Abstract
Introduction:
Almost all cases of malignant acanthosis nigricans with oral manifestations occurred in older age groups. Here, we report a case of malignant acanthosis nigricans in a young female presented with chief complaints of oral mucosal hyperplasia, who had previously been diagnosed with allergies.
Case presentation:
A 30-year-old female developed oral hyperplasia and rash following seafood consumption, with subsequent resolution of the rash but persistent oral lesions and the appearance of pigmentation on her hands, neck, and axillae. Clinical examination revealed papillomatosis, hyperemia, and velvety hyperplasia in the oral cavity. Biopsy results confirmed papillary hyperplasia. Despite the patient’s belief in good health, she was advised to undergo further systemic examinations. Elevated serum tumor markers and histologic analysis of an endoscopic biopsy confirmed gastric cancer with duodenal infiltration, leading to the diagnosis of malignant acanthosis nigricans. Unfortunately, the patient passed away due to heart failure during chemotherapy treatment.
Conclusions:
The majority of patients with malignant acanthosis nigricans present with oral lesions before the underlying malignancy is detected, emphasizing the importance of timely comprehensive systemic examination. Furthermore, our case suggests that age may not be a restrictive factor for the development of malignant acanthosis nigricans, and the presence of a rash can potentially obscure the cutaneous manifestations associated with this condition.
1 Introduction
Acanthosis nigricans is a rare mucocutaneous disorder characterized by skin hyperpigmentation and thickening in specific regions, such as the neck, axillae, and groin (1). Additionally, some patients exhibit filiform growths on the oral mucosa (2), which bear resemblance to lesions induced by human papillomavirus.
There were several different classifications for acanthosis nigricans, with malignant acanthosis nigricans included in each of them (3–5). Malignant acanthosis nigricans is considered a paraneoplastic syndrome, associated with cancers of the stomach, ovary, bladder, breast, liver, and kidney (6). Mucous membrane involvement is indicative of the malignant form.
Here, we report a case of a patient presenting with filiform papillomas on oral mucosa who was ultimately diagnosed with malignant acanthosis nigricans. While malignant acanthosis nigricans has mainly been reported in older populations (7), the patient in this case was only 30 years old. She had confidence in her physical health and denied all relevant systemic symptoms at her initial visit.
2 Case report
A 30-year-old woman presented to the Oral Medicine Department of Peking University School and Hospital of Stomatology with a complaint of 4-month hyperplasia in the mouth. She recalled that the oral manifestation and skin eruptions occurred after consuming seafood and had previously been diagnosed with atopic dermatitis at other institutions. The rash resolved after treatment, whereas pigmentation appeared on the hands, neck, and axillae. However, there was no improvement in the oral lesions. The patient underwent laboratory tests (blood routine, blood biochemistry, erythrocyte sedimentation rate, ANA spectrum, and T-cell subtype), and the results were all within normal ranges. The patient denied weight loss, a history of cancer, drug use, diabetes, unconventional sexual contact, venereal disease, and other endocrine disorders.
Oral examination results identified papillomatosis on the lips, hard palate mucosa, and gingiva with apparent hyperemia. Velvety hyperplasia was observed on the buccal mucosa and the dorsum of the tongue. Dermatological examination showed hyperpigmentation on the neck, axillae, and hands (Figure 1). Biopsies were performed on the lower lip and axillae, revealing papillary hyperplasia (Supplementary Figure S1).
Figure 1
The patient underwent a systemic examination for underlying malignancy. Enhanced computed tomography results showed gastric wall thickening in the angle and enlarged lymph nodes in the lesser curvature, suggesting a possibility of gastric cancer (Supplementary Figure S2). Gastroscope examination results showed ulcers and papillary hyperplasia on the gastric wall and esophagus (Figures 2A, B). Histologic analysis of endoscopic biopsy confirmed gastric carcinoma with duodenal infiltration (Figures 2C, D). Immunohistochemistry results showed cytokeratin-7 (CK7) (+++), cytokeratin-20 (CK20) (+++), mucin-5 (MUC5) (+++), and caudal type homeobox 2 (CDX2) (+++), indicating primary gastric adenocarcinoma (poorly differentiated). Levels of serum tumor markers, including carcinoembryonic antigen (11.25 ng/mL, normal range: <5.0 ng/mL), carbohydrate antigen 19-9 (>1,000 U/mL, normal range: <37.0 U/mL), carbohydrate antigen 125 (165.30 U/mL, normal range: <35.0 U/mL), carbohydrate antigen 72-4 (57.87 U/mL, normal range: <6.9 U/mL), and tissue polypeptide antigen (2236.00 U/L, normal range: <120 U/L), were significantly elevated.
Figure 2
The diagnosis of malignant acanthosis nigricans was established. The patient received chemotherapy for the metastatic gastric carcinoma. Unfortunately, the patient died of heart failure during the treatment period. The timeline of the patient’s condition, medical visits, and outcome is presented in Figure 3.
Figure 3
3 Discussion
Malignant acanthosis nigricans in young populations is rare. In this report, we present a case of malignant acanthosis nigricans with multiple papillomatous and velvety oral lesions in a young female. Upon systemic examination, gastric cancer was detected. To the best of our knowledge, this is the first reported case of a young individual with malignant acanthosis nigricans presenting primarily with oral manifestations.
The differential diagnosis of acanthosis nigricans on oral mucosa holds particular importance for patient prognosis. Similar oral changes may occur in inflammatory papillary hyperplasia and HPV infection. Inflammatory papillary hyperplasia primarily presents as multiple small fibrous papillary growths, usually caused by wearing dentures and candidiasis, visible mainly on the denture-bearing hard palate (8). HPV-13 and HPV-32 infection can lead to multifocal, verrucous papules of the lips, buccal mucosa, and tongue (9), whereas HPV-6 and HPV-11 infections manifest as nodular or stalky masses with papillary surfaces (10). HPV tests help exclude these diseases.
Some skin disorders and syndromes also present with oral papillary lesions. Cowden syndrome (11) and ectrodactyly–ectodermal dysplasia–clefting syndrome (12) showed no evidence of skin hyperpigmentation. Linear epidermal nevus (13) and sebaceous nevus syndrome (14) can present both oral and cutaneous lesions resembling our case. The main point of differential diagnosis is that verrucous papules or pigmentation in these diseases appear in a linear configuration along skin tension lines. Focal dermal hypoplasia (15) is characterized by developmental disorders in multiple tissues and organs. Compared to this case, the above syndrome exhibits relatively small-range oral lesions, limited areas of skin lesions, and lighter pigmentation, with a tendency for family history. Specific genetic tests help make a correct diagnosis.
Extensive areas of papillary growth in oral mucosa and skin pigmentation in folds suggested that the patient might have acanthosis nigricans. Given that the benign and malignant forms of acanthosis nigricans can hardly be distinguished by mucocutaneous examination alone (2), we advised a thorough examination despite the young patient’s lack of discomfort, pain, or weight loss. This led to the discovery of gastric adenocarcinoma.
It is worth mentioning that Krawczyk (16) previously reported a case of papular rash with excessive keratosis, skin discoloration, and pruritus occurring simultaneously. Our patient also presented with a rash and was diagnosed with “allergy”. The presence of rash with excessive keratosis, oral papillary growth, and other manifestations should be carefully evaluated by clinicians to avoid overlooking the symptoms of malignant acanthosis nigricans.
Ramirez-Amador documented 12 cases of malignant acanthosis nigricans with oral manifestations prior to 1999 (17). Our literature review identified 23 additional cases since then. Nearly all reported cases involved patients older than 40 years. Papillomatosis emerged as the most prevalent oral manifestation, observed in 72.2% of cases, primarily affecting the lips. Among these malignancies, 42% were gastric cancers. Notably, 59.1% of patients exhibited oral lesions preceding the diagnosis of the malignancy. We present the cases in Table 1 and summarize them in Supplementary Figure S3.
Table 1
| Reference | Age, years | Sex | Duration, months | Chief complaint | Oral mucosa | Cutaneous | Oral manifestation before/after cutaneous | Underlying malignancy | Diagnosis before/after malignancy detected | ||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Manifestation | Site | Manifestation | Site | ||||||||
| 30 | F | 4 | Allergy | Papillomatosis and velvety hyperplasia | Lips, buccal mucosa, gingiva, hard palate mucosa, and tongue | Hyperpigmentation | Neck, axillae, and hands | Before | Gastric adenocarcinoma | Before | |
| Liu et al., 2024 (18) | 67 | F | Velvety and papillary lesions | Upper lip, buccal mucosa, gingiva, and hard palate | Pigmentation | Around the mouth, neck, hands, and around the armpits | Ovarian cancer | Before | |||
| Al-Zahawi et al., 2024 (19) | 58 | F | Thickening | Lips and oral mucosa | Hyperpigmented and velvety thickening | Nose, neck, axilla, groins, palms, and soles | Gastric adenocarcinoma | After | |||
| Fayne et al., 2023 (20) | 87 | F | 4 | Verrucous papules | Verrucous papules coalescing into plaques | Upper lip, buccal mucosa, hard palate, tongue, and posterior aspect of the oropharynx | Verrucous papules coalescing into plaques | Left eyelid margin | After | Urothelial carcinoma | After |
| Yun et al., 2022 (21) | 41 | M | 4 | Hyperpigmentation | Lips | Hyperpigmented and pruritic plaques | Neck, axillae, and hands | After | Pancreatic neuroendocrine tumor | After | |
| Zhang et al., 2021 (7) | 71 | F | 4 | Burning sensation | Hypertrophic lesions and papillomatosis | Buccal mucosa, gingiva, and tongue | Hyperpigmentation, thickened skin, and mild pruritus | Face, hands, feet, fold areas, and axillary and inguinal regions | After | Urinary bladder cancer | After |
| Rizwan et al., 2019 (22) | 62 | M | 8 | Velvety verrucous plaques | Lips, buccal mucosa, and hard palate | Hyperpigmentation, papular lesions, and velvety and hyperkeratotic plaques | Scalp, face, neck, lower abdomen, limbs, palms, and instep of soles | Hepatic ductal undifferentiated malignant neoplasm | After | ||
| Yu et al., 2017 (6) | 74 | M | 7 | Florid papillomatosis | Buccal mucosa | Hyperkeratotic plaques | Face, dorsal skin of fingers, and heels | Before | Gastric cardia tubular adenocarcinoma | Before | |
| Wang et al., 2017 (23) | 41 | M | Verrucous lesions | Lips, buccal mucosa, and tongue | Hyperpigmented and thickened areas | Axillae and hands | Gastric adenocarcinoma | After | |||
| Karakas et al., 2016 (24) | 55 | M | 3 | Oral mucosal ulcers | Multiple mucosal oral ulcers | Hyperpigmented and velvety skin lesions | Lower and upper extremities, face, palms, axillary, inguinal, and anal regions | Squamous cell lung cancer | Before | ||
| Lee et al., 2015 (25) | 70 | F | Warty growths, oral discomfort, and difficulty eating | Papillomatosis | Lips, palate, and tongue | Verrucous or velvety pigmented plaques | Axillae, posterior neck, periumbilical region, and groin | Renal urothelial carcinoma | |||
| Chu et al., 2014 (5) | 59 | F | 3 | Tumefaction lips | Scab and tumefaction | Lips | Hyperkeratotic and hyperpigmented skin, and velvety patchy lesions | Face, elbows, pudendum, groins, and axilla | Abdomen and pelvis metastases carcinoma | Before | |
| Abu-Safieh et al., 2011 (26) | 29 | F | 1 | Blood oozing | Lips | Thickened, hyperpigmented, and warty skin | Axillae | Gastric adenocarcinoma | Before | ||
| Mignogna et al., 2009 (27) | 74 | F | Diffuse micropapillary lesions, “cerebriform” aspect | Inner upper lips, right cheek, and hard palate | Velvety rugose appearance | Palms and palmar surface of the fingers | Diffuse large B-cell lymphoma | Before | |||
| Krawczyk et al., 2009 (16) | 44 | 2 | Excessive keratosis and discoloration | Tongue | Excessive keratosis, skin discoloration, and pruritus | Trunk and axilla area | After | Gastrointestinal adenocarcinoma | After | ||
| Canjuga et al., 2008 (28) | 78 | F | Papillomatous growth | Lips, buccal mucosa, and hard palate | Verrucous changes and tiny pigmented macules | Right ear auricle | Bladder papillary transitional cell carcinoma | After | |||
| Schnopp et al., 2007 (29) | 44 | F | 15 | Papillomatosis, thickened and furrowed changes | Lips, buccal mucosa, and tongue | Darkening skin, small and velvety plaques | Neck | After | Gastric adenocarcinoma | Before | |
| McGinness et al., 2006 (30) | 81 | F | Burning and soreness | Verrucous papillomatous papules and plaques | Lips, buccal mucosa, and tongue | Accentuation | Palms | Before | Pancreatic adenocarcinoma | Before | |
| Pentenero et al., 2004 (31) | 53 | M | Sore palate | Thickened mucosa with a velvety and papillomatous surface | Lips, buccal mucosa and palate | Velvety rugose appearance, hyperkeratotic verrucous, pigmented, and brownish papules | Palms, back, and axillae | Gastric adenocarcinoma | After | ||
| Cairo et al., 2001 (32) | 73 | M | Burning sensation and pain | Papillomatosis | Vestibular mucosa, gingiva, palate, and dorsum of the tongue | Hyperpigmented and thickened skin | Neck, axillae, and the internal surface of the thighs | Lung carcinoma | Before | ||
| Scully et al., 2001 (33) | 69 | F | 9 | Painless gingival lesions | Swelling, increased stippling, and diffuse thickening | Lower labial mucosa, gingival, and palate but not the edentulous areas | Slightly keratotic, warty lesions, and florid seborrhoeic warts | Palms, soles, axillae, and proximal limbs | Cholangiocarcinoma | ||
| Yeh et al., 2000 (34) | 69 | M | 6 | Papillomatous involvement | Thickened and hyperpigmented skin, papillomatous involvement, and seborrheic keratoses | Face, nape of the neck, axillae, groins, limbs, and trunk | Gastric adenocarcinoma | Before | |||
| Bottoni et al., 2000 (35) | 80 | M | 12 | Papillomatous and verrucous lesions | Lips and oral mucosa | Diffuse brownish hyperpigmentation, velvety thickening, and warty lesions | Neck, axillae groins, and limbs | Non-small cell lung carcinoma | Before | ||
| Ramirez et al., 1999 (17) | 55 | F | 12 | Sore palate | Painless extensive papillomatosis | Upper vermilion and lip mucosa, buccal mucosa, gingiva, palate, and dorsum of the tongue | Hair loss | Axillary, palpebral, and scalp | Gallbladder adenocarcinoma | Before |
Malignant acanthosis nigricans with oral manifestation literature search (1999–2024).
In conclusion, a significant percentage of malignant acanthosis nigricans patients exhibited oral lesions prior to the detection of the underlying malignancy. Therefore, clinicians, especially oral healthcare professionals, should remain vigilant. Detailed differential diagnosis is necessary, and a comprehensive systemic examination is required to facilitate early diagnosis of malignancies and improve patient prognosis. Furthermore, in contrast to previous cases, our patient was only 30 years old and considered herself to be in a healthy condition. This suggests that age may not be a restrictive factor for malignant acanthosis nigricans. On the other hand, the rash may coexist with skin and mucosal lesions, warranting that differentiation from allergies and clinical observations of mucosal manifestations after the regression of the rash are important.
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.
Ethics statement
Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.
Author contributions
ZL: Data curation, Formal analysis, Funding acquisition, Investigation, Writing – original draft. WC: Data curation, Investigation, Writing – original draft. YL: Conceptualization, Funding acquisition, Supervision, Validation, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the Fujian Provincial Health Technology Project (2022QNB027) and Program for New Clinical Techniques and Therapies of Peking University School and Hospital of Stomatology (PKUSSNCT-23A05). The funders had no role in the study design, data collection and analysis, and decision on publication or manuscript preparation.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fonc.2024.1459148/full#supplementary-material
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Summary
Keywords
malignant acanthosis nigricans, malignancy, papillomatosis, velvety hyperplasia, gastric cancer, case report
Citation
Liu Z, Cao W and Liu Y (2024) Malignant acanthosis nigricans with oral manifestations in a young female: a case report and literature review. Front. Oncol. 14:1459148. doi: 10.3389/fonc.2024.1459148
Received
03 July 2024
Accepted
02 September 2024
Published
24 September 2024
Volume
14 - 2024
Edited by
Hem Chandra Jha, Indian Institute of Technology Indore, India
Reviewed by
M. Badawy Abdel-Naser, New York University, United States
Walter Belda, University of São Paulo, Brazil
Marcela Saeb Lima, National Institute of Medical Sciences and Nutrition Salvador Zubirán, Mexico
Updates
Copyright
© 2024 Liu, Cao and Liu.
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*Correspondence: Yang Liu, shannon13579@163.com
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.