<abstract xmlns="http://www.w3.org/1999/xhtml">

<p>
<bold>Aim of the study:</bold> Ultrasonographic examination of intraosseous jaw pathologies may reveal interesting incidental, mobile hyperechoic particles (“snowflakes”) in anechoic areas. Purpose of this study is to explain and discuss this snowing-like ultrasonographic feature of intraosseous jaw pathologies. <bold>Material and methods:</bold> This study included 113 patients admitted to our clinic for examination: 43 (38.05%) males and 70 (61.9%) females with a mean age of 34.9 ± 17.2 years (range: 6–72 years). A total of 120 intraosseous lesions were evaluated prior to surgery using ultrasonography; these included non-neoplastic, odontogenic, and non-odontogenic lesions. <bold>Results:</bold> In total, 5 (4.1%) of the 120 lesions exhibited snowing-like feature on ultrasonography, including 2 (1.6% of total) of 3 incisive canal cysts, 2 (1.6% of total) of 7 dentigerous cysts, and 1 (0.8% of total) of 19 odontogenic keratocysts. <bold>Conclusions:</bold> Snowflakes evident on ultrasonography of intraosseous jaw lesions may be specific to certain pathologies. Future studies correlating radiologic and pathologic features of intraosseous jaw lesions should focus on ultrasonographic snowing-like appearance in different types of lesions and explore why they occur.</p>
</abstract>

Aim of the study: Ultrasonographic examination of intraosseous jaw pathologies may reveal interesting incidental, mobile hyperechoic particles (“snowflakes”) in anechoic areas. Purpose of this study is to explain and discuss this snowing-like ultrasonographic feature of intraosseous jaw pathologies. Material and methods: This study included 113 patients admitted to our clinic for examination: 43 (38.05%) males and 70 (61.9%) females with a mean age of 34.9 ± 17.2 years (range: 6–72 years). A total of 120 intraosseous lesions were evaluated prior to surgery using ultrasonography; these included non-neoplastic, odontogenic, and non-odontogenic lesions. Results: In total, 5 (4.1%) of the 120 lesions exhibited snowing-like feature on ultrasonography, including 2 (1.6% of total) of 3 incisive canal cysts, 2 (1.6% of total) of 7 dentigerous cysts, and 1 (0.8% of total) of 19 odontogenic keratocysts. Conclusions: Snowflakes evident on ultrasonography of intraosseous jaw lesions may be specific to certain pathologies. Future studies correlating radiologic and pathologic features of intraosseous jaw lesions should focus on ultrasonographic snowing-like appearance in different types of lesions and explore why they occur.


<div xmlns="http://www.w3.org/1999/xhtml">
<sec id="j_jou.2020.0053_s_001" sec-type="introduction">
<div>Introduction</div>
<p>Intraosseous odontogenic, non-odontogenic, neoplastic, and non-neoplastic pathologies are common in the maxilla and mandible<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>)</sup>. Imaging data are required for diagnosis, treatment planning, and follow-up<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>)</sup>. Clinical examination is used first to diagnose intra- and extra-bone jaw lesions, followed by radiological evaluation<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_003">3</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_004">4</a>)</sup>. Traditional radiography modalities (orthopantomography, and occlusal and periapical radiography) are primarily used to evaluate maxillofacial lesions, but these methods have disadvantages including magnification errors, distortion, and structural misrepresentation<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_005">5</a>)</sup>. Although computed tomography (CT) and magnetic resonance imaging (MRI) are useful for assessment of jawbone lesions, they have several disadvantages. Low-dose cone-beam CT (CBCT) is particularly suited for evaluation of the maxillofacial region<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_006">6</a>)</sup>. However, both CT and CBCT expose patients to ionizing radiation and yield limited data on lesional contents. MRI does not employ ionizing radiation but is the best-suited modality for imaging of intracranial and soft-tissue lesions. In addition, the equipment is costly, and the screening time is long; moreover, this imaging technique is contraindicated in claustrophobic patients, and in those with certain types of surgical clips, pacemakers, and cochlear implants<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_007">7</a>)</sup>. Ultrasonography (US) is a new and promising diagnostic imaging modality for evaluation of head and neck lesions in lymph nodes and salivary glands, as well as facial bone fractures<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_008">8</a>)</sup>. US reveals the contents of intraosseous jaw lesions<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_008">8</a>–<a ref-type="bibr" href="#j_jou.2020.0053_ref_011">11</a>)</sup>, and currently plays auxiliary and supportive roles. US enhances our understanding of lesional histology<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_012">12</a>)</sup>. Also, US is safe; no ionizing radiation is used. US is indicated for pregnant and pediatric patients, being simple, painless, repeatable, non-invasive, and economical. US provides useful information on intraosseous jaw lesions<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_008">8</a>–<a ref-type="bibr" href="#j_jou.2020.0053_ref_011">11</a>)</sup>.</p>
<p>In our previous study on intraosseous US pathologies, we sometimes observed mobile hyperechoic particles in anechoic areas<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_009">9</a>)</sup> which we termed “snowflakes appearance”, have not been discussed previously. The purpose of this study is to explain and discuss this incidental snowing-like appearance and describe the patient populations that exhibit them.</p>
</sec>
<sec id="j_jou.2020.0053_s_002" sec-type="materials|method">
<div>Materials and methods</div>
<sec id="j_jou.2020.0053_s_002_s_001">
<div>Patient selection</div>
<p>Preoperative US images of 120 intraosseous jaw lesions from 113 patients admitted to our clinic were reviewed retrospectively. The study group consisted of 43 (38.05%) males and 70 (61.9%) females, with a mean age of 34.9 ± 17.2 years (range: 6–72 years); all patients provided written informed consent. This retrospective study adhered to all relevant principles of the Declaration of Helsinki. The Clinical Research Ethics Committee of the Eskisehir Osmangazi University Faculty of Medicine approved the study (permit no. 13; October 8, 2019). Biopsy data were collected prior to surgery. Lesional diagnoses were histopathologically confirmed.</p>
</sec>
<sec id="j_jou.2020.0053_s_002_s_002">
<div>Imaging/US devices</div>
<p>Two US devices were used to evaluate pathologies. Extra-oral sonograms were obtained in the transverse and longitudinal planes using both an Aplio 300 device (Toshiba Corporation, Tokyo, Japan) fitted with an 8-MHz linear array transducer and a Mindray DC N3 device (Shenzhen, China) fitted with a 4–10-MHz linear array transducer. To ensure standardization of all US examinations, patients sat upright with the sagittal plane perpendicular to the floor and the occlusal plane of the jaw with the localized lesion parallel to the floor.</p>
</sec>
<sec id="j_jou.2020.0053_s_002_s_003">
<div>Snowing-like appearance</div>
<p>Mobile hyperechoic particles like snowflakes in anechoic areas were encountered as incidentally in ultrasonographic images. This apperance resembles a snowfall. Because of this, this view was named the ‘‘Snowing-like appearance’’ inspired snowing.</p>
</sec>
</sec>
<sec id="j_jou.2020.0053_s_003" sec-type="results">
<div>Results</div>
<p>The 120 pathologies included neoplastic, non-neoplastic, odontogenic, and non-odontogenic lesions. Five (4.1%) lesions exhibited snowflakes (Fig. <a ref-type="fig" href="#j_jou.2020.0053_fig_001">1</a> and Video 1): 2 (1.6% of total) (localized maxillar anterior region and histopathological examinations show that microscopically, cyst lined by ciliated pseudostratified columnar epithelium) of 3 incisive canal cysts, 2 (1.6% of total) (localized maxillar anterior region and histopathological examinations show that nonkeratinized, stratified squamous epithelium) of 7 dentigerous cysts, and 1 (localized maxillar anterior-canine-premolar region and histopathological examination shows that microscopically, cyst lined by mature squamous epithelium and parakeratotic keratinaceous debris) (0.8% of total) of 19 odontogenic keratocysts (Tab. <a ref-type="table" href="#j_jou.2020.0053_tab_001">1</a>). All these lesions had cystic content. Characteristics of the lesions with the appearance of snowing-like were summarized Tab. <a ref-type="table" href="#j_jou.2020.0053_tab_002">2</a>.</p>
<figure id="j_jou.2020.0053_fig_001" position="float" fig-type="figure">
<h2>Fig. 1.</h2>
<figCaption>
<p>
<bold>A.</bold>
<italic>Occlusal radiographs show that well-defined radiolucent lesion in anterior maxilla. (incisive duct cyst)</italic> <bold>B.</bold>
<italic>The snowflakes-like appearance of intraosseous lesions on ultrasonography (incisive duct cyst)</italic>
</p>
</figCaption>
<img xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="graphic/j_jou.2020.0053_fig_001.jpg" src="https://sciendo-parsed.s3.eu-central-1.amazonaws.com/64722dda215d2f6c89dbeb9f/j_jou.2020.0053_fig_001.jpg?X-Amz-Algorithm=AWS4-HMAC-SHA256&amp;X-Amz-Date=20240629T214511Z&amp;X-Amz-SignedHeaders=host&amp;X-Amz-Expires=17999&amp;X-Amz-Credential=AKIA6AP2G7AKP25APDM2%2F20240629%2Feu-central-1%2Fs3%2Faws4_request&amp;X-Amz-Signature=760c27c65a9b38248b3d195b95de8b42e1ee86c6f58bba627c4e1f34794d28db" class="mw-100"/>
</figure>
<table-wrap id="j_jou.2020.0053_tab_001" position="float">
<label>Tab. 1.</label>
<caption>
<p>
<italic>The snowing-like features of various intraosseous jaw pathologies</italic>
</p>
</caption>
<table frame="hsides" rules="groups">

<thead>
<tr>
<th align="center" valign="top">Intraosseous jaw pathologies</th>
<th align="center" valign="top">Incisive duct cyst</th>
<th align="center" valign="top">Dentigerous cyst</th>
<th align="center" valign="top">Odontogenic keratocyst</th>
</tr>
</thead>
<tbody>
<tr>
<td align="center" valign="top">
<bold>Total pathologies</bold>
</td>
<td align="center" valign="top">3</td>
<td align="center" valign="top">7</td>
<td align="center" valign="top">19</td>
</tr>
<tr>
<td align="center" valign="top">
<bold>Number of snowflakes appearance</bold>
</td>
<td align="center" valign="top">2</td>
<td align="center" valign="top">2</td>
<td align="center" valign="top">1</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="j_jou.2020.0053_tab_002" position="float">
<label>Tab. 2.</label>
<caption>
<p>
<italic>Characteristics of the lesions with the appearance of sno-wing-like</italic>
</p>
</caption>
<table frame="hsides" rules="groups">

<thead>
<tr>
<th align="center" valign="top"></th>
<th align="center" valign="top">Lesion localization</th>
<th align="center" valign="top">Lesion size</th>
<th align="center" valign="top">Content of the lesion</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="top">
<bold>Incisive duct cyst (1)</bold>
</td>
<td align="center" valign="top">Maxilla-anterior</td>
<td align="center" valign="top">25.2 × 23.2 × 24.6 mm</td>
<td align="center" valign="top">Cystic</td>
</tr>
<tr>
<td align="left" valign="top">
<bold>Incisive duct cyst (2)</bold>
</td>
<td align="center" valign="top">Maxilla-anterior</td>
<td align="center" valign="top">29.8 × 27.6 × 32.4 mm</td>
<td align="center" valign="top">Cystic</td>
</tr>
<tr>
<td align="left" valign="top">
<bold>Dentigerous cyst (1)</bold>
</td>
<td align="center" valign="top">Maxilla-anterior</td>
<td align="center" valign="top">32.5 × 23.1 × 23.8 mm</td>
<td align="center" valign="top">Cystic</td>
</tr>
<tr>
<td align="left" valign="top">
<bold>Dentigerous cyst (2)</bold>
</td>
<td align="center" valign="top">Maxilla-anterior</td>
<td align="center" valign="top">26.7 × 23.2 × 25.3 mm</td>
<td align="center" valign="top">Cystic</td>
</tr>
<tr>
<td align="left" valign="top">
<bold>Odontogenic keratocyst</bold>
</td>
<td align="center" valign="top">Maxilla-anterior-canine-premolar</td>
<td align="center" valign="top">33.1 × 30.1 × 36.1 mm</td>
<td align="center" valign="top">Cystic</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec id="j_jou.2020.0053_s_004" sec-type="discussion">
<div>Discussion</div>
<p>Many studies have used US to evaluate intraosseous lesions, principally in terms of lesional contents, margins, and vascularity<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>,<a ref-type="bibr" href="#j_jou.2020.0053_ref_008">8</a>–<a ref-type="bibr" href="#j_jou.2020.0053_ref_011">11</a>)</sup> Lauria <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>)</sup> compared the US and histopatho-logical findings of 72 intraosseous jaw lesions. US revealed lesional contents prior to surgery<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_001">1</a>)</sup>. However, no specific data were provided. Ishii <italic>et al</italic>. used US for preoperative evaluation of palatal salivary gland tumors<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_008">8</a>)</sup>. Cotti <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_013">13</a>)</sup> employed US for differential diagnosis of cystic lesions and granulomas among 11 periapical lesions. The US and histopathological findings were consistent<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_013">13</a>)</sup>. Subsequently, Gundappa <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_014">14</a>)</sup> showed that US differentiated cysts from granulomas<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_014">14</a>)</sup>. Yee <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_011">11</a>)</sup> used US to evaluate osteosarcomas, describing a pathognomic “sunray appearance”. This was the first report on the US features of mandibular osteosarcomas. The importance of early US in terms of detecting pathognomic images was emphasized. Although US is not definitively diagnostic of bone pathologies, early US is valuable<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_011">11</a>)</sup>. Preoperatively, Sumer <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>)</sup> used power Doppler US to accurately evaluate the vascularity of 22 intraosseous lesions<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_002">2</a>)</sup>. Bayrakdar <italic>et</italic> <italic>al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_009">9</a>)</sup> employed US to preoperatively examine 89 intraosseous lesions. Histopathological and US findings were compared in this study. US sometimes revealed hyperechoic snowflakes in anechoic areas, which may be epithelial or keratin remnants, or dead fragments of previously infected tissues. They observed snowflakes in 3 of 89 intraosseous lesions, including 2 (2.3%) incisive canal cysts and 1 (1.1%) odontogenic keratocyst. They also observed snowflakes in 1 of 18 odontogenic keratocysts and 2 of 3 incisive duct cysts<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_009">9</a>)</sup>. In this present study, we observed this phenomenon in 2 dentigerous cysts in addition to these lesions. Snowflakes were not present in all dentigerous or incisive duct cysts, or odontogenic keratocysts, possibly because US does not reveal all features of intraosseous lesions. Thick cortical bone may complicate evaluation of lesional contents; this is the most important limitation of our study. Although we evaluated 120 intraosseous jaw lesions, all were above a certain size, where size may influence lesional content. We observed snowflakes in only five lesions. These lesions we encountered with snowing-like appearance had sizes greater than 20 mm. Maybe, smaller lesions do not mature enough containing predominantly fluid, maybe it was too early in lesion development for the “snowing” appearance to be observed.</p>
<p>Ferreira <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_015">15</a>)</sup>, in a preliminary study on pig jaws, showed that lesions can be examined via US if the cortical bone is thin<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_015">15</a>)</sup>. Musu <italic>et al</italic>.<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_016">16</a>)</sup> confirmed that US significantly assisted differential diagnosis of jawbone lesions<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_016">16</a>)</sup>. However, the snowflakes, as incidental findings, have not been previously evaluated. A dentigerous cyst is covered with a nonkeratinized, stratified squamous epithelium reflecting proliferation of the reduced enamel epithelium<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_017">17</a>)</sup>. A nasopalatine canal cyst reflects proliferation of epithelial remnants of the nasopalatine canal, the epithelium of which is mostly squamous<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_018">18</a>)</sup>. An odontogenic keratocyst is lined with keratinized epithelium from residual cells of the dental lamina<sup>(<a ref-type="bibr" href="#j_jou.2020.0053_ref_019">19</a>)</sup>. Thus, the snowflakes may be epithelial, infective, or keratin-like remnants. This appearance could influence diagnosis based on ultrasonographic examination. It could be a clue whether it is infected or not, includes keratin-like remnants or epithelial remnant. It can be help the clinical diagnosis of the lesions.</p>
<p>However, we studied only a few lesions; this is a limitation of our work that we will address in future studies. Besides, we used two different linear array transducers for imaging of jaw lesions. Frequency of both probes was relatively low when considering examinations of small parts, even if we get the chance to view of snowing-like appearance in imaging of the intraosseous jaw lesions. Future studies should be eliminated this limitation using high frequency transducers.</p>
</sec>
<sec id="j_jou.2020.0053_s_005" sec-type="conclusion">
<div>Conclusion</div>
<p>The interesting snowflakes incidentally noted on US may be specific for certain pathologies, indicative of epithelial, infective, or keratin remnants. Future studies correlating pathology and radiology findings should aim to clarify when and why snowflakes occur, and which lesions are involved.</p>
</sec>
</div>

Evaluation of the snowing-like ultrasonographic features of intraosseous jaw pathologies

Journal of Ultrasonography

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Aim of the study: Ultrasonographic examination of intraosseous jaw pathologies may reveal interesting incidental, mobile hyperechoic particles (“snowflakes”)...

Evaluation of the snowing-like ultrasonographic features of intraosseous jaw pathologies

Article Category: research-article

Data publikacji: 18 gru 2020

Zakres stron: 307 - 310

Otrzymano: 10 cze 2020

Przyjęty: 27 sie 2020

DOI: https://doi.org/10.15557/jou.2020.0053

Słowa kluczowe
intraosseous jaw pathology, snowflakes, ultrasonography

© 2021 Polish Ultrasound Society. Published by Medical Communications Sp. z o.o.

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1.

Characteristics of the lesions with the appearance of sno-wing-like

The snowing-like features of various intraosseous jaw pathologies

	Lesion localization	Lesion size	Content of the lesion
Incisive duct cyst (1)	Maxilla-anterior	25.2 × 23.2 × 24.6 mm	Cystic
Incisive duct cyst (2)	Maxilla-anterior	29.8 × 27.6 × 32.4 mm	Cystic
Dentigerous cyst (1)	Maxilla-anterior	32.5 × 23.1 × 23.8 mm	Cystic
Dentigerous cyst (2)	Maxilla-anterior	26.7 × 23.2 × 25.3 mm	Cystic
Odontogenic keratocyst	Maxilla-anterior-canine-premolar	33.1 × 30.1 × 36.1 mm	Cystic

Evaluation of the snowing-like ultrasonographic features of intraosseous jaw pathologies

Article Category: research-article

Data publikacji: 18 gru 2020

Zakres stron: 307 - 310

Otrzymano: 10 cze 2020

Przyjęty: 27 sie 2020

DOI: https://doi.org/10.15557/jou.2020.0053

Słowa kluczoweintraosseous jaw pathology, snowflakes, ultrasonography

© 2021 Polish Ultrasound Society. Published by Medical Communications Sp. z o.o.

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1.

Characteristics of the lesions with the appearance of sno-wing-like

The snowing-like features of various intraosseous jaw pathologies

Słowa kluczowe
intraosseous jaw pathology, snowflakes, ultrasonography