Improvement of Metabolic Syndrome and Its Components in Patients Who Underwent Transsphenoidal Resection for Pituitary Adenoma

doi:10.21203/rs.3.rs-1717354/v1

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Improvement of Metabolic Syndrome and Its Components in Patients Who Underwent Transsphenoidal Resection for Pituitary Adenoma

https://doi.org/10.21203/rs.3.rs-1717354/v1

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Purpose. The aim of this paper is to evaluate changes in the metabolic status of patients with PA before and after the surgical treatment, and to look for differences in the metabolic outcomes among patients according to the adenoma type and the success rate of the surgery.

Methods. We assessed patients with PA who went through TSS for its treatment, documenting metabolic parameters (height, weight, fasting glucose, blood pressure, triglycerides, and HDL-cholesterol) before and after surgery, analyzed whole sample changes, and then stratified them according to adenoma type (non-producing, somatotroph, lactotroph, and corticotroph), and surgery success (total resection, near total resection, partial resection, subtotal resection).

Results. A total of 214 patients were enrolled for this study. The prevalence of MetSx with AACE criteria went from 51.52% before surgery to 28.99% after surgery (p <0.001). Hyperglycemia was the most benefited component, which went from 56% pre-surgery to 40.51% post-surgery (p= 0.03). Total resection group had the best improvement, with significant decrease of prevalence in MetSx from 83% to 16% (p< 0.001), and every component, excepting Hα: obesity went from 96% to 67% (p< 0.001), HT 59 to 24% (p< 0.001), HGlu 74 to 23 % (p<0.001), and HTri from 81 to 54% (p< 0.001). According to MetSx prevalence, there was no difference of the improvement PA type, as this improvement showed to be significant in all of them.

Conclusion. MetSx improves in patients with PA after surgical treatment.

Trial registration number. DI/20/403/03/87

Pituitary adenoma

metabolic syndrome

transsphenoidal surgery

metabolic components

Pituitary adenomas (PA) are benign tumors of the anterior pituitary gland. They represent approximately 15% of all intracranial tumors [1], and a 25% of all surgically treated intracranial neoplasms [2]. Moreover, PA are the most common type of pituitary disorder. PA clinical presentation varies according to the affected hormonal axis and to the affected surrounding structures mainly by mass effect. Compression of the optic chiasm is common, and patients present with visual field defects. The production of hormones or lack thereof constitutes the main criterion for classifying PAs as: functioning, and non-functioning. Functioning adenomas can be further classified according to the excess hormone secretion: lactotrophs/prolactinomas produce and secrete excess prolactin (PL); somatotrophs growth hormone (GH); corticotropes adrenocorticotrophic hormone (ACTH); thyrotropes thyrotrope-stimulating hormone (TSH); and gonadotrophs luteinizing hormone (LH) and follicle-stimulant hormone (FSH). If none of these hormones is hyper-secreted, then the adenoma is considered as a non-functioning one.

Currently, transsphenoidal surgery (TSS) is the standard of treatment for PA [3], except for prolactinomas, which only under specific circumstances, such as pharmacological treatment failure, are managed with surgery.

Metabolic syndrome (MetSx) is defined as a clinical entity comprising of obesity, hypertension (HT), hyperglycemia (HG), and dyslipidemia, which predisposes patients to develop insulin resistance, and ultimately Diabetes Mellitus (DM) [4]. This syndrome is gaining interest in Mexico since the estimated prevalence in 2018 was 31%, however actual numbers could be higher [5].

PAs cause aberrant hormone secretion, which in turn carries a wide range of consequences, affecting whole-body metabolism. Metabolic dysregulation leads to higher frequency of MetSx and its markers (54%) in patients living with PA compared to general population [6], [7].

Furthermore, mass effect from the tumor leads to compression of the pituitary stalk and portal vessels, causing decreased dopamine delivery to the anterior pituitary and subsequent hyperprolactinemia [6]. This phenomenon can be present in non-functioning PAs as well as functioning PAs. In this way, PRL contributes to the metabolic dysregulation as it stimulates secretion of interleukine-6 (IL-6), adiponectin, and leptin and regulates the transcription of lipid-metabolism-related genes [8], [9].

Similarly, the GH is involved in metabolism stimulating lipolysis and lipid oxidation [10], whereas the activation of lipolysis in adipose tissue and the inhibition of glucose uptake is stimulated by cortisol [11].

Furthermore, adenomas which extent to suprasellar regions can produce hypothalamic dysfunction, conditioning dysregulations in circadian rhythms and feeding disturbances, among other functions which are associated with MetSx [7], [12].

Each type of PA can have different clinical manifestations, however all of them converge in one direction: metabolic dysregulation. In recent years, this association has been studied with some limitations, leading to some authors to agree that this field needs research assessing the metabolic parameters of patients with PA before and after treatment [6], [13], agreement which is here addressed. Therefore, the aim of this paper is first, to evaluate the metabolic status of patients with PA before and after the surgical treatment; secondly, look for differences in the metabolic outcomes among patients according to the adenoma type and the success rate of the surgery.

PATIENTS

We retrospectively evaluated patients diagnosed with PA between 2015 and 2020 at the General Hospital of Mexico. Diagnosis was based on signs and symptoms of PA, biochemical hormonal abnormalities, and presence of the tumor in magnetic resonance image (MRI). Only patients who underwent TSS for treatment of PA were included. Patients with recurrence or persistence of PA diagnosed before 2015 were excluded. Patients with recurrence or persistence of PA diagnosed between 2015 and 2020 were included, documenting only data from the first surgery (basal). Patients’ clinical records were reviewed, and the following data was retrieved: sex, age, date of PA diagnosis, type of PA, size of the PA and surgery date. Presurgical and postsurgical metabolic status were characterized by the following parameters: size of the PA according to MRI, height, weight, body mass index (BMI), blood pressure (BP), glucose (Glu), high-density cholesterol (HDL-C), and triglycerides (TG); and the date of each sample.

Time between samples and surgery was measured and patients were excluded when available samples were taken longer than 3 months apart from surgery [14]– [16]. Demographic characteristics of the population were determined: age and sex

To assess the variation of metabolic parameters, the general sample was stratified by groups. These groups were created according to two parameters: extent of resection (surgery success), and PA hormone type. Extent of resection (surgery success) was determined by calculating the ellipsoidal volume of the tumor observed in MRI before and after surgery to estimate the resected volume percentage, classifying them into total resection (TR) (100%), near total resection (NTR) (> 95%), subtotal resection (SR) (70–95%), and partial resection (PR) (< 70%) [17]. Patients with recurrence were eliminated (> 100%).

Patients were divided according to the PA type into non-producing (NP), lactotroph (PL), somatotroph (GH), and corticotroph (ACTH). Thyrotroph (TSH) and gonadotroph (LH/FSH) were excluded from group analysis due to lack of patients. PA type was determined based on registered clinical diagnosis and immunohistochemistry.

Patients who met criteria for MetSx parameters (obesity, hyperglycemia, hypertension, hypoalphalipoproteinemia, and hypertriglyceridemia), and MetSx according to the American Association of Clinical Endocrinology (AACE 2003) criteria[18] were identified and included. Since abdominal perimeter is seldom reported in routine care of these patients, we used MetSx definitions that characterize obesity through BMI, not abdominal perimeter.

MEASUREMENTS

Imaging of all patients was done with 1.5 Tesla equipment (Magnetom Avanto and Magnetom Essenza; Siemens, Germany), using an 8-channel skull coil. MRIs were obtained according to the following sella turcica protocol: T1 coronal and sagittal planes (TR repetition time/TE echo time = 400/12 ms) with a 256 × 256 matrix, 200 × 250 field of view mm² and fine cuts of 3 mm; Coronal plane T2 (TR/TE = 3600/97 ms); with a 261 × 384 matrix, 250 × 250 mm² field of view and 3 mm thin slices. Fluid-attenuated inversion recovery (FLAIR) axial plane (TR/TE = 4000/117 ms), 380 × 380 matrix, 224 × 256 mm² field of view, 5 mm slices. For microadenomas, T1 images were taken after the intravenous injection of a 0.05–0.1 mmol/kg dose of gadolinium, after which, every 10 seconds, 4 consecutive sets of images were obtained. Three images in a coronal plane; with 256 × 380 high resolution matrix, 200 × 250 mm² field of view and 3 mm fine slices; T1 sequences were also added in axial, sagittal and coronal planes in the late phase, with a matrix size of 380 × 380, slice thickness of 5 mm and a field of view of 200 × 240 mm². For macroadenomas, T1 sequences were performed after the intravenous injection of a 0.05–0.1 mmol/kg dose of gadolinium; in axial, sagittal, and coronal planes with a matrix size of 380 × 380, slice thickness of 5 mm, and a field of view of 200 × 240 mm².

For biochemical analysis, Glu was measured by enzymatic UV (hexokinase method) in a Beckman Coulter AU, USA 2018 analyzer. HDL-C and TG were measured by enzymatic colorimetric test in a Beckman Coulter AU, USA 2012 analyzer − 2018. To measure HDL-C and TG, chemiluminescence immunoassay was performed using the Access Beckman Coulter Immunoassay systems, USA 2007–2019.

TSS for the PA adenectomy was performed through endoscopic or microscopic approach according to each patient’s case.

STATISTICS

Continuous variables are presented as mean ± standard deviation or median and interquartile range, according to their distribution. Categorical variables are presented in frequency and percentages. Changes in the frequency of metabolic syndrome components were analyzed using paired Chi-square test. These models were stratified according to PA type in order to assess the differences in effect attributable to the type of adenoma and extent of resection (surgery success) rate, defining statistically significant results if p ≤ 0.05.

COMPLIANCE WITH ETHICAL STANDARDS

Ethical approval was waived by the Ethics Committee of General Hospital of Mexico in view of the retrospective nature of the study and all the procedures being performed as part of the routine care. Protocol’s register number is DI/20/403/03/87. Informed consent was obtained from all individual participants included in the study.

PATIENTS

214 patients were included in this study; demographics are presented in Table 1. Mean age was 44.9 ± 13.12 years old, with 118 women (55.23%) and 96 men (44.77%), and a majority of macroadenomas (92.93%) versus 7.07% of microadenomas revealed by MRI. Non-producing adenomas (51.74%) were the most common type of PA, followed by somatotroph adenomas (26.57%), prolactinomas (12.58%), corticotroph adenomas (7.69%), and rarely thyrotroph and gonadotroph adenomas (0.69 and 0% respectively). Extent of resection (Surgery success rate) groups are presented in Table 2, 10.59% had total resection, 17.65% near-total resection, 44.71% subtotal resection, 22.35% partial resection, and 4.7% presented recurrence. These last 10 patients were eliminated from the study, leaving for the analysis 104 patients.

PERIOPERATIVE STUDIES

The mean number of days between perioperative studies and TSS are summarized in Figure 1. The mean number of days between presurgical studies and TSS was 86.66 (±20.4 SD) days, specifically, 109 days between presurgical MRI and TSS, a mean of 82 days between presurgical somatometric measurements (height, weight, BMI, and BP), and TSS, and a mean of 69 days between TSS and measurement of biochemical parameters (Glu, HDL-C, and TG). Similarly, the mean number of days between surgery and postsurgical measurements was 170 (±2.08 SD), with a mean of 168 days between surgery and postsurgical MRI, 172 between TSS and postsurgical somatometry, and 171 between TSS and postsurgical biochemical measurements.

METABOLIC OUTCOMES

General sample results (Figure 2)

The prevalence of MetSx decreased from 51.52% before surgery to 28.99% after surgery, demonstrating a statistically significant decline (p <0.001). Analyzing each individual component: obesity increased after surgery, with a prevalence of 85.54% before surgery to 90.91% after surgery; HT dropped from 39.68% to 33.80% after surgery; HGly from 56% to 40.51%; Hα from 64.71% to 53.70%; and HTri from 66.67% to 62.07%. Hyperglycemia was the only component that demonstrated a statistically significant decline (p = 0.03).

Moreover, Figure 3 presents only observational results, disclosing the distribution of MetSx components in patients before and after TSS. Before surgery, most patients had between 2 to 4 components of MetSx and after surgery patients had between 0 to 2 components. TSS decreases not only MetSx diagnosis, but also most of the MetSx components individually.

Surgery success rate stratification (Figure 4)

Frequency of each MetSx component and MetSx was analyzed in each group according to extent of resection (surgery success rate), demonstrating that the TR group benefited the most, with a significant decrease in the prevalence of MetSx from 83% before surgery to 16% after surgery (p< 0.001), as well as its components, except for Hα which, in fact, increased. The prevalence of obesity went from 96% before surgery to 67% after (p< 0.001), HT 59% to 24% (p< 0.001), HGlu 74% to 23 % (p<0.001), and HTri from 8%1 to 54% (p< 0.001). The NTR group had a significant improvement in the prevalence of obesity from 86% before surgery to 67% after (p= 0.002), HT from 41% to 25% (p= 0.01), and HGlu from 33% to 11% (p< 0.001) but not MetSx, that went from 42% before TSS to 33% after (p= 0.189). The STR group showed a significant improvement in MetSx as well, from 64% before surgery to 48% after (p= 0.023), HT from 48% to 26% (p< 0.001), and HTri from 82% to 65% (p= 0.006). Finally, the PR group improved nearly every MetSx component except for Hα and obesity; HT went from 59% to 43% (p= 0.02), HGlu 18% to 4% (p= 0.002), and HTri from 97% to 67% (p< 0.001). Only TR and STR significantly decreased the prevalence of MetSx, and MetSx prevalence did not improve significantly (from 61% to 48%, p= 0.065).

Adenoma type stratification (Figure 5)

The MetSx prevalence significantly decreased in all PA groups. In NP from 71% before TSS to 41% after (p< 0.001), GH from 50% to 30% (p= 0.004), PL from 67% to 40% (p< 0.001), and ACTH from 80 to 67% (p= 0.037). However, there were differences between groups when analyzing each MetSx component.

MetSx prevalence declined in the NP group at the expense of the significant decrease in HGlu from 42 to 23% (p= 0.004), GH group improved significantly in terms of HT from 49% to 27% (p= 0.001), HGlu from 46% to 8% (p< 0.001), and HTri from 67% to 44% (p= 0.001). Furthermore, MetSx prevalence diminished in PL group mainly due to HTri improvement from 50% before TSS to 9% after (p< 0.001), as no other component decreased significantly, whereas ACTH group decreased significantly in HT from 67% to 50% (p= 0.01), HGlu from 67% to 25% (p< 0.001), and Hα from 87% to 43% (p< 0.001). Remarkably, obesity did not improve in any group, and Hα only did in ACTH group.

Currently, there are few reports of patients with PA involving the parameters here assessed altogether. Some studies evaluate only one type of adenoma, or only few of the metabolic syndrome components, leaving aside substantial aspects of the MetSx. Furthermore, most studies measure the parameters but do not consider that some measurements could be within normal range and might not find differences. However, we reported data in terms of prevalence and were able to demonstrate how many “sick” patients turn into “healthy” patients after treatment.

General sample outcomes

Leães and collaborators [19] found that only waist-hip ratio decreased after TSS for PA, among other variables related to body composition like BMI and waist circumference. This supports our results demonstrating no change in BMI. Other MetSx components are rarely documented when surgical outcomes are assessed. Moreover, most authors focus only on one type of PA, which leads to the lack of reports for the general PA population.

Surgery success stratification outcomes

To our knowledge, this is the first study to report the effects of TSS and the amount of tumor resected on metabolic parameters. Only a few reports mention similar findings, for example, Cheng et al. reported that PA invasiveness or size did not associate proportionally with abnormal glucose metabolism [20]. Moreover, Harbeck and colleagues only report differential prevalence of overweight and obesity between patients with macro and microadenomas, with a higher prevalence in individuals with macroadenomas [21].

Additionally, Leães et al., referred that 31.8% of the cases had a total tumor reduction but documented no difference between patients with complete tumor resection and the rest of the patients in any of the metabolic components they measured [19]. Altuntas and Evran in 2019, discussed the relationship between lipid parameters and the PA diameter in patients with NP PA [13].

Adenoma type stratification outcomes

Baba and Kameda et al. in 2021 [22], who assessed NP adenomas, described improvements in glucose tolerance and blood pressure levels following PA resection, which is concordant with our results. HGlu prevalence decreased after surgical treatment in patients with NP and GH adenomas, however, HT only decreased in GH group. This same study by Baba and Kameda et al, reported no significant differences in the rates of obesity, glucose tolerance or hyperlipidemia between groups of the different lineages being clinically NP, which is a point to consider when comparing equivalent producing PAs. On the other hand, Altuntas and Evran discussed in 2019 [13] that in patients with NP-PAs glucose metabolism disorders may persist despite remission being achieved, contrary to our results, as we found that NP group improved significantly, at least in terms of hyperglycemia defined as a fasting glucose >100 mg/dl. Furthermore, Vargas-Ortega et al. reported in 2018 that patients with NP-PAs who were treated multimodally [7] , the proportion of patients with MetSx decreased from 52% before surgery to 48% after with the NCEP-ATP III MetSx criteria, like the results here reported where MetSx decreased from 71% to 41% following AACE MetSx criteria. Moreover, in this same study obesity prevalence diminished significantly from 47% to 40% according to NCEP-ATP III MetSx criteria. Notably, we did not find changes regarding obesity in the NP group according to AACE criteria, which can be determining factor when comparing previous studies to our results.

For somatotroph adenomas, the improvement of glucose metabolism has been well documented once normal GH activity pattern has been achieved following treatment [20], [23], being the most studied MetSx component in this group before and after treatment.

Regarding prolactinomas, results among authors are contradictory. Some authors have correlated the normalization of serum PL levels to the improvement of the metabolic profile [24], whereas other authors have concluded that some parameters do not benefit at all despite PL level normalization [6]. Most studies focus on outcomes after medical management, with little information regarding surgical treatment. Iglesias and collaborators concluded that the serum concentrations of Glu, TC and TG did not vary significantly after normalization of PL levels with cabergoline treatment. These were identical results as the ones previously documented by Schewtz et al. in 2016 [25]. Both studies in agreement with the present study regarding Glu and CT, but not TG, which we found that improved after TSS. Posawets and colleagues reported no changes in TG nor HDL-C of men with prolactinomas after a median of 10 weeks of treatment with cabergoline, which is partially similar to what we document here, with improvement of HTri prevalence after treatment, but not for Hα [26]. Finally, Iglesias et al. in 2016 stated that these discordances could be explained by different confounding variables such as hypogonadism, hormone replacement therapy, treatment with cholesterol and glucose lowering drugs, etcetera [24].

Regarding to ACTH PAs, in Leães et al. report [19], patients with Cushing’s disease had a lower mean BMI after surgery, reclassifying them from obese to overweight, however this finding can be challenging to compare to our results, given that we consider obesity as a BMI >25 according to MetSx AACE criteria, hindering the distinction between overweight and obesity.

Some MetSx components require special mention, such as HT, which is seldom evaluated in PA studies, with the last study addressing it in 1983 [27], stating the presence of HT in acromegaly and Cushing’s disease. In Acromegaly the cure of the disease does not correlate with a decrease in blood pressure, whereas in Cushing’s disease, HT improves following successful treatment. We cannot completely agree with these antique results, as we found a decrease in HT prevalence for both groups after surgical treatment.

Additionally, as Harbeck et al. report [21], apparently, body weight is not influenced by hormonal activity in PA patients, since both individual with hormone secreting tumors and controls suffer from overweight or obesity. This was confirmed by our results, where we did not find differences in weight between PA types.

Finally, hypopituitarism following treatment and hypothalamic dysfunction can be another explanation for the presence of impaired metabolism in these patients[7], [13], [12], These two factors could explain why some parameters do not improve after TSS, or even get worse.

In this study we provide a general vision regarding all types of PAs and their relation to MetSx and each individual component. This study demonstrates that the prevalence of MetSx and some of its components improves after TSS, especially for patients who had a total resection of the tumor. Moreover, this study sets the foundation for further studies regarding PAs’ sizes, extent of resection (surgery success), and their relationship with metabolic status. Finally, we emphasize that current assessment and therapies for PA should assess the metabolic status as well, always looking forward the best outcomes for patients.

STATEMENTS AND FUNDING DECLARATIONS:

The authors did not receive support from any organization for the submitted work. The authors have no relevant financial or non-financial interests to disclose.

AUTHORS CONTRIBUTION

All authors contributed to the study conception and design. Material preparation was driven by Dr. Carrillo-Ruiz and Dr. Navarro-Olvera. Data recollections were performed by medical students Salazar-Pigeon, González-Almazán and Cortés-Contreras. Analysis, and the first draft of the manuscript was written by Cortés-Contreras and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

COMPETING INTERESTS

The authors did not receive support from any organization for the submitted work. The authors have no relevant financial or non-financial interests to disclose.

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Table 1 and 2 are available in the Supplementary Files section.

No competing interests reported.

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Improvement of Metabolic Syndrome and Its Components in Patients Who Underwent Transsphenoidal Resection for Pituitary Adenoma

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Material And Methods

PATIENTS

MEASUREMENTS

STATISTICS

COMPLIANCE WITH ETHICAL STANDARDS

Results

Discussion

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Supplementary Files

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