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Role of diffusion weighted magnetic resonance imaging DW-MRI in choice of the surgical approach for pituitary macroadenoma resection
The Egyptian Journal of Radiology and Nuclear Medicine xxx (2018) xxx–xxx
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Original Article
Role of diffusion weighted magnetic resonance imaging DW-MRI in choice of the surgical approach for pituitary macroadenoma resection Mohamed Alhousini Alashwah a,⇑, Mohamed A. Moharram a, Amira S. Allakany b a
Radiodiagnosis Department, Faculty of Medicine, Tanta University, Tanta, Egypt Damanhur General Hospital, Egypt
b
a r t i c l e
i n f o
Article history: Received 2 June 2017 Accepted 2 August 2017 Available online xxxx Keywords: Pituitary macroadenoma Diffusion weighted magnetic resonance imaging DW MRI
a b s t r a c t Background and purpose: Consistency of pituitary macroadenoma is a crucial information for neurosurgeons. We aimed to assess the role of DW-MRI as non invasive imaging modality in predicting the tumour consistency of pituitary macroadenoma. Materials and methods: Twenty patients with pituitary macroadenoma underwent conventional MR imaging sequences, pre contrast, post contrast MRI and diffusion weighted MRI with ADC map. The tumour consistency was determined both macroscopic by neurosurgeons and microscopic by histopathologists. Results: Our study included 12 soft, 4 intermediate and 4 hard tumours. The tumour consistency and the collagen contents were correlated with diffusion and ADC values. The mean ADC value of patients with soft tumours was 0.54 10 3 mm2/s while for intermediate tumour was 0.82 10 3 mm2/s and for hard tumours was 1.11 10 3 mm2/s. Soft and intermediate consistency tumours were successfully managed by endoscopic transsphenoidal approach; suction and curettage. While, hard tumours could not be managed by the transsphenoidal approach and needed further transcranial procedure with sensitivity 95% and specificity 95%. Conclusion: DWI-MRI is a useful tool to predict the pituitary macroadenoma consistency and the suitable surgical approach for resection. Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
1. Introduction The pituitary gland is the master gland of the body because it controls most of the body’s endocrine functions by means of the hypothalamic-pituitary axis [1]. Pituitary macroadenomas are common seller space occupying lesions greater than 10 mm in diameter and they are benign proliferation of cells of the anterior lobe of the pituitary gland. The clinical presentation depends primarily on whether they are functioning (secretory) or nonfunctioning (non-secretory), those nonfunctioning are more common. The first signs and symptoms produced by non-secretory macro adenomas are related to mass effect. Macroadenomas usually extend beyond the sella with enlargement of the Sella, the most common pattern is supra seller extension [2].
Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ⇑ Corresponding author. E-mail address: [email protected] (M.A. Alashwah).
ADC value (apparent diffusion coefficient) is a measure of the magnitude of diffusion of water molecules within the tissues and is calculated using different b values (B value measures the degree of diffusion weighting) (0–1000 s/mm2). DW MR imaging can be used to determine the consistency of the pituitary macroadenomas that cannot be obtained by conventional MR images, this can be obtained by correlation between tumor cellularity and ADC values where ADC values are inversely proportional to the tumor cellularity; tumors with higher cellularity have lower ADC values. ADC value of lesser than 1 will have highly successful transsphenoidal approach, limitation of transsphenoidal approach is macro adenoma with significant lateral and supraseller extension. Tumor consistency can also be a limitation; where soft one is easily resectable, about 10% of pituitary macro adenomas are fibrous and have increased consistency; hard consistency need more extensive approach [3]. Correlation between tumor cellularity and ADC values can be used preoperatively to determine the suitable surgical approach whether using the recent endoscopic transsphenoidal technique
https://doi.org/10.1016/j.ejrnm.2017.08.001 0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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M.A. Alashwah et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2018) xxx–xxx
as minimally invasive procedure compared to transcranial approach [3]. Preoperative evaluation of pituitary macroadenoma tumor consistency is important for neurosurgery to decide the appropriate type of surgery to use; whether transsphenoidal or transcranial approach, as those tumors with soft consistency are easily removable by suction through the transsphenoidal approach while the more fibrous; hard ones are difficult to be properly removed by suction and curettage through the same technique but indicate using the transcranial approach. Thus, we aimed to assess the role of Diffusion weighted MR imaging (DWI) in prediction of the tumor consistency of pituitary macroadenomas to help in proper surgical planning, and decreasing the risk of incomplete excision and the possibility of recurrence [4].
2.3. Surgery All patients with pituitary macro adenoma had received surgical resection of the macro adenoma using the transsphenoidal approach. At surgery, the neurosurgeon who was blinded to findings of DW imaging and ADC values of the cases, had assessed the macro adenomas consistency and classified them to three groups; soft, intermediate and hard in consistency. The soft macro adenomas were easily removed by suction, the intermediate group was removed with difficulty by suction or curettage and the hard group couldn’t be removed by suction and the surgeon recommended for further transcranial surgery for them. 2.4. Post-operative histopathology
2. Patients and methods This study was carried out on twenty patients who were suspected to have pituitary macroadenoma on clinical basis and referred from neurosurgery departments to MRI unit of Tanta University and other private centers and proved histopathologically later. Our study protocol was explained to our patients and informed consent was obtained. 2.1. For all patients the following were done Careful history taking and clinical examination which includes: Name, sex, age, marital status and symptoms & signs due to: AIncreased intracranial pressure (headache, vomiting) B-Visual apparatus disturbances (decreased visual acuity, blurring of vision) C-Hormonal disturbances (acromegaly, Cushing disease, amenorrhea, infertility, and galactorrhea) D-Cranial nerve palsies. 2.2. Imaging and image analysis: (pre-operative MRI) All MR images were acquired on Toshiba and Philips 1.5 T, closed configuration. Patient position is supine, to obviate head mal-rotation; the patient head was positioned in a vacuum pillow. Coil configuration is head coil. – The following protocol was used for all patients: I. Conventional MRI (c MRI): Non contrast axial, coronal, and sagittal T1WIs: Repetition time (TR):550 m/s. An echo time (TE):15 m/s. Field of view (FOV):250 mm. Acquisition matrix (ACQ): 95 120. Section thickness: 3 mm. Inter slice gap: 0.3 mm. Flip angle (FA): 90° Axial T2 WI : TR: 4844 m/s, TE: 110 m/s, FOV: 250 mm, ACQ: 184 256, slice thickness: 5 mm, inter slice gap: 1 mm Post Contrast Coronal T1WI: By administration of gadolinium 0.1 mm/ kg body weight. TR: 550 m/s, TE: 15 m/s, FOV: 250 mm, ACQ: 120 120, slice thickness: 3 mm, inter slice gap: 0.3 mm II. Diffusion weighted MR image (DWI) & ADC maps Prior to contrast agent administration, breath hold and DW images were done with single shot, spin-echo, and echo planner sequence as the following: TR: 2460–3690, TE: 70.72, ACQ: 108 108, section thickness: 6 mm, inter slice gab: 1 mm, B value: 0, 500, 1000 s/mm2. ADC maps were calculated automatically and ADC values were measured by using circumferential ROI in solid appearing portions of macro adenomas and excluding cystic and hemorrhagic areas where b-value 0, 500, 1000 sec/mm2.
For confirmation of the consistency of the macro adenomas which obtained by the pre-operative ADC values; histopathological examination was done for all patients through: A-Routine processing using haematoxylin and eosin (H.E.) stain. B-Examination of collagen percentage by Masson trichrome staining. C-Detection of reticulin content by Reticulin stain. Collagen content (+): the extracellular matrix accounts for less than 5% of the stained tissues. Collagen content (++): the extracellular matrix accounts for 5–15% of the stained tissues. Collagen content (+++): the extracellular matrix accounts for more than 15% of the stained tissues. 2.5. Statistical analysis of the data Data were fed to the computer and analyzed using IBM SPSS software package version 20.0. Qualitative data were described using number and percent. The Kolmogorov-Smirnov test was used to verify the normality of distribution. Quantitative data were described using range (minimum and maximum), mean, standard deviation and median. Significance of the obtained results was judged at the 5% level. The used tests were: F-test (ANOVA): For normally quantitative variables, to compare between more than two groups. Post Hoc test (LSD): for pairwise comparisons. Roc curve, sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) to detect the cut off value and accuracy of ADC maps to determine macro adenomas consistency and resectability. 3. Results Twenty patients were included in the current study; composed of 10 males and 10 females, they were ranging in age from 19 years to 57 years, with a mean age of 38.40 years. According to surgical opinion of tumor consistency and diffusion weighted magnetic resonant imaging and ADC maps analysis; the pituitary macroadenomas were classified to soft, intermediate and hard groups. The mean ADC values of the adenomas were found as the following: (Table 1) The mean ADC value of all patients (n = 20) was (0.7063) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (1.16) 10 3 mm2/s. The mean ADC value of patients with soft macroadenomas (n = 12) was (0.54) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (0.78) 10 3 mm2/s. The mean ADC value of patients with intermediate macroadenomas (n = 4) was (0.82) 10 3 mm2/s; ranging from (0.75) 10 3 mm2/s to (0.90) 1 0 3 mm2/s. The mean ADC value of patients with hard macroadenomas (n = 4) was (1.11) 10 3 mm2/s; ranging from (1.05) 10 3 mm2/s to (1.16) 10 3 mm2/s.
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M.A. Alashwah et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2018) xxx–xxx Table 1 Comparison between the three studied groups according to ADC value of DW MR imaging. Soft (n = 12)
Intermediate (n = 4)
Hard (n = 4)
F
p
ADC Min. Max. Mean SD. Median
0.34 0.78 0.54 0.14 0.53
0.75 0.90 0.82 0.05 0.83
1.05 1.16 1.11 0.03 1.11
36.957*
<.001*
Sig. bet. groups
p1 = .001*, p2 < .001*, p3 = .004*
F, p: F and p values for ANOVA test, Sig. bet. Groups was done using test (LSD) for ANOVA. * The results are statistically significant at p .05.
Table 2 Comparison between consistency of pituitary macroadenoma and signal intensity on T2WI. Consistency of macroadenoma
T2WI Iso intense
Hypo intense
Hyper intense
Total
Soft Intermediate Hard Total
3 1 1 5
1 1 – 2
8 2 3 13
12 4 4 20
The statistical analysis found that the three groups of pituitary macroadenomas, classified according to their consistency during surgery, shows dissimilarity in their mean ADC values (p .05). Relative statistical significance were indicated with p value as the following: o p1: p value for comparing between Soft and Intermediate p1 = .001, p2: p value for comparing between Intermediate and Hard p2 < .001, p3: p value for comparing between Soft and Hard. p3 = .004. Association between T2WI signal intensity and pituitary macroadenoma consistency are statistically significant only when p .05 (Table 2). According to successful rate of tumor resection by endoscopic transsphenoidal approach; pituitary macroadenomas were classified to resectable and non resectable groups. The resectable group was successfully managed by the transsphenoidal approach including the macroadenomas of soft and intermediate consistency (see Figs. 1 and 3) and had ADC value <1 10 3 mm2/s. The irresectable group could not be managed by transsphenoidal approach and needed surgery by transcranial approach and had ADC value >1 10 3 mm2/s. The cut off value between the resectable (soft and intermediate consistency) and the non resectable (hard consistency) was calculated statistically using ROC curve (receiver operating characteristic curve). The best accepted cut off value was = 1 10 3 mm2/s with sensitivity 95% and specificity 95% with area under curve (AUC) = 1. 4. Discussion Pituitary macroadenomas are common seller space occupying lesion and are generally regard as benign proliferation of cells of the anterior lobe of the pituitary gland. Pituitary macroadenomas are those greater than 10 mm in diameter. Pituitary surgery is indicated for excision, debulking or sellar decompression of mass lesions causing central nervous system pressure effects, visual compromise, compromised pituitary function. Urgent surgical decompression is required for acute pituitary hemorrhage, espe-
cially in patients who have developed sudden visual field compromise [5–9]. The used approach in this study was transsphenoidal endoscopic surgery or craniotomy (subfrontal or pterional). The choice of the suitable approach depends partly on an inner feature of the tumors; its consistency. Transsphenoidal endoscopic surgery is more suitable for the tumors with soft consistency which are easy to pull out, while craniotomy is suitable for harder ones. So, preoperative evaluation of tumor consistency can help to determine the best operative methods and treatments, which will not only increase the possibility of complete tumor removal, but also reduce recurrence rates [10,11]. The transsphenoidal endoscopic surgery are less invasive, provide direct access to the tumor with preservation of normal pituitary tissue have a quicker recovery of vision and visual field defects due to minimal manipulation of the optic nerves and chiasm. Limitation of transsphenoidal approach is macroadenoma with significant lateral and supra seller extension. Tumor consistency is also a limitation; where soft one is easily resectable, about 10% of pituitary macroadenomas are fibrous and have increased consistency; hard consistency need more extensive approach [12,13]. Currently, MRI is the examination of choice for sellar and parasellar pathologies due to its superior soft tissue definition, multiplanar capability and lack of ionizing radiation. In addition, MRI also provides useful information about the relationship of the gland with adjacent anatomical structures and it is the mainstay of diagnosis, surveillance, planning medical or surgical strategy and assessment of response to treatment [14–19]. Our study suggest that DW MR imaging can be used to determine the consistency of the pituitary macroadenomas as a predictive method of successful transsphenoidal surgery, this can be obtained by correlation between tumor cellularity and ADC maps where ADC values are inversely proportional to the tumor cellularity; tumors with higher cellularity (soft in consistency) have lower ADC values (see Fig. 3) and those with low cellularity (hard in consistency) have higher ADC values (see Fig. 2). In our patients, heterogeneous signal intensities were detected in DWI and ADC maps. According to surgical opinion about the macroadenomas consistency, the majority of cases (60%) were of soft consistency and we detected low ADC values on their ADC maps. other group (20% of patients) was described surgically as intermediate in consistency shows slightly higher ADC values than the soft group with some overlap between ADC values of the two groups, while the hard consistency (20%) is noted to have high ADC values (more than the other groups). Both soft and intermediate groups were managed successfully by endoscopic transsphenoidal approach, while the hard group wasn’t completely resectable by the same approach and needed further transcranial surgery.
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Fig. 1. MRI study of the sella shows large sellar mass that extends suprasellar abutting the optic chiasm with invasion of the sphenoid sinus displaying isointense tumor tissue compared to normal brain tissue on both axial T2WI (A) and Coronal T1WI (B) while appears as hyperintense lesion on DW imaging (C) with ADC map (b = 1000) showing decreased ADC value of the tumor tissue measuring (0.8014) 10 3 mm2/s. Tumor consistency was described as intermediate in consistency at surgery and was removed through endonasal transsphenoidal approach by curettage.
According to our study, we considered a cutoff value of 1 mm2/ sec for ADC maps for differentiation between resectable macroadenomas by aspiration through transsphenoidal approach (soft and intermediate consistency) and the irresectable ones (hard consistency). Our study was in accordance to Pierallini et al. 2006 their studies considered an ADC value of 1.0 10 3 mm2/s as a cutoff value to differentiate macroadenomas that are liable to be managed by aspiration from the others. Also, our study was in accordance to Pierallini et al. [20] studies in Mean ADC map values for all studied patients with pituitary macroadenomas was (0.7063) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (1.16) 10 3 mm2/s. The mean ADC value of those of soft consistency (n = 12) was (0.54) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (0.78) 10 3 mm2/s. The mean ADC value of those of an intermediate consistency (n = 4) was (0. 82) 10 3 mm2/s; ranging from (0.75) 10 3 mm2/s to (0.90) 10 3 mm2/s. The mean ADC value of patients with hard macroadenomas (n = 4) was (1.11) 10 3 mm2/s; ranging from (1.05) 10 3 mm2/s to (1.16) 10 3 mm2/s. Pierallini et al. [20] found in study performed on twenty-two patients with pituitary macroadenomas that ADC values are decreased in macroadenomas with increased cellularity. This was supported histologically where the hard macroadenomas on surgery with high ADC values, showed low cellularity with more fibrous extracelulear matrix where adenomas with a soft consistency showed higher cellularity, scant fibrous stroma and lower ADC values.
They correlated collagen contents histologically with ADC values and diffusion manner; lower ADC values correlated to low collagen contents and soft consistency. Our results appear to be disagree with those of Suzuki et al. [21] as they found that two tumors (one soft and one intermediate) had ADC values greater than 1.0 10 3 mm2/s and mean ADC value of the intermediate consistency group was slightly lower than that of the soft group with ADC values of no significant difference between the two the groups. The explanation of the disagreement between findings of Suzuki et al. [21] and Pierallini et al. is completely unknown but using a different DWI techniques (line scan DWI in Pierallini et against EPWI in Suzuki et al. can be taken in consideration as ADC values could vary with different DWI techniques due to the artifacts which are highly available for pituitary macroadenomas from air sinuses and surrounding bones. However, other factors may also be involved so further studies should be carried out using different DWI techniques to clarify this relationship. Boxerman et al. [22] considered ADC values of DWI as a reflection of structural integrity and microscopic components of the solid macroadenoma better than does the T2WI signal intensity with linear relationship between ADC values and resectability; the higher ADC values correspond to higher resectability. In our study, we disagree with Boxerman et al. [22] in the linear relationship between ADC values and resectability of the macroadenoma, as we detected in our study inverse relation between resectability and ADC values (ADC values >1 had lower resectability rate than those with ADC values <1).
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Fig. 2. MRI study of the sella shows a large sellar mass with supra-sellar and parasellar extension reaching/compressing the 3rd ventricle with right cavernous sinus invasion displaying avid homogenous enhancement of the tumor tissues in coronal T1WI post contrast (A) with evident invasion of the sphenoid sinus in sagittal T1WI (B), ADC map (b = 1000) showing increased ADC value of the tumor tissue measuring (1.160) 10 3 mm2/s. Tumor consistency was described as hard in consistency at surgery and was removed through transcranial surgery with recommendation for further endoscopic transsphenoidal surgery for residual.
Fig. 3. MRI study of the sella shows a sellar mass with area of necrosis and heterogenous enhancement, inferiorly the lesion invading the sphenoid sinus in both coronal T1WI (A) and sagittal T1WI (B) while displaying hyperintense signal in DWI (C) with increased ADC value on ADC map (b = 1000) that measures (1.160) 10 3 mm2/s. Tumor consistency was described as soft in consistency at surgery and was removed through transsphenoidal approach by suction.
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We also detected no significant relation between pituitary macroadenoma consistency and T2WI signal intensities of our three studied groups where soft pituitary macroadenomas showed hyperintense (8 cases), isointense (3 cases) and hypointense (1 case) signals on T2WI while in the intermediate group; two cases were hyperintense, one was isointense and one was hypointense. The hard group showed hyperintense signal on (3 cases) and isointense signal on one case. Yamamoto [23] found that pituitary macroadenoma consistency had correlated to its collagen contents as soft macroadenoma had low collagen contents and few reticulin fibers and this agree with our study. Romano et al. [24] found in their study that there is correlation between post contrast T1WI signal intensity and pituitary macroadenoma consistency as early enhancement inversely correlated with percentage of fibrosis and perivascular fibrosis and these findings correlate with the soft components of the tumor. Our study did not coincide with this study in correlation between post contrast enhancement manner and consistency as we detected no relation between them; we found variable patterns of enhancement in each group. 4.1. Several hypotheses can support our results histologically First, the decrease in ADC values can be explained by increased cellularity with reduction of cytoplasmic contents and high nucleus to cytoplasm ratio leading to restriction in water diffusion as seen in soft consistency. Second, the increase in ADC values can be explained by decreased cellularity with increase in cytoplasmic contents and low nucleus to cytoplasm ratio leading to more free water diffusion as seen in hard consistency. The previously mentioned hypotheses were supported histologically as pituitary macroadenomas which described as soft in consistency at surgery and had lower ADC values on MR imaging were more cellular with scanty fibrous stroma while those described as hard in consistency at surgery and had higher ADC values were less cellular (with smaller cells) and more fibrous. 4.2. However there are some limitations of our study First, histopathological quantitative analysis of fibrous contents of the tumor is not so accurate with lack of a quantitative analysis of extracellular space and of nucleus-to-cytoplasm ratio; because it was difficult with suction through transsphenoidal approach to preserve intact tissue architecture of the entire tumor tissues. Second, the incidence of hard adenomas was low so it was difficult to collect enough number of that group being perfectly assessed. And finally, we compared the quantitative values of ADC maps with subjective assessment of tumor consistency by the neurosurgeon so tumor consistencies could be assessed differently with many neurosurgeons. 5. Summary and conclusion The cut off value of ADC of 1 10 3 mm2/s can be used to differentiate between pituitary macroadenomas liable to aspiration (soft and intermediate consistency) against those not liable to aspiration (hard consistency). ADC values of pituitary macroadenomas of the soft and intermediate consistency were <1 10 3 mm2/s and they were successfully managed by endoscopic transsphenoidal approach; suction or suction and curettage. While, the ADC values of the hard consistency were more than 1 10 3 mm2/s and they could not be managed by the transsphenoidal approach and needed further transcranial procedure.
Our study found correlation between ADC values of DWI and tumor consistencies and so; we recommend inclusion of DWI and ADC maps in routine pre-operative imaging of pituitary macroadenomas which is valuable in pre-operative assessment of the tumor consistency and very important in planning of the appropriate surgical approach. Finally, recent studies show the added value of diffusion tensor imaging DTI and fiber tracking for enhanced visualization of the optic chiasm which improves surgical planning for patients with sellar region tumors. So, we recommend further study with DTI.
Conflict of interest The authors declared that there is no conflict of interest.
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Original Article
Role of diffusion weighted magnetic resonance imaging DW-MRI in choice of the surgical approach for pituitary macroadenoma resection Mohamed Alhousini Alashwah a,⇑, Mohamed A. Moharram a, Amira S. Allakany b a
Radiodiagnosis Department, Faculty of Medicine, Tanta University, Tanta, Egypt Damanhur General Hospital, Egypt
b
a r t i c l e
i n f o
Article history: Received 2 June 2017 Accepted 2 August 2017 Available online xxxx Keywords: Pituitary macroadenoma Diffusion weighted magnetic resonance imaging DW MRI
a b s t r a c t Background and purpose: Consistency of pituitary macroadenoma is a crucial information for neurosurgeons. We aimed to assess the role of DW-MRI as non invasive imaging modality in predicting the tumour consistency of pituitary macroadenoma. Materials and methods: Twenty patients with pituitary macroadenoma underwent conventional MR imaging sequences, pre contrast, post contrast MRI and diffusion weighted MRI with ADC map. The tumour consistency was determined both macroscopic by neurosurgeons and microscopic by histopathologists. Results: Our study included 12 soft, 4 intermediate and 4 hard tumours. The tumour consistency and the collagen contents were correlated with diffusion and ADC values. The mean ADC value of patients with soft tumours was 0.54 10 3 mm2/s while for intermediate tumour was 0.82 10 3 mm2/s and for hard tumours was 1.11 10 3 mm2/s. Soft and intermediate consistency tumours were successfully managed by endoscopic transsphenoidal approach; suction and curettage. While, hard tumours could not be managed by the transsphenoidal approach and needed further transcranial procedure with sensitivity 95% and specificity 95%. Conclusion: DWI-MRI is a useful tool to predict the pituitary macroadenoma consistency and the suitable surgical approach for resection. Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
1. Introduction The pituitary gland is the master gland of the body because it controls most of the body’s endocrine functions by means of the hypothalamic-pituitary axis [1]. Pituitary macroadenomas are common seller space occupying lesions greater than 10 mm in diameter and they are benign proliferation of cells of the anterior lobe of the pituitary gland. The clinical presentation depends primarily on whether they are functioning (secretory) or nonfunctioning (non-secretory), those nonfunctioning are more common. The first signs and symptoms produced by non-secretory macro adenomas are related to mass effect. Macroadenomas usually extend beyond the sella with enlargement of the Sella, the most common pattern is supra seller extension [2].
Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ⇑ Corresponding author. E-mail address: [email protected] (M.A. Alashwah).
ADC value (apparent diffusion coefficient) is a measure of the magnitude of diffusion of water molecules within the tissues and is calculated using different b values (B value measures the degree of diffusion weighting) (0–1000 s/mm2). DW MR imaging can be used to determine the consistency of the pituitary macroadenomas that cannot be obtained by conventional MR images, this can be obtained by correlation between tumor cellularity and ADC values where ADC values are inversely proportional to the tumor cellularity; tumors with higher cellularity have lower ADC values. ADC value of lesser than 1 will have highly successful transsphenoidal approach, limitation of transsphenoidal approach is macro adenoma with significant lateral and supraseller extension. Tumor consistency can also be a limitation; where soft one is easily resectable, about 10% of pituitary macro adenomas are fibrous and have increased consistency; hard consistency need more extensive approach [3]. Correlation between tumor cellularity and ADC values can be used preoperatively to determine the suitable surgical approach whether using the recent endoscopic transsphenoidal technique
https://doi.org/10.1016/j.ejrnm.2017.08.001 0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Alashwah MA et al. . Egypt J Radiol Nucl Med (2018), https://doi.org/10.1016/j.ejrnm.2017.08.001
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M.A. Alashwah et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2018) xxx–xxx
as minimally invasive procedure compared to transcranial approach [3]. Preoperative evaluation of pituitary macroadenoma tumor consistency is important for neurosurgery to decide the appropriate type of surgery to use; whether transsphenoidal or transcranial approach, as those tumors with soft consistency are easily removable by suction through the transsphenoidal approach while the more fibrous; hard ones are difficult to be properly removed by suction and curettage through the same technique but indicate using the transcranial approach. Thus, we aimed to assess the role of Diffusion weighted MR imaging (DWI) in prediction of the tumor consistency of pituitary macroadenomas to help in proper surgical planning, and decreasing the risk of incomplete excision and the possibility of recurrence [4].
2.3. Surgery All patients with pituitary macro adenoma had received surgical resection of the macro adenoma using the transsphenoidal approach. At surgery, the neurosurgeon who was blinded to findings of DW imaging and ADC values of the cases, had assessed the macro adenomas consistency and classified them to three groups; soft, intermediate and hard in consistency. The soft macro adenomas were easily removed by suction, the intermediate group was removed with difficulty by suction or curettage and the hard group couldn’t be removed by suction and the surgeon recommended for further transcranial surgery for them. 2.4. Post-operative histopathology
2. Patients and methods This study was carried out on twenty patients who were suspected to have pituitary macroadenoma on clinical basis and referred from neurosurgery departments to MRI unit of Tanta University and other private centers and proved histopathologically later. Our study protocol was explained to our patients and informed consent was obtained. 2.1. For all patients the following were done Careful history taking and clinical examination which includes: Name, sex, age, marital status and symptoms & signs due to: AIncreased intracranial pressure (headache, vomiting) B-Visual apparatus disturbances (decreased visual acuity, blurring of vision) C-Hormonal disturbances (acromegaly, Cushing disease, amenorrhea, infertility, and galactorrhea) D-Cranial nerve palsies. 2.2. Imaging and image analysis: (pre-operative MRI) All MR images were acquired on Toshiba and Philips 1.5 T, closed configuration. Patient position is supine, to obviate head mal-rotation; the patient head was positioned in a vacuum pillow. Coil configuration is head coil. – The following protocol was used for all patients: I. Conventional MRI (c MRI): Non contrast axial, coronal, and sagittal T1WIs: Repetition time (TR):550 m/s. An echo time (TE):15 m/s. Field of view (FOV):250 mm. Acquisition matrix (ACQ): 95 120. Section thickness: 3 mm. Inter slice gap: 0.3 mm. Flip angle (FA): 90° Axial T2 WI : TR: 4844 m/s, TE: 110 m/s, FOV: 250 mm, ACQ: 184 256, slice thickness: 5 mm, inter slice gap: 1 mm Post Contrast Coronal T1WI: By administration of gadolinium 0.1 mm/ kg body weight. TR: 550 m/s, TE: 15 m/s, FOV: 250 mm, ACQ: 120 120, slice thickness: 3 mm, inter slice gap: 0.3 mm II. Diffusion weighted MR image (DWI) & ADC maps Prior to contrast agent administration, breath hold and DW images were done with single shot, spin-echo, and echo planner sequence as the following: TR: 2460–3690, TE: 70.72, ACQ: 108 108, section thickness: 6 mm, inter slice gab: 1 mm, B value: 0, 500, 1000 s/mm2. ADC maps were calculated automatically and ADC values were measured by using circumferential ROI in solid appearing portions of macro adenomas and excluding cystic and hemorrhagic areas where b-value 0, 500, 1000 sec/mm2.
For confirmation of the consistency of the macro adenomas which obtained by the pre-operative ADC values; histopathological examination was done for all patients through: A-Routine processing using haematoxylin and eosin (H.E.) stain. B-Examination of collagen percentage by Masson trichrome staining. C-Detection of reticulin content by Reticulin stain. Collagen content (+): the extracellular matrix accounts for less than 5% of the stained tissues. Collagen content (++): the extracellular matrix accounts for 5–15% of the stained tissues. Collagen content (+++): the extracellular matrix accounts for more than 15% of the stained tissues. 2.5. Statistical analysis of the data Data were fed to the computer and analyzed using IBM SPSS software package version 20.0. Qualitative data were described using number and percent. The Kolmogorov-Smirnov test was used to verify the normality of distribution. Quantitative data were described using range (minimum and maximum), mean, standard deviation and median. Significance of the obtained results was judged at the 5% level. The used tests were: F-test (ANOVA): For normally quantitative variables, to compare between more than two groups. Post Hoc test (LSD): for pairwise comparisons. Roc curve, sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) to detect the cut off value and accuracy of ADC maps to determine macro adenomas consistency and resectability. 3. Results Twenty patients were included in the current study; composed of 10 males and 10 females, they were ranging in age from 19 years to 57 years, with a mean age of 38.40 years. According to surgical opinion of tumor consistency and diffusion weighted magnetic resonant imaging and ADC maps analysis; the pituitary macroadenomas were classified to soft, intermediate and hard groups. The mean ADC values of the adenomas were found as the following: (Table 1) The mean ADC value of all patients (n = 20) was (0.7063) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (1.16) 10 3 mm2/s. The mean ADC value of patients with soft macroadenomas (n = 12) was (0.54) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (0.78) 10 3 mm2/s. The mean ADC value of patients with intermediate macroadenomas (n = 4) was (0.82) 10 3 mm2/s; ranging from (0.75) 10 3 mm2/s to (0.90) 1 0 3 mm2/s. The mean ADC value of patients with hard macroadenomas (n = 4) was (1.11) 10 3 mm2/s; ranging from (1.05) 10 3 mm2/s to (1.16) 10 3 mm2/s.
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M.A. Alashwah et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2018) xxx–xxx Table 1 Comparison between the three studied groups according to ADC value of DW MR imaging. Soft (n = 12)
Intermediate (n = 4)
Hard (n = 4)
F
p
ADC Min. Max. Mean SD. Median
0.34 0.78 0.54 0.14 0.53
0.75 0.90 0.82 0.05 0.83
1.05 1.16 1.11 0.03 1.11
36.957*
<.001*
Sig. bet. groups
p1 = .001*, p2 < .001*, p3 = .004*
F, p: F and p values for ANOVA test, Sig. bet. Groups was done using test (LSD) for ANOVA. * The results are statistically significant at p .05.
Table 2 Comparison between consistency of pituitary macroadenoma and signal intensity on T2WI. Consistency of macroadenoma
T2WI Iso intense
Hypo intense
Hyper intense
Total
Soft Intermediate Hard Total
3 1 1 5
1 1 – 2
8 2 3 13
12 4 4 20
The statistical analysis found that the three groups of pituitary macroadenomas, classified according to their consistency during surgery, shows dissimilarity in their mean ADC values (p .05). Relative statistical significance were indicated with p value as the following: o p1: p value for comparing between Soft and Intermediate p1 = .001, p2: p value for comparing between Intermediate and Hard p2 < .001, p3: p value for comparing between Soft and Hard. p3 = .004. Association between T2WI signal intensity and pituitary macroadenoma consistency are statistically significant only when p .05 (Table 2). According to successful rate of tumor resection by endoscopic transsphenoidal approach; pituitary macroadenomas were classified to resectable and non resectable groups. The resectable group was successfully managed by the transsphenoidal approach including the macroadenomas of soft and intermediate consistency (see Figs. 1 and 3) and had ADC value <1 10 3 mm2/s. The irresectable group could not be managed by transsphenoidal approach and needed surgery by transcranial approach and had ADC value >1 10 3 mm2/s. The cut off value between the resectable (soft and intermediate consistency) and the non resectable (hard consistency) was calculated statistically using ROC curve (receiver operating characteristic curve). The best accepted cut off value was = 1 10 3 mm2/s with sensitivity 95% and specificity 95% with area under curve (AUC) = 1. 4. Discussion Pituitary macroadenomas are common seller space occupying lesion and are generally regard as benign proliferation of cells of the anterior lobe of the pituitary gland. Pituitary macroadenomas are those greater than 10 mm in diameter. Pituitary surgery is indicated for excision, debulking or sellar decompression of mass lesions causing central nervous system pressure effects, visual compromise, compromised pituitary function. Urgent surgical decompression is required for acute pituitary hemorrhage, espe-
cially in patients who have developed sudden visual field compromise [5–9]. The used approach in this study was transsphenoidal endoscopic surgery or craniotomy (subfrontal or pterional). The choice of the suitable approach depends partly on an inner feature of the tumors; its consistency. Transsphenoidal endoscopic surgery is more suitable for the tumors with soft consistency which are easy to pull out, while craniotomy is suitable for harder ones. So, preoperative evaluation of tumor consistency can help to determine the best operative methods and treatments, which will not only increase the possibility of complete tumor removal, but also reduce recurrence rates [10,11]. The transsphenoidal endoscopic surgery are less invasive, provide direct access to the tumor with preservation of normal pituitary tissue have a quicker recovery of vision and visual field defects due to minimal manipulation of the optic nerves and chiasm. Limitation of transsphenoidal approach is macroadenoma with significant lateral and supra seller extension. Tumor consistency is also a limitation; where soft one is easily resectable, about 10% of pituitary macroadenomas are fibrous and have increased consistency; hard consistency need more extensive approach [12,13]. Currently, MRI is the examination of choice for sellar and parasellar pathologies due to its superior soft tissue definition, multiplanar capability and lack of ionizing radiation. In addition, MRI also provides useful information about the relationship of the gland with adjacent anatomical structures and it is the mainstay of diagnosis, surveillance, planning medical or surgical strategy and assessment of response to treatment [14–19]. Our study suggest that DW MR imaging can be used to determine the consistency of the pituitary macroadenomas as a predictive method of successful transsphenoidal surgery, this can be obtained by correlation between tumor cellularity and ADC maps where ADC values are inversely proportional to the tumor cellularity; tumors with higher cellularity (soft in consistency) have lower ADC values (see Fig. 3) and those with low cellularity (hard in consistency) have higher ADC values (see Fig. 2). In our patients, heterogeneous signal intensities were detected in DWI and ADC maps. According to surgical opinion about the macroadenomas consistency, the majority of cases (60%) were of soft consistency and we detected low ADC values on their ADC maps. other group (20% of patients) was described surgically as intermediate in consistency shows slightly higher ADC values than the soft group with some overlap between ADC values of the two groups, while the hard consistency (20%) is noted to have high ADC values (more than the other groups). Both soft and intermediate groups were managed successfully by endoscopic transsphenoidal approach, while the hard group wasn’t completely resectable by the same approach and needed further transcranial surgery.
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Fig. 1. MRI study of the sella shows large sellar mass that extends suprasellar abutting the optic chiasm with invasion of the sphenoid sinus displaying isointense tumor tissue compared to normal brain tissue on both axial T2WI (A) and Coronal T1WI (B) while appears as hyperintense lesion on DW imaging (C) with ADC map (b = 1000) showing decreased ADC value of the tumor tissue measuring (0.8014) 10 3 mm2/s. Tumor consistency was described as intermediate in consistency at surgery and was removed through endonasal transsphenoidal approach by curettage.
According to our study, we considered a cutoff value of 1 mm2/ sec for ADC maps for differentiation between resectable macroadenomas by aspiration through transsphenoidal approach (soft and intermediate consistency) and the irresectable ones (hard consistency). Our study was in accordance to Pierallini et al. 2006 their studies considered an ADC value of 1.0 10 3 mm2/s as a cutoff value to differentiate macroadenomas that are liable to be managed by aspiration from the others. Also, our study was in accordance to Pierallini et al. [20] studies in Mean ADC map values for all studied patients with pituitary macroadenomas was (0.7063) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (1.16) 10 3 mm2/s. The mean ADC value of those of soft consistency (n = 12) was (0.54) 10 3 mm2/s; ranging from (0.34) 10 3 mm2/s to (0.78) 10 3 mm2/s. The mean ADC value of those of an intermediate consistency (n = 4) was (0. 82) 10 3 mm2/s; ranging from (0.75) 10 3 mm2/s to (0.90) 10 3 mm2/s. The mean ADC value of patients with hard macroadenomas (n = 4) was (1.11) 10 3 mm2/s; ranging from (1.05) 10 3 mm2/s to (1.16) 10 3 mm2/s. Pierallini et al. [20] found in study performed on twenty-two patients with pituitary macroadenomas that ADC values are decreased in macroadenomas with increased cellularity. This was supported histologically where the hard macroadenomas on surgery with high ADC values, showed low cellularity with more fibrous extracelulear matrix where adenomas with a soft consistency showed higher cellularity, scant fibrous stroma and lower ADC values.
They correlated collagen contents histologically with ADC values and diffusion manner; lower ADC values correlated to low collagen contents and soft consistency. Our results appear to be disagree with those of Suzuki et al. [21] as they found that two tumors (one soft and one intermediate) had ADC values greater than 1.0 10 3 mm2/s and mean ADC value of the intermediate consistency group was slightly lower than that of the soft group with ADC values of no significant difference between the two the groups. The explanation of the disagreement between findings of Suzuki et al. [21] and Pierallini et al. is completely unknown but using a different DWI techniques (line scan DWI in Pierallini et against EPWI in Suzuki et al. can be taken in consideration as ADC values could vary with different DWI techniques due to the artifacts which are highly available for pituitary macroadenomas from air sinuses and surrounding bones. However, other factors may also be involved so further studies should be carried out using different DWI techniques to clarify this relationship. Boxerman et al. [22] considered ADC values of DWI as a reflection of structural integrity and microscopic components of the solid macroadenoma better than does the T2WI signal intensity with linear relationship between ADC values and resectability; the higher ADC values correspond to higher resectability. In our study, we disagree with Boxerman et al. [22] in the linear relationship between ADC values and resectability of the macroadenoma, as we detected in our study inverse relation between resectability and ADC values (ADC values >1 had lower resectability rate than those with ADC values <1).
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Fig. 2. MRI study of the sella shows a large sellar mass with supra-sellar and parasellar extension reaching/compressing the 3rd ventricle with right cavernous sinus invasion displaying avid homogenous enhancement of the tumor tissues in coronal T1WI post contrast (A) with evident invasion of the sphenoid sinus in sagittal T1WI (B), ADC map (b = 1000) showing increased ADC value of the tumor tissue measuring (1.160) 10 3 mm2/s. Tumor consistency was described as hard in consistency at surgery and was removed through transcranial surgery with recommendation for further endoscopic transsphenoidal surgery for residual.
Fig. 3. MRI study of the sella shows a sellar mass with area of necrosis and heterogenous enhancement, inferiorly the lesion invading the sphenoid sinus in both coronal T1WI (A) and sagittal T1WI (B) while displaying hyperintense signal in DWI (C) with increased ADC value on ADC map (b = 1000) that measures (1.160) 10 3 mm2/s. Tumor consistency was described as soft in consistency at surgery and was removed through transsphenoidal approach by suction.
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We also detected no significant relation between pituitary macroadenoma consistency and T2WI signal intensities of our three studied groups where soft pituitary macroadenomas showed hyperintense (8 cases), isointense (3 cases) and hypointense (1 case) signals on T2WI while in the intermediate group; two cases were hyperintense, one was isointense and one was hypointense. The hard group showed hyperintense signal on (3 cases) and isointense signal on one case. Yamamoto [23] found that pituitary macroadenoma consistency had correlated to its collagen contents as soft macroadenoma had low collagen contents and few reticulin fibers and this agree with our study. Romano et al. [24] found in their study that there is correlation between post contrast T1WI signal intensity and pituitary macroadenoma consistency as early enhancement inversely correlated with percentage of fibrosis and perivascular fibrosis and these findings correlate with the soft components of the tumor. Our study did not coincide with this study in correlation between post contrast enhancement manner and consistency as we detected no relation between them; we found variable patterns of enhancement in each group. 4.1. Several hypotheses can support our results histologically First, the decrease in ADC values can be explained by increased cellularity with reduction of cytoplasmic contents and high nucleus to cytoplasm ratio leading to restriction in water diffusion as seen in soft consistency. Second, the increase in ADC values can be explained by decreased cellularity with increase in cytoplasmic contents and low nucleus to cytoplasm ratio leading to more free water diffusion as seen in hard consistency. The previously mentioned hypotheses were supported histologically as pituitary macroadenomas which described as soft in consistency at surgery and had lower ADC values on MR imaging were more cellular with scanty fibrous stroma while those described as hard in consistency at surgery and had higher ADC values were less cellular (with smaller cells) and more fibrous. 4.2. However there are some limitations of our study First, histopathological quantitative analysis of fibrous contents of the tumor is not so accurate with lack of a quantitative analysis of extracellular space and of nucleus-to-cytoplasm ratio; because it was difficult with suction through transsphenoidal approach to preserve intact tissue architecture of the entire tumor tissues. Second, the incidence of hard adenomas was low so it was difficult to collect enough number of that group being perfectly assessed. And finally, we compared the quantitative values of ADC maps with subjective assessment of tumor consistency by the neurosurgeon so tumor consistencies could be assessed differently with many neurosurgeons. 5. Summary and conclusion The cut off value of ADC of 1 10 3 mm2/s can be used to differentiate between pituitary macroadenomas liable to aspiration (soft and intermediate consistency) against those not liable to aspiration (hard consistency). ADC values of pituitary macroadenomas of the soft and intermediate consistency were <1 10 3 mm2/s and they were successfully managed by endoscopic transsphenoidal approach; suction or suction and curettage. While, the ADC values of the hard consistency were more than 1 10 3 mm2/s and they could not be managed by the transsphenoidal approach and needed further transcranial procedure.
Our study found correlation between ADC values of DWI and tumor consistencies and so; we recommend inclusion of DWI and ADC maps in routine pre-operative imaging of pituitary macroadenomas which is valuable in pre-operative assessment of the tumor consistency and very important in planning of the appropriate surgical approach. Finally, recent studies show the added value of diffusion tensor imaging DTI and fiber tracking for enhanced visualization of the optic chiasm which improves surgical planning for patients with sellar region tumors. So, we recommend further study with DTI.
Conflict of interest The authors declared that there is no conflict of interest.
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