1 Skin Cancer Research Group, School of Public Health and Tropical Medicine, James Cook University, Townsville, Queensland, Australia.
2 Queensland Institute of Medical Research, Brisbane, Queensland, Australia.
3 Victorian Melanoma Service and Dermatology Unit, Monash University Department of Medicine, Alfred Hospital, Melbourne, Victoria, Australia.
4 Division of Dermatology, Department of Medicine, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
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ABSTRACT |
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melanoma; nevi and melanomas; nevus, pigmented
Abbreviations: CI, confidence interval; SD, standard deviation
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INTRODUCTION |
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The skin's pigmented lesions have the advantage of being visible. Recognizing melanocytic nevi in adults can be difficult even for trained observers, because of the effects of sun damage, the presence of solar lentigines, and the appearance of other pigmented lesions such as seborrheic keratoses. However, these factors are less problematic in children. Studies investigating agreement among medical professionals in diagnosing morphologic features of pigmented lesions, especially clinical atypia of melanocytic nevi, have shown limited reliability (18, 19
). On the other hand, several studies found reasonable-to-good agreement between counts of melanocytic nevi when similarly trained observers were compared (20
24
), particularly when the subjects were children or adolescents (21
, 22
, 24
). The observers with the greatest access to children are their parents or guardians. This group has tremendous potential for monitoring of melanocytic nevi in children.
The purpose of this study was to evaluate the ability of parents, using simple illustrated instructions, to recognize, count, record, and measure melanocytic nevi on the backs of their children and to identify factors that might be responsible for inaccuracies in their assessments. In addition, the usefulness of photographs in assessing melanocytic nevi was investigated.
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MATERIALS AND METHODS |
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Parental assessment of skin lesions
The parents of each child were sent 1) illustrated instructions teaching them how to recognize melanocytic nevi, 2) a clear plastic film imprinted with thin black circles 2 mm and 5 mm in diameter with which to measure nevus size, and 3) an outline of the human back on which to record the position and size of each nevus observed. The shoulders were defined as the area above the scapulae, because of the potential for large numbers of freckles and solar lentigines on the shoulders and their possible misclassification. Color photographs showed parents the features of countable melanocytic nevi and noncountable lesions. The parents were asked to: study the instructions provided; examine their child's back for melanocytic nevi under bright lighting; measure lesions they recognized as melanocytic nevi with the skin unstretched using the circles on the plastic film; record each nevus that was greater than or equal to 2 mm in diameter by marking its location on the anatomic diagram; and indicate which melanocytic nevi were greater than or equal to 5 mm in diameter. Melanocytic nevi were considered greater than or equal to 2 mm in diameter if the widest part of the lesion touched both sides of the 2-mm circle, and they were considered greater than or equal to 5 mm in diameter if both sides of the lesion touched or overlapped the 5-mm circle.
The parents of 324 children (77 percent of the available sample of 421 children) counted their child's melanocytic nevi and returned a completed diagram to us prior to the commencement of the clinical examinations.
Dermatologic examination
Seventy-seven of the 324 children whose parents had counted their melanocytic nevi were examined by an experienced dermatologist (J. K. R.) according to a standard international protocol (25). The other 247 children were examined by two dermatology trainees. Only the findings of the experienced dermatologist were treated as the "gold standard." In postpubertal girls, the skin of the breasts was not examined, and brassieres were not removed. During the clinical examination, a small round adhesive sticker was placed in the center of an imaginary line drawn from the tips of the acromion to the superior margins of the spines of the scapulae to mark the upper boundary of the back. A similar sticker was placed in the center of the lower boundary of the back, defined by a line from the iliac crests to the posterior superior iliac spines. These boundaries matched the upper and lower boundary lines drawn on the anatomic map of the back given to parents. An adhesive millimeter scale was labeled with the child's name and identification number and placed centrally between the shoulders, above the spines of the scapulae.
Lesions counted as melanocytic nevi were brown-to-black macules or papules greater than or equal to 2 mm in diameter and darker than the surrounding skin (9, 25
). Nevus size was measured with the skin unstretched using a clear plastic film with thin black circles 2 mm and 5 mm in diameter drawn on it. No attempt was made to differentiate lentigo simplex from junctional melanocytic nevi. Lesions with the clinical characteristics of freckles, solar lentigines, and café-au-lait spots were recorded separately. The distribution and density of freckling on the face, arms, and shoulders were assessed quantitatively (on a scale of 0100, in increments of 10) using standard drawings (8
, 26
). Skin reflectance at 685 nm was determined for the left inner upper arm using an Evans Electroselenium reflectance spectrophotometer (Diffusion Systems Ltd., London, United Kingdom). Skin reflectance was categorized as fair (
67 percent), medium (64.066.9 percent), or olive (<64.0 percent) using previously established cutoff points (9
, 11
, 27
). Hair and eye color were assessed through comparisons with standard hair samples from wig manufacturers and color prints of a range of eye colors.
Photographic assessment
Directly after the clinical examination, a slide photograph of the back of each child was taken (by R. M.) using Kodachrome 64 film (Eastman Kodak Company, Rochester, New York) and a Nikon F3 camera with a type E (matte) focusing screen, a 55-mm Micro-Nikkor lens, and an SB17 electronic angle flash unit with a diffuser covering the flash tube (Nikon Corporation, Tokyo, Japan). The slides were later projected and compared (by S. L. H.) with the anatomic diagrams of the children's backs that had been completed by parents. The overall pattern of melanocytic nevi drawn on the diagrams was compared with the pattern of countable lesions evident from the slides, and results were classified as very similar, similar, or dissimilar. A divider from a geometric instrument set was calibrated against the projected millimeter scale to an opening of 2 mm. Melanocytic nevi were then measured from the projected image, and those greater than or equal to 2 mm in diameter were identified. Melanocytic nevi greater than or equal to 5 mm were similarly identified. The assessor of the slides was "blind" to the dermatologist's counts.
Lesions which were marked by parents on the diagram in positions that were likely to be obscured by clothing in the photograph (brassieres, waist-high underpants, swimsuits) could not be assessed and were excluded from the comparison. Lesions designated false-positive included those drawn by parents which could not be seen on the projected slide and those which had been misclassified as melanocytic nevi. The numbers of lesions that were correctly identified by parents as melanocytic nevi but either were too small to be counted (<2 mm) or could not be located in the diagrammed area of the back (melanocytic nevi visible on the shoulders, buttocks, or arms) were recorded separately.
Statistical analysis
Counts of melanocytic nevi are described here in terms of median values and ranges, because the distributions were skewed. Agreement between counts of melanocytic nevi was assessed graphically by plotting the difference between counts against the average of counts (28), separately for parental counts versus dermatologist counts (figure 1), parental counts versus counts obtained from photographs (figure 2), and dermatologist counts versus counts obtained from photographs (figure 3). The mean differences and standard deviations of the differences were calculated. In a case of good agreement, the plot of differences against mean values results in differences that are normally distributed around zero irrespective of the average values. The relations between differences and averages were assessed using linear regression analyses. The equations of the linear regression lines are given here along with Pearson's correlation coefficient (r).
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As appropriate, parametric and nonparametric bivariate statistical tests were used to assess relations between similarity of melanocytic nevus patterns and differences in melanocytic nevus counts by age, skin reflectance, eye color, hair color, freckling, and total melanocytic nevus count. Nonparametric tests were used to compare differences between parental and dermatologist counts according to the participating parent's gender and education and the birthplace of the participating parent's parents. Multiple linear regression analysis was used to determine whether any parental factors had a significant impact on the accuracy of parental counts. Differences between parental and dermatologist counts were characterized dichotomously as parental undercounting (yes/no) of nevi greater than or equal to 2 mm in diameter and parental undercounting of nevi greater than or equal to 5 mm in diameter. Multiple logistic regression analyses were used to identify predictors of undercounting by parents. Predictors of undercounting for parental counts versus photograph counts and for photograph counts versus dermatologist counts were similarly identified. Statistical analyses were performed with SPSS for Windows (version 6.3.1), and p values less than 0.05 were considered statistically significant. All p values shown are two-sided.
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RESULTS |
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Agreement between parental nevus counts and counts made by an experienced dermatologist
Compared with counts made by the dermatologist (n = 77), parents on average underestimated the number of melanocytic nevi greater than or equal to 2 mm in diameter (mean difference = -3.2, standard deviation (SD) 6.8; figure 1). Approximately 68 percent of parents underestimated the number of melanocytic nevi greater than or equal to 2 mm in diameter. There was a significant negative relation between differences and averages (r = -0.56, p < 0.0001; regression line: difference = 1.47 - 0.59 x average), showing that the likelihood of parents' underestimating the number of melanocytic nevi greater than or equal to 2 mm in diameter on their child's back increased with the number of melanocytic nevi. Logistic regression analysis revealed that freckling (odds ratio = 1.04, 95 percent confidence interval (CI): 1.00, 1.08; p = 0.083) and the other phenotypic and demographic variables investigated were not significant predictors of underestimation by parents. Neither the gender (nevi 2 mm: p = 0.88; nevi
5 mm: p = 0.73) nor the educational level (nevi
2 mm: p = 0.37; nevi
5 mm: p = 0.18) of the participating parent had a significant influence on the accuracy of counting. Participating parents whose parents had both been born in Australia were more likely to undercount melanocytic nevi greater than or equal to 2 mm in diameter (median difference = -2 (interquartile range: -7.75 to -0.25)) than were participants with at least one parent who had been born outside of Australia (median difference = -0.5 (interquartile range: -2.75 to 1); p = 0.034). Participating parents with two Australian-born parents may have undercounted melanocytic nevi greater than or equal to 2 mm in diameter more often because their children had more melanocytic nevi, according to the dermatologist's assessment (median number of nevi
2 mm = 8.5 (interquartile range: 4 to 14.5)), than the children of participating parents whose mother or father or both had been born overseas (median number of nevi
2 mm = 4.5 (interquartile range: 2 to 8.75)) (p = 0.016). Multiple linear regression analysis confirmed the effect of number of melanocytic nevi (p < 0.0001) on the difference between parental counts and dermatologist counts, but the birthplace of the participating parent's parents was no longer significant (p = 0.43).
The concordance correlation coefficient assessing agreement between parental counts of melanocytic nevi greater than or equal to 2 mm in diameter and dermatologist counts was the lowest out of all of the assessments made (rc = 0.51) (table 2). On average, parents slightly overestimated the number of melanocytic nevi greater than or equal to 5 mm in diameter (mean difference = 0.35, SD 1.3). The relation between differences and averages of counts of melanocytic nevi greater than or equal to 5 mm in diameter was not significant (r = 0.22, p = 0.054; regression line: difference = 0.17 + 0.15 x average). Eight parents (10.4 percent) underestimated the number of melanocytic nevi greater than or equal to 5 mm in diameter.
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Agreement between nevus counts obtained from photographs and dermatologist counts
Compared with the dermatologist counts, nevus counts obtained from photographs underestimated the number of melanocytic nevi greater than or equal to 2 mm in diameter (mean difference = -2.9, SD 4.0; figure 3). There was a significant negative relation between differences and averages (r = -0.65, p < 0.0001; regression line: difference = -0.09 - 0.35 x average), showing that differences between counts of melanocytic nevi greater than or equal to 2 mm in diameter obtained from photographs and those made by the dermatologist increased with the number of melanocytic nevi on the child's back as assessed by the dermatologist. In 79.2 percent of photographs, counts of melanocytic nevi greater than or equal to 2 mm in diameter were lower than those made by the dermatologist. Logistic regression analysis identified number of melanocytic nevi greater than or equal to 2 mm in diameter as assessed by the dermatologist (odds ratio = 1.16, 95 percent CI: 1.02, 1.31; p = 0.025) as the only significant predictor of undercounting from photographs. Counts of melanocytic nevi greater than or equal to 5 mm taken from photographs were slightly lower than counts made by the dermatologist (mean difference = -0.17, SD 0.87), and there was a significant relation between differences and averages (r = -0.38, p = 0.001; regression line: difference = 0.02 - 0.20 x average). According to the concordance correlation coefficient, agreement between photographic and dermatologic counts was high for melanocytic nevi greater than or equal to 2 mm in diameter and very high for melanocytic nevi greater than or equal to 5 mm in diameter (table 2). The number of melanocytic nevi greater than or equal to 5 mm was underestimated on nine photographs (11.7 percent).
Parental problems in assessing melanocytic nevi
Of the 324 diagrams of the back that were assessed, 159 (49.1 percent) showed a pattern of melanocytic nevi that was subjectively very similar to that seen on the photograph; 148 diagrams (45.7 percent) showed a pattern similar to that seen on the photograph; and 17 diagrams (5.2 percent) showed a pattern judged to be unlike that of the photograph. Diagrams of children with low counts of melanocytic nevi greater than or equal to 2 mm in diameter were less likely to have a pattern considered similar to the one seen in the photograph than diagrams of children with many melanocytic nevi (p = 0.027). No other factors were found to significantly influence the subjective assessment of similarity.
A direct comparison of the diagrams completed by the parents with the slides allowed an evaluation of the problems parents had encountered when assessing their children's melanocytic nevi. Parents identified a total of 2,178 assessable lesions as melanocytic nevi. Of these lesions, 167 (7.7 percent) were classified as melanocytic nevi less than 2 mm in diameter by the experienced non-medical-examiner (S. L. H.) who reviewed the photographs. Seventy-six parents (23.5 percent) had difficulty in adhering to the 2-mm cutoff; however, most (73.7 percent) of the parents who included melanocytic nevi under 2 mm in their counts generally included only one or two such lesions. A total of 120 parents (37.0 percent) included melanocytic nevi that were outside the area defined as the back, with lesions on the shoulders causing the greatest amount of error (113 parents' marking 223 lesions). Similarly, 12 parents included 14 lesions that were on the buttocks and four parents included four lesions that were on the arm in their melanocytic nevus counts for the back. Nine of these parents included lesions from more than one site other than the back in their counts of "back" melanocytic nevi. Eleven (0.5 percent) of the 2,178 assessable lesions detected by parents were incorrectly classified as melanocytic nevi, and another 63 lesions (2.9 percent) were not visible to the observer when the photographs were studied. In comparison with the photographs, parents correctly classified 1,696 lesions (77.9 percent) as back melanocytic nevi greater than or equal to 2 mm in diameter.
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DISCUSSION |
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The results of the few studies that have compared self-reports of melanocytic nevi with clinical assessments are difficult to compare directly because of differences in design and analysis (3034
). Three studies concluded that self-assessment of melanocytic nevi (whole-body self-counts of large (
5 mm) melanocytic nevi, counts of palpable melanocytic nevi on the arm and counts of large melanocytic nevi on the whole body, and counts of melanocytic nevi on the trunk) was quite comparable to counts derived from clinical examinations, and self-assessment was therefore suggested as a useful way of identifying people at risk for cutaneous melanoma (31
, 32
, 35
). In contrast, three other studies found rather poor agreement between self-reports of melanocytic nevi and physician-conducted counts (counts of atypical melanocytic nevi on the lower extremities in women, four categories of severity of "moliness" shown in whole-body diagrams compared with counts of melanocytic nevi on the arm, and whole-body counts of melanocytic nevi and atypical melanocytic nevi) (30
, 33
, 34
). In addition, one study showed that the reproducibility of self-counts of palpable melanocytic nevi on the arm was inadequate (36
).
Assessment of melanocytic nevi by another person (e.g., a parent assessing a child) is arguably an improvement over skin self-examination. Therefore, it is not surprising that in this study, agreement between the parental counts, the dermatologist's counts, and the counts obtained from photographs was reasonably good, particularly for melanocytic nevi greater than or equal to 5 mm in diameter. However, these findings do not necessarily imply that minimally instructed laypersons are capable of distinguishing melanocytic nevi from other pigmented lesions in adult subjects.
Parental estimates of melanocytic nevi greater than or equal to 2 mm in diameter were lower on average than counts made by the dermatologist and counts obtained from the photographs, and the likelihood of underestimation increased with the number of nevi. Parents were instructed not to count a pigmented lesion if they were not certain it was a melanocytic nevus. Although this approach may have led to underestimation of melanocytic nevi, the benefits of this approach were evident in that relatively few false-positive lesions were recorded. The conservative instructions given to parents may explain why the presence of freckling contributed to parental underestimation of melanocytic nevi greater than or equal to 5 mm in diameter in comparison with the photograph counts (n = 324). Although freckling was not found to be a significant predictor of parental underestimation of melanocytic nevi greater than or equal to 2 mm in diameter relative to the dermatologist's counts (p = 0.083), the sample was relatively small (n = 77).
Although we do not believe that parents should replace physicians in the counting of melanocytic nevi in epidemiologic surveys, our results suggest that parents are quite capable of recognizing and counting melanocytic nevi on their children's skin using an instrument that includes simple text and color photographs showing what to count and what not to count. Parents should be encouraged to examine their children's skin regularly, since this practice may imprint the routine of skin examination on the children and lead to greater skin familiarity in adulthood and an increased likelihood of detecting suspicious changes sooner (37). This practice would also facilitate the early identification of children at increased risk of developing melanoma in the future, so that their families could be educated to be vigilant in protecting them from overexposure to sunlight.
Assessment of melanocytic nevi from good-quality standardized photographs (25) offers a number of advantages. Firstly, evaluation of photographs can occur after a physical examination in a standardized manner and with a smaller number of trained examiners. This approach removes the time constraints and other pressures (e.g., crying, wriggling children) that may diminish the accuracy of counts of melanocytic nevi made in the field. Secondly, photographs can be reviewed repeatedly and by independent observers, improving the ease with which intra- and interobserver reliability studies can be undertaken. Lastly, photographs make it possible to follow the natural history of individual melanocytic nevi and accurately monitor their growth in cohort studies. The only obvious disadvantage of using photographs to replace counting in the field is the need to adhere to an arbitrary size cutoff. The naked eye can distinguish melanocytic nevi on the skin that are very much smaller than 2 mm in diameter, while the resolution of a photograph is such that it is not always possible to see these tiny melanocytic nevi on a projected image (24
). Further investigation is required to determine whether this problem can be overcome using high-resolution digital images.
The present study showed that agreement between counts of melanocytic nevi obtained from photographs and counts performed by an experienced dermatologist was high for nevi greater than or equal to 2 mm in diameter and almost perfect for nevi greater than or equal to 5 mm in diameter. However, similar to the case with the parents, photograph counts were significantly more likely to underestimate numbers of melanocytic nevi in comparison with dermatologist counts when the subject had many melanocytic nevi greater than or equal to 2 mm in diameter. These findings are in good concordance with the results of the only other published study that compared photograph counts with direct counts made by trained examiners (21). Thus, future epidemiologic studies in children might safely replace dermatologist field counts of melanocytic nevi greater than or equal to 2 mm in diameter with high-quality photographs, if only the posterior trunk is being assessed. However, before nevus counts from photographs can replace whole-body counts conducted by physicians in the field, a standard approach to taking such photographs must be developed for body sites other than the back (25
). For example, it may be necessary to draw a boundary between the inner and outer surfaces of some body sites (e.g., limbs) before taking photographs, to ensure comparability in the areas counted. In addition, reliability studies of nevus counts obtained from photographs should be conducted.
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ACKNOWLEDGMENTS |
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NOTES |
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REFERENCES |
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