Reliability of Ultrasonography in differentially diagnosing periapical lesions of endodontic origin in comparison with Intra-oral periapical radiography and Cone-beam computed tomography: An in vivo study.

Background: Periapical granuloma, radicular cyst, and periapical abscess represent periapical changes of frequent occurrence. Addressing this diagnostic dilemma is a matter of great concern, as it aids in governing the treatment planning and predicting its outcome. Aim: To evaluate the comparative accuracy of ultrasonography (USG), intraoral periapical (IOPA) radiography, and cone-beam computed tomography (CBCT) in differentially diagnosing periapical lesions of endodontic origin.
Methods: Thirty-five patients having periapical lesions associated with anterior teeth requiring endodontic therapy were included in the study. The lesions were analyzed using IOPA radiographs, CBCT scans, and USG with color Doppler (CD). Periapical surgery ensued and enucleated tissue samples were subjected to histopathological analysis. To evaluate the accuracy, diagnoses made by each of the three modalities were compared with the gold standard histopathological reports, and the diagnostic accuracy, sensitivity, and specificity of each were calculated. Statistical Analysis: Cohen kappa (κ) was used for interrater reliability, and Pearson's contingency coefficient (C) was used for correlating findings of USG with histopathology.
Results: USG showed good concordance with histopathological findings (contingency coefficient: 0.664). It also showed a higher accuracy rate compared to IOPA radiography and CBCT in differentially diagnosing periapical lesions.
Conclusion: USG with CD holds the potential to be used as a noninvasive adjunct in periapical diagnostics. Copyright:

INTRODUCTION

Periapical lesions of endodontic origin are majorly produced by an inflammatory response at the root apices of teeth with nonvital pulp tissue, which can be mainly ascribed to the imbalance between microbial factors and host defenses.[1]

As it is said that the journey to a definitive treatment lies in a correct diagnosis, the crucial element for establishing the fact of whether the periapical pathology will heal or not after a nonsurgical endodontic therapy would involve a pretreatment identification of the nature of the lesion. Although a histopathological examination remains the gold standard in this context, a nonionizing and minimally invasive modality is desirable.

In routine practice, intraoral periapical (IOPA) radiographs are generally used in conjunction with clinical examination to diagnose periapical pathoses, but their accuracy is relatively low (47.6%–54.3%) as proved by various studies owing to its two-dimensional representation of the lesion.[23] The advent of cone-beam computed tomography (CBCT) has enabled three-dimensional visualization of oral and maxillofacial structures. In a recent study, CBCT has shown a higher diagnostic accuracy in detecting complex endodontic pathoses, especially dehiscence and fenestration of cortical plate compared to conventional radiography; however, its accuracy in detecting a periapical disease remains moderate (61%–76%.).[4567] Ionizing radiations, higher cost, and subjectiveness in the interpretation of the number of greyscale values in the images are its limitations.[89]

Cotti et al. pioneered the use of ultrasonography (USG) in differentially diagnosing a periapical lesion of endodontic origin.[10] It has proved to be a highly accurate (76.7%–100%) tool in periapical diagnostics.[101112] Of late, it has proved to be even beneficial in assessing the bone healing postoperatively and also in tracing sinus tracts of endodontic origin.[1314] It is based on the phenomenon of sound waves reflection at the interface between two tissues having a different acoustic impedance. Diagnostic ultrasound utilizes a high-frequency sound wave (1–20 MHz), which is generated and transmitted into the body by a transducer containing piezoelectric crystals which transform electrical signals into sound vibrations and vice versa, later processed by the system's computer to produce the sonographic image. The sonographic images are identified in terms of echoes as hypoechoic (low echo intensity), hyperechoic (high echo intensity), and anechoic (lacking echo intensity) images.[12]

Given the above observations, this study was premeditated to compare the usefulness and diagnostic validity of USG with that of IOPA radiography and CBCT in the evaluation of periapical lesions.

METHODS

Thirty-five patients with a periapical lesion in the anterior region of either arch diagnosed by their clinical signs, symptoms, and radiographic findings who attended the outpatients' section of the department of conservative dentistry and endodontics of the dental college and hospital were selected for the study. Only those patients who had a lesion size measuring 5 mm or more in diameter on IOPA radiographs[1516] and were reluctant to accept the attempt of the nonsurgical method due to constraints of long-term follow-ups were included in the study. The study protocol was approved by the institutional ethics committee, and informed consent was obtained from all selected patients under the Helsinki Declaration.

Intraoral periapical examination

Periapical radiolucency was first imaged by the bisecting angle technique with a dental X-ray unit (X-Mind, Satelec) with 68 kVp, 8 mA, 2 mm filtration, and E-speed film (No: 2, 31 mm × 41 mm) manufactured by Carestream Dental®.

A differential diagnosis of periapical lesions was made based on the criteria suggested by Lalonde and Luebke.[17]

Periapical cyst: Well-defined periapical radiolucency with sclerotic border measuring >1.6 cm in diameter [Figure 1 (IA)]

Figure 1

(I) Periapical cyst: (A) IOPA radiograph, (B) (a-d) CBCT views (c) ultrasonogram (arrow showing posterior edge enhancement) (d) histopathology section) (×10) (arrow showing arcading epithelium pattern. (II) Periapical granuloma: (A) IOPA radiograph (b) (a-d) CBCT views (c) ultrasonogram (arrow showing vascularity on Doppler) (d) Histopathology section (×10). (III) Periapical abscess: (a) IOPA radiograph (B) (a-d) CBCT views (C) ultrasonogram (arrow showing mixed echotexture) (D) histopathology section (×10). IOPA: Intraoral periapical, CBCT: Cone-beam computed tomography

Periapical granuloma: Periapical radiolucency measuring <1.6 cm in diameter [Figure 1 (IIA)].

Cone-beam computed tomography examination

Following this, the selected patients were scanned by CBCT with SkyView CBCT® Scanner (My-Ray Dental Imaging, Imola, Italy). An attempt was made to keep the field of view as narrow as possible (7 cm × 7 cm × 7 cm) to limit the radiation exposure as per the ALARA (as low as reasonably achievable) principle. The scanner was operated at 90 kV and 10 mA with gray levels of 4096 (12 bit). The digital images were then exported from Skyview CBCT Scanner™ and imported into iRYS viewer software, and the diagnosis was based on the following criteria, suggested by White and Pharoah, which were simplified and statistically ratified by Guo et al. and were also followed in the study of Chanani and Adhikari.[151618]

Six radiologic diagnostic criteria of the periapical cyst which were looked for in CBCT scan of each lesion were[18] [Figure 1 (IB and II-B)]:

Location: Apex of the involved tooth

Distinct corticated border

Shape of lesion: Curved or circular

Internal structure of the lesion: radiolucent

Displacement and resorption of the roots of adjacent teeth

Presence of cortical plate perforation.

After evaluating the lesion based on the six predefined criteria, a diagnosis of the cyst was reported if ≥4 positive findings were present, and if it was <4, it was suggestive of a granuloma.[1516]

Ultrasound examination

The lesion was then subjected to a USG examination using an E-CUBE 8® machine (Alpinion Medical Systems, Korea) with a linear, multifrequency (7.5–10 MHz), and an endocavitary USG probe (frequency: 3–10 MHz) at the Department of Radiodiagnosis of an adjoining reputed medical college and hospital. An experienced sonologist obtained transverse and longitudinal scans by placing the probe extraorally overlying the apical area of the affected teeth. Color Doppler (CD) was then applied to assess the vascularity of the lesion [Figure 2].

Figure 2

(a) Ultrasound machine, (b) endocavitary ultrasound probe, (c) linear ultrasound probe, (d) ultrasonography examination on maxillary anterior region: (I) transverse scan, (II) longitudinal scan, (e) ultrasonogram showing: (I) transverse scan, (II) longitudinal scan with color Doppler

According to the echogenicity and other relevant features, the pathoses were outlined according to the following criteria: [1012]

Cystic lesion: A well-contoured hypoechoic area surrounded by reinforced bony walls, filled with fluid and with no indication of internal vascularization on CD examination [Figure 1 (IC)]

Granuloma: A poorly demarcated hypoechoic area, showing rich vascularity on CD examination [Figure 1 (IIC)]

Mixed lesion/abscess: Predominantly hypoechoic area with some focal anechoic area, maybe displaying vascularity in some areas on CD examination [Figure 1 (IIIC)].

The lesions were evaluated concurrently by two blinded observers. For interrater reliability, evaluations of each observer were tested through Cohen's Kappa (κ) (κ ≥0.81 – almost perfect; 0.61≤ κ <0.80 – substantial; 0.41≤ κ <0.60 – moderate; 0.21≤ κ <0.40 – fair; and κ <0.20 – poor). Following which, endodontic therapy was initiated. Subsequently, after proper investigations, periapical surgery was performed. The enucleated tissue sample was sent for histopathological evaluation.

The findings of IOPA radiographs, CBCT, and USG were cross-tabulated with histopathological reports as the gold standard. The values of sensitivity, specificity, and diagnostic accuracy were obtained [Tables 1 and 2].

Table 1

Diagnoses by the three modalities (intraoral periapical radiography, cone-beam computed tomography imaging, and ultrasonography) versus gold standard histopathology diagnosis

Diagnostic modality	Histopathological diagnosis
	Cyst	Granuloma	Abscess
IOPA R
Cyst	17*	7	0
Granuloma	6	2*	3
CBCT
Cyst	21*	7	2
Granuloma	2	2*	1
USG
Cyst	23*	4	2
Granuloma	0	5*	0
Mixed lesion/abscess	0	0	1*

*Concordant findings with HP. IOPA R: Intraoral periapical radiograph, CBCT: Cone-beam computed tomography, USG: Ultrasonography, HP: Histopathology

Table 2

Diagnostic validity of the three modalities for different lesions

Lesion type	Diagnostic modality
	IOPA R		CBCT		USG
	Cyst (%)	Granuloma (%)	Cyst (%)	Granuloma (%)	Cyst (%)	Granuloma (%)	Mixed lesion/abscess (%)
	Sensitivity	73.91	22.20	91.30	22.20	100	55.50	33.30
Specificity	41.67	65.38	25.00	88.46	50	100	100
Diagnostic accuracy	62.86	54.28	68.57	71.43	82.85	88.57	94.28

IOPA R: Intraoral periapical radiograph, CBCT: Cone-beam computed tomography, USG: Ultrasonography

The collected data were then subjected to statistical analysis using SPSS Statistics for Windows, version 16.0 (SPSS Inc., Chicago, IL, USA) and using the Pearson contingency coefficient (C) to corroborate the findings of USG with histopathology. The alpha level was set to P < 0.05.

RESULTS

The study population comprised a total of 35 patients (males: n = 23, 65.7%; females: n = 12, 34.3%) ranging in age between 14 and 50 years (mean age was 26.57 ± 9.20 years).

Kappa analysis revealed an almost perfect interobserver reliability in the case of IOPA radiographs (κ =0.87) and USG evaluation (κ =0.93) and a substantial agreement in the case of CBCT scans (κ =0.8).

IOPA radiographs were able to diagnose cystic lesions with 62.8% accuracy and granuloma with 54.29%. CBCT could diagnose cystic lesions with 68.57% accuracy and granuloma with 71.43%. USG technique was seen to diagnose cystic lesions with 82.85% accuracy and granuloma with 88.57% and for abscess; the accuracy was 94.28% [Table 2].

The Pearson's contingency coefficient (C) was found to be 0.664 with P < 0.001, which shows that the association between the histopathological diagnoses and USG is highly significant.

On comparison of the diagnoses of IOPA radiography, CBCT, and USG with histopathology, it indicated that USG is a more accurate tool in differentially diagnosing a periapical lesion than IOPA radiography and CBCT.

DISCUSSION

Nair had reported that surgical intervention is a necessity in the management of a true periapical cyst.[1] However, recently, Ricucci et al. have proposed that some periapical cysts can heal after root canal treatment as no difference exists between a true and a pocket cyst.[919] However, in that article, the initial diagnosis was made using only radiographic images. Furthermore, the assumption that a true cyst might heal after nonsurgical endodontics can be only authenticated through outcome-based studies and literature is sparse in this regard. Therefore, an accurate preoperative diagnosis of a periapical lesion is still necessary.[79]

Prevention of inconsistent application of periapical surgery based on unsupported radiographic diagnosis and research into alternative noninvasive and nonionizing imaging techniques is necessary. All of these formed the central objective of this study. Moreover, only a few studies on a very small population have been published in the literature reporting the use of USG in diagnosing periapical lesions. Furthermore, to the best of the authors' knowledge, no study with such a larger sample size has been conducted to compare the diagnostic accuracy of USG with IOPA radiographs and CBCT in diagnosing a periapical lesion of endodontic origin preoperatively.

After proper evaluation, it was found that IOPA radiographs correctly diagnosed a total of 19 lesions (17 cysts and 2 granulomas); CBCT diagnosed 23 lesions (21 cysts and 2 granulomas), whereas USG identified the nature and contents of 29 lesions (23 cysts, 5 granulomas, and 1 mixed lesion/abscess) accurately [Table 1].

In the present study, the accuracy of USG in diagnosing cyst was found to be 82.86%, which harmonized with the study of Prince et al.[20] On the other hand, Cotti et al. and Gundappa et al. found an accuracy of 100%, who studied on a relatively smaller population.[1012] For granuloma, it was found to be 88.5%, and for abscess, it was 94.28%. Both findings go close to a study by Saeed et al.[21]

The lack of total concordance of the USG findings with the histopathology reports in the diagnosis can be attributed to the inability of an in toto removal of the lesion, along with the resected root tip/root tips in few cases, thereby preventing the true reflection of characteristics of the enucleated lesion. The lower values of specificity in diagnosing a cyst and low sensitivity values in diagnosing a granuloma and an abscess in the present study can be attributed to the strict adherence of diagnostic criteria. Furthermore, in deep intrabony lesions where the overlying cortical plate was thicker or not perforated, USG might have yielded an inaccurate result owing to the hindrance of transmission of ultrasonic waves through the thicker bone.[92223] Further research is, thus, required for the development of specialized intraoral USG probes that can diagnose a lesion accurately irrespective of overlying bone thickness.

Nevertheless, the results of this study confirm that USG can provide clinicians with substantial diagnostic information regarding periapical lesions of endodontic origin. An endodontist, if trained to carry out an ultrasound examination, would be able to diagnose the exact nature of a periapical lesion in case of a dilemma, without subjecting the patient to unnecessary radiation exposures. In addition, USG can diagnose mixed lesions such as abscesses, which might be occult and remain undiagnosed by IOPA radiographs and CBCT. Previous assumptions of correlating the lesion size and the presence of sclerotic borders with increased cystic preponderance have been disregarded.[24] Therefore, as USG helps in determining the underlying disease process with good accuracy, it might help the clinician to decide to undertake nonsurgical treatment (for granuloma), along with surgical or intracanal drainage (for abscess), adopting a “wait and watch” policy or intercede surgically (for cysts).[9]

CONCLUSION

USG with CD is a convenient, reproducible, and relatively affordable tool. Its real-time image production ability enables the provision of a working diagnosis instantly, besides being radiation free, thereby enabling the formulation of a correct treatment plan, and predicting its outcome, thus reducing the increased incidence of endodontic treatment failures, affiliated with incongruent diagnoses made by the routinely used IOPA radiographs and CBCT. Therefore, considering the limitations and parameters of the present study, it can be concluded that USG with CD unequivocally holds the potential to be used as a noninvasive adjunct in periapical diagnostics preoperatively. However, further research needs to be carried out with a greater number of cases in exploring the potential of ultrasound imaging in the field of endodontics.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.