Wilke HJ, Halbig S, Lischke V, Westphal K. Percutaneous tracheostomy: ciaglia blue rhino versus the basic ciaglia technique of percutaneous dilational tracheostomy. Anesth Analg 2000; 91
Marelli D, Paul A, Manolidis S, Walsh G, Odim JN, Burdon TA, et al
. Endoscopic guided percutaneous tracheostomy: early results of a consecutive trial. J Trauma 1990; 30
Moore-Gillon V. The nose after laryngectomy. J R Soc Med 1985; 78
Proctor DF. The upper airways. Am Rev Resp Dis 1977; 97
Sakakura Y, Ukai K, Majima Y, Murai S, Harada T, Miyoshi Y. Nasal mucociliary clearance under various conditions. Acta Otolaryngol 1983; 96
Quinlan MF, Salman SD, Swift DL, Wagner HN, Proctor DF. Measurement of mucociliary function in man. Am Rev Resp Dis 1969; 99
Jaeger JM, Littlewood KA, Durbin CG. The role of tracheostomy in weaning from mechanical ventilation. Respir Care 2002; 47
Wong DT, Pradhu AJ, Coloma M, Imasogie N, Chung FF. What is the minimum training required for successful cricothyroidotomy? Anesthesiology 2003; 98
Yuannan I, Klinhorm K, Boonpoon S, Madee W, Thongsai S. The development of clinical practice guideline for patients on tracheostomy tube. IATED. InINTED 2010 Proceedings; 2010. p. 5650-5.
Ozgursoy OB, Dursun G. Influence of long-term airflow deprivation on the dimensions of the nasal cavity: a study of laryngectomy patients using acoustic rhinometry. Ear Nose Throat J 2007; 86
Sesterhenn AM, Fielder G, Muller HH, Wiegand S, Folz BJ, Werner JA. Incidence of sinunasal disease in laryngectomized patients. ORL 2008; 70
American Society of Anesthesiologists Task Force on Difficult Airway management. Practice guidelines for management of the difficult airway. Anesthesiology 2003; 98
Hellin Mesequer D, Merino Gálvez E, Garcia Ortega F, Rosique Arias M. The mucociliary function and the morphology of the nasal mucous membrane in laryngectomees compared with normal subjects. An Otorrinolaringol Ibero Am 1996; 23:
Deniz M, Uslu C, Ogredik EA, Akduman D, Gursan SQ. Nasal mucociliary clearance in total laryngectomized patients. Eur Arch Otorhinolaryngol 2006; 263:
Holmes G. The history of laryngology from the earliest times until to the present. translated from German. Berlin: Hirschwald; 1887. p. 21.
Karaca CT, Gültekin E, Yelken MK, Iğdem AA, Külekçi M. Long-term histologic changes in nasal mucosa after total laryngectomy. Int J Otolaryngol 2010; 2010
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]