Current Reviews

Atrophic Rhinitis

Mostafa A. Shehata, MD

Atrophic rhinitis is a chronic nasal disease characterized by progressive atrophy of the mucosa and underlying bone of the turbinates and the presence of a viscid secretion, which rapidly dries and forms crusts that emit a characteristic foul odor, sometimes called ozena (a stench). There is usually an abnormal patency of the nasal passages.1-3 HISTORY This disease was known to ancient Egyptians, nearly 4,000 years ago as evidenced in their medical papyri. The Edwin papyrus (1700 BC) prescribed date wine and breast milk for the treatment of this disease. The ancient Greeks and Indians were also familiar with atrophic rhinitis. The disease was first described as a separate clinical entity of the nose by Fraenkel in 1876.4 INCIDENCE The disease appears to be endemic in subtropical and temperate countries, hence its prevalence in South Asia, Africa, Eastern Europe, and the Mediterranean. It is also found in Egypt, Greece, Hungary, and Yugoslavia,4 as well as in Brazil, Malaysia, the Philippines, and India.5 Heredity is an important factor, and there appears to be a racial influence in that the Asians, Latinos, and black Americans are more susceptible than natives of equatorial Africa.l In affected areas, the general incidence is
From the Department of Otolaryngology, Faculty of Medicine, Alexandria University, Alexandria, Egypt. Address reprint requests to Mostafa Shehata, ENT Department, Faculty of Medicine, Alexandria, Egypt. Copyright 0 1996 by W.B. Saunders Company 0196-0709/96/l 702-0001$5.00/0 American Journal of Otolaryngology,

0.3% to 7.8% of the ear, nose and throat outpatients in China,6 whereas it is about 1% in Egypt.7 There is also a strong family history among patients, who are usually poor and live in unhygienic conditions.7 The disease usually starts in childhood, especially in girls at the onset of puberty. This supports the hormonal theory that estrogen has an etiological role in atrophic rhinitis. ETIOLOGY The exact etiology is still uncertain, however, many possibilities and suggestions have been described by investigators. 1. Chronic bacterial infection of the nose or the sinuses has been suggested by Grunwald,8 Adam,g Cullom,g Surgan,g Rosen et a1,g Henriksen and Gundersen,O and Zohar et a1.3 In this respect, many organisms have been cited as the cause, including: Coccobacillus,l Bacillus mucosus,12 Coccobacillus foetidus ozaena, Diphtheroid bacilli, Bacillus pertussis,j and Klebsiella ozaena?O Although it is true that these organisms may be found in cultures, there is little evidence that they cause the disease.13 2. Nutritional deficiencies,3 such as iron deficiency14 and Vitamin A deficiency.gJ5 3. Endocrine imbalance, mainly estrogen deficiency, evidenced by the common occurrence of the disease in girls at the onset of puberty and the aggravation of symptoms during menstruation and the improvement of some cases by estrogen therapy.3,gs15 4. Developmental disorder resulting in poor pneumatization of antra and wide nose.3,7 5. Autonomic imbalance resulting in excessive vasoconstriction was suggested by Ruskin in 1932 (overly sympathetic activity).
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6. Collagen disorder as an auto-immune disease was suggested by Ricci.g 7. Hereditary disorder, as a racial Mandelian hereditary inhibition of development of nasal mucosa, is a theory suggested by Fleishman.7 8. Chronic exposure to irritant and toxic agents such as cocaine and others, which is supported by the report from Mickiewicz et all6 in which atrophic rhinitis was found in workers exposed to phosphorite and apatide dusts. Other possible causes are chronic sinusitis; excessive surgical destruction of the nasal mucous membranel; healed chronic granulomata, such as scleroma, leprosy, syphilis, and lupus vulgaris; narcotic inhalations; repeated cautery to nasal mucosa; and radiotherapy. It seems likely that atrophic rhinitis results from a number of separate factors working simultaneously.

PATHOLOGY The initial examination shows chronic nonspecific inflammation with accumulation of chronic inflammatory cells, such as lymphocytes and plasma cells. Nasal exfoliation is characteristic with nearly absence of columnar and goblet cells. Ciliary destruction is common and crusts are formed on the nasal mucosa.4 There is excessive reduction in the size and amount of the mucosal and submucosal structures (Fig 1).

Most investigators agree that there are patches of metaplasia from columnar ciliated to squamous epithelium, that there is a decrease in the number and size of the compound alveolar glands, and that there are dilated capillaries and active bone absorption.*J Some investigators such as Taylor and Young,15 were unable to show end-arteritis and peri-arteritis of the terminal arterioles, which were described by other investigators. Therefore, it is possible that there are two types of atrophic rhinitis: Type 1 is characterized by endarteritis and periarteritis of the terminal arterioles, which are the result of chronic infection and might benefit from the vasodilator effect of estrogen therapy and, Type 2 shows vasodilatation of the capillaries, which might be made worse with estrogen therapy. The result of either type is a scanty, thick mucous discharge, forming colored crusts that may harden into large casts obstructing the nose.? CLINICAL PICTURE

The disease usually manifests itself in childhood, especially in girls. The onset may begin at puberty, and the symptoms worsen during menstruation. The presenting symptoms are most commonly nasal obstruction, headache, and epistaxis. Anosmia and halitosis may be present,

Fig 1. Atrophic mucosa, subepithelial fibrosis, chronic inflammatory cells, and edema of the lamina propria (original magnification x 120).

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and patients are often only made aware of the presence of these symptoms by the reluctance of others to come within their vicinity. Sometimes the symptoms are mainly pharyngeal and are caused by the pharyngitis sicca that often accompanies the condition or by the choking which occurs when detached crusts slip from the nasopharynx to the oropharynx.l The cruel social rejection, beginning early in childhood, that is experienced by those with ozena, together with sleep disturbances caused by nasal obstruction, often result in marked psychotic behavior.4 Examination confirms the presence of fetor oris in all but in the earliest cases. The nasal cavities are found to be lined with green, yellow, and black crusts. Detachment of crusts shows a bleeding and ulcerated mucosa. The nasopharynx can be clearly seen through the wide nasal cavities. Atrophy of the inferior turbinate, and occasionally the middle turbinate, is frequent and may be complete (Fig 2).*

INVESTIGATIONS The following investigations are necessary to study the cases: 1. Nasal swab to be cultured and identified, but the results are usually of little value 2. Sinus puncture is required to exclude concomitant sinus infection 3. Radiography of the sinuses to exclude the presence of sepsis 4. Computed tomography has been recently used for imaging of atrophic rhinitis17 5. Serological tests to exclude syphilis 6. Blood picture, serum proteins, and iron levels should also be checked1 TREATMENT There is no cure for atrophic rhinitis; all medical and surgical measures have short or prolonged palliative effect. Conservative Measures

Fig 2. Radiograph frontal view, showing atrophy of the inferior

of the nose and sinuses, occipitowide, roomy nose with marked and middle turbinates.

Regular nasal cleaning was performed by syringing the nasal cavities with a solution of diluted sodium bicarbonate (250 mL warm water in which was dissolved 25 g sodium bicarbonate, 25 g sodium biborate, and 50 g sodium chloride).l* Balanced physiological saline was also tried with good symptomatic relief.lg Application of nasal cotton wool tampons, soaked in 25% glucose in glycerine for 24 hours, inhibit the proteolytic organisms and loosens dry, adherent crusts. The use of lubricating oily nasal drops as menthol 2% in paraffin is also helpfuLl Estrogen therapy, used systematically and locally, has been suggested by some investigators with relief of symptoms. Vitamin A, administered orally in large doses of 12,500 to 15,000 U daily was claimed to give the best results, especially in mild and moderately severe cases.6 Potassium iodide taken orally helped to increase nasal secretion to moisten the mucosa.7 Autogenous vaccines were tried by some investigators with very limited therapeutic effect. Antibacterial vaccines, made of formalin-

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killed whole cells of toxigenic Pasteurella multocida and Bordetella bronchiseptica, were also tried with some immunoprotective improvement.20-22 Sinha et al5 reported promising results by the use of local and general tissue therapy in the form of human placenta extract. They claim 80% improvement for two years. Antibiotics were preferred by many investigators, especially streptomycin injections that act on proteolytic organisms. Specific antibiotics, according to antibiotic susceptibility of the organisms, were also tried.2 Vasodilators and corticosteroids were also suggested and have some palliation effect1 Acetylcholine, used locally, and pilocarpine, injected subcutaneously, were mentioned by Ballenge9 to be of some value for their vasodilatation and reactivation of mucosa glands. Chen Han Sen6 advised the use of large doses of vitamin A, combined with streptomycin injection. He claimed good results after such therapy. Surgical Treatment

Many surgical techniques were described in the past and many others are presently used with variable therapeutic results. None of them were fully successful or cured the disease. Cavity-narrowing operations. These operations include: 1. the displacement of the lateral wall of the nose medially to narrow the nasal cavity (Lautenschlagers operation, 1982),23 2. nasal closure operations, 3. pharyngoplasty, and 4. nasal implants. Encouraging results have been obtained following complete closure of one or both nostrils by plastic surgery,24 using a skin flap of the nasal vestibule. Closure is maintained for a period of 6 months to 3 years. This gives good curative result but recurrence rate is high.24 Sinha, Sardana, and Rajvanshi5 reported that partial closure of both nostrils is better tolerated by patients than complete closure with similar results. Bela1 et alz5 advocated closure of the posterior choana with rubber foam for 6 months and claimed good results. However, after removing the choanal plug, all symptoms recur.25 All types of nasal occlusion gave good amelioration results in which dryness of the

nasal mucosa disappears and formation of nasal crusts stops. Histologically, the nasal mucosa shows an increase in the number of goblet cells and tunica glands, and improvement in the microcirculation of the nasal mucosa. There is also a return of ciliated, pseudo-stratified columnar epithelium in many areas of the nasal mucosa.24 Ultrastructural study of nasal mucosa after the operations also showed reverse change in its microanatomy.26 However, the recurrence of the symptoms after nasal occlusion indicates that it is not the final treatment of ozena. Pharyngoplasty, with caudally based pharyngeal flap to reduce nasal airflow advocated by Huffstadt and Hoeksemaz7 and nasal implants are also treatment options. Autogenous tissue implants, such as fat, dermofat, bone, or cartilage, were all tried, but because of their gradual absorption, the symptoms recur.4,7J8-30Implanting placental tissue was also tried by Ramajaneyulu in 19765 with limited cure results. An osteoperiostal flap taken from the anterior wall of the maxilla to narrow the nasal cavity was thought to give better results.31 Synthetic implants, such as submucosal injection of paraffin oil, were first suggested and performed by Gersuny in 1990,28 who started the era of synthetic implants, but the results were unfavorable.28 Many other sorts of synthetic materials including acrylic, silicone, Teflon, polythene, and Silastic were later tried as implants under the mucoperichondrium of the septum, floor, or lateral wa11.5~32*33 In 1964, Wilson34 reported better results from the submucosal injection of a suspension of powdered Teflon in 50% glycerine paste. Proplast, a polytertra fluoroethylene carbon (Vitek, Inc, Houston, TX), was used by Whitehead for its advantage of enabling the tissue to grow through the implant to stabilize it in situ with minimal extrusion. Boplant, or processed cancellous calf bones (Squipp and Sons, Inc, New York] was used as small strips and implanted submucosally under the mucosa of septum, floor, and lateral wall. This was reported by Huizing36 to give more promising results. All types of implants give immediate successful results, but the cure rate decreases gradually because of the frequent gradual absorption of the tissue implant or the occasional extrusion of synthetic implants. The frequency of extru-

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sion was estimated by some investigators to be as high as 80%.37 Our own studies were performed to evaluate surgical synthetic implants in treatment of atrophic rhinitis. A research trial was performed in 1986 in which 30 patients of both sexes and of different age groups were treated surgically.38 The material used for implantation was Silastic, a polymer of dimethyl siloxane (Dow Corning Corp, Midland, MI). The implant was placed subperiosteally or subperichondrially under the mucosa of the septum or the nasal floor. The obtained curative results were very encouraging. After several years of follow-up, the success rate decreased slightly, but it remained higher than most of the previously mentioned surgical techniques.38 Denervation operations. A sympathectomy operation in the form of a cervical sympathectomy was performed by Bertein,3g whereas stellate ganglion block has been used with some success by Bahl,40 and Sharma and Sardana. Sphenopalatine ganglion block or extirpation was performed by Girgis7 with some success. Parasympathectomy, in which the great superficial petrosal nerve is cut, was described by Krmptotic and Sunoric41 who claimed it was also an effective method. Other operations. There are a number of other operations. Local injections of placental extract was described and used by Sinha et al5 with the some success. The salivary irrigation operation as advocated by Wittmaak in 191g7 entails the reimplantation of the parotid duct into the maxillary sinus. This has the advantage of continuous wetting of the nasal cavity but carries the disadvantage of watery rhinorrhea during food mastication.7 Rethi devised a modified surgical technique in which a septal flap is raised to act as a baffle to narrow the nasal cavity, with amelioration of the symptoms.42 Considering all these surgical techniques and their modifications that have evolved over the last 50 years, it becomes evident that atrophic rhinitis has attracted the interest of many investigators worldwide, but has proved very resistant to therapy as evidenced by the investigators disappointing long-term results. Although there are over 100 surgical techniques, none have proved to be

fully successful, and the disease still needs further study and research to discover a more effective curative method of treatment. PROGNOSIS The disease manifests itself in childhood, especially in girls at a very active stage in their lives. The long-standing symptom of halitosis is very annoying and deeply affects the psychological condition of such young patients. The cruel social rejection, beginning early in life, that is experienced by those with ozena, together with sleep disturbances caused by nasal obstruction and often result in marked psychotic behavior that may lead to suicide. Although the symptoms persist for many years, the disease does not affect the capability of the patient or endanger his life. All available lines of treatment are still symptomatic for palliation of the disease, and there is no known cure. Fortunately, after 40 years of age, a good percentage of patients show spontaneous arrest of the active disease, in which the discharge, crusts, and bad odor disappear, despite the wide nasal cavity. REFERENCES
1. Weir N: Acute and chronic inflammation of the nose, in Mackay IS, Bull TR (eds): Scott-Browns Otolaryngology, ~013, (ed 5). London, United Kingdom Butterworths, 1987, pp 115-141 2. Dudlev JP: Atrophic rhinitis, antibiotic treatment. Am J Otolaryngol8:38?-390, 1987 3. Zohar Y, Talmi YP. Strauss M, et al: Ozaena revisited. J Otolaryngol19:345-349,199O 4. Goodman WS, de Souza FM: Atrophic rhinitis. J Otolaryngol Clin North Am 6:773-782,1973 5. Sinha SM, Sardana DS, Rajvanshi VS: A nine year review of 273 cases of atrophic rhinitis and its management. J Laryngol Otol91:591-600,1977 6. Sen HC: The ozaena problem, clinical analysis of atrophic rhinitis in 100 cases. Acta Otolaryngol 93:461464,1982 7. Girgis IH: Surgical treatment of ozaena by dermofat graft. J Laryngol Otol80:615-627,1966 8. Ballenger JJ: Chronic atrophic rhinitis. Diseases of the Nose, Throat and Ear (ed 12). Philadelphia, PA, Lea & Febiger, 1977, pp 129-130 9. Barbary AS, Yassin A, Fouad H, et al: Histopathological and histochemical studies on atrophic rhinitis. J Laryngol Otol84:1103-1112,197O 10. Henricksen SD, Gundersen WB: The etiology of ozaena. APMIS 47:380,1959 11. Lewenberg B: La microbe de lozena. Ann Institut Pasteur 8:292, 1894 12. Ab el P: Die aetiologie der ozaena. Z Hygiene Infektionskrankeiten 21:89, 1885 13. Ferguson JL, MC Caffrey TV, Kern EB, et al: Effect of

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Klebsiella ozaenae on ciliary activity in vitro, implication in the pathogenesis of atrophic rhinitis. J Head Neck Surg 102:207-211,199O 14. Bernat I: Ozaena, a manifestation of iron deficiency. Oxford, United Kingdom, Pergamon, 1965 15. Taylor M, Young A: Histological and histochemical studies on atrophic rhinitis. J Laryngol Otol 75:574-589, 1961 16. Mickiewicz L, Mekluski T, Kuzna Grygrel W, et al: Assessment of the nasal mucosa in workers exposed to prolonged effect of phosphorite and apatite dusts. Pol J bccupMed Environ-Health 6:277-285, i993 17. Pace Balzam A. Shankar L. Hawke M: Comuuted tomographic findings in atrophic rhinitis. J Otolarngol 20:428-432,1991 18. Emkart 0: Rhinitis review. Rev Chil Pediatr 60:4853,1989 19. Nuutinen J, Holopainen E, Haahtela T, et al: Balanced physiological saline in the treatment of chronic rhinitis. J Rhinology 24:265-269,1986 20. Foged NT, Neilsen JP, Jorsal SE: Protection against progressive atrophic rhinitis by vaccination with Pasteurella multocida toxin, purified by monoclonal antibodies. Vet Ret 125:7-11, 1989 21. Nielsen JP, Foged NT, Sorensen V, et al: Vaccination against progressive atrophic rhinitis with a recombinant Pasteurella multocida toxin derivative. Can J Vet Res 55:128-138,1991 22. Kabay MJ, Mercy AR, Lloyd JM, et al: Vaccine efficacy for reducing turbinate atrophy and improving growth rate in piggeries with endemic atrophic rhinitis. Aust VetJ 69:1oi-i<3,1992 23. Lautenschlaaer A: Die rhinitis atroohicans. Handbuk der Hals, Nasen and Ohren, vol 2. Heilkunde, Germany 1952, p 604 24. Young A: Closure of the nostrils in atrophic rhinitis. J Laryngol Otol85:715-718,197l 25. Bela1 A, Talaat AM, Maher A, et al: Temporary chronic occlusion for the management of ozaena. Egyptian J Otolaryngol, 2:29-39, 1985

26. El-Wany S: Ultrastructural observations on primary atrophic rhinitis, effect of partial closure of the nostrils. ORL J Otorhinolaryngol Relat Spec 50:389-396,1988 27. Huffstadt AJC, Hoeksema PE: Pharyngoplasty in atrophic rhinitis. Br J Plast Surg 29:132-133, 1976 28. Cottle MH: Atrophic rhinitis, medical and surgical treatment. J Internatl Collegium Surg 29:472-484,1958 29. Ogura JH: Bone graft in atrophic rhinitis. Laryngoscope 64:20-28, 1954 30. Saunders WH: Atrophic rhinitis, results of surgical treatment. Arch Otolaryngol68:342-345,1958 31. Rasmy E: Osteoperiosteal flap in the treatment of ozaena, new technique. Ann Otol Rhino1 Laryngol95:645646,1986 32. Proud CP: Acrycic resin implant in atrophic rhinitis. Laryngoscope 57:256-262,1947 33. Berkstein A: The treatment of atrophic rhinitis with injectable silicone. J Laryngol Otol80:634,1960 34. Wilson TG: Teflon in glycerine paste in rhinology. J Laryngol Otol 78:953-957,1964 35. Whitehead E: Atrophic rhinitis, proplast implant in surgical treatment. Can J Otolaryngol4:505-507,1975 36. Husizing FH: Surgery of the lateral nasal wall in atrophic rhinitis and ozaena. J Rhinology 14:79-81,1976 37. Wilson WR, Montgomery WW: Atrophic rhinitis. in Paparella MM, Shumrick DA (eds): Otolaryngology, vol 3 (ed 21, Philadelphia, PA, Saunders, 1980, PP 1972-1983 38. Shehata M, Dogheim Y: Surgical treatment of primary atrophic rhinitis and evaluation of silastic implants. J Laryngol Otol 100:803-807,1986 39. Sharma AN, Sardana DS: Stellate ganglion block in atrophic rhinitis. J Laryngol Otol80:184-186,1966 40. Bahl CP: Stellate ganglion block. Br J Anaesth 33:592, 1961 41. Krmptotic J, Sunoric: The effect of section of the great superficial petrosel nerve in ozaena. Practical Otol Rhino1 Laryngol20:239-247,1964 42. Rethi A: Operative treatment of ozaena. J Laryngol Otol62:139-146, 1948