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Published online before print February 28, 2006, 10.1148/radiol.2391042176
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(Radiology 2006;239:181-186.)
© RSNA, 2006

Head and Neck Imaging

Sclerosis of the Pterygoid Process in Untreated Patients with Nasopharyngeal Carcinoma1

Deborah R. Shatzkes, MD, Daniel E. Meltzer, MD, Jane A. Lee, MD, James S. Babb, PhD, Nicholas J. Sanfilippo, MD and Roy A. Holliday, MD2

1 From the Department of Radiology, New York University Medical Center, New York, NY. From the 2004 RSNA Annual Meeting. Received December 22, 2004; revision requested February 23, 2005; revision received April 1; accepted April 25; final version accepted June 17. Address correspondence to D.R.S., Department of Radiology, St Lukes-Roosevelt Hospital Center, 1000 Tenth Ave, New York, NY 10019 (e-mail: DShatzkes{at}chpnet.org).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Purpose: To retrospectively evaluate the prevalence of pterygoid process sclerosis in patients with untreated nasopharyngeal carcinoma.

Materials and Methods: This retrospective HIPAA-compliant study was performed after the institutional review board deemed it to be exempt from review and patient informed consent. Contrast material–enhanced computed tomographic (CT) scans of the neck obtained in 31 patients (22 men, nine women; mean age, 42 years; age range, 27–68 years) with untreated nasopharyngeal carcinoma and in 31 control subjects (17 men, 14 women; mean age, 43 years; age range, 19–62 years) were evaluated independently by two neuroradiologists. The presence of sclerosis of the pterygoid process—defined as increased attenuation in the medullary cavity and/or thickening of the cortical bone—was assessed. Other findings noted included pterygoid process erosion, enhancing tumor adjacent to the pterygoid process, and CT evidence of parapharyngeal extension of the tumor. The data were evaluated by using generalized estimating equations based on a binary logistic regression model.

Results: The prevalence of pterygoid process sclerosis averaged for the two readers was 60% (37 of 62 subjects) among the patients with nasopharyngeal carcinoma but only 3% (two of 62 subjects) among the control subjects, indicating a highly significantly increased prevalence (P < .001) of this finding in the patients with nasopharyngeal carcinoma. The overall prevalences of pterygoid process erosion, parapharyngeal extension of tumor, and enhancing tumor adjacent to the pterygoid process were 27% (17 of 62 subjects), 47% (29 of 62 subjects), and 77% (48 of 62 subjects), respectively. Pterygoid process sclerosis was the sole skull base abnormality in 36% (11 of 31) of the patients with nasopharyngeal carcinoma.

Conclusion: Sclerosis of the pterygoid process, which was present in about half of the patients with untreated nasopharyngeal carcinoma, may reflect tumor proximity to or tumor invasion of the pterygoid process.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Nasopharyngeal carcinoma is a form of squamous cell carcinoma that is particularly prevalent among natives of southern provinces of mainland China and immigrants from these regions (1–4). Primary therapy is nonsurgical and involves either radiation therapy alone or a combination of radiation therapy and chemotherapy (5–8). For nasopharyngeal carcinoma, as for other malignancies, the American Joint Committee on Cancer has developed staging criteria that are useful in prognostication and as guidelines for patient treatment (9). Precise tumor mapping is essential in assigning the correct stage and in designing a radiation port that will encompass the full extent of disease. The latter issue has become increasingly important with the increasing availability of intensity-modulated radiation therapy (IMRT) and its tight confinement to the margins of disease (10–12).

Because nasopharyngeal carcinoma is relatively inaccessible at clinical examination, imaging has a vital role in tumor staging, particularly in defining the deep margins of disease. Involvement of the skull base is common and may manifest as permeative or erosive bone changes or perineural spread along foraminal pathways (1,13–18). We have observed an additional finding in untreated patients with nasopharyngeal carcinoma: sclerosis of the pterygoid process ipsilateral to the side of disease and occurring with or without other evidence of skull base involvement. Thus, the purpose of our study was to retrospectively evaluate the prevalence of pterygoid process sclerosis in patients with untreated nasopharyngeal carcinoma.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Nasopharyngeal Carcinoma and Control Patient Groups
This retrospective study, performed after our institutional review board deemed it to be exempt from review and patient informed consent, was compliant with all Health Insurance Portability and Accountability Act regulations. Contrast material–enhanced computed tomographic (CT) scans of the neck obtained in 31 consecutive patients (22 men, nine women; mean age, 42 years; age range, 27–68 years) with untreated nasopharyngeal carcinoma and in 31 consecutive control subjects (17 men, 14 women; mean age, 43 years; age range, 19–62 years) were evaluated independently by two attending neuroradiologists (D.R.S. and J.A.L., with 13 and 4 years experience interpreting head and neck images, respectively). All scans in both the nasopharyngeal carcinoma and the control groups were obtained between January 2000 and September 2003.

Patient charts were reviewed to identify any intercurrent diagnosis that might have resulted in a skull base abnormality. The diagnosis of nasopharyngeal carcinoma was made following biopsy, with undifferentiated carcinoma (World Health Organization type III) present in the majority (n = 25) of the 31 cases. The demographic data and tumor stages of the patients with nasopharyngeal carcinoma are summarized in Table 1. The control group consisted of patients who underwent CT scanning for benign processes unrelated to the skull base (Table 2).


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  		Table 1. Characteristics of Patients with Nasopharyngeal Carcinoma

 

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  		Table 2. Control Subject Diagnoses

 
Imaging and Evaluation
CT was performed by using helical scanners (CTi and HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis) and a multi–detector row scanner (LightSpeed QX/I; GE Medical Systems) and involved the acquisition of contiguous 3-mm transverse images that were reconstructed by using a soft-tissue algorithm and viewed by using both soft-tissue (window level, 70 HU; window width, 220 HU) and bone (window level, 150 HU; window width, 2500 HU) window settings. One hundred fifty milliliters of iopamidol (Isovue 300; Bracco Diagnostics, Princeton, NJ) was administered at a rate of 2 mL/sec through a 20- or 22-gauge venous angiographic catheter. In the nasopharyngeal carcinoma group, 11 image cases were viewed on film hard copies. The remaining cases in the nasopharyngeal carcinoma group and all of the control group cases were viewed on a picture archiving and communication system workstation monitor (EasyVision; Philips Medical Systems, Andover, Mass).

The presence of sclerosis—defined as increased attenuation in the medullary cavity and/or thickening of the cortical bone—of the pterygoid process, including the medial and lateral plates and their fused superior portion, was assessed. Other findings noted included pterygoid process erosion, enhancing tumor visible adjacent to the pterygoid process, and CT evidence of parapharyngeal extension of the tumor.

Statistical Analyses
Generalized estimating equations based on a binary logistic regression model were used to compare the nasopharyngeal carcinoma and control groups with respect to the prevalence of pterygoid process sclerosis; evaluate the association between pterygoid process sclerosis and presence of adjacent enhancing tumor; and assess differences between the readers in terms of the proportion of diagnoses positive for pterygoid process sclerosis, pterygoid process erosion, parapharyngeal invasion, or enhancing tumor adjacent to the pterygoid process. In each case, the dependent variable was the binary indicator of a positive diagnosis, the logistic regression model included reader and subject type (having nasopharyngeal carcinoma vs control) as fixed classification factors, and compound symmetry was used to model the correlation structure—that is, observations were considered to be correlated or independent when they were associated with the same or different subjects, respectively.

All statistical computations were performed by using SAS for Windows software, version 9.0 (SAS Institute, Cary, NC), and the results were deemed to be significant at the two-sided 5% comparison-wise significance level (ie, P < .05). Because of the relatively complex nature of generalized estimating equations analysis, no attempt to generate an exact significance level for the effect of any factor was made. Consequently, all P values are based on asymptotic approximations; given the relatively small sample size (n = 31), care must be given to their interpretation.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Nasopharyngeal Carcinoma Group
Pterygoid process sclerosis was seen in 16 (52%) of the 31 patients with nasopharyngeal carcinoma (Fig 1) by reader 1 and in 21 (68%) of these patients by reader 2 (prevalence averaged for two readers, 37 [60%] of 62 patients). The discrepancy between the readers' findings was not significant (P = .075). The overall prevalence of pterygoid process erosion (Fig 2), as averaged for the two readers, was 27% (17 of 62 patients); again, the difference between the readers was not significant (nine [29%] vs eight [26] of 31 patients; P = .31). Pterygoid process sclerosis was the sole skull base abnormality in 11 (36%) of the 31 patients with nasopharyngeal carcinoma.


Figure 1
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  		Figure 1a: Transverse bone window CT images obtained in two patients with nasopharyngeal carcinoma—(a) a 27-year-old man and (b) a 44-year-old man—show pterygoid process sclerosis (white arrow). Note the ipsilateral mastoid effusion (black arrow) in b.

 

Figure 1
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  		Figure 1b: Transverse bone window CT images obtained in two patients with nasopharyngeal carcinoma—(a) a 27-year-old man and (b) a 44-year-old man—show pterygoid process sclerosis (white arrow). Note the ipsilateral mastoid effusion (black arrow) in b.

 

Figure 2
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  		Figure 2: Transverse bone window CT image obtained in a 43-year-old man with nasopharyngeal carcinoma shows erosion (arrow) and sclerosis of the pterygoid process.

 
The diagnosis of parapharyngeal invasion (Fig 3) had an overall prevalence of 47% (29 of 62 patients), with no significant difference in findings between the two readers (14 [45%] vs 15 [48%] of 31 patients; P = .99). Enhancing soft tissue adjacent to the pterygoid process (Fig 4) had an overall prevalence of 77% (48 of 62 patients), with a significant difference between the two readers (22 [71%] vs 26 [84%] of 31 subjects; P = .042). There was a significant association (P = .006) between pterygoid process sclerosis and presence of adjacent enhancing tumor, with reader 1 believing both entities to be present concurrently in 15 (94%) of 16 patients with pterygoid process sclerosis and reader 2 believing both entities to be present concurrently in 17 (81%) of 21 patients with pterygoid process sclerosis. There was no significant difference (P > .25) between the readers with respect to the propensity to make coincident positive diagnoses of pterygoid sclerosis and adjacent tumor. Patient chart reviews revealed no intercurrent process that might have resulted in a central skull base abnormality.


Figure 3
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  		Figure 3: Transverse soft-tissue window CT image obtained in a 31-year-old woman with nasopharyngeal carcinoma shows clear invasion of the parapharyngeal space, as evidenced by enhancing tumor that is inseparable from the pterygoid musculature (arrow).

 

Figure 4
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  		Figure 4: Transverse soft-tissue window CT image obtained in a 57-year-old man with nasopharyngeal carcinoma shows nodular tumor (arrow) abutting the left pterygoid process.

 
Control Group
Pterygoid process sclerosis was detected in only one of the control subjects by both readers; thus, there was a highly significantly increased prevalence (P < .001) of this finding in the patients with nasopharyngeal carcinoma. The single positive case in the control group was that of a patient with a long-standing ipsilateral maxillary odontogenic infection.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Because the primary therapy for patients with nasopharyngeal carcinoma is nonsurgical, it is not possible to observe a direct pathologic correlation for the finding of pterygoid process sclerosis in these patients. It seems intuitive, however, that this finding, which is found ipsilateral to and is frequently demonstrably adjacent to enhancing tumor, would reflect the bone's response to the presence of nearby tumor. As such, an analogy to the finding of laryngeal cartilage sclerosis in squamous cell carcinoma of the larynx seems potentially useful. By using histopathologic correlation to CT findings, Munoz et al (19) found that the positive predictive value of sclerosis of the laryngeal cartilage for the detection of cartilaginous invasion was 46%, with tumor adjacent to the perichondrium in 11 of 12 cases and thus suggestive of imminent invasion. Becker et al (20) found that sclerosis was the most sensitive—although not the most specific—criterion for determining the presence of cartilaginous invasion (eg, as opposed to lysis or visible adjacent tumor). In patients with laryngeal squamous cell carcinoma, sclerosis has been thought to reflect local hypervascularity or humeral tumoral factors (19). Should this analogy be valid, pterygoid process sclerosis would indicate the presence of tumor invasion of or contiguity with the pterygoid process. According to the current staging criteria of the American Joint Committee on Cancer (9), pterygoid process bone invasion would indicate tumor stage T3 at least and thus stage III disease at least.

Alternatively, in those cases in which pterygoid process sclerosis might indicate tumor proximity without frank invasion, results of analyses of the anatomy of this region strongly suggest that parapharyngeal extension is present. The pharyngobasilar fascia forms the medial boundary of the parapharyngeal space (1,21–26) (Fig 5). This fascia arises from the posterior aspect of the medial pterygoid plate. Thus, it seems reasonable to assume that tumor proximity to the pterygoid process implies that invasion of the pharyngobasilar fascia is present or imminent.


Figure 5
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  		Figure 5: Schematic illustration of the relevant transverse anatomy of the suprapalatine parapharyngeal space. The heavy black outline indicates the position of the pharyngobasilar fascia. The cross-hatched areas are muscles.

 
In the American Joint Committee on Cancer recommendations for tumor staging of nasopharyngeal carcinoma, the presence of parapharyngeal space invasion has particular importance. In 1996, Chua et al (27) observed a higher rate of local tumor recurrence in patients who had parapharyngeal space invasion at the time of diagnosis. This finding resulted in the modification of tumor staging criteria so that stage T2 (ie, tumor extending to soft tissues of the oropharynx and/or nasal fossa) is now subdivided into stages T2a and T2b, indicating without evidence and with evidence of parapharyngeal extension, respectively (9).

Because paranasopharyngeal extension of nasopharyngeal carcinoma has been shown to be a clinically important negative prognostic factor, the recently closed (November 2005) Radiation Oncology Group protocol 0225, a phase II study evaluating the use of IMRT for the treatment of nasopharyngeal cancer, required that patients with stage T2b or more severe cancer receive chemotherapy in addition to radiation therapy (28). Thus, it has become particularly important for the interpreting radiologist to render an opinion regarding the presence of parapharyngeal invasion, because this area is inaccessible at clinical examination. When nasopharyngeal tumor is inseparable from the pterygoid musculature (which is in the masticator space), invasion of the masticator space and thus the intervening parapharyngeal space is highly likely (Fig 3). In many cases, however, the findings are more subtle. Sclerosis of the pterygoid process may prove to be a helpful finding in this often difficult determination. It should be noted, however, that only one patient in our study had early-stage (ie, T2a or lower) disease at presentation; thus, the practical clinical importance of this hypothesis is uncertain.

A more immediate use for the finding of pterygoid process sclerosis in nasopharyngeal carcinoma may be in treatment planning. The current state of the art in radiation therapy for nasopharyngeal carcinoma is IMRT (10–12). With this technique, the targeting of tumor and the sparing of normal tissue are maximized by using highly contoured radiation fields. These fields require very precise mapping of tumor margins. If one considers pterygoid process sclerosis as an indicator of tumor invasion of or tumor contiguity with the pterygoid process, then this structure should be included in the IMRT field.

The primary limitation of our study was the absence of histopathologic correlation for the finding of pterygoid process sclerosis in our population of untreated patients with nasopharyngeal carcinoma, for whom the primary therapy was nonsurgical. Another study limitation was related to our proposed analogy to laryngeal cartilage sclerosis in the setting of laryngeal carcinoma. The cartilage of the laryngeal skeleton, even when fully ossified, may be intrinsically different from the bone of the central skull base and thus may react differently to the presence of proximal tumor. The significant discrepancy between the two readers' determinations of the presence of enhancing soft tissue adjacent to the pterygoid process may have represented a third study limitation. At subsequent simultaneous review of the cases, we believed that we had not formulated criteria that were sufficiently coherent for this determination. This limitation, however, may reflect a more global difficulty in demarcating margins of disease by using soft-tissue findings rather than using the often more straightforward method of determining bone abnormalities.

In this study, we found sclerosis of the pterygoid process to be present in 60% of patients with untreated nasopharyngeal carcinoma. Although the cause of pterygoid process sclerosis is uncertain, we suggest that this abnormality may reflect tumor invasion of or tumor proximity to the pterygoid process. In lieu of histopathologic correlation, which is generally unavailable, longitudinal follow-up findings may help to support our postulates regarding the cause of pterygoid process sclerosis. For example, it may be informative to examine the relative tumor recurrence rate at the skull base in both patients with and those without sclerosis of the pterygoid process. Until such data can be accrued, we propose that the reasonable likelihood of present or imminent skull base invasion be considered in tumor staging and in the formulation of IMRT fields when pterygoid process sclerosis is present in patients with untreated nasopharyngeal carcinoma.


   FOOTNOTES
 

Abbreviations: IMRT = intensity-modulated radiation therapy

2 Current address: New York Eye and Ear Infirmary, New York, NY Back

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, D.R.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, D.R.S., D.E.M.; clinical studies, D.R.S., J.A.L.; statistical analysis, J.S.B.; and manuscript editing, D.E.M.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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