Methods of evaluation of smell in victims of subarachnoid hemorrhage patients: a systematic review

Sandro Júnior Henrique Lima Hildo Rocha Cirne de Azevedo Filho Hilton Justino da Silva About the authors

RESUMO

Objetivos:

Revisar de forma sistemática os métodos para avaliação do olfato em vítimas de hemorragia subaracnóidea aneurismática, e identificar as alterações encontradas com a utilização desses métodos.

Estratégia de pesquisa:

A pesquisa bibliográfica foi realizada na plataforma de busca PubMed e nas bases de dados Web of Science, Scopus, PsycINFO, CINAHL e ScienceDirect, tendo a busca de dados ocorrida em agosto e setembro de 2014.

Critérios de seleção:

Artigos originais publicados em qualquer língua que abordassem as alterações de olfato na hemorragia subaracnóidea aneurismática, com objetivo de avaliar essa função através de métodos específicos. Foram excluídos estudos de revisão; estudos de caso; capítulos de livro; editoriais e estudos que abordassem a hemorragia subaracnóidea não aneurismática.

Análise dos dados:

Foram consideradas como variáveis na análise dos dados: autor/ano, país, amostra/idade, tratamento, método utilizado, momento da avaliação do olfato e resultados.

Resultados:

A busca de artigos resultou em 1.763 artigos, desses, 9 artigos originais foram selecionados para esta revisão. Foi observado que todos os artigos foram desenvolvidos em países europeus e asiáticos e na avaliação do olfato utilizou-se desde testes padronizados e não padronizados a questionários, cujos objetivos variaram entre avaliar o olfato antes e/ou após o tratamento cirúrgico nessa população.

Conclusão:

Foi observada heterogeneidade nos métodos utilizados para avaliação do olfato na hemorragia subaracnóidea aneurismática, como também no momento selecionado para aplicação das avaliações. Além disso, os estudos evidenciaram a existência de déficit olfatório nos pacientes, e a relação entre o tratamento cirúrgico e a disfunção olfatória.

Descritores:
Olfato; Hemorragia Subaracnóidea; Aneurisma Intracraniano; Círculo Arterial do Cérebro.

ABSTRACT

Purpose:

To systematically review the methods for evaluation of smell in aneurysmal subarachnoid hemorrhage victims and to identify the changes found with the use of these methods.

Research strategy:

The literature search was performed in PubMed search platform and in the databases Web of Science, Scopus, PsycINFO, CINAHL, and ScienceDirect in August and September 2014.

Selection criteria:

Original articles published in any language, which addressed smell changes in aneurysmal subarachnoid hemorrhage and addressed to evaluate this function through specific methods were included. Review studies, case studies, book chapters, editorial, and studies that address the nonaneurysmal subarachnoid hemorrhage were excluded.

Data analysis:

The following variables were considered in data analysis: author/year, country, sample/age, treatment, method, the moment of smell evaluation, and results.

Results:

The search for articles resulted in 1,763 articles, of which, 9 original articles were selected for this review. It was observed that all articles were from European and Asian countries. Standardized and nonstandardized tests and questionnaires were used in olfactory assessment, and the goals ranged from assessing the smell before and/or after surgery in this population.

Conclusion:

Heterogeneity was observed in the methods used to evaluate the smell in aneurysmal subarachnoid hemorrhage and in the methods selected for application of evaluations. In addition, studies have demonstrated the existence of olfactory deficits in patients and the relationship between surgery and olfactory dysfunction.

Keywords:
Smell; Subarachnoid Hemorrhage; Intracranial Aneurysm; Circle of Willis.

INTRODUCTION

The aneurysmal subarachnoid hemorrhage (SAH) is characterized as the rupture and leakage of blood between the pia mater and arachnoid membrane11. Pulsinelli WA. Doenças vasculares cerebrais - princípios. In: Goldman L, Bennett JC. Cecil: tratado de medicina interna. Rio de Janeiro: Guanabara Koogan; 2001. p. 2352-9.. Its occurrence results in abrupt changes in the intracranial midst owing to associated factors, such as the presence of bruises, edema, cerebral vasospasm and hydrocephaly22. Clinchot DM, Kaplan P, Murray DM, Pease WS. Cerebral aneurysms and arteriovenous malformations: implications for rehabilitation. Arch Phys Med Rehabil. 1994;75(12):1342-51., which makes the aneurysmal SAH a clinical even of great importance.

It has a high mortality rate, reaching out to 40% of the affected population, in addition to frequent occurrence of sequelae among survivor patients, of which about one-third ends up having some kind of disorder of motor, cognitive, or even behavioral nature33. Burgos RE, Diaz RC. Hemorragia subaracnoidea espontanea: diagnostico y tratamiento. Univ Med. 2002;43(4):260-5. 44. Machado FS, Akamine N. Hemorragia subaracnóidea. In: Knobel E. Terapia intensiva: neurologia. São Paulo: Atheneu; 2002. p. 123-36. 55. Mocco J, Komotar RJ, Lavine SD, Meyers PM, Connolly S, Solomon R. The natural history of unruptured intracranial aneurysms. Neurosurg Focus. 2004;17(5):E3..

A change that may be triggered with the occurrence of blood leakage in the subarachnoid space is the olfactory dysfunction, possibly because of the anatomical closeness of the location of the hemorrhage to the olfactory system, being subject to factors associated to aneurysmal SAH, such as direct mechanical damage to the tissues, inflammatory processes, increased intracranial pressure, and local cortical ischemia66. Crowley RW, Medel R, Kassell NF, Dumont AS. New insights into the causes and therapy of cerebral vasospasm following subaracnoided hemorrhage. Drug Discov Today. 2008;13(5-6):254-60. 77. Griz MFL. Relação entre déficit da olfação e hemorragia subaracnoidea aneurismática antes e após tratamento [doutorado]. Recife: Universidade Federal de Pernambuco; 2014..

Besides that, owing to its characteristics, the surgical treatment for aneurysmal SAH may also influence the sense of smell; in this case, the alterations in this function may arise through the impact of the traction of brain tissues during exposure to the bleeding site77. Griz MFL. Relação entre déficit da olfação e hemorragia subaracnoidea aneurismática antes e após tratamento [doutorado]. Recife: Universidade Federal de Pernambuco; 2014..

Considering this, many methods to evaluate smell are described in the literature, and they may be either qualitative or even quantitative in the evaluation of the olfactory system88. Moura RGF, Cunha DA, Gomes ACLG, Silva HJ. Instrumentos quantitativos para avaliação do olfato na população infantil: artigo de revisão. CoDAS. 2014;26(1):96-101.. It is also described that, for the verification of the integrity of the system, the tests use means that evaluate the psychophysical, electrophysiological, and psychophysiological processes, related to the olfactory sense, and the analysis of image tests that define the situation of the structures connected to smell99. Doty RL. Olfaction in Parkinson's disease and related disorders. Neurobiol Dis. 2012;46(3):527-52..

However, there is little description of how the evaluation of smell is made in patients with aneurysmal SAH, and this knowledge is not only important in order to identify the characteristics of the olfactory alterations caused by this disease and its modifications by surgical treatment, but it can also help determine and disseminate the methods to be used in clinical practice for the evaluation of this function in neurological patients.

Thus, the objective of this study is to systematically review the methods for evaluation of smell in patients with aneurysmal SAH and to identify the alterations found with the use of such methods.

RESEARCH STRATEGY

The bibliographic research was carried out in the PubMed search platform and in Web of Science, Scopus, PsycINFO, CINAHL, and ScienceDirect databases, considering the data search happened in August and September 2014. In the research for articles, the following descriptors were used - Health Sciences descriptors (descritores em ciências da saúde [DeCS]) and medical subject headings (MESH) - for the recovery of subjects of scientific literature. The following crossings in English, Portuguese, and Spanish languages were made: smell AND circle of Willis; smell AND subarachnoid hemorrhage; smell AND intracranial aneurysm; olfaction disorders AND circle of Willis; olfaction disorders AND subarachnoid hemorrhage; and olfaction disorders AND intracranial aneurysm.

The research was carried out by two researchers, independently and blindly. In the cases where there were disagreements, the third researcher was consulted, with the objective of reaching a consensus. The researchers followed a search protocol developed before the research

SELECTION CRITERIA

The inclusion criteria for articles in the research were: articles originally published in any language, which would approach smell alterations in patients with aneurysmal SAH, with the objective of evaluating this function through specific tests.

Original articles with no reference in the title, in the abstract, or in the text with the subject addressed in this review, review studies, case studies, book chapters, editorials, and studies addressing the nonaneurysmal SAH were excluded.

DATA ANALYSIS

The data analysis followed a convergent selection method of three stages.

Initially, an identification of the articles was made from the crossing of descriptors, and then the first exclusion process was done from the reading of the titles, following the eligibility criteria.

Next, reading of the abstracts and subsequent exclusion of the articles that were unsuitable for the research was done. The remaining articles were fully read for the selection of studies for this review.

The methodological characteristics of the articles were analyzed according to the presence of randomization, inclusion and exclusion criteria, blinding, statistical analysis, and statistical comparison between groups in the selected studies. Such evaluation items were based on the Physiotherapy Evidence Database scale (PEDro) (Chart 1). It is described in the literature that this scale has moderate levels of reliability among evaluators, with a intraclass correlation coefficient (ICC) of 0.68 and confidence interval of 95% (95%CI) of 0.57-0.761010. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713-21..

Chart 1:
Methodological classification of the articles selected

The results were presented according to the following variables of the selected artciles: author/year, country, sample/age, treatment, method used (smell evaluation), moment of evaluation of smell, and results (Chart 2).

Chart 2:
Results of the studies selected following the anlyzed variables

RESULTS

The search for data resulted in a total of 1,763 articles. In the PubMed platform, crossing the descriptors, 30 articles were found; in Web of Science, 17 articles were found; in the Scopus base, 66 articles were found; in PsycINFO, 1 article was found; in CINAHL, 8 articles were found; and in the ScienceDirect database, 1,641 articles were found.

Considering the inclusion and exclusion criteria adopted and after the withdrawal of repreated studies, only nine articles were included and analyzed in this systematic review (Figure 1).

Figure 1:
Flowchart of the number of articles found and selected after the apllying of the inclusion and exclusion criteria

In a preliminary analysis of the articles, it was possible to identify a methodological heterogeneity, which made it impossible to use statistical treatment (meta-analysis). Nevertheless, relevant conclusions could be extracted through this study.

It was observed that, from the studies analyzed, a part of the method were not presented: random allocation, secrecy in the allocation, and blinding of the research subjects; besides that, only part of them, equivalent to 55.5%, revealed preestablished selection criteria1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9.. It was also observed that most of them (77.7%) used statistical analysis of the data1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1616. Hiroaki F, Nobuyuki Y, Edgar NV, Akifumi S. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric ans basal interhemispheric approaches. 1995;38(2):325-28. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8., and yet, owing to not being fully rigid as for the methodology used when developing the studies, there was difficulty in the use of integration statistical analysis of independent results.

On the basis of the period of publications, it was observed that few articles approached the theme in the 1990s1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3., with the first study in the year of 19901010. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713-21.. From the studies analyzed, 66.6%1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1616. Hiroaki F, Nobuyuki Y, Edgar NV, Akifumi S. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric ans basal interhemispheric approaches. 1995;38(2):325-28. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8.were published from the year of 2007 onward, reflecting a period of 11 years without research. It was noticeable that the three first articles produced1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3. investigated the alterations in smell after surgical intervention for the SAH and not ruptured aneurysms, showing greater concern with the repercussions in this function deriving from the microsurgery.

It is believed that such concerns was related to the evolution of surgical techniques, which initially happened in the 1960s to the 1970s with the description of pterional craniotomy2121. Yasargil MG, Fox JL, Ray MW. The operative approach to aneurysms of the anterior communicating artery. In: Krayenbül H, editor. Advances and technical standards in neurosurgery. 2nd ed. Wien: Springer-Verlag; 1975. p. 114-70.. Possibly, in this period, with the increase of surgeries directly involving the olfactory nerve, there were observed deficits in olfaction, which aroused interest from neurosurgeons.

Despite such evidence, it was observed that 77.7%1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3. of the studies selected were concerned about investigating the olfactory situation of patients after treatment, highlighting a much greater interest in the functional situation resulting from surgery.

According to the location of the studies, most of them were from European countries1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. and two from Asia1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8.. Besides that, Turkey, which is considered a Eurasian country, was the study site of one of the articles2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3..

Four European articles were from Netherlands1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8.: three of them1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8. were carried out in a school hospital in Utrecht, becoming one of the most concerned centers not only with the investigation of the association between smell and the surgical procedures used in the treatment of ruptured aneurysms but also with the repercussions resulting from this function by SAH itself, because it was in this center that the only studies evaluating the smell condition both pre and posttreatment were conducted1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9..

According to the results of the Global Burden of Disease, Injures and Risk Factors (GBD), countries with low and medium income showed, in 2010, more elevated rates of incidence and mortality connected to strokes, which included SAH2222. Krishnamurthi RV, Moran AE, Forouzanfar MH, Bennett DA, Mensah GA, Lawes CM, et al. The global burden of hemorrhagic stroke: a summary of findings from the GBD 2010 study. Glob Heart. 2014;9(1):101-6..

Despite showing that the concern with the disease seems to be higher in these developing countries, possibly owing to more balanced health conditions in high-income countries, in addition to greater research resources, they end up developing more studies in the area, as observed in the articles found.

Another relevant factor in this review is that there were no studies from America, highlighting a greater interest by European and Asian countries in the development of studies evaluating the alterations in smell caused by aneurysmal SAH.

Considering information on the sample and the age range of the patients, it was verified that there was a great variation between articles, with a minimum of 131515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. and maximum of 315 participants1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3.. In addition, a variation in age of inclusion of the studies of at least 18 years of age2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3. and a maximum of 91 years of age was observed1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3., showing heterogeneity in the conduction of the researches. It is believed that such variation is associated with the selection of the patients, motivated also by the demand for hospital admissions.

Another aspect pointing out to the definition of sampling of these studies is the incidence of aneurysmal SAH, which, though rare within the two first decades of life, it affects a broad age range, increasing the frequency up to 60 years of age2323. Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol. 1990;34(6):361-5..

It was also observed in the articles that the treatments used for aneurysmal SAH varied. These information show that the objectives set out in the studies were modified with the evolution of medical interventions, considering the period of publication, since that the first articles addressed the craniotomy1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. and the most recent ones are set out to analyze smell also in embolization1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8., which is a more recent technique2424. Conrad MD, Pelissou-Guyotat I, Morel C, Madarassy G, Schonauer C, Deruty R. Estudo comparativo entre aneurismas rotos tratados por cirurgia e por via endovascular. Arq Neuro-Psiquiatr. 2002;60(1):96-100..

In the evaluation of smell, from standardized and nonstandardized tests to subjective questionnaires and an association of both were used. From the articles, two of them evaluated the olfactory function through questionnaires filled out in person or by phone, along with the impact scales of alteration in quality of life1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8..

Despite being able to rise important information on the functional perception of the patient in relation to smell, the questionnaires used in these studies have a subjective nature and this characteristics is strengthened by the way they were applied. In addition to that, the translation of the results obtained in these instruments is made in a generic way, which makes it difficult to reproduce the findings.

However, the importance given to the quality of life, related to olfactory deficit, is a positive aspect of these studies, which highlights the effects caused by the functional decline of smell in this population.

Some articles used initial interviews in order to identify the patients with olfactory deficit, and later on, specific tests were performed1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8.. This strategy appears to be negative, in that it may mask out the more subtle changes in olfactory function and not be revealed in the interviews.

Other studies used as means of investigation of the olfactory function the Sniffin' Sticks Test (Korean version)1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32., University of Pennsylvania Smell Identification Test (UPSIT)1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62., Sniffin' Sticks Test (validated in Europe)1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6.,Sniffin' Sticks Test battery1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9., modified olfactometry (using saturated phenyl ethyl alcohol vapor)1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5., and use of vanilla extract1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. and butanol solutions2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3..

It was possible to verify that 55.5% of the studies used standardized olfactory tests1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5., in some cases with regional validation, revealing that the standardization of the method is a criterion, which reinforced the choice of the kind of test of smell in the researches carried out.

The most often used test was the Sniffin' Sticks Test1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9., which consists of a standardized battery for the evaluation of smell, using felt pens with different odors. It is noteworthy that the results of this test are subject to regional influences. Thus, two artciles used a regionally validated version of this test1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6., which suggests the higher accuracy in the results found in these studies.

In one of the articles analyzed, the UPSIT1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. was used, which is a widely accepted smell test and considered the most often used one, specially owing to its accuracy and practicality in the application2525. Doty RL, Shaman P, Dann M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav. 1984;32(3):489-502. 2626. Doy RL, Newhouse MG, Azzalina JD. Internal consistency and short-term test-retest reliability of the University of Pennsylvania Identification Smell Test. Chem Senses. 1985;10(3):297-300.. The UPSIT has four booklets, each containing ten microencapsulated olfactory stimuli, which are released when its surface is scratched. The marking of answers is made by four multiple choice alternatives, three of them represented by distractive odors and one alternative with the correct answer corresponding to the odor smelled.

Given the characteristics of this test, the answers may also experience the influence of the regions where it is carried out, which explains the several numbers of validations made for different countries. Nevertheless, in the study analyzed1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62., it was not informed whether or not there was adequacy in this sense.

On the basis of this, the increasing importance of regional adjustment to which the standardized tests should be submitted to in order to ensure the reliability of their results was observed, which was seen in only two studies in this review1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6..

The olfactometry was also described in one of the analyzed studies1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5., and owing to being able to provide qualitative results of olfaction, it appears as a relevant means, which needs greater investigation in order to better identify the effectiveness of its use in the evaluation of this function.

The moment of application of the smell evaluation varied considerably between articles, from 72 hours after hemorrhage1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. up to 7.5 years on average after the surgery1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3.. This period varied thus mainly because of the method used in the study, which had a marked heterogeneity. Two of the studies were retrospective in nature1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3., another one was a cross-sectional observation1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9., while three of them did not inform for sure the time of application of the evaluation1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8..

A percentage of 44.4% of the studies evaluated patients through a longitudinal model of investigation1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8., which may reflect the need to observe lasting olfactory alterations resulting from hemorrhage and surgical intervention.

This fact is owing to the recovery of the olfactory nerve after a lesion, which may occur even 5 years after the trauma. It is believed that permanent alterations are those that present after 35 months or more1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3..

In relation to the results of the studies, in all of them, subjects with some kind of deficit in smell after SAH or after surgical treatment were observed. In the studies in which the treatment used in the participants was the craniotomy, through different accesses, there was an association between the olfactory dysfunction with the side of operation and the anatomical manipulation of adjacent regions to the olfactory nerve, for access to the hemorrhage site1111. Park J, Lee SH, Kang DH, Kim JS. Olfactory dysfunction after ipsilateral and contralateral pterional approaches for cerebral aneurysms. Neurosurgery. 2009;65(4):727-32. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5. 1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3..

It was suggested by the authors that the emerging of smell alterations in microsurgery is related to mechanical lesions caused to the olfactory nerve, during tissue retraction for the exposure of the ruptured artery1919. Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A. Anosmia after anterior communicating artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery. 1996;38(2):325-8. 2020. Aydin IH, Kadioğlu HH, Tüzün Y, Kayaoğlu CR, Takçi E, Oztürk M. Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional approach. Minim Invasive Neurosurg. 1996;39(3):71-3.. It is also said that even the minimum pressure levels in the retraction of the frontal lobe may lead to temporary or permanent alterations in smell.

In the studies in which there were comparisons between the treatments by craniotomy and embolization, despite having been observed a greater incidence of olfactory alteration in patients treated by microsurgery, there was the presence of olfactory deficit even after endovascular embolization1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3., which was also seen in the study that aimed at evaluating this function only after embolization1717. Bor AS, Niemansburg SL, Wermer MJ, Rinkel GJ. Anosmia after coiling of ruptured aneurysms: prevalence, prognosis, and risk factors. Stroke. 2009;40(6):2226-8..

On the basis of that, authors comment the existence of other factors that may trigger smell alteration, in addition to the direct mechanical damage to the olfactory nerve during surgery. These would be: contact between the extravasated blood, during hemorrhage, and the nerve; increased intracranial pressure at the moment of rupture of the aneurysm; ischemia in the cortical regions involved with the processing of olfactory information; and the occurrence of cerebral vasospasm, which may compromise the blood flow of the structures related to smell1212. Martin GE, Junqué C, Juncadella M, Gabarrós A, de Miquel MA, Rubio F. Olfactory dysfunction after subarachnoid hemorrhage caused by ruptured aneurysms of the anterior communicating artery. Clinical article. J Neurosurg. 2009;111(5):958-62. 1414. Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ. Anosmia after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;61(5):918-22; discussion 922-3..

The results also demonstrate the difference in tracking olfactory alterations in face of subjective evaluations and tests, in which greater number of cases of alterations during the performing of the tests, whether or not standardized1313. Moman MR, Verweij BH, Buwalda J, Rinkel GJ. Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg. 2009;110(3):482-6. 1515. De Vries J, Menovsky T, Ingels K. Evaluation of olfactory nerve function after aneurysmal subarachnoid hemorrhage and clip occlusion. J Neurosurg. 2007;107(6):1126-9. 1818. Eriksen KD, Bøge-Rasmussen T, Kruse-Larsen C. Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg. 1990;72(6):864-5., was observed. This difference shows the importance of concern with the selection of method for the evaluation of the olfactory function, in which subjective alternatives must be used as a complement to the evaluation in order to avoid false-negative results.

Considering the results found in the studies analyzed, the need for researches that propose to evaluate the olfactory function both before and after surgical treatment of aneurysmal SAH was verified, in order to better clarify the influence of both the blood leakage and the surgical intervention in the onset of olfactory alterations. Besides, it is important to use resources of standardized investigation, so that the answers are safer and allow greater reproducibility of the findings.

CONCLUSION

From this review, it was possible to observe that, in the evaluation of smell in patients with SAH, the studies used from standardized and nonstandardized tests to subjective means for alteration tracking, bringing about possibly lower accuracy in the results obtained owing to methodological heterogeneity. Besides, the moment of evaluation varied considerably in the articles seen, which implies in difficulties in the comprehension of trigger factors for olfactory alterations found in this disease.

The studies showed evidence of deficit in the olfactory function of these patients and the relation between surgical treatment and the trigger for olfactory dysfunction. In spite of this, the results of the analyzed articles do not explain in detail the real damage of the hemorrhage and of surgical intervention in the genesis of the functional change.

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Publication Dates

  • Publication in this collection
    Feb 2016

History

  • Received
    26 Jan 2015
  • Accepted
    08 June 2015
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