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Magnetic resonance imaging characteristics predict pituitary function in non-functional pituitary macro-adenoma undergoing trans-sphenoidal surgery

Magnetic resonance imaging characteristics predict pituitary function in non-functional pituitary... Introduction: Maintaining the pituitary function after surgery is highly important. The aim of this study was to inves‑ tigate the relationship between preoperative magnetic resonance imaging (MRI) characteristics and pituitary function after surgery of non‑functional pituitary macroadenoma. Methods: This retrospective study was performed between 2016 and 2018. Preoperative and postoperative MRI imaging data were retrieved from electronic registration system. The relationship between preoperative MRI char‑ acteristics and postoperative pituitary function as well as reconstruction of pituitary gland was investigated using regression models. Results: Complete data were available for 44 patients. Before surgery, invisible normal tissue was observed in 23 patients (53.5%). Suprasellar extension and cavernous sinus invasion were seen in 36 patients (each one 49.1%). There was a significant reverse relationship between preoperative tumor size and postoperative thyroid stimulating hor ‑ mone ( TSH) (odds ratio (OR): − 0.99 (− 0.18, − 0.003), p = 0.04). In addition, we found a significant positive correlation between prolactin level after surgery and tumor size before surgery, (OR: 5.29 (1.65, 8.92), p = 0006). Moreover, post‑ operative panhypopituitarism was observed in 25% of patients with complete morphologic reconstitution of pituitary tissue. While the rate was 50% in patients with no or partial morphologic reconstruction of pituitary tissue. Conclusion: Preoperative MRI characteristics predict TSH and prolactin level after operation. Furthermore, the ade‑ noma size and volume prior to surgery are the main determinants of normal morphologic reconstruction of pituitary gland. Keywords: Pituitary gland function, Non‑functional pituitary macroadenoma, Surgery, Imaging features, Magnetic resonance imaging Introduction Non-functional pituitary macroadenomas (more than one centimeter in diameter) comprise about one-third *Correspondence: manizhe.ataei64@gmail.com of all pituitary adenomas and are managed with trans Behrooz Hassani and Nahid Hashemi‑Madani contributed equally to this sphenoidal surgery [1, 2]. Restoration of normal pitui- manuscript as co‑first authors. tary function after surgery is important and has been Department of Radiology, Firouzgar Clinical Research Development Center(FCRDC), Firouzgar General Hospital, Iran University of Medical reported in various studies from 20 to 50% [3, 4]. Pan- Sciences(IUMS), Valadi Street, Valiasr Sq., Tehran, Iran hypopituitarism, deficiency in production of at least two Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hassani et al. BMC Medical Imaging (2022) 22:60 Page 2 of 7 pituitary hormones, is a most common complication a history of radiotherapy as well as those with repeated after pituitary surgery [5]. Inadequate secretion of lute- pituitary surgery were excluded from the study. inizing hormone (LH) and follicle stimulating hormone (FSH), growth hormone (GH), thyroid stimulating hor- Data collection mone (TSH) and adrenocorticotropic hormone (ACTH) All demographic, clinical, and biochemical information were observed after pituitary surgery in 99%, 98.6%, 96% were extracted from the electronic record system at the and 81.8% of cases after pituitary surgery [6, 7]. Methods Institute of Endocrinology and Metabolism affiliated to for predicting the possible occurrence of these complica- Iran University of Medical Sciences. Hormone profile tions have also been studied. Various studies have shown before surgery and at the last follow-up visit were used in that some findings in magnetic resonance imaging (MRI) this analysis. are associated with post-operative complications. There - The pre-operative MRI scan as well as the first post- fore, identification of these findings in patients’ MRI can operative MRI scan obtained during 3 months after sur- be helpful in prediction and, possibly, prevention of the gery were also reviewed using the picture archiving and related complications [8, 9]. Researches evaluated the communication system (PACS). The required informa - post-operative MRI characteristics over one year after tion about size, volume, consistency and direction of trans sphenoidal surgery of the non-functional pitui- mass displacement were evaluated by two expert radiolo- tary macroadenomas. The results showed the residual of gists. Size was obtained by measuring the tallest tumor pituitary adenoma in 18% of patients at 3  months after diameter in coronal view. Macroadenoma was defined as surgery [10, 11]. On the other hand, since the pituitary greatest tumor diameter greater than 10 mm. gland plays an essential role in the control of other endo- Adenoma volume was calculated using the largest ante- crine glands, maintaining the function of this gland after rior-posterior, external and rostrocaudal radius dimen- surgery is very important and determinating the amount sions. To measure the consistency of macroadenoma, the of the normal pituitary tissue after surgery can be very signal intensity of macroadenoma and that of pons were helpful in predicting of the reversibility of pituitary func- calculated with quantitative analysis of MRI signal inten- tion [12, 13]. Due to the fact that MRI is the method of sity. Then, the consistency was estimated in each case choice for imaging pituitary tumors and evaluation of by calculating the ratio of signal intensity of adenoma to changes in the tumor after surgery, MRI before and after pons according to cut point of 1.49 in previous studies; surgery is necessary for selection of proper treatment and consistency of less than 1.49 was considered as firm and appropriate postoperative management [12]. Therefore, fibrous and more than 1.49 as soft tumors [13]. In this the aim of this study was to investigate the relationship study we used Knosb grading method for assessment of between pituitary function after trans sphenoidal sur- cavernous sinus invasion. Normal gland locations were gery and MRI characteristics in non-functional pituitary demonstrated against the pituitary adenoma accord- macroadenoma. ing to degree of enhancement on preoperative dynamic MR images. After surgery, the normal gland differentia - tion from the residual enhancing lesion were diagnosed Method by analyzing the preoperative location and degree of Study design and data collection enhancement on dynamic MR imaging and also the posi- This study was a retrospective cohort study which tion of hypophysial stalk in some cases. Normal hypo- included patients with non-functional pituitary macroad- physial tissue enhancement is more than adenoma in enoma registered at Iran Pituitary tumor registry (IPTR) overall. between 2016 and 2018. The written informed consent was obtained from the participants and the study was Statistical analysis approved by the Ethical Committee at Iran University The continuous and discrete variables are described of medical sciences. (Approval number: IR.IUMS.FMD. using number (percent) and median [interquartile range REC.1398.154). (IQR)], respectively. To measure the impact of the preop- erative MRI findings (tumor size, tumor volume, appar - Patients ent normal pituitary tissue, and cystic change) on the This study included patients with non-functional pitui - pituitary function after surgery (TSH, ACTH, LH, GH, tary macroadenoma who underwent trans sphenoidal and PRL), the univariate regressions models were fitted. surgery. Inclusion criteria were all patients with biochem- Moreover, to assess the MRI characteristics of patients ically and histologically confirmed non-functional pitui - with preoperative pituitary macroadenoma as predictors tary macroadenoma with available MRI scan who had of normal pituitary gland normal residual pituitary gland hormone profile before and after surgery. Patients with (NRPG) after surgery, the univariate logistic regression Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 3 of 7 models were fitted and odds ratios (ORs) were reported. Hypothyroidism was detected before and after surgery The analyses were performed using the statistical soft - in 20% and 61.9% of patients, respectively. Hypercorti- ware Stata (ver. 12). The significance level was set to be solism was diagnosed in 32.3% of patients before and in 0.05. 48.8% after surgery. Hypogonadism was also observed in 74.2% of patients before and 54.8% of patients after Results surgery. Low insulin-like Growth Factor-1 (IGF-1) was Data were available for 44 patients who met the inclusion observed in 22.6% and 12% of patients before and after criteria. Demographic and clinical characteristics of the surgery, respectively. Moreover, hyperprolactinemia was participants at the time of diagnosis are demonstrated in detected in 45% of patients before surgery and in 27.8% Table 1. of patients after surgery (Fig. 1). Preoperative MRI characteristics and postoperative pituitary function Table 1 Demographic and MRI characteristics prior to surgery There was a significant, adverse relationship between preoperative tumor size and serum TSH level after sur- Variables Prevalence gery (odds ratio (OR): − 0.99 (− 0.18, − 0.003), p = 0.04). Age ( yrs) 55 (38–61) There was also a significant relationship between preop - Male (%) 27/44 (61.4%) erative tumor size and postoperative prolactin level (OR: Duration of follow‑up (mos.) 6.8 (3.6–10.9) 5.29 (1.65, 8.92), p = 0.006). Moreover, a significant rela - Tumor size (mm) 28 (22–33) tionship was observed between preoperative tumor vol- Tumor volume (mm ) 6845.5 (4041.2–1034.9) ume and postoperative prolactin level (OR: 0.006 (0.0008, Giant adenoma (%) 3/44 (6.8%) 0.01), p = 0.02) (Table  2). There was no significant rela - Apparent normal pituitary tissue (%) tionship between preoperative imaging characteristics No visible tissue 23/43 (53.5%) and the amount of other pituitary hormones after sur- Normal 7/43(16.3%) gery (p ≥ 0.05). Distorted 13/43 (30.2%) Cystic change (%) 15/42 (35.7%) Preoperative MRI characteristics and postoperative Tumor extension (%) morphologic reconstruction of pituitary gland Suprasellar 18/43(41.9%) Morphologic Reconstruction pattern of pituitary gland Cavernous sinus 18/43(41.9%) after surgery was as followed: invisible normal pituitary infrasellar 7/43(16.3%) tissue in 21.4% (9/42) of patients, complete normal pitui- Consistency of tumor (%) tary tissue in 45.3% (19/42), and partial remnants of nor- Fibrotic 3/43(7%) mal pituitary tissue in 33.3% (14/42) patients. There was Soft 40/43(93%) a significant, adverse relationship between tumor size Yrs.; years, mos.: months, mm; millimeter, mm ; cubic millimeter, data are before surgery and normal morphologic reconstruction presented as number (%), median and interquartile range (IQR) Fig. 1 Bar chart of hormonal changes before and after surgery [Insulin‑like growth factor ‑1 (IGF‑1), Prolactin (PRL)] Hassani et al. BMC Medical Imaging (2022) 22:60 Page 4 of 7 Table 2 Relationship between preoperative MRI findings and pituitary function after surgery Variables TSH ACTH LH GH PRL Coefficient Coefficient Coefficient Coefficient Coefficient (95%CI) (95%CI) (95%CI) (95%CI) (95%CI) Tumor size − 0.09 0.36 − 0.2 − 0.005 5.29 (− 0.18, − 0.003) (− 1.6,2.32) (− 0.42, 0.0091) (− 0.52, 0.4) (1.65, 8.92) p = 0.04 p = 0.6 p = 0.06 p = 0.8 p = 0.006 Tumor volume − 0.0001 0.001 − 0.0002 − 6.40 0.006 (− 0.0002, 0.00001) (− 0.002, 0.004) (− 0.0005, 0.00005) (− 0.0008, 0.00007) (0.0008,0.01) p = 0.08 p = 0.43 p = 0.11 p = 0.8 p = 0.02 Apparent normal − 1.04 11.06 − 1.61 − 0.14 37.44 pituitary tissue (− 2.7, 0.65) (− 67.74, 13.13) (− 5.64, 2.42) (− 0.95, 0.67) (− 39.13, 114.01) p = 0.23 p = 0.15 p = 0.41 p = 0.72 p = 0.3 Cystic change 0.45 2.67 − 0.55 − 0.32 − 36.4 (− 1.41, − 2.3) (− 53.73, 59.06) (− 5.5, 4.4) (− 1.2, 0.58) (− 117.8, 44.88) p = 0.61 p = 0.91 p = 0.82 p = 0.5 p = 0.37 CI confidence interval, TSH thyroid-stimulating hormone, ACTH adrenocorticotropic hormone, LH luteinizing hormone, GH growth hormone, PRL prolactin non-functional pituitary macroadenoma indicated post- Table 3 Preoperative MRI characteristics and odds of the normal residual pituitary gland (NRPG) after surgery operative TSH and prolactin levels are more likely to be associated with some MRI characteristics before surgery Variables OR (95% CI) p Value namely size and volume of the tumor. Moreover, size and Tumor size 0.80 (0.68,0.94) 0.007 volume of tumor in MRI images before trans sphenoidal Tumor volume 0.9998 (0.9996,0.9999) 0.007 surgery (TSS) showed an adverse association with the Cystic change (No as Ref.) 1.71 (0.30,9.87) 0.546 percentage of normal residual of pituitary gland. In the Tumor extension 4 (0.8376,19.1022) 0.082 conducted study by Di Maio et  al. in 2012, NRPG was (Cavernous as Ref.) versus identified in 79% of the patients on preoperative MRI (Supra or Infra) [12]. Our research showed that NRPG was diagnosed in NRPG normal residual pituitary gland 21.4% of the patients on postoperative MRI, and there was a strong significant relationship between the size and volume of the tumor before surgery and NRPG. MRI of pituitary gland after surgery (OR: 0.80 (0.68, 0.94), with or without administration of gadolinium contrast p = 0.007). There was also a significant, adverse relation - agent also allows accurate assessment of the position and ship between tumor volume before surgery and NRPG function of the tumor before and after surgery [12, 13]. after surgery (OR: 0.99 (0.99, 0.99), p = 0.007) (Table 3). But gadolinium uptake significantly improves diagnosis of the pituitary gland, especially in severe deformity cases Pituitary function after surgery and NRPG in MRI scan of the pituitary gland. Improved diagnosis of the pitui- Among patients with no visible pituitary tissue (no mor- tary gland, after gadolinium uptake is due to the rapid phologic reconstruction), normal pituitary function, and pronounced contrast of the pituitary gland, which is partial hypopituitarism and pan hypopituitarism were more than the adenoma [12]. observed in 16.7%, 33.3% and 50% of patients, respec- In the study performed by Nomikos et al. in 2004, 721 tively. In patients with partial morphologic reconstruc- patients with non-functional macroadenoma pituitary tion of pituitary tissue, these features were observed in surgery were evaluated. 24.4% of patients had hypothy- 10% (1 patient), 40% (4 patients) and 50% (5 patients), roidism after surgery, the prevalence of which was lower respectively. The patients who had complete morpho - than our study (61.9%). Also in the Nomikos study, 1 year logic reconstruction of pituitary tissue experienced nor- after surgery, preoperative prolactin levels were slightly mal pituitary function (25%), partial hypopituitarism increased in 25.3% (only 5 patients); increasing preopera- (50%) and panhypopituitarism (25%) (Fig. 2). tive and postoperative prolactin was observed in 45% and 27.5% of patients in the present study, respectively; that Discussion was more that Nomikos study [14]. MRI is universally used in postoperative care pituitary In 2015, Lee et  al. conducted a study on 45 patients adenomas, for the diagnosis of residual or recurrent undergoing sphenoid surgery. In this study, hypo- tumors [11, 12]. This retrospective cohort study con - gonadism was defined as total serum testosterone ducted among 44 patients who underwent TSS due to Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 5 of 7 Fig. 2 Ratio of patients with different pituitary functions according to the type of morphologic reconstruction of normal pituitary gland on MRI after surgery level < 4.2  ng/ml. Tumor volume was calculated based of this disorder in our study with compared with Ono on MRI images before and after surgery. Examination et al. [16] results. of the MRI results showed that the need for long-term In other hand, one of the most common symptoms postoperative testosterone replacement was significantly of dysfunctional pituitary macroadenomas is hypog- associated with a larger volume of preoperative tumor onadism, which may require long-term hormone replace- and preoperative testosterone levels. Preoperative tumor ment. In addition, reducing the pressure on the normal volume and testosterone levels affect postoperative pituitary gland may lead to postoperative recovery of the hypogonadism. By measuring tumor volume and testos- pituitary gland [15, 17]. terone levels, surgeons will be able to predict postopera- The rate and type of changes in hormone’s level after tive hypogonadism and the need for long-term hormone surgery can be different because pituitary function and replacement [15]. preservation of normal pituitary tissue after surgery In 2021, Ono et  al. examined the clinical features and depends on several factors such as tumor characteristic, surgical outcomes of 79 patients with dysfunctional the amount of pressure caused by the tumor on normal pituitary adenoma. Reduction of growth hormone lev- pituitary tissue, the type of surgery selected (for example, els was observed in 37.7% of patients. In our study, also in patients undergoing cranial surgery, the incidence of a deficiency of postoperative IGF-1 was observed in 12% this deterioration is significantly higher) and the age of of patients, which indicated a lower prevalence of this patients [7, 13, 18, 19]. disorder in the present study. Ono et  al. also showed For example in study performed by Jahangiri et  al. that, hypogonadism after surgery was developed in 19% in 2016, patients with preoperative endocrine deficits of patients, but in our study, the prevalence of hypog- (n = 153, 50%) were significantly older (mean age 60) and onadism was 54.8% postoperatively, which was higher had larger adenomas. Postoperative endocrine deficits than the Ono et  al. results. A deficiency of TSH was occurred in 42 (13.7%) patients (y Th roid axis 3%, cortisol observed in 6.3% of patients in the Ono et  al. results, axis 6%, and GH/IGF-1 axis 4%). In our study, decreased deficiency of TSH was 61.9% in patients studied in our cortisol was observed in 32.3% and 48.8% of patients research, and this matter indicates the higher prevalence before and after surgery, respectively and a deficiency Hassani et al. BMC Medical Imaging (2022) 22:60 Page 6 of 7 of postoperative IGF-1 was observed in 12% of patients. patient’s position, the intensity of the adenohypophysis In similar to Jahangiri et  al. [20] results, deficits were and neurohypophysis signals [13]. occurred in hormones production. Disorders of cortisol Given the prevalence of pituitary adenomas and espe- levels can also vary before and after pituitary surgery. For cially their non-functional types, often diagnosed at example, in patients who have had low blood pressure higher stages, pre- and post- operative MRI scan can be during anesthesia, or who have been taking medications used to choose the right treatment approach before. such as phenytoin, ketoconazole, corticosteroid, and nar- cotics, the disorder is more pronounced [21, 22]. Conclusion Guinto-Nishimura et  al. in 2020 performed preop- There was a significant relationship between preopera - erative MRI in patients with non-functional pituitary tive tumor size and volume and postoperative pituitary macroadenoma to determine tumor severity alone and hormone production. Moreover, preoperative MRI char- in association with the right cerebellar peduncle in 26 acteristics could predict normal pituitary morphologic patients. Tumor consistency was assessed as soft in reconstruction after pituitary surgery. 20 (76.92%) patients. In the present study, 93% of the tumors had a soft consistency, which was higher than the Abbreviations Guinto-Nishimura study. Guinto-Nishimura et  al. also MRI: Magnetic resonance imaging; TSH: Thyroid stimulating hormone; showed that preoperative tumor volume was 28.7 ± 26.3 IUMS: Iran University of Medical Science; FCRDC: Firouzgar Clinical Research Development Center; NRPG: Normal reconstruction of pituitary gland; LH: cm and the rate of tumor resection was not significantly Luteinizing hormone; FSH: Follicle stimulating hormone; GH: Growth hor‑ associated with tumor consistency [23]. mone; ACTH: Adrenocorticotropic hormone; IPTR: Iran Pituitary tumor registry; Onofrj et al. in 2018 reported that the mean preopera- PACS: Picture Archiving and Communication System; IQR: Interquartile range; PRL: Prolactin; ORs: Odds ratio; IGF‑1: Insulin‑like Growth Factor ‑1; TSS: Trans tive tumor volume was 24.66 cm . A progressive tumor sphenoidal surgery. volume decrease was noted during follow-up, and symp- toms improved in 78% of patients. They conducted the Acknowledgements N/A. duration of symptoms prior of surgery is a more impor- tant factor than tumor resection volume alone when Author contributions considering the long-term outcome of symptoms. In our NHM, MAK and MEKh conceived of the present idea. MAK and BH designed the study. Data acquisition was performed by BH. BH, NHM and MAK con‑ study preoperative mean tumor volume was 6845.5 mm tributed to the data analysis and interpretation. BH and NHM were major and a significant relationship was observed between pre - contributors and contributed equally to writing the manuscript. MEKh operative tumor volume and postoperative production of critically revised the manuscript. All the authors read and approved the final manuscript. prolactin hormone [24]. Juthani et  al. in 2020 performed a study on the 212 Funding patients with pituitary MRI before and after surgery. 62% N/A. of patients underwent resection of the tumor based on Availability of data and materials postoperative MRI findings and comparison with pre - The datasets analyzed during the current study are not publicly available due operative resection, and as a result, the remnants of the to limitations of ethical approval involving the patient data and anonymity but are available from the corresponding author on reasonable request. tumor had to be removed. Tumor resection due to post- operative MRI results was significantly associated with Declarations increased survival and pituitary function as well as hor- mone therapy. These results suggest that using preopera - Ethics approval and consent to participate tive MRI is a safe method leading to the increase in the This study was approved by the Ethical Committee at Iran University of medi‑ cal sciences, and written informed consent was obtained from all participants. resection rate of pituitary adenomas. Especially when (Approval Code: IR.IUMS.FMD.REC.1398.154). All methods in the study were MRI is combined with endoscopy, it provides the abil- carried out in accordance with the Helsinki guidelines and declaration. ity to adapt to the removal of tumors while optimizing Consent for publication pituitary function, resulting in a high rate of recovery of Not applicable. secretory hormone [25]. In the results of the present study, normal tissue was Competing interests The authors declare that they have no competing interests. not observed in 21.4% of MRI cases after surgery. MRI with or without administration of gadolinium contrast Author details agent also allows accurate assessment of the position of Department of Radiology, Firouzgar Clinical Research Development Center(FCRDC), Firouzgar General Hospital, Iran University of Medical the tumor before surgery and staging of pituitary tumors Sciences(IUMS), Valadi Street, Valiasr Sq., Tehran, Iran. Endocrine Research [13, 23]. Manifestations of normal pituitary gland tissue Center, Institute of Endocrinology and Metabolism, Iran University of Medical on MRI images include the size and shape of the gland Science (IUMS), Tehran, Iran. reflecting pituitary function, which depends on the Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 7 of 7 Received: 2 October 2021 Accepted: 28 March 2022 19. Yagasaki Y, Katayama Y, Kinoshita Y, Nagata T, Kawakami Y, Miyata M. Macrophages are activated in the rat anterior pituitary under chronic inflammatory conditions. Neurosci Lett. 2021;748:135688. 20. 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Magnetic resonance imaging characteristics predict pituitary function in non-functional pituitary macro-adenoma undergoing trans-sphenoidal surgery

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Abstract

Introduction: Maintaining the pituitary function after surgery is highly important. The aim of this study was to inves‑ tigate the relationship between preoperative magnetic resonance imaging (MRI) characteristics and pituitary function after surgery of non‑functional pituitary macroadenoma. Methods: This retrospective study was performed between 2016 and 2018. Preoperative and postoperative MRI imaging data were retrieved from electronic registration system. The relationship between preoperative MRI char‑ acteristics and postoperative pituitary function as well as reconstruction of pituitary gland was investigated using regression models. Results: Complete data were available for 44 patients. Before surgery, invisible normal tissue was observed in 23 patients (53.5%). Suprasellar extension and cavernous sinus invasion were seen in 36 patients (each one 49.1%). There was a significant reverse relationship between preoperative tumor size and postoperative thyroid stimulating hor ‑ mone ( TSH) (odds ratio (OR): − 0.99 (− 0.18, − 0.003), p = 0.04). In addition, we found a significant positive correlation between prolactin level after surgery and tumor size before surgery, (OR: 5.29 (1.65, 8.92), p = 0006). Moreover, post‑ operative panhypopituitarism was observed in 25% of patients with complete morphologic reconstitution of pituitary tissue. While the rate was 50% in patients with no or partial morphologic reconstruction of pituitary tissue. Conclusion: Preoperative MRI characteristics predict TSH and prolactin level after operation. Furthermore, the ade‑ noma size and volume prior to surgery are the main determinants of normal morphologic reconstruction of pituitary gland. Keywords: Pituitary gland function, Non‑functional pituitary macroadenoma, Surgery, Imaging features, Magnetic resonance imaging Introduction Non-functional pituitary macroadenomas (more than one centimeter in diameter) comprise about one-third *Correspondence: manizhe.ataei64@gmail.com of all pituitary adenomas and are managed with trans Behrooz Hassani and Nahid Hashemi‑Madani contributed equally to this sphenoidal surgery [1, 2]. Restoration of normal pitui- manuscript as co‑first authors. tary function after surgery is important and has been Department of Radiology, Firouzgar Clinical Research Development Center(FCRDC), Firouzgar General Hospital, Iran University of Medical reported in various studies from 20 to 50% [3, 4]. Pan- Sciences(IUMS), Valadi Street, Valiasr Sq., Tehran, Iran hypopituitarism, deficiency in production of at least two Full list of author information is available at the end of the article © The Author(s) 2022. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hassani et al. BMC Medical Imaging (2022) 22:60 Page 2 of 7 pituitary hormones, is a most common complication a history of radiotherapy as well as those with repeated after pituitary surgery [5]. Inadequate secretion of lute- pituitary surgery were excluded from the study. inizing hormone (LH) and follicle stimulating hormone (FSH), growth hormone (GH), thyroid stimulating hor- Data collection mone (TSH) and adrenocorticotropic hormone (ACTH) All demographic, clinical, and biochemical information were observed after pituitary surgery in 99%, 98.6%, 96% were extracted from the electronic record system at the and 81.8% of cases after pituitary surgery [6, 7]. Methods Institute of Endocrinology and Metabolism affiliated to for predicting the possible occurrence of these complica- Iran University of Medical Sciences. Hormone profile tions have also been studied. Various studies have shown before surgery and at the last follow-up visit were used in that some findings in magnetic resonance imaging (MRI) this analysis. are associated with post-operative complications. There - The pre-operative MRI scan as well as the first post- fore, identification of these findings in patients’ MRI can operative MRI scan obtained during 3 months after sur- be helpful in prediction and, possibly, prevention of the gery were also reviewed using the picture archiving and related complications [8, 9]. Researches evaluated the communication system (PACS). The required informa - post-operative MRI characteristics over one year after tion about size, volume, consistency and direction of trans sphenoidal surgery of the non-functional pitui- mass displacement were evaluated by two expert radiolo- tary macroadenomas. The results showed the residual of gists. Size was obtained by measuring the tallest tumor pituitary adenoma in 18% of patients at 3  months after diameter in coronal view. Macroadenoma was defined as surgery [10, 11]. On the other hand, since the pituitary greatest tumor diameter greater than 10 mm. gland plays an essential role in the control of other endo- Adenoma volume was calculated using the largest ante- crine glands, maintaining the function of this gland after rior-posterior, external and rostrocaudal radius dimen- surgery is very important and determinating the amount sions. To measure the consistency of macroadenoma, the of the normal pituitary tissue after surgery can be very signal intensity of macroadenoma and that of pons were helpful in predicting of the reversibility of pituitary func- calculated with quantitative analysis of MRI signal inten- tion [12, 13]. Due to the fact that MRI is the method of sity. Then, the consistency was estimated in each case choice for imaging pituitary tumors and evaluation of by calculating the ratio of signal intensity of adenoma to changes in the tumor after surgery, MRI before and after pons according to cut point of 1.49 in previous studies; surgery is necessary for selection of proper treatment and consistency of less than 1.49 was considered as firm and appropriate postoperative management [12]. Therefore, fibrous and more than 1.49 as soft tumors [13]. In this the aim of this study was to investigate the relationship study we used Knosb grading method for assessment of between pituitary function after trans sphenoidal sur- cavernous sinus invasion. Normal gland locations were gery and MRI characteristics in non-functional pituitary demonstrated against the pituitary adenoma accord- macroadenoma. ing to degree of enhancement on preoperative dynamic MR images. After surgery, the normal gland differentia - tion from the residual enhancing lesion were diagnosed Method by analyzing the preoperative location and degree of Study design and data collection enhancement on dynamic MR imaging and also the posi- This study was a retrospective cohort study which tion of hypophysial stalk in some cases. Normal hypo- included patients with non-functional pituitary macroad- physial tissue enhancement is more than adenoma in enoma registered at Iran Pituitary tumor registry (IPTR) overall. between 2016 and 2018. The written informed consent was obtained from the participants and the study was Statistical analysis approved by the Ethical Committee at Iran University The continuous and discrete variables are described of medical sciences. (Approval number: IR.IUMS.FMD. using number (percent) and median [interquartile range REC.1398.154). (IQR)], respectively. To measure the impact of the preop- erative MRI findings (tumor size, tumor volume, appar - Patients ent normal pituitary tissue, and cystic change) on the This study included patients with non-functional pitui - pituitary function after surgery (TSH, ACTH, LH, GH, tary macroadenoma who underwent trans sphenoidal and PRL), the univariate regressions models were fitted. surgery. Inclusion criteria were all patients with biochem- Moreover, to assess the MRI characteristics of patients ically and histologically confirmed non-functional pitui - with preoperative pituitary macroadenoma as predictors tary macroadenoma with available MRI scan who had of normal pituitary gland normal residual pituitary gland hormone profile before and after surgery. Patients with (NRPG) after surgery, the univariate logistic regression Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 3 of 7 models were fitted and odds ratios (ORs) were reported. Hypothyroidism was detected before and after surgery The analyses were performed using the statistical soft - in 20% and 61.9% of patients, respectively. Hypercorti- ware Stata (ver. 12). The significance level was set to be solism was diagnosed in 32.3% of patients before and in 0.05. 48.8% after surgery. Hypogonadism was also observed in 74.2% of patients before and 54.8% of patients after Results surgery. Low insulin-like Growth Factor-1 (IGF-1) was Data were available for 44 patients who met the inclusion observed in 22.6% and 12% of patients before and after criteria. Demographic and clinical characteristics of the surgery, respectively. Moreover, hyperprolactinemia was participants at the time of diagnosis are demonstrated in detected in 45% of patients before surgery and in 27.8% Table 1. of patients after surgery (Fig. 1). Preoperative MRI characteristics and postoperative pituitary function Table 1 Demographic and MRI characteristics prior to surgery There was a significant, adverse relationship between preoperative tumor size and serum TSH level after sur- Variables Prevalence gery (odds ratio (OR): − 0.99 (− 0.18, − 0.003), p = 0.04). Age ( yrs) 55 (38–61) There was also a significant relationship between preop - Male (%) 27/44 (61.4%) erative tumor size and postoperative prolactin level (OR: Duration of follow‑up (mos.) 6.8 (3.6–10.9) 5.29 (1.65, 8.92), p = 0.006). Moreover, a significant rela - Tumor size (mm) 28 (22–33) tionship was observed between preoperative tumor vol- Tumor volume (mm ) 6845.5 (4041.2–1034.9) ume and postoperative prolactin level (OR: 0.006 (0.0008, Giant adenoma (%) 3/44 (6.8%) 0.01), p = 0.02) (Table  2). There was no significant rela - Apparent normal pituitary tissue (%) tionship between preoperative imaging characteristics No visible tissue 23/43 (53.5%) and the amount of other pituitary hormones after sur- Normal 7/43(16.3%) gery (p ≥ 0.05). Distorted 13/43 (30.2%) Cystic change (%) 15/42 (35.7%) Preoperative MRI characteristics and postoperative Tumor extension (%) morphologic reconstruction of pituitary gland Suprasellar 18/43(41.9%) Morphologic Reconstruction pattern of pituitary gland Cavernous sinus 18/43(41.9%) after surgery was as followed: invisible normal pituitary infrasellar 7/43(16.3%) tissue in 21.4% (9/42) of patients, complete normal pitui- Consistency of tumor (%) tary tissue in 45.3% (19/42), and partial remnants of nor- Fibrotic 3/43(7%) mal pituitary tissue in 33.3% (14/42) patients. There was Soft 40/43(93%) a significant, adverse relationship between tumor size Yrs.; years, mos.: months, mm; millimeter, mm ; cubic millimeter, data are before surgery and normal morphologic reconstruction presented as number (%), median and interquartile range (IQR) Fig. 1 Bar chart of hormonal changes before and after surgery [Insulin‑like growth factor ‑1 (IGF‑1), Prolactin (PRL)] Hassani et al. BMC Medical Imaging (2022) 22:60 Page 4 of 7 Table 2 Relationship between preoperative MRI findings and pituitary function after surgery Variables TSH ACTH LH GH PRL Coefficient Coefficient Coefficient Coefficient Coefficient (95%CI) (95%CI) (95%CI) (95%CI) (95%CI) Tumor size − 0.09 0.36 − 0.2 − 0.005 5.29 (− 0.18, − 0.003) (− 1.6,2.32) (− 0.42, 0.0091) (− 0.52, 0.4) (1.65, 8.92) p = 0.04 p = 0.6 p = 0.06 p = 0.8 p = 0.006 Tumor volume − 0.0001 0.001 − 0.0002 − 6.40 0.006 (− 0.0002, 0.00001) (− 0.002, 0.004) (− 0.0005, 0.00005) (− 0.0008, 0.00007) (0.0008,0.01) p = 0.08 p = 0.43 p = 0.11 p = 0.8 p = 0.02 Apparent normal − 1.04 11.06 − 1.61 − 0.14 37.44 pituitary tissue (− 2.7, 0.65) (− 67.74, 13.13) (− 5.64, 2.42) (− 0.95, 0.67) (− 39.13, 114.01) p = 0.23 p = 0.15 p = 0.41 p = 0.72 p = 0.3 Cystic change 0.45 2.67 − 0.55 − 0.32 − 36.4 (− 1.41, − 2.3) (− 53.73, 59.06) (− 5.5, 4.4) (− 1.2, 0.58) (− 117.8, 44.88) p = 0.61 p = 0.91 p = 0.82 p = 0.5 p = 0.37 CI confidence interval, TSH thyroid-stimulating hormone, ACTH adrenocorticotropic hormone, LH luteinizing hormone, GH growth hormone, PRL prolactin non-functional pituitary macroadenoma indicated post- Table 3 Preoperative MRI characteristics and odds of the normal residual pituitary gland (NRPG) after surgery operative TSH and prolactin levels are more likely to be associated with some MRI characteristics before surgery Variables OR (95% CI) p Value namely size and volume of the tumor. Moreover, size and Tumor size 0.80 (0.68,0.94) 0.007 volume of tumor in MRI images before trans sphenoidal Tumor volume 0.9998 (0.9996,0.9999) 0.007 surgery (TSS) showed an adverse association with the Cystic change (No as Ref.) 1.71 (0.30,9.87) 0.546 percentage of normal residual of pituitary gland. In the Tumor extension 4 (0.8376,19.1022) 0.082 conducted study by Di Maio et  al. in 2012, NRPG was (Cavernous as Ref.) versus identified in 79% of the patients on preoperative MRI (Supra or Infra) [12]. Our research showed that NRPG was diagnosed in NRPG normal residual pituitary gland 21.4% of the patients on postoperative MRI, and there was a strong significant relationship between the size and volume of the tumor before surgery and NRPG. MRI of pituitary gland after surgery (OR: 0.80 (0.68, 0.94), with or without administration of gadolinium contrast p = 0.007). There was also a significant, adverse relation - agent also allows accurate assessment of the position and ship between tumor volume before surgery and NRPG function of the tumor before and after surgery [12, 13]. after surgery (OR: 0.99 (0.99, 0.99), p = 0.007) (Table 3). But gadolinium uptake significantly improves diagnosis of the pituitary gland, especially in severe deformity cases Pituitary function after surgery and NRPG in MRI scan of the pituitary gland. Improved diagnosis of the pitui- Among patients with no visible pituitary tissue (no mor- tary gland, after gadolinium uptake is due to the rapid phologic reconstruction), normal pituitary function, and pronounced contrast of the pituitary gland, which is partial hypopituitarism and pan hypopituitarism were more than the adenoma [12]. observed in 16.7%, 33.3% and 50% of patients, respec- In the study performed by Nomikos et al. in 2004, 721 tively. In patients with partial morphologic reconstruc- patients with non-functional macroadenoma pituitary tion of pituitary tissue, these features were observed in surgery were evaluated. 24.4% of patients had hypothy- 10% (1 patient), 40% (4 patients) and 50% (5 patients), roidism after surgery, the prevalence of which was lower respectively. The patients who had complete morpho - than our study (61.9%). Also in the Nomikos study, 1 year logic reconstruction of pituitary tissue experienced nor- after surgery, preoperative prolactin levels were slightly mal pituitary function (25%), partial hypopituitarism increased in 25.3% (only 5 patients); increasing preopera- (50%) and panhypopituitarism (25%) (Fig. 2). tive and postoperative prolactin was observed in 45% and 27.5% of patients in the present study, respectively; that Discussion was more that Nomikos study [14]. MRI is universally used in postoperative care pituitary In 2015, Lee et  al. conducted a study on 45 patients adenomas, for the diagnosis of residual or recurrent undergoing sphenoid surgery. In this study, hypo- tumors [11, 12]. This retrospective cohort study con - gonadism was defined as total serum testosterone ducted among 44 patients who underwent TSS due to Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 5 of 7 Fig. 2 Ratio of patients with different pituitary functions according to the type of morphologic reconstruction of normal pituitary gland on MRI after surgery level < 4.2  ng/ml. Tumor volume was calculated based of this disorder in our study with compared with Ono on MRI images before and after surgery. Examination et al. [16] results. of the MRI results showed that the need for long-term In other hand, one of the most common symptoms postoperative testosterone replacement was significantly of dysfunctional pituitary macroadenomas is hypog- associated with a larger volume of preoperative tumor onadism, which may require long-term hormone replace- and preoperative testosterone levels. Preoperative tumor ment. In addition, reducing the pressure on the normal volume and testosterone levels affect postoperative pituitary gland may lead to postoperative recovery of the hypogonadism. By measuring tumor volume and testos- pituitary gland [15, 17]. terone levels, surgeons will be able to predict postopera- The rate and type of changes in hormone’s level after tive hypogonadism and the need for long-term hormone surgery can be different because pituitary function and replacement [15]. preservation of normal pituitary tissue after surgery In 2021, Ono et  al. examined the clinical features and depends on several factors such as tumor characteristic, surgical outcomes of 79 patients with dysfunctional the amount of pressure caused by the tumor on normal pituitary adenoma. Reduction of growth hormone lev- pituitary tissue, the type of surgery selected (for example, els was observed in 37.7% of patients. In our study, also in patients undergoing cranial surgery, the incidence of a deficiency of postoperative IGF-1 was observed in 12% this deterioration is significantly higher) and the age of of patients, which indicated a lower prevalence of this patients [7, 13, 18, 19]. disorder in the present study. Ono et  al. also showed For example in study performed by Jahangiri et  al. that, hypogonadism after surgery was developed in 19% in 2016, patients with preoperative endocrine deficits of patients, but in our study, the prevalence of hypog- (n = 153, 50%) were significantly older (mean age 60) and onadism was 54.8% postoperatively, which was higher had larger adenomas. Postoperative endocrine deficits than the Ono et  al. results. A deficiency of TSH was occurred in 42 (13.7%) patients (y Th roid axis 3%, cortisol observed in 6.3% of patients in the Ono et  al. results, axis 6%, and GH/IGF-1 axis 4%). In our study, decreased deficiency of TSH was 61.9% in patients studied in our cortisol was observed in 32.3% and 48.8% of patients research, and this matter indicates the higher prevalence before and after surgery, respectively and a deficiency Hassani et al. BMC Medical Imaging (2022) 22:60 Page 6 of 7 of postoperative IGF-1 was observed in 12% of patients. patient’s position, the intensity of the adenohypophysis In similar to Jahangiri et  al. [20] results, deficits were and neurohypophysis signals [13]. occurred in hormones production. Disorders of cortisol Given the prevalence of pituitary adenomas and espe- levels can also vary before and after pituitary surgery. For cially their non-functional types, often diagnosed at example, in patients who have had low blood pressure higher stages, pre- and post- operative MRI scan can be during anesthesia, or who have been taking medications used to choose the right treatment approach before. such as phenytoin, ketoconazole, corticosteroid, and nar- cotics, the disorder is more pronounced [21, 22]. Conclusion Guinto-Nishimura et  al. in 2020 performed preop- There was a significant relationship between preopera - erative MRI in patients with non-functional pituitary tive tumor size and volume and postoperative pituitary macroadenoma to determine tumor severity alone and hormone production. Moreover, preoperative MRI char- in association with the right cerebellar peduncle in 26 acteristics could predict normal pituitary morphologic patients. Tumor consistency was assessed as soft in reconstruction after pituitary surgery. 20 (76.92%) patients. In the present study, 93% of the tumors had a soft consistency, which was higher than the Abbreviations Guinto-Nishimura study. Guinto-Nishimura et  al. also MRI: Magnetic resonance imaging; TSH: Thyroid stimulating hormone; showed that preoperative tumor volume was 28.7 ± 26.3 IUMS: Iran University of Medical Science; FCRDC: Firouzgar Clinical Research Development Center; NRPG: Normal reconstruction of pituitary gland; LH: cm and the rate of tumor resection was not significantly Luteinizing hormone; FSH: Follicle stimulating hormone; GH: Growth hor‑ associated with tumor consistency [23]. mone; ACTH: Adrenocorticotropic hormone; IPTR: Iran Pituitary tumor registry; Onofrj et al. in 2018 reported that the mean preopera- PACS: Picture Archiving and Communication System; IQR: Interquartile range; PRL: Prolactin; ORs: Odds ratio; IGF‑1: Insulin‑like Growth Factor ‑1; TSS: Trans tive tumor volume was 24.66 cm . A progressive tumor sphenoidal surgery. volume decrease was noted during follow-up, and symp- toms improved in 78% of patients. They conducted the Acknowledgements N/A. duration of symptoms prior of surgery is a more impor- tant factor than tumor resection volume alone when Author contributions considering the long-term outcome of symptoms. In our NHM, MAK and MEKh conceived of the present idea. MAK and BH designed the study. Data acquisition was performed by BH. BH, NHM and MAK con‑ study preoperative mean tumor volume was 6845.5 mm tributed to the data analysis and interpretation. BH and NHM were major and a significant relationship was observed between pre - contributors and contributed equally to writing the manuscript. MEKh operative tumor volume and postoperative production of critically revised the manuscript. All the authors read and approved the final manuscript. prolactin hormone [24]. Juthani et  al. in 2020 performed a study on the 212 Funding patients with pituitary MRI before and after surgery. 62% N/A. of patients underwent resection of the tumor based on Availability of data and materials postoperative MRI findings and comparison with pre - The datasets analyzed during the current study are not publicly available due operative resection, and as a result, the remnants of the to limitations of ethical approval involving the patient data and anonymity but are available from the corresponding author on reasonable request. tumor had to be removed. Tumor resection due to post- operative MRI results was significantly associated with Declarations increased survival and pituitary function as well as hor- mone therapy. These results suggest that using preopera - Ethics approval and consent to participate tive MRI is a safe method leading to the increase in the This study was approved by the Ethical Committee at Iran University of medi‑ cal sciences, and written informed consent was obtained from all participants. resection rate of pituitary adenomas. Especially when (Approval Code: IR.IUMS.FMD.REC.1398.154). All methods in the study were MRI is combined with endoscopy, it provides the abil- carried out in accordance with the Helsinki guidelines and declaration. ity to adapt to the removal of tumors while optimizing Consent for publication pituitary function, resulting in a high rate of recovery of Not applicable. secretory hormone [25]. In the results of the present study, normal tissue was Competing interests The authors declare that they have no competing interests. not observed in 21.4% of MRI cases after surgery. MRI with or without administration of gadolinium contrast Author details agent also allows accurate assessment of the position of Department of Radiology, Firouzgar Clinical Research Development Center(FCRDC), Firouzgar General Hospital, Iran University of Medical the tumor before surgery and staging of pituitary tumors Sciences(IUMS), Valadi Street, Valiasr Sq., Tehran, Iran. Endocrine Research [13, 23]. Manifestations of normal pituitary gland tissue Center, Institute of Endocrinology and Metabolism, Iran University of Medical on MRI images include the size and shape of the gland Science (IUMS), Tehran, Iran. reflecting pituitary function, which depends on the Hassani  et al. BMC Medical Imaging (2022) 22:60 Page 7 of 7 Received: 2 October 2021 Accepted: 28 March 2022 19. Yagasaki Y, Katayama Y, Kinoshita Y, Nagata T, Kawakami Y, Miyata M. Macrophages are activated in the rat anterior pituitary under chronic inflammatory conditions. Neurosci Lett. 2021;748:135688. 20. 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Journal

BMC Medical Imaging – Springer Journals

Published: Apr 1, 2022

Keywords: Pituitary gland function; Non-functional pituitary macroadenoma; Surgery; Imaging features; Magnetic resonance imaging

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