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Meta-Analysis
. 2018 Dec 4;12(12):CD013187.
doi: 10.1002/14651858.CD013187.

Exfoliative cytology for diagnosing basal cell carcinoma and other skin cancers in adults

Lavinia Ferrante di Ruffano  1 , Jacqueline Dinnes, Naomi Chuchu, Susan E Bayliss, Yemisi Takwoingi, Clare Davenport, Rubeta N Matin, Colette O'Sullivan, Derek Roskell, Jonathan J Deeks, Hywel C Williams; Cochrane Skin Cancer Diagnostic Test Accuracy Group
Affiliations
Meta-Analysis

Exfoliative cytology for diagnosing basal cell carcinoma and other skin cancers in adults

Lavinia Ferrante di Ruffano et al. Cochrane Database Syst Rev. .

Abstract

Background: Early accurate detection of all skin cancer types is essential to guide appropriate management, reduce morbidity and improve survival. Basal cell carcinoma (BCC) is usually localised to the skin but has potential to infiltrate and damage surrounding tissue, while cutaneous squamous cell carcinoma (cSCC) and melanoma have a much higher potential to metastasise and ultimately lead to death. Exfoliative cytology is a non-invasive test that uses the Tzanck smear technique to identify disease by examining the structure of cells obtained from scraped samples. This simple procedure is a less invasive diagnostic test than a skin biopsy, and for BCC it has the potential to provide an immediate diagnosis that avoids an additional clinic visit to receive skin biopsy results. This may benefit patients scheduled for either Mohs micrographic surgery or non-surgical treatments such as radiotherapy. A cytology scrape can never give the same information as a skin biopsy, however, so it is important to better understand in which skin cancer situations it may be helpful.

Objectives: To determine the diagnostic accuracy of exfoliative cytology for detecting basal cell carcinoma (BCC) in adults, and to compare its accuracy with that of standard diagnostic practice (visual inspection with or without dermoscopy). Secondary objectives were: to determine the diagnostic accuracy of exfoliative cytology for detecting cSCC, invasive melanoma and atypical intraepidermal melanocytic variants, and any other skin cancer; and for each of these secondary conditions to compare the accuracy of exfoliative cytology with visual inspection with or without dermoscopy in direct test comparisons; and to determine the effect of observer experience.

Search methods: We undertook a comprehensive search of the following databases from inception up to August 2016: Cochrane Central Register of Controlled Trials; MEDLINE; Embase; CINAHL; CPCI; Zetoc; Science Citation Index; US National Institutes of Health Ongoing Trials Register; NIHR Clinical Research Network Portfolio Database; and the World Health Organization International Clinical Trials Registry Platform. We also studied the reference lists of published systematic review articles.

Selection criteria: Studies evaluating exfoliative cytology in adults with lesions suspicious for BCC, cSCC or melanoma, compared with a reference standard of histological confirmation.

Data collection and analysis: Two review authors independently extracted all data using a standardised data extraction and quality assessment form (based on QUADAS-2). Where possible we estimated summary sensitivities and specificities using the bivariate hierarchical model.

Main results: We synthesised the results of nine studies contributing a total of 1655 lesions to our analysis, including 1120 BCCs (14 datasets), 41 cSCCs (amongst 401 lesions in 2 datasets), and 10 melanomas (amongst 200 lesions in 1 dataset). Three of these datasets (one each for BCC, melanoma and any malignant condition) were derived from one study that also performed a direct comparison with dermoscopy. Studies were of moderate to poor quality, providing inadequate descriptions of participant selection, thresholds used to make cytological and histological diagnoses, and blinding. Reporting of participants' prior referral pathways was particularly poor, as were descriptions of the cytodiagnostic criteria used to make diagnoses. No studies evaluated the use of exfoliative cytology as a primary diagnostic test for detecting BCC or other skin cancers in lesions suspicious for skin cancer. Pooled data from seven studies using standard cytomorphological criteria (but various stain methods) to detect BCC in participants with a high clinical suspicion of BCC estimated the sensitivity and specificity of exfoliative cytology as 97.5% (95% CI 94.5% to 98.9%) and 90.1% (95% CI 81.1% to 95.1%). respectively. When applied to a hypothetical population of 1000 clinically suspected BCC lesions with a median observed BCC prevalence of 86%, exfoliative cytology would miss 21 BCCs and would lead to 14 false positive diagnoses of BCC. No false positive cases were histologically confirmed to be melanoma. Insufficient data are available to make summary statements regarding the accuracy of exfoliative cytology to detect melanoma or cSCC, or its accuracy compared to dermoscopy.

Authors' conclusions: The utility of exfoliative cytology for the primary diagnosis of skin cancer is unknown, as all included studies focused on the use of this technique for confirming strongly suspected clinical diagnoses. For the confirmation of BCC in lesions with a high clinical suspicion, there is evidence of high sensitivity and specificity. Since decisions to treat low-risk BCCs are unlikely in practice to require diagnostic confirmation given that clinical suspicion is already high, exfoliative cytology might be most useful for cases of BCC where the treatments being contemplated require a tissue diagnosis (e.g. radiotherapy). The small number of included studies, poor reporting and varying methodological quality prevent us from drawing strong conclusions to guide clinical practice. Despite insufficient data on the use of cytology for cSCC or melanoma, it is unlikely that cytology would be useful in these scenarios since preservation of the architecture of the whole lesion that would be available from a biopsy provides crucial diagnostic information. Given the paucity of good quality data, appropriately designed prospective comparative studies may be required to evaluate both the diagnostic value of exfoliative cytology by comparison to dermoscopy, and its confirmatory value in adequately reported populations with a high probability of BCC scheduled for further treatment requiring a tissue diagnosis.

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Conflict of interest statement

Lavinia Ferrante di Ruffano: none known. Jac Dinnes: none known. Naomi Chuchu: none known. Susan E Bayliss: none known. Yemisi Takwoingi: none known. Clare Davenport: none known. Rubeta N Matin: "my institution received a grant for a Barco NV commercially sponsored study to evaluate digital dermoscopy in the skin cancer clinic. My institution also received Oxfordshire Health Services Research Charitable Funds for carrying out a study of feasibility of using the Skin Cancer Quality of Life Impact Tool (SCQOLIT) in non melanoma skin cancer. I have received royalties for the Oxford Handbook of Medical Dermatology (Oxford University Press) and payment from the UK Photopheresis Society for a lecture on cutaneous graft versus host disease (October 2017). I have received payment from Public Health England for the "Be Clear on Cancer" skin cancer report. I have no conflicts of interest to declare that directly relate to the publication of this work." Colette O'Sullivan: none known. Derek Roskell: none known. Jonathan J Deeks: none known. Hywel C Williams is the director of the NIHR HTA Programme. HTA is part of the NIHR, which also supports the NIHR systematic reviews programme from which this work is funded.

Figures

1
1
Sample photographs of BCC (left) and cSCC (right). Copyright © 2012 Dr Rubeta Matin: reproduced with permission.
2
2
Cytological image of BCC using Papanicoloau stain showing a tissue fragment of BCC on the left and anucleate squamous cells from the epidermis on the right. Copyright © 2017 Derek Roskell: reproduced with permission.
3
3
Cytological image of a BCC using Giemsa stain. Focally the nuclei are aligned perpendicular to the basement edge of the cluster (peripheral palisading), a feature characteristic of BCC. Copyright © 2017 Derek Roskell: reproduced with permission.
4
4
Cytological image of a BCC using Giemsa stain. The BCC cells are tightly cohesive in a cluster with a distinct edge to the group. Copyright © 2017 Derek Roskell: reproduced with permission.
5
5
Current clinical pathway for people with skin lesions.
6
6
PRISMA flow diagram.
7
7
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study. One study, Durdu 2011, was assessed in the comparative domain as 'unclear' for both risk of bias and applicability concerns.
8
8
Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies. One study, Durdu 2011, was assessed in the comparative domain as 'unclear' for both risk of bias and applicability concerns.
9
9
Forest plot of exfoliative cytology to detect BCC in patients with suspected BCCs, showing classification of 'possible BCCs' as test positives or as test negatives.
10
10
Summary ROC plot of exfoliative cytology to detect BCC in patients with suspected BCCs, showing classification of 'possible BCCs' as test positives or as test negatives.
11
11
Forest plot of studies pooled for accuracy of exfoliative cytology to detect any skin cancer in patients with suspected BCCs, comparing: classification of 'possible BCCs' as test positives versus classification of 'possible BCCs' as test negatives.
12
12
Summary ROC plot of pooled studies for accuracy of exfoliative cytology to detect any skin cancer in patients with suspected BCCs, comparing: classification of 'possible BCCs' as test positives versus classification of 'possible BCCs' as test negatives.
1
1. Test
Exfoliative cytology ‐ BCC (possible BCCs classified as test positives).
2
2. Test
Exfoliative cytology ‐ BCC (possible BCCs classified as test negatives).
3
3. Test
Exfoliative cytology ‐ BCC (pigmented lesion population).
4
4. Test
Dermoscopy ‐ BCC (pigmented lesion population).
5
5. Test
Exfoliative cytology ‐ BCC (mixed population, Munchener diagnostic criteria).
6
6. Test
Exfoliative cytology ‐ cSCC (suspected BCC population).
7
7. Test
Exfoliative cytology ‐ cSCC (mixed population, Munchener diagnostic criteria).
8
8. Test
Exfoliative cytology ‐ melanoma (pigmented lesion population).
9
9. Test
Dermoscopy ‐ melanoma (pigmented lesion population).
10
10. Test
Exfoliative cytology ‐ any skin cancer (suspected BCC population, possible BCCs classified as test positives).
11
11. Test
Exfoliative cytology ‐ any skin cancer (suspected BCC population, possible BCCs classified as test negatives).
12
12. Test
Exfoliative cytology ‐ any skin cancer (pigmented lesion population).
13
13. Test
Dermoscopy ‐ any skin cancer (pigmented lesion population).
14
14. Test
Exfoliative cytology ‐ any skin cancer (mixed population, Munchener diagnostic criteria).
15
15. Test
Exfoliative cytology (Papanicolaou + MGG stain) ‐ BCC (stain comparison).
16
16. Test
Exfoliative cytology (MGG stain) ‐ BCC (stain comparison).
17
17. Test
Exfoliative cytology (Papanicolaou stain) ‐ BCC (stain comparison).
See this image and copyright information in PMC

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