{"paper_id":"125569e3-5901-4f4d-923e-e311991145d9","body_text":"Mast cells (MCs) are immune cells of the myeloid lineage, present in connective tissues, which mature under the influence of the c-kit ligand and stem cell factor in the presence of other growth factors. Regulation of various physiological processes, including vascular homeostasis, innate and adaptive immune response, and angiogenesis, has been attributed to MCs. They have also been implicated in the pathophysiology of allergy, anaphylaxis, gastrointestinal disorders, and malignancies [ 1 ]. Notwithstanding mounting evidence of MC accumulation in tumors, their exact role in tumorigenesis and progression is poorly understood [ 2 ].\nThe human uterus is considered to be relatively rich in MCs compared to other tissues of the body. The greatest number was found in the inner (luminal) surface of the myometrium, while the endometrium contained significantly fewer MCs [ 3 ].\nUterine fibroids are among the most common benign tumors affecting women, originating from the uterine smooth muscle cells (myometrium). Although uterine leiomyomata are well recognized as hormone-dependent tumors, the contribution of immune and stromal components to their pathogenesis remains incompletely understood [ 4 ].\nSeveral studies have reported increased MC density in uterine leiomyomas compared to normal myometrium. However, the available literature shows differences in methodology, quantification techniques, and sample size. Furthermore, limited data exist regarding the association of MC density with age, tumor site, and degenerative changes within leiomyomas.\nGiven these inconsistencies and the gaps in existing evidence, the present study was undertaken to evaluate the distribution of MCs in uterine leiomyomas, compare their density with that of the adjacent myometrium, and assess their association with various clinicopathological parameters, including age, site, and degeneration.\n\nThis was a retrospective and observational study conducted from January 2019 to December 2021 in the Department of Pathology, Jawaharlal Nehru Medical College, Karnataka Lingayat Education (KLE) Academy of Higher Education and Research (KAHER), Belagavi. The study was approved by the Institutional Ethics Committee of Jawaharlal Nehru Medical College, Belagavi (Approval No: MDC/DOME/120). As this was a retrospective study on archived specimens, informed consent was waived.\nAll consecutive hysterectomy specimens diagnosed with uterine leiomyoma during the study period (January 2019 to December 2021) were retrieved from the departmental archives. From the eligible cases, 100 cases were selected using a computer-generated random number sequence to minimize selection bias. These tissue blocks formed the source of data. Excluded from the study were patients on hormonal therapy, including oral contraceptive pills, and those with adenomyosis.\nFrom each case, one representative formalin-fixed paraffin-embedded tissue block containing both leiomyoma and adjacent grossly normal myometrium was selected. The adjacent myometrium was defined as non-tumorous myometrial tissue located at least 5 mm from the tumor margin to avoid peritumoral reactive changes. Two sections, each 4 µm thick, were taken from the leiomyoma and its adjacent myometrium, processed routinely, and stained with hematoxylin and eosin and 1% toluidine blue.\nMCs can be stained with hematoxylin and eosin, toluidine blue, Giemsa, MC tryptase, chymase, and CD117, although studies have revealed that the best results were obtained with CD117 and toluidine blue [ 5 ]. However, there exists no standardization for counting them.\nMC counting\nMC quantification was performed using a hotspot method, similar to approaches used in tumor angiogenesis studies, using a Labomed LX 300 microscope (Labomed, Inc., Los Angeles, CA). Each toluidine blue-stained slide was initially scanned at low magnification (10× eyepiece and 10× objective, total magnification 100×) to identify areas with the highest MC density. From each slide, three non-overlapping hotspot areas were selected. MCs were then counted at high-power magnification with a 40× objective and a 10× eyepiece (total magnification 400×) in 10 consecutive high-power fields (HPFs) within each hotspot, and the mean value was recorded. The high-power field diameter was 0.45 mm, corresponding to a field area of 0.159 mm². All slides were evaluated under identical optical settings to maintain consistency.\nDegenerative changes were assessed on hematoxylin- and eosin-stained sections, and MCs were counted on toluidine blue sections. Hyaline degeneration was defined as the presence of homogeneous, eosinophilic, acellular material replacing smooth muscle bundles without evidence of necrosis or a significant inflammatory infiltrate. No other types of degeneration (cystic, red, or calcific) were identified in the present study. The number of MCs/10 HPF in leiomyomas with degeneration was recorded.\nAll slides were evaluated by a single pathologist to avoid interobserver variability.\nStatistical analysis\nData were entered into Microsoft Excel 2013 (Microsoft Corporation, Redmond, WA, USA) and analyzed using IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Version 17. Armonk, NY: IBM Corp. Continuous variables were expressed as mean ± standard deviation (SD), and categorical variables were presented as frequencies and percentages. Data distribution was assessed for normality prior to the application of parametric tests.\nThe mean MC counts per 10 HPF were compared across age groups and sites of leiomyoma using one-way analysis of variance (ANOVA). Post-hoc analysis was performed where applicable.\nComparison of MC counts between leiomyoma and adjacent myometrium was performed using a paired Student’s t-test, as the samples were derived from the same specimen. The association between MC density categories and age groups was analyzed using the chi-square test. Karl Pearson’s correlation coefficient was used to assess the relationship between MC counts in leiomyoma and adjacent myometrium. A p-value of < 0.05 was considered statistically significant at a 95% confidence level. Fisher’s exact test was used to study the association between leiomyoma with degeneration and MC counts.\n\nA total of 100 hysterectomy specimens with uterine leiomyoma were analyzed. The cases were evaluated with respect to age distribution, site of origin, MC counts in leiomyomas, and comparison with adjacent myometrium. Hematoxylin- and eosin-stained slides of leiomyomas without degeneration showed well-circumscribed neoplasms arranged in interlacing fascicles of spindle cells with a moderate amount of eosinophilic cytoplasm and cigar-shaped nuclei (Figure  1 ).\nSections of leiomyomas with hyaline degeneration showed interlacing fascicles of spindle cells separated by homogenous, eosinophilic collagenous material. No necrosis, cellular atypia, or mitosis was noted (Figure  2 ).\nMicroscopic examination of toluidine blue-stained slides revealed MCs, which were round-to-oval cells with inconspicuous nuclei and coarse, violet metachromatic cytoplasmic granules (Figure  3 ).\nHotspot areas, i.e., areas where maximum MCs were seen, were identified under low-power magnification and then were counted under high power (400× magnification) for 10 consecutive fields in each slide. This was labeled as \"MC counts/10 HPF\" (Figures  4 ,  5 ).\nAge distribution\nUterine leiomyomas showed a perimenopausal predominance, with 49% of cases occurring in the 40-50-year age group. The mean age of patients was 45.94 ± 6 years; 18% of cases were in the reproductive age group (<40 years), while 33% were postmenopausal (>50 years) (Table  1 ).\nSite distribution\nThe bulk of leiomyomas in this study, i.e., 59%, were found to be intramural in location, while submucosal leiomyomas constituted the smallest volume of cases (15%) (Table  2 ).\nMC counts in the adjacent myometrium\nThe mean MC count per 10 HPF in adjacent myometrium was highest in the reproductive age group (17.59 ± 9.02), followed by the perimenopausal group (14.94 ± 6.39) and lowest in the postmenopausal group (14.06 ± 5.66). This difference across age groups was modest but statistically significant (ANOVA, p = 0.0458, F-value = 3.193), with higher MC counts noted in the younger age group (Table  3 ).\nANOVA: analysis of variance test applied; MC: mast cells; HPF: high-power field\nMC counts in leiomyoma across age groups\nThe mean MC count per 10 HPF in leiomyomas was 40.76 ± 23.14 in the reproductive age group, 30.88 ± 12.26 in the perimenopausal group, and 28.62 ± 9.68 in the postmenopausal group. The difference was statistically highly significant (ANOVA, p = 0.0005, F-value = 8.166), indicating a significant inverse relationship between MC count and advancing age (Table  4 ).\nMC: mast cells; ANOVA: analysis of variance (ANOVA) test applied\nMC counts were categorized as <20, 20-40, and >40 for chi-square analysis. Chi-square analysis also demonstrated a significant association between MC count categories and age groups (chi-square = 9.789, p = 0.0442) (Table  5 ).\nChi-square test applied\nMC: mast cells; HPF: high-power field\nMC counts according to the site of leiomyoma\nThe mean MC count per 10 HPF was highest in intramural leiomyomas (45.76), followed by subserosal (34.88) and submucosal (28.62) leiomyomas. This difference was statistically significant (ANOVA, p = 0.0054, F-value = 5.505) (Table  6 ).\nMC/10 HPF: mast cells per 10 high-power fields; ANOVA: analysis of variance test applied\nComparison between leiomyoma and adjacent myometrium\nThe distribution pattern showed a rightward shift in MC counts in leiomyoma compared with the adjacent myometrium. While the majority of myometrial samples (65%) exhibited fewer than 20 MC per 10 HPF, nearly one-third of leiomyomas demonstrated counts exceeding 40 per 10 HPF.\nA paired Student's t-test demonstrated that MC counts were significantly higher in leiomyomas compared to adjacent myometrium (t = 18.65, p < 0.001). A strong positive correlation was observed between MC counts in leiomyoma and adjacent myometrium (Pearson’s correlation coefficient, r = 0.886, p < 0.001) (Table  7 ).\nMC counts in leiomyoma with and without degeneration\nOf the 100 cases, 10 showed hyaline degeneration; 80% of leiomyomas with degeneration had fewer than 20 MCs/10 HPF, while none of the leiomyomas without degeneration fell into this lowest category.\nFisher's exact test performed on this data showed a statistically significant association between degeneration and lower MC counts (p < 0.001) (Table  8 ).\nFisher's exact test applied\nMC: mast cells; HPF: high-power field\n\nThere is scarce literature regarding the distribution and potential relationship between MC and various conditions of the myometrium, with several authors disagreeing with the conclusions. The human uterus is considered relatively rich in MCs compared to other tissues of the body. The present study was undertaken to evaluate the distribution of MCs in uterine leiomyomas, to compare their density with that of the adjacent myometrium, and to analyze their association with clinicopathological parameters.\nMCs were stained with toluidine blue, a metachromatic stain, which provided good contrast and stained the granules bright purple-pink. However, there exists no standardization regarding the selection of hotspot areas for MC counting. Therefore, the slides were all evaluated by a single pathologist to avoid interobserver variability.\nIn our study, uterine leiomyomas showed a perimenopausal age predominance, with 49% of the cases in the ages between 40 and 50 years, the mean age being 45.94 years. These findings were concurrent with those of Ulin et al. [ 6 ], Delamater and Santoro [ 7 ], and Wise and Laughlin-Tommaso [ 8 ], who reported that uterine fibroids peak in the perimenopausal years and decline following menopause. Studies done by Casini et al. [ 9 ], Pritts et al. [ 10 ], and Gousuddin et al. [ 11 ] reported intramural to be the most common site of origin of uterine leiomyomas, which was consistent with the findings of this study, in which 59% of the cases were intramural in origin.\nThere exists no consensus regarding the minimum number of MCs that should be present in uterine leiomyomas or the adjacent myometrium, with different authors proposing varied ranges. In the myometrium, mean MC counts/10 HPF were found to be the highest in the reproductive age group (17.59/10 HPF) and the lowest in the postmenopausal age group (14.06/10 HPF). A similar finding was emphasized by Mori et al. [ 3 ] and Drudy et al. [ 12 ], who found that the lowest number of MCs was seen after menopause.\nAn inverse correlation was found between the MC count per 10 HPF in leiomyomas and increasing age in the present study. The greatest MC count of 88 cells/10 HPF in leiomyoma was found in the reproductive age group. These findings were similar to those of Maluf and Gersell [ 13 ] and Orii et al. [ 14 ], who observed a decreasing trend in the mean number of MCs with advancing age in leiomyomas.\nThe distribution of MC in leiomyoma according to site of origin was studied, and the maximum number was found in the intramural leiomyoma. This was synchronous with the findings of Gousuddin et al. [ 11 ], who concluded that intramural leiomyoma showed the highest MC count.\nOur study revealed an approximate twofold increase in the distribution of MC in uterine leiomyoma in comparison with the adjacent myometrium, which was statistically significant. In 65% of the cases, the myometrium had fewer than 20 MC/10 HPF. These observations were consistent with those of multiple authors, including Maluf and Gersell [ 13 ], who reported that MC counts were consistently higher in leiomyomas than in the myometrium, with ratios ranging from 3:1 to 12:1.\nDespite the presence of various degenerations in uterine leiomyomas, only hyaline degeneration was observed in our study. Of the 100 cases of leiomyomas, only 10 had degeneration, and 80% of leiomyomas with degeneration showed a much lower MC count (<20 cells/10 HPF) as compared to a majority (67.78%) of leiomyomas without degeneration, which revealed average MC counts in the range of 20-40 cells/10 HPF. These findings were in conformity with those of Abeyratne NVA et al., who reported that MC counts were low in leiomyomas with hyaline degeneration [ 5 ].\nThis study has several important strengths. First, the paired tissue comparison design, in which leiomyoma tissue was compared with adjacent myometrium from the same specimen, is methodologically robust. This approach minimizes inter-patient biological variability, including hormonal influences and systemic confounders, thereby strengthening internal validity. Second, the sample size of 100 cases (despite the constraints posed by COVID-19) is substantial for a single-center histopathological study and enhances the statistical reliability of subgroup analyses. Third, multiple complementary statistical methods were employed, including paired t-tests, ANOVA, Fisher’s exact test, and Pearson correlation analysis. This comprehensive analytical approach allowed for rigorous evaluation of both continuous and categorical associations, thereby improving the robustness of the findings.\nNevertheless, certain limitations must be acknowledged. As a retrospective observational study, the design is inherently subject to selection bias and limited control over potential confounding variables. MC quantification was performed using hotspot-based assessment, which, although commonly utilized in histopathological studies, may introduce focal sampling bias and affect reproducibility. Furthermore, slide evaluation was conducted by a single observer without formal assessment of intraobserver or interobserver reliability, which may introduce observational bias. Blinding to clinical and histopathological variables was not performed, potentially influencing the assessment. The number of leiomyomas with degeneration was relatively small (n = 10), limiting the generalizability of conclusions regarding degenerative changes. As this was a cross-sectional observational study, the findings demonstrate associations rather than causation. Finally, as this was a single-center study conducted on a defined regional population, the generalizability of findings to other demographic groups may be limited.\n\nThe present study showed a significant increase in MC counts in uterine leiomyoma compared with the adjacent myometrium, with higher counts observed in reproductive-age patients and in leiomyomata without degeneration. MC counts were observed to be higher in intramural leiomyomata. A significant inverse association of leiomyoma with advancing age was also demonstrated. The reduced MC counts observed in leiomyoma with degeneration suggest that MC density varies with tumor characteristics.\nThe findings in this study highlight a probable relationship between MC counts and the stromal microenvironment of uterine leiomyomata. However, being an observational study, the results reflect associations rather than a direct causal relationship. Further mechanistic studies may be done to elucidate the functional significance of MC in leiomyoma pathogenesis.","source_license":"CC-BY-4.0","license_restricted":false}