Ultrasound Characteristics of the Hair Follicles and Tracts, Sebaceous Glands, Montgomery Glands, Apocrine Glands, and Arrector Pili Muscles

Home , Arrector pili muscle, Hair follicle, Sebaceous hyperplasia

ORIGINAL RESEARCH

Ximena Wortsman, MD , Laura Carreño, MD, Camila Ferreira-Wortsman, MS, Rafael Poniachik, MS, Kharla Pizarro, MD, Claudia Morales, MD, Perla Calderon, MD, Ariel Castro, MSc

Video online at jultrasoundmed.org Objectives—To explore the capability of very high-frequency ultrasound (US; 50–71 MHz) to detect the normal morphologic characteristics of the hair follicles and tracts, sebaceous glands, Montgomery glands, apocrine glands, and arrector pili muscles. Methods—A retrospective study, approved by the Institutional Review Board, evaluated the normal US morphologic characteristics of the hair and adnexal structures in a database of very high-frequency US images extracted from the perilesional or contralateral healthy skin of 1117 consecutive patients who underwent US examinations for localized lesions of the skin and 10 healthy Received September 26, 2018, from the individuals from December 2017 to June 2018. These images were matched with Institute for Diagnostic Imaging and Research their counterparts from the database of normal histologic images according to for the Skin and Soft Tissues, Santiago, the corporal region. The Cohen concordance test and regional mean diameters Chile (X.W.); Departments of Dermatol- of the hair follicles and adnexal structures were analyzed. ogy (X.W., P.C.) and Pathology, Dermo- Results—The normal hair follicles and tracts, sebaceous glands, Montgomery pathology Section (L.C., K.P., C.M.), Faculty glands, apocrine glands, and arrector pili muscles were observed on US images of Medicine (R.P.), and Office for Clinical and matched their histological counterparts in all the corporal regions. There Research Support, Hospital Clínico Universi- was signiﬁcant US concordance (κ = 0.82; P = .0001) among observers. dad de Chile (A.C.), University of Chile, Regional mean diameters (millimeters) of the hair follicles, sebaceous glands, Santiago, Chile; and Faculty of Medicine, and apocrine glands are provided. University Finis Terrae, Santiago, Chile Conclusions— (C.F.-W.). Manuscript accepted for publica- The hair follicles and tracts, sebaceous glands, Montgomery tion November 11, 2018. glands, apocrine glands, and arrector pili muscles are detectable with very high- frequency US, including some regional and anatomic variants. Knowledge of Address correspondence to: Ximena their normal US appearances is a requisite for detecting subclinical changes, Wortsman, MD, Institute for Diagnostic understanding the physiopathologic characteristics, and supporting the early Imaging and Research of the Skin and Soft diagnosis and management of common dermatologic diseases. Tissues, Department of Dermatology, Faculty of Medicine, University of Chile, Lo Fontecilla Key Words—apocrine gland ultrasound; arrector pili muscle ultrasound; 201, Of 734, Las Condes, Santiago, Chile. dermatologic ultrasound; hair ultrasound; Montgomery gland ultrasound; E-mail: [email protected] sebaceous gland ultrasound; skin ultrasound; ultrasound dermatology

Abbreviation kin conditions are among the leading causes of the global US, ultrasound burden of disease.1 However, to date, common dermatologic disorders still present unclear points in their physiopathologic S 2 doi:10.1002/jum.14888 characteristics and management. The ability to noninvasively

detect the normal morphologic characteristics of the Review Board (approval number 055-2018) was per- hair and adnexal glands can allow identification of formed from December 2017 to June 2018. Before early subclinical abnormalities in many dermatologic the US examinations, all patients signed an informed conditions that affect millions of people worldwide, consent form following the standardized protocol for such as alopecia and acne.3,4 education and research of our center, and all of the Hair is a complex and dynamic structure that is examinations and images were analyzed under the one of the main hallmarks of mammals and a distinc- Helsinki principles of medical ethics. In the case of tive characteristic of an individual.5 The presence of children, the parents or guardians signed the an excessive amount or its loss can strongly affect informed consent, and all images were deidentified. self-esteem.6 The database was composed of 1127 examinations; Sebaceous glands contribute to the lubrication of 1117 of them were consecutive patients examined by the skin and hair.7 Variants of these glands are located dermatologists. The rest were 10 healthy adults. in some parts of the body, such as Montgomery In patients’ examinations, the dermatologic US glands in the areola.8 protocol typically includes a comparison with the Apocrine sweat glands provide support to the healthy skin located in the perilesional area or the thermoregulation and supposedly influence the scent contralateral side. The patients underwent very high- of an individual.9 These are located in some parts of frequency US studies of the healthy skin after examina- the body, such as the scalp, ciliary glands of the eyelids tions with another US device (LOGIQ E9 XD Clear; (Moll glands), external meatus (ceruminous glands), GE Healthcare, Waukesha, WI) equipped with a trans- and axillary and perineal regions, among others.10 ducer working at a maximum frequency of 18 MHz. Currently, ultrasound (US) is a suitable and rap- The healthy individuals underwent very high-frequency idly growing imaging modality for studying skin and US examinations of the face (right cheek), right axillary nail disorders because of the development of high- region (middle third), and right thigh (upper and inner frequency transducers (≥15 MHz).11 Although the third) region, and the diameters (millimeters) of the US characteristics of the hair follicles and tracts have hair follicles, sebaceous glands, and apocrine glands been reported at 15 MHz,12,13 this frequency does were measured. All cases were studied with the same not allow distinction of the internal part of the hair very high-frequency transducer that operates at a range tract located inside the hair follicle or the adjacent of frequencies from 29 to 71 MHz (Vevo MD, UHF adnexal structures, such as sebaceous glands, apocrine 70; VisualSonics, Toronto, Ontario, Canada). This glands, and the arrector pili muscle. transducer had an axial resolution of 30 μm and a Besides a few attempts to describe the morpho- lateral resolution of 65 μm. An automatic setting for logic characteristics of the hair and sebaceous glands superficial structures that comprises a range from – using experimental US devices in small series,14 16 to 50 MHz (center) to 71 MHz (maximum), a minimum date, there are no reports on the US morphologic gain of 43 dB, low persistence, and a dynamic range of characteristics of the rest of the adnexal structures 65 dB was used. Automatic adjustment of the fre- such as the apocrine glands and the arrector pili mus- quency of the transducer according to the depth of the cle on devices that are available worldwide. This study observation was enabled. Since the targets were com- aimed to explore the capability of very high-frequency posed of very superficial structures located in the first (≥50 MHz) US for detecting the normal morpho- 5 mm; the transducer automatically set the frequency logic characteristics of the hair follicles and tracts, at the higher values of the bandwidth. The maximum sebaceous glands, apocrine glands, Montgomery depth for this transducer is 10 mm; the focal depth is glands, and arrector pili muscles. 5 mm; and the view was adjusted by using a copious amount of gel, according to the diameter and depth of the structure and the thickness of the skin in each cor- Materials and Methods poral region. The spatial resolution was 0.05 mm (50 μm). There were 2 more transducers available for A retrospective study of the database of dermatologic use with the very high-frequency device (Vevo MD; US examinations approved by the Institutional VisualSonics): UHF 48 (range, 20–46 MHz) and

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UHF 22 (range, 10–22 MHz). However, neither of A tutorial with comparative histologic and US these very high-frequency transducers nor the available images of the same cutaneous structures was devel- 18-MHz transducer (maximum frequency) working on oped. Then a questionnaire with US images that were the LOGIQ E9 XD Clear machine was used in the different from the ones used in the tutorial was built. study for detecting or identifying structures. Both the tutorial and questionnaire were sent to 5 med- The inclusion criteria were patients with localized ical observers from different medical backgrounds and skin lesions on one side of a corporal segment who levels of training who were not involved in the genera- were otherwise healthy and healthy adults with no tion of the data. These observers included a dermato- history of cutaneous procedures or surgery in the pathologist, a resident of pathology (second year), a examination regions. The exclusion criteria were a dermatologist, and 2 medical students (second year). history of systemic dermatologic diseases and a his- These observers blindly and separately answered tory of cosmetic or plastic surgery procedures. 15 questions focused on the US identification of structures after a review of the tutorial. Ultrasound Technique and Staff A copious amount of gel was applied on top of the Statistical Analysis skin, and the structures were registered in at least The statistical analysis was performed by an indepen- 2 perpendicular axes. The axis of the transducer was dent statistician and included a concordance test aligned with the major axis of the hairs and adjacent (Cohen κ test) with Stata version 12.1 software structures in the different corporal regions. The (StataCorp, College, Station, TX), which was applied protocol of the study followed the previously pub- to the group of 5 observers of different medical back- lished guidelines for performing dermatologic US grounds who were not involved in the generation of examinations.17 data. P ≤ .05 was considered significant. The US and histologic matching of the images was performed by a single senior radiologist trained and working on dermatologic US for more than Results 15 years and 2 senior dermatopathologists, both with more than 15 years of experience. The US morpho- The 1117 patients in the study had a mean age of logic characteristics of the hairs and glands were ana- 36 years (SD, Æ21.2 years; range, 1 month– lyzed according to the corporal regions (head, neck, 100 years) and included 1066 adults and 61 children trunk, and upper and lower extremities) and subdi- (58% female and 42% male). The 10 healthy adults vided into more specific anatomic areas when particu- had a mean age of 40 years (SD, Æ 17 years; 50% lar characteristics were noticed. male and 50% female). The normal hair follicles and tracts, arrector pili Detection and Identification of Structures muscles, sebaceous glands, Montgomery glands, and The structures were detected and identified on US apocrine glands were detected and matched their histo- images according to their published and available his- logical counterparts in all cases (Figures 1–6and tologic representations in the database of normal his- Videos 1–9). The statistical analysis of concordance tologic patterns of the Department of Pathology. A among observers showed a significant, very good pilot catalog of US images and videos was created to κ value (κ =0.82;P = .0001). The mean diameters start the identification of the structures. This catalog (millimeters) in 2 perpendicular axes (depth and was developed by a radiologist and a dermatopatholo- thickness according to the major structural axis) of the gist. The histologic specimen was considered the ref- hair follicles, sebaceous glands, and apocrine glands in erence standard for matching the US and histologic different body regions are presented in Table 1. images. During this process, comparisons and matching of the US and histologic images of the normal Normal US Morphologic Characteristics of the Hair hair and adnexal structures at higher and lower levels Follicles and Tracts of magnification, and according to the corporal The normal morphologic characteristics of the hair region, were performed. follicles consisted of oblique hypoechoic dermal

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Figure 1. Hair follicles and tracts. A–D, Normal US morphologic characteristics of the hair follicles in different corporal regions (A, thigh; B, groin; C, face; D, scalp) and the hair tract (A). E, Histologic specimen of a hair follicle and its parts (scalp region; hematoxylin-eosin, original magniﬁcation ×40). Notice the bilaminar morphologic characteristics of the hair tract at the thigh region (A).

bands that matched previous descriptions.13 Their frequency transducers (15–48 MHz), which were also depth and thickness varied according to the corporal available. However, these lower-frequency transducers region, being shorter and thinner on the face and dee- were not used for identifying the cutaneous structures per and thicker on the scalp (Figure 1 and Videos in this study. 1–3). Even though the hair follicles were already The hair tracts inside the hair follicles were detected and identiﬁed in most of the corporal observed in some corporal regions such as the axil- regions, the bottoms of the hair follicles located on lary, perineal, lower extremities, eyebrows, and eye- the hypodermis of the scalp were not fully observed lids. The morphologic characteristics of the internal in all cases with the 50–71-MHz transducer and set- parts of the hair tracts were similar to the echo struc- ting, and their complete view required lower- ture already reported in their visible parts on the

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Figure 2. Eyelash hair follicles and tracts (lower eyelid). A, Normal US morphologic characteristics of the hair follicles and tracts of the eyelashes. B, Histologic correlation (hematoxylin-eosin, original magniﬁcation ×20). On the US image, notice the bilaminar pattern of the hair tracts of the eyelashes both outside and within the hair follicle.

surface of the skin for the same regions.12,13 This pat- the hair follicle region and ran to the upper dermis. It tern was predominantly hyperechoic and bilaminar was possible to observe these muscles in parts of the except the eyebrows and anterior part of the eyelids, trunk and limbs (Figure 3 and Video 3). which showed monolaminar hairs in their superﬁcial parts. A bifurcation and slight dilatation of the base of Normal US Morphologic Characteristics of the the hair tract was detected in some regions, which Sebaceous and Montgomery Glands corresponded to the bulb of the hair (Figures 1 and 2 The morphologic characteristics of sebaceous glands and Videos 1 and 2). consisted of oval hyperechoic structures attached to the hair follicles. They were more easily detected on Normal US Morphologic Characteristics of the the face and proximal parts of the limbs (Figure 4 Arrector Pili Muscles and Videos 4 and 5). The arrector pili muscles appeared as well-deﬁned, The Montgomery glands appeared as clusters of oblique, hypoechoic, thin bands that emerged from sebaceous glands without distinguishable hair follicles.

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Figure 3. Arrector pili muscle. A and B, Normal US morphologic characteristics of the arrector pili muscles, hair follicles, and apocrine glands in the anterior thoracic region (A) and the thigh (B). C and D, Histologic correlations (hematoxylin-eosin, original magniﬁcations ×20 [C] and ×40 [D]).

These glands were observed in the areolar and periar- (Figure 6C and Video 9). This variant was not eolar regions of the breast and, in some cases, in the observed in the groin regions. mons pubic and perineal regions (Figure 5 and Video 6). Discussion Normal US Morphologic Characteristics of the Apocrine Glands The US detection and in vivo identification of the nor- These glands appeared as round or oval hypoechoic mal morphologic characteristics of the hair and adnexal structures that contained multiple and tiny anechoic structures, considering variants and without having to lacunar regions that resembled an ovary; therefore, use a contrast medium, provide a safe and powerful their appearance was named a “pseudo-ovary pat- tool for detecting and identifying early subclinical tern.” These glands were observed in the axillary, per- abnormalities in a wide range of dermatologic condi- ineal, perianal, and inner aspects of the proximal parts tions and can support research in this field. To our of the arms and thighs (Figure 6 and Videos 7–9). knowledge, the ability to observe the apocrine glands, In 16 cases (80% of them female), there were which has not previously been reported, may be prominent apocrine glands in the axillary regions. relevant in the clarification of its role in the physiopath- Some of these cases showed a second row of apocrine ologic characteristics of devastating inflammatory cuta- glands in the middle thirds of both axillary regions neous diseases such as hidradenitis suppurativa.18,19

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Figure 4. Sebaceous glands (arrows). A and B, Normal US morphologic characteristics of the sebaceous glands in the anterior thoracic region (A) and the nasal tip (B). C–E, Histologic correlations in the scalp (C; hematoxylin-eosin, original magnification ×40), anterior thorax (D; hematoxylin-eosin, original magnification ×20) and inframammary area (E; hematoxylin-eosin, original magnification ×20). Notice the variable numbers of sebaceous glands in the different corporal regions, which are higher in the facial area.

This work also describes the US appearance of common dermatologic inﬂammatory entities such as the normal Montgomery glands that, to our knowl- acne and rosacea20 and the detection of benign and edge, has not been reported previously and has been malignant sebaceous tumors.21 suggested as the origin of areolar cysts. The descrip- The appearance of the hair tracts within the hair tion of the US appearance of sebaceous glands may follicles conﬁrmed the previous descriptions of support the subclinical diagnosis and treatment of their outer echo structure pattern12 and can provide a

Figure 5. Montgomery glands. A, Normal US appearance of the Montgomery glands. B, Histologic specimen (hematoxylin-eosin, original magniﬁcation ×40) at the periareolar region.

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Figure 6. Apocrine glands (arrows). A–C, Normal US morphologic characteristics of the apocrine glands with a pseudo-ovary pattern in different body regions and cases (A, proximal and inner parts of the thigh; B and C, axillary regions). Notice the variable presentations of apocrine glands with different sizes and numbers of apocrine glands, including a second row of glands in C. D and E, Histologic specimens (axillary region; hematoxylin-eosin, original magniﬁcations ×20 [D] and ×100 [E]) showing similar morphologic characteristics of the apocrine glands (arrows).

noninvasive tool for observing anomalies in the gen- an important advance in the dermatologic imaging eration of hair. The description of the mean diame- field. Although imaging is not intended to replace his- ters of these structures in different corporal regions, tologic analysis, it could support a more reasonable use as well as the presence of normal regional variants, of biopsies and prevent the sequelae of scars. can help in understanding the physiopathology The locations of these structures, including the characteristics, early detection, and management of depth, did not present a limitation for their US detec- common abnormalities such as sebaceous hyperplasia tion using a 50-MHz or higher-frequency transducer and folliculitis. except the observation of the bottoms of the hair folli- The high concordance in the interpretation of cles of the scalp in some cases, which required a the images among observers with different levels of lower-frequency transducer because of their deeper medical training can be related to the high definition location; however, the identification of these struc- of very high-frequency US images. Hence, US and his- tures has already been performed with a very high- tologic matching of images may potentially represent frequency transducer.

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Table 1. Diameters of Structures in Healthy Individuals as well as a growing number of articles and books on 24,25 Diameter, mm this topic. Moreover, nowadays, the possibility of training is available in several countries, and annual Mean Mean fi Structures Depth (SD) Thickness (SD) courses are provided by international scienti corgani- zations such as the American Institute of Ultrasound in Hair follicles Medicine (www.aium.org) and the European Federa- Axilla 3.00 (1.27) 0.30 (0.09) Thorax 2.29 (0.83) 0.33 (0.10) tion of Societies for Ultrasound in Medicine and Biol- Thigh 1.28 (0.78) 0.29 (0.13) ogy (www.efsumb.org), among others. Sebaceous As presented in this study, the detection of what glands is normal is a requisite for assessing abnormal US pat- Face 0.60 (0.23) 0.35 (0.15) Thorax 0.56 (0.18) 0.44 (0.11) terns of dermatologic conditions. Furthermore, the Thigh 0.33 (0.02) 0.25 (0.13) high correlations between US and histologic findings Apocrine glands can give a confident base for interpreting and validat- Axilla 1.70 (0.73) 0.90 (0,46) ing the imaging findings. In conclusion, the normal hair follicles and tracts, In contrast, other imaging techniques commonly sebaceous glands, Montgomery glands, apocrine used in dermatology have relevant issues due to their glands, and arrector pili muscles are detectable with light-based technology, which has low penetration. US, including anatomic variants. Knowledge of their For example, confocal microscopy had a maximum US morphologic characteristics may provide a valu- penetration that goes from 0.2 to 0.3 mm in depth, able and powerful noninvasive tool for detecting and optical coherence tomography has a maximum subclinical changes, improving the understanding of penetration that varies between 1.8 and 2.0 mm.22 the physiopathologic characteristics, and supporting These limitations in penetration mean that a lesion the diagnosis, management, and research of common located or involving an area beyond these points dermatologic diseases. could be partially or not seen, which, for example, could be a critical factor for diagnosing the real extent or the origin of a skin tumor. On the other hand, the current commercially References available imaging techniques, such as computed tomography and magnetic resonance imaging, do not 1. Hay RJ, Johns NE, Williams HC, et al. The global burden of skin have enough resolution to distinguish hair follicles disease in 2010: an analysis of the prevalence and impact of skin and adnexal glands. Magnetic resonance imaging conditions. J Invest Dermatol 2014; 134:1527–1534. requires immobilization, motion correction, and pow- 2. Rocha MA, Bagatin E. Adult-onset acne: prevalence, impact, and man- – erful devices of 7 T or higher for detecting dermal agement challenges. Clin Cosmet Investig Dermatol 2018; 11:59 69. abnormalities,23 which can be very expensive in com- 3. Salman KE, Altunay IK, Kucukunal NA, Cerman AA. Frequency, parison with the capabilities of the current US severity and related factors of androgenetic alopecia in dermatol- machines that are available worldwide. ogy outpatient clinic: hospital-based cross-sectional study in Turkey. An Bras Dermatol 2017; 92:35–40. Limitations of this study were structures that mea- 4. Bez Y, Yesilova Y, Kaya MC, Sir A. High social phobia frequency sured less than 0.05 mm and the detection of and related disability in patients with acne vulgaris. Eur J Dermatol pigments. Other potential limitations were that the 2011; 21:756–760. performance and interpretation of these images 5. Buffoli B, Rinaldi F, Labanca M, et al. The human hair: from anat- required physicians trained on US examinations of – fi omy to physiology. Int J Dermatol 2014; 53:331 341. super cial structures. However, at the same time, this 6. Davis DS, Callender VD. Review of quality of life studies in could also have been an advantage and could have pro- women with alopecia. Int J Womens Dermatol 2018; 4:18–22. fi vided consistency to the study because any eld of 7. Picardo M, Ottaviani M, Camera E, Mastrofrancesco A. Sebaceous medicine requires proper training for interpreting the gland lipids. Dermatoendocrinol 2009; 1:68–71. results correctly. Regarding the dermatologic US field, 8. Blech H, Friebe K, Krause W. Inflammation of Montgomery 17 there is a broad range of practical applications of US glands. Acta Derm Venereol 2004; 84:93–94.

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