RHINOLOGY European Archives of Oto-Rhino-Laryngology https://doi.org/10.1007/s00405-024-09077-y bilaterally in the ventral part of the frontal lobe in the cerebral hemispheres. Known as the primary center of the olfactory center, the OB serves as a station for transmitting olfactory impulses to the cortex [1]. Introduction The axons of the olfactory nerve, called olfactory fila, pass through small holes in the cribriform plate of the ethmoidal bone to form the olfactory bulb (OB). The OB is located Hilal Irmak Sapmaz hisapmaz@yahoo.com Sefa Sonmez sefa.sonmez@gop.edu.tr Merve Nur Ozgen mervenur.ozgen@gop.edu.tr Sadik Bugrahan Simsek sadik.simsek@gop.edu.tr Ahmet Depreli ahmetdep@gmail.com Elif Kaya Celik elifkayacelikdr@gmail.com 1 Department of Anatomy, Faculty of Medicine, Tokat Gaziosmanpasa University, Tokat, Turkey 2 Tokat Forensic Medicine Branch Directorate, Forensic Medicine Institute, Tokat, Turkey 3 Department of Otolaryngology Head and Neck Surgery, Faculty of Medicine, Tokat Gaziosmanpasa University, Tokat, Turkey Abstract Purpose The pathophysiology of COVID-19 remains unclear. Olfactory dysfunction is one of the neurological symptoms of the disease. There is no evidence to evaluate whether there is a morphometric change in the olfactory pathways. This study aimed to examine the effect of COVID-19 on olfactory center sections through morphometric measurements obtained from autopsy cases. Methods Our study was conducted on 63 autopsy cases (COVID-19 [ n = 37], control (non-COVID) [ n = 26]) between the ages of 18–80 years who came to Tokat Forensic Medicine Institute. The anatomical structures of the olfactory tracts were determined on the brains removed during routine autopsy. The dimensions of the structures belonging to the olfactory center sections were measured with a precision digital caliper, weights were measured with a precision digital scale, and volumes were measured with a 0.01 cm³ graduated cylinder. The Archimedes principle method was used for volume calculations. Results In the autopsy cases examined, it was found that there was a significant decrease in bilateral olfactory bulb (OB) and olfactory tract (OT) volumes in COVID-19 group ( p < 0.001). In addition, OB and OT weights were lighter in COVID- 19 group on both sides ( p < 0.001). The length, width and depth measurements of the examined anatomical structures were found to be shorter in COVID-19 group ( p < 0.01). Conclusion Autopsy findings showed damage in olfactory center sections in COVID-19 group. We believe that knowing the OB and OT morphology in particular will make significant contributions to both clinical approaches and future studies in the pathology of infectious diseases. Keywords Autopsy · Anosmia · Infectious diseases · Olfactory bulb · Olfactory tract Received: 13 September 2024 / Accepted: 6 November 2024 © The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2024 Changes in olfactory bulb volume and olfactory sulcus depth in COVID-19 infection: an autopsy study Sefa Sonmez 1 · Merve Nur Ozgen 1 · Sadik Bugrahan Simsek 1 · Ahmet Depreli 2 · Elif Kaya Celik 3 · Hilal Irmak Sapmaz 1 1 3 European Archives of Oto-Rhino-Laryngology The SARS-CoV-2 virus reaches the central nervous sys- tem (CNS) through sensory neurons in the mucosa of the olfactory region. It can spread to many parts of the brain by following neuroanatomical pathways. Therefore, complete loss or reduction of the sense of smell indicates that the virus directly affects the olfactory center [ 2–4]. There are radiological studies in which olfactory center sections are evaluated morphometrically in individuals with olfactory dysfunction. It has been reported that individuals diagnosed with COVID-19 have structural abnormalities in the OB, which is a part of the olfactory center, and OBs are smaller in volume [5–7]. In the literature, structural changes in the olfactory center sections associated with COVID-19 were mainly analyzed through magnetic resonance (MR) imaging [8–11]. To our knowledge, no autopsy study that has made morphometric measurements in olfactory center sections related to COVID-19. Therefore, it is a matter of curiosity whether there are structural changes in olfactory center due to atrophy in the central nervous system in indi- viduals who have had COVID-19. In this study, the rela- tionship between COVID-19 and structural changes in OB, olfactory tract (OT), olfactory sulcus (OS), and anterior commissure (AC) in forensic autopsy cases was examined. Methods Study population In this study, 138 cases autopsied in Tokat Forensic Medi- cine Branch Directorate between September 2023 and June 2024 were examined. As a result of this examination, the cerebral hemispheres of 63 cases between the ages of 18–80 that met our study criteria were obtained. These cases were examined in two groups based on their history of COVID- 19 infection. The COVID-19 group consisted of 37 cases (24 males, 13 females), and the control group consisted of 26 cases (22 males, 4 females). Exclusion criteria In our study, individuals who developed signs of decay had a history of intracranial surgery, had brain anatomy dis- torted as a result of trauma, were diagnosed with a disease that could affect brain morphology, had smell/taste disor - ders before the pandemic, could not obtain information about COVID-19 history, and were under the age of 18 were excluded. Study procedure After routine autopsy, the basal surface of the frontal lobe was examined in the removed brains (Fig. 1). Morphometric measurements of the OB and OT were made without remov- ing the arachnoid mater (Fig. 2). Then, using microsurgical dissection instruments, the arachnoid mater was cut from the front of the optic chiasma to the frontal pole. OB + OT were dissected for weight and volume measurements. For AC measurement, the brain was dissected from the median line, and the two hemispheres were separated and made suitable for measurement. Measurement procedure The length, width, and depth of the structures were measured with a Valkyrie brand digital stainless steel caliper with an accuracy of 0.01 mm, OB + OT weight was measured with a Swock brand balance with an accuracy of 0.001 g (Fig. 2), and volume was measured using a graduated cylinder with an accuracy of 0.01 cm³ (Fig. 3). The brain weight was cal- culated with a digital scale with a sensitivity of 2 g. The Archimedes principle (the structure to be measured was placed in a graduated cylindrical water-filled container, and the amount of water it displaced) was used for volume calcu- lations. In addition, AC measurements were performed from the medial surface of the cerebral hemisphere as shown in Fig. 1. Details of the parameters and landmarks used for the measurements in our study are given in Table 1. All mea- surements were performed carefully and in accordance with standardized procedures. Our study did not affect routine classical autopsy procedures in any way. Patient record reports of autopsy cases After all measurements were completed, the medical history reports of the patients were evaluated retrospectively. In the medical history reports of the patients, the symptom of acute loss of smell was documented in line with the anamnesis taken when they applied to the health institution with typical COVID-19 symptoms. Patients with anosmia were included in the study. In these patients, the diagnosis of COVID-19 was confirmed by polymerase chain reaction (PCR) testing with nasopharyngeal swabs or the presence of typical inter- stitial pneumonia on radiologic examinations. PCR tests were performed while individuals were alive and during the disease. In the COVID-19 group, the interval between the positive PCR test date and the autopsy date was 235–1005 (min-max) days. In addition, there were no hospital records of Otorhinolaryngology or any other specialty related to the complaint of loss of smell, except for the first admission due to COVID-19 while the autopsied cases were alive. None of 1 3 European Archives of Oto-Rhino-Laryngology the cases included in the study died due to COVID-19 and its complications. Statistical analysis Data analysis was conducted using IBM SPSS V25. Descriptive statistics (mean ± standard deviation) were cal- culated for the measurement. The suitability of the variables for normal distribution was evaluated with Shapiro-Wilk and Kolmogorov-Smirnov tests. COVID-19 and control group measurement parameters were found to be normally distributed. An independent two-sample t-test was used to compare the parametric data between the groups. The strength of the relationship between the age of the individu- als in the COVID-19 and control groups and the parameters of the olfactory center was evaluated with the Pearson cor- relation coefficient. In addition, the strength of the relation - ship between the onset of the disease and the date of autopsy for the COVID-19 group was also analyzed with the Pear- son correlation coefficient. A p-value of < 0.05 in all tests was considered statistically significant. Fig. 2 A Olfactory tract width, B Olfactory bulb width, C Olfactory bulb length, D Olfactory bulb + olfactory tract weight Fig. 1 A View of the olfactory bulb + olfactory tract on the basal surface of the cerebral hemispheres, B Width measurement of the anterior com - missure from the medial surface of the cerebral hemisphere 1 3 European Archives of Oto-Rhino-Laryngology ( p = 0.825). In addition, there was no significant correlation between the age of the individuals in the COVID-19 and control groups and the length, width, depth, weight, and vol- ume parameters of the structures belonging to the olfactory center ( p > 0.05). It was determined that all measured parameters were sig- nificantly lower in COVID-19 group compared to control group ( p < 0.01). Morphometric data regarding the olfactory tracts are given in Table 2, and weight and volume measure- ment values are given in Table 3. In COVID-19 group, the average period between the pos- itive PCR test date and autopsy date was 23.4 ± 7 months. No relationship existed between the time elapsed after Results In our study, the age of 24 male individuals who were COVID-19 group was 52.38 ± 16.29 years, and the age of 13 female individuals was 44.31 ± 17.82 years. There was no significant difference between the sexes regarding mean age ( p = 0.189). The average age of 22 male individuals in the control group is 50.91 ± 19.32 years, and the average age of 4 female individuals is 48.5 ± 18.69 years. There was no sig- nificant difference between genders regarding average age Table 1 Parameters and landmarks used for morphometric measure- ments Parameter Landmarks OB Length (OBL) Distance between the front edge of the OB and the OT OB Width (OBW) The widest place OT Length (OTL) The distance between the beginning of OT and OTr OT Width (OTW) Width of the middle section OB + OTr Length (OB + OTrL) Distance between the front edge of the OB and the back edge of the OTr OS Depth (OSD) Depth of the middle section OS Length (OSL) Antero-posterior length of the OS AC Length (ACL) Long axis of the AC AC Width (ACW) Short axis of the AC OB Olfactory bulb, OT Olfactory tract, OTr Olfactory trigone, OB + OTr Olfactory bulb + olfactory trigone, OS Olfactory sulcus, AC Anterior commissure Table 2 Comparison of morphometric data of rhinencephalon accord- ing to groups Parameters (mm) Side COVID-19 Group ( n = 37) Control Group ( n = 26) p OB Lenght Right 7.81 ± 1.68 14.36 ± 1.29 < 0.001* Left 8.27 ± 1.77 14.26 ± 1.37 < 0.001* OB Width Right 4.14 ± 1.25 5.01 ± 0.86 0.002* Left 4.06 ± 1.21 4.81 ± 0.7 0.003* OT Lenght Right 19.79 ± 4.83 26.84 ± 4.99 < 0.001* Left 20.5 ± 5.28 27.26 ± 4.61 < 0.001* OT Width Right 3.04 ± 0.77 3.81 ± 0.96 0.001* Left 3.04 ± 0.72 3.82 ± 1.09 0.003* OB + OTr Lenght Right 34.84 ± 4.53 47.16 ± 4.14 < 0.001* Left 35.46 ± 4.67 46.3 ± 4.06 < 0.001* OS Depth Right 11.71 ± 2.02 14.43 ± 2.36 < 0.001* Left 11.79 ± 2.28 13.95 ± 2.28 < 0.001* OS Lenght Right 34.84 ± 4.53 47.16 ± 4.14 < 0.001* Left 35.46 ± 4.67 46.3 ± 4.06 < 0.001* AC Lenght 4.49 ± 1.12 5.53 ± 0.91 < 0.001* AC Width 3.47 ± 0.87 4.49 ± 1.15 < 0.001* Mean ± Standart deviation, Independent samples t-test, OB Olfac- tory bulb, OT Olfactory tract, OB + OTr Olfactory bulb + olfactory trigone, OS Olfactory sulcus, AC Anterior commissure, * p < 0.05 Table 3 Comparison of weight and volume data of rhinencephalon sections and encephalon between groups Side COVID-19 Group ( n = 37) Control Group ( n = 26) p OB + OT Weight (g) Right 0.118 ± 0.032 0.159 ± 0.014 < 0.001* Left 0.117 ± 0.032 0.158 ± 0.017 < 0.001* OB + OT Volume (cm 3 ) Right 0.106 ± 0.033 0.146 ± 0.021 < 0.001* Left 0.102 ± 0.027 0.148 ± 0.026 < 0.001* Brain Weight (g) 1132.9 ± 59.5 1139.0 ± 50.0 0.672 Brain Volume (cm 3 ) 1081.1 ± 56.2 1078.9 ± 45.2 0.866 Mean ± Standart deviation, Independent samples t-test, OB Olfactory bulb, OT Olfactory tract, * p < 0.05 Fig. 3 Schematic view olfactory bulb + olfactory tract volume measurement 1 3 European Archives of Oto-Rhino-Laryngology group, with no significant difference on the left side. They also found no significant difference between the groups when they compared total brain volumes [25]. Our study found no difference between the total brain volumes; how - ever, the OB volume on both sides was lower in COVID-19 group. In the limited number of cross-sectional studies to date, it has been suggested that the morphometric and volumetric structure of the OB may change over time due to COVID- 19 infection and that these changes may even be permanent. The duration of olfactory dysfunction following infection has also been reported to be highly variable [12, 26]. In our study, the atrophy caused by COVID-19 in the OB and OT can be explained by the loss of regeneration abilities of the axons in the mucosa of the structures that form the olfactory tract. In addition, the decrease in OS depth and AC diam- eter, which are associated with the olfactory tract, suggests that the infection was also influential in these regions. It has been reported that OS depth decreases with viral infections, which is related to the degeneration and regen- eration abilities of cells in the OB [23]. Our study observed a decrease in OS depth in COVID-19 group. Therefore, the demonstration of structural and functional damages in the olfactory epithelium with quantitative data suggests that the depth of OS may be related to COVID-19 infection. OS depth and OB volume are important clinical measures in the assessment of olfactory dysfunction. It is known that age-related degenerative changes affect OB and OS mor - phology and lead to a decrease in OB volume and OS depth in the general population [14]. However, in our study, no sig- nificant correlation was found between age and these mea - surements in the COVID-19 and control groups. There is no consensus in the literature on normal values for measure- ments made in the normal population. It has been reported in various studies that these values may vary depending on age [27, 28]. Our study suggests that the morphological changes observed in the COVID-19 group may be attributed to the direct effects of infection rather than age-related degenera - tion, which is consistent with previous studies showing that COVID-19 has a more pronounced effect on olfactory struc - tures compared to age-related changes [18]. A precious aspect of our study is the direct measurement of the effects of COVID-19 on the olfactory center sec - tions, as well as the length, width, depth, weight, and vol- ume parameters of anatomical structures, through the study population created with forensic autopsy cases, through the brain sections removed during autopsy. The human brain volume and structures vary significantly in size. We are nor - malizing OB and OT volumes to brain volume, allowing for more accurate results when considering changes in physi- cal appearance. In this context, making measurements in COVID-19 diagnosis and the morphometry of the measured structures ( r < 0.4, p > 0.05). Discussion COVID-19 affects olfactory function [ 5, 12]. In the litera- ture, studies show changes in the anatomical structures that form the olfactory pathways in COVID-19 [5, 13, 14]. In our study, bilateral atrophy was observed in the OB, OT, and AC in the olfactory center sections of autopsy cases diagnosed with COVID-19 in their lives, compared to cases without a COVID-19 diagnosis. Our findings were consis - tent with the literature. In many studies in the literature, MR images have been used to evaluate olfactory center Sects. [13, 15, 16]. Because the OB is a minimal structure, the boundary between the OB and the cerebrospinal fluid is not clear in MRI images. Additionally, it needs to be clearly stated whether OT was included in the measurements. OS depth and OB volume measurement data obtained from radiological images are inconsistent with our results [17–20]. In our study, we think our results are superior because direct morphometric mea- surements of the anatomical structures of the olfactory tract in forensic autopsy cases were performed. Wang et al. in their study on 15 adult cadavers fixed with formalin, they reported that the median value of the OB length was 11.1 mm (9.0–14.5), and its width was 4.6 mm (2.8–5.4). The median value of OT length was measured as 28.2 mm (22.5–34.0) [21]. Cömert et al. their study of 40 adult cadavers found the average OB length to be 13.22 ± 3.14 mm and width to be 4.87 ± 1.83 mm. The mean OT length and width were 25.53 ± 7.11 mm and 2.87 ± 2.64 mm, respectively [22]. The morphometric mea- surements made in these studies did not separate the sides. These data are similar to our results, although Wang and Cömert’s findings were slightly lower than our findings. We think that this difference may be due to the cadavers being fixed with formalin. Altundag et al. in their study, it was reported that there was no significant difference between the OB volumes of 24 cases of anosmia due to SARS-CoV-2 and 38 individu- als with olfactory disorders due to postviral infections other than SARS-CoV-2 [23]. It is reported in the literature that there is a decrease in OB volumes due to damage to olfac- tory receptor cells in anosmia due to postviral infections [24]. In our study, it was found that there was a decrease in OB + OT volumes in COVID-19 group. These results are similar to the literature. Perlaki et al. when they compared the bilateral OB vol- umes of the COVID-19 and control groups, they reported a decrease in the right-side OB volume in the COVID-19 1 3 European Archives of Oto-Rhino-Laryngology Financial disclosures None. Competing interests The authors declare that they have no conflict of interest. References 1. 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A secondary limitation was that olfactory dysfunction tests were not performed. Therefore, it was not possible to examine the relationship between OB, OT, and AC atrophy and olfactory dysfunction severity. Conclusion In this study, the olfactory center and brain sections of autopsy cases confirmed by clinical tests to have been diagnosed with COVID-19 in their lives and cases with- out a history of COVID-19 in their lives were compared. Structural and volumetric decreases were found in those who had the disease. It is thought that differences between studies may result from measurement methods or variability in the people performing the measurements. We think that the measurement values of this study are original, provide a different perspective to the literature, and shed light on future studies. In addition, we believe that knowing the mor- phometry of the anatomical structures of the olfactory tract will contribute to the diagnostic and surgical approaches of clinicians. Author contributions Conceptualization: Sefa Sonmez, Merve Nur Ozgen, Sadik Bugrahan Simsek; Methodology: Sefa Sonmez, Merve Nur Ozgen; Formal analysis and investigation: Sefa Sonmez, Sadik Bugrahan Simsek; Writing - original draft preparation: Sefa Sonmez, Merve Nur Ozgen, Sadik Bugrahan Simsek, Elif Kaya Celik, Hilal Ir- mak Sapmaz; Writing - review and editing: Sefa Sonmez, Merve Nur Ozgen, Sadik Bugrahan Simsek, Elif Kaya Celik, Hilal Irmak Sapmaz, Ahmet Depreli; Analysis - interpretation of data: Sefa Sonmez, Sa - dik Bugrahan Simsek, Ahmet Depreli; Major role in the acquisition of data: Ahmet Depreli, Sefa Sonmez, Sadik Bugrahan Simsek, Merve Nur Ozgen. All authors contributed to the study conception and design. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. 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