ORIGINAL
ARTICLE
Turning the tide? Changes in treatment rates for keratinocyte cancers in Australia 2000 through 2011 Catherine M. Olsen, PhD,a Patricia F. Williams, MD,b and David C. Whiteman, MBBS, PhDa Queensland, Australia, and Richmond, Virginia Background: Keratinocyte cancers (basal cell carcinoma, squamous cell carcinoma) are the commonest cancers in human beings. Population data on incidence trends are scant because few jurisdictions reliably record diagnoses or treatments. Objective: We sought to examine temporal trends of treating keratinocyte cancers in Australia. Methods: We analyzed Medicare Australia data relating to the diagnosis and treatment of keratinocyte skin cancer between 2000 and 2011. We examined counts and rates for each procedure, and the average annual percentage rate of change. Results: There were significant increases in excision rates for keratinocyte cancers (3.3% per annum for men and 2.2% per annum for women), however temporal trends differed significantly by age group. Although annual increases in excision rates were highest for men aged 75 to 84 years (8.6% per annum), they declined significantly for men and women younger than 45 years. Skin biopsy rates increased substantially in all age groups over the study period, suggesting no lessening in skin cancer surveillance in any age group. Limitations: The Medicare data do not include services provided in public hospitals, however fewer than 2% of skin cancers are treated in these settings. Conclusions: Although overall treatment rates for keratinocyte cancers have increased substantially during the past decade, excision rates are declining in younger Australians. ( J Am Acad Dermatol http:// dx.doi.org/10.1016/j.jaad.2014.02.011.) Key words: basal cell carcinoma; skin cancer; squamous cell carcinoma.
A
ustralia has the highest incidence of keratinocyte cancers (basal cell carcinoma [BCC], squamous cell carcinoma [SCC]) in the world.1 Each year, almost 2% of the population is estimated to develop BCC or SCC,2 and the costs of treating these cancers are higher than for any other cancer in Australia.3,4 In response, campaigns to reduce population sun exposure have been implemented with the goal of reducing the incidence of keratinocyte cancers.5 Commencing in the 1980s with the Slip! Slop! Slap! Campaign in Queensland,6
these strategies evolved into the comprehensive SunSmart program in the 1990s,7 which has continued to the present day. Primary prevention programs with similar intent have been enacted in other populations around the world.8-10
From the Cancer Control Group, Population Health Department, QIMR Berghofer Medical Research Institute,a and Virginia Commonwealth University Dermatology Residency Program.b Drs Olsen and Williams contributed equally to this manuscript and are recognized as equal first authors. Dr Whiteman is a Future Fellow of the Australian Research Council. Dr Williams was supported by the Virginia Commonwealth University School of Medicine. Conflicts of interest: None declared.
Accepted for publication February 5, 2014. Reprint requests: Catherine M. Olsen, PhD, QIMR Berghofer Medical Research Institute, Post Office Royal Brisbane Hospital, Q 4029 Australia. E-mail: Catherine.Olsen@ qimrberghofer.edu.au. Published online March 28, 2014. 0190-9622/$36.00 Ó 2014 by the American Academy of Dermatology, Inc. http://dx.doi.org/10.1016/j.jaad.2014.02.011
Abbreviations used: AAPC: BCC: SCC:
average annual percentage rate of change basal cell carcinoma squamous cell carcinoma
1
2 Olsen, Williams, and Whiteman
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To gauge the impact of prevention programs, it is and thus for which the relevant period was 2006 necessary to monitor incidence rates over time. through 2011. Population-based data for keratinocyte cancers are For each item number, we obtained the number of scarce,11,12 but the available data suggest that inciprocedures performed for each Australian state and dence rates have been increasing in all populations territory for every year of the past decade from the where reliable records exist,13 including in statistics page of the Medicare World Wide Web Sweden,14 the United States,15 The Netherlands,16 site (https://www.medicareaustralia.gov.au/statistics/ and Australia.2 mbs_item.shtml). We queried Medicare is Australia’s ‘‘counts,’’ and ‘‘counts per CAPSULE SUMMARY universal health care system, capita’’ of services, stratified which subsidizes virtually all by calendar year from Population data to monitor performance medical services outside of January 2000 to December of prevention programs for keratinocyte the public hospital system for 2011. All data were imported cancers are scant. all citizens and permanent into Microsoft Excel In Australia, between 2009 through 2011, residents, regardless of age (Microsoft, Redmond, WA) there was a significant decline in excision or other factors; the total for analysis. For first surgical rates for keratinocyte cancers among Medicare-registered populatreatment of keratinocyte those younger than 45 years. tion closely approximates cancer, cryotherapy and the total estimated resident serial curettage or excision Continued monitoring will determine population.17 The near comof histologically confirmed whether these declines are sustained malignant lesions and also plete uptake of Medicare into the future. diagnostic biopsy proceservices, coupled with site-, dures, we examined the size-, and histology-specific data stratified by sex and age group (5-year age item codes for skin conditions, makes it possible to groups). estimate the national incidence of procedures for To assess whether trends identified in treatment diagnosing and treating keratinocyte cancers in the services were specific for keratinocyte cancers or Australian population, and to examine trends over reflected broader trends in dermatologic practice, we time. also collected data on the surgical and nonsurgical By analyzing these data,18 we sought to describe the treatment of benign skin lesions and melanomas, and trends in clinical diagnosis and treatment of BCC and the nonsurgical treatment of premalignant skin leSCC in Australia during the period 2000 through 2011. sions. We plotted the counts and counts per capita of services by year to identify trends. We calculated the average annual percentage rate of change (AAPC) for METHODS counts per capita for the period 2000 through 2011 We obtained all data from the Medicare Australia using the Joinpoint Regression Program, Version 4.0.4. World Wide Web site (http://www.medicareaustralia. May 2013 (Statistical Research and Applications gov.au; accessed between May-June, 2012). We Branch, National Cancer Institute, Bethesda, MD).20 identified all item numbers representing procedures All but 1 of the 25 item numbers relating to residual and for the diagnosis and treatment of skin cancers using recurrent disease were first designated in 2005. Upon the Medicare Benefits Schedule Book of Therapeutic review, we excluded data for these 24 items for the Procedures, Category 3, operating from May 1, 201218 year 2005 as unreliable, as indicated by very low (item numbers are summarized in Appendix I). procedure counts in this first year of implementation, Surgical excision is the recommended treatment for and there were insufficient time points to calculate the all primary melanoma and most keratinocyte skin AAPC for this group of items. To test for differences in cancers, although various nonsurgical treatments are AAPC by sex, we used the pairwise comparison option appropriate for some lesions.19 For the item codes in the Joinpoint Regression Program (Statistical relating to cryotherapy, curettage, and excision, Research and Applications Branch, National Cancer Medicare Australia requires that the diagnosis of Institute), which uses a classic approximate F-test to malignancy is proven by histopathology or compare 2 sets of trend data.21 confirmed by specialist opinion before benefits are claimed. All of the item numbers analyzed in this report were unchanged for the entire study period RESULTS 2000 through 2011, except for the 24 items relating to The past decade has seen substantial increases ‘‘surgical removal of a BCC or SCC that was initially in the number of services to diagnose and treat treated surgically,’’ which were introduced in 2005 keratinocyte cancers in Australia. Table I presents the d
d
d
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Olsen, Williams, and Whiteman 3
Table I. Counts and counts per capita with average annual percent rate of change for specific procedures Counts per 100,000 persons
Counts Procedure
2000*
2011
Surgical excision Benign lesions (8 items) 535,106 541,793 BCC and SCC, first surgical 329,850 552,098 treatment (8 items) 19,886 23,834 Residual and recurrent BCC and SCC, previously treated surgically* (24 items) Mohs micrographic surgery 3385 10,536 Total 888,227 1,128,261 Biopsy 228,264 738,067 Other treatment (cryotherapy or serial curettage) Benign lesion 90,910 175,493 Premalignant lesion 390,535 614,843 Malignant lesion (5 items) 129,386 201,513 Total 839,095 1,729,916 Grand total 1,727,322 2,858,177
2000*
2011
2709 1671
2402 2448
95
106
17 4492 1155
47 5003 3272
460 1977 654 4246 8738
778 2726 895 7671 12,674
AAPC, % (95% CI) Women
1.3 (e2.0 to 2.2 (1.6-2.8)
Men
0.6)
0.8 (e1.5 to 3.3 (2.6-4.0)
9.3 (7.9-10.6)
11.7 (10.3-13.1)
7.3 (5.2-9.4)
8.0 (5.5-10.6)
3.1 (0.7-5.6) 1.4 (e0.1 to 2.8) 1.6 (0.7-2.6)
4.5 (2.2-6.9) 2.9 (1.3-4.6) 3.3 (2.3-4.3)
Py
0.1) \.001 \.001
\.001 .001
\.001 \.001 .004
AAPC, Average annual percentage rate of change; BCC, basal cell carcinoma; CI, confidence interval; SCC, squamous cell carcinoma. *Residual and recurrent BCC and SCC surgical treatment were itemized for the first time in 2005 and there were insufficient data points to calculate the AAPC. y For pairwise comparison between men and women.
counts and rates for the years 2000 and 2011 with the AAPC over the decade for skin cancer treatment and diagnosis. To assess whether these trends were specific for keratinocyte cancers, we generated equivalent data for excisions for melanoma. Surgical treatment of skin cancer Temporal trends in rates of first-time excisions of keratinocyte cancers are presented in Fig 1 and Table I. The AAPC for first-time excisions of keratinocyte cancer was 3.3% per annum for men and 2.2% for women and the difference between the sexes, for all age groups, was significant (P \.001). There were marked differences in the AAPC for skin cancer surgery by age group. For BCC and SCC, the excision rates declined significantly for both men and women younger than 45 years between 2000 and 2011. In contrast, the highest rates of change for BCC and SCC excisions were for men aged 75 to 84 years (8.6% per annum) and for women aged 85 and older (5.6%) (Fig 2, A). For melanoma excisions the trends were similar to those observed for BCC and SCC excisions; that is, trends of increasing excision rates among older men and women but significantly declining rates of excision for both men and women younger than 35 years (data not shown). Although a relatively uncommon approach to skin cancer treatment in Australia, Mohs procedures have increased dramatically over the time period (AAPC
Fig 1. Basal cell carcinoma (BCC )/squamous cell carcinoma (SCC ) excision rate for the time period 2000 through 2011. Number of first-time surgical excisions of BCC and SCC per 100,000 persons. See item codes in Appendix I.
9.3% per annum for women and 11.7% per annum for men) (Table I). The rates of Mohs procedures among those younger than 45 years was very low, and was highest among men aged 75 to 84 years. Diagnostic procedures for skin cancer Skin biopsies have increased more than any other skin cancererelated procedure during the past decade; in absolute terms, the skin biopsy rate
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4 Olsen, Williams, and Whiteman
per annum for men and 7.3% for women. The number of excisions for benign skin lesions, including those conducted to exclude a diagnosis of melanoma, has fluctuated over the past decade without a steady trend of increase or decrease (Table I). Nonsurgical treatment of skin cancer Other skin cancer treatments (including cryotherapy and serial curettage) are also presented in Table I. Overall numbers of these treatments for benign, premalignant, and malignant lesions all increased over the time period. In accord with the trend for surgical treatments, other treatments of histologically confirmed keratinocyte cancers over the time period declined significantly for women younger than 45 years and men younger than 55 years (Fig 2, C ).
DISCUSSION
Fig 2. Average annual percentage rate of change (APC ) of counts per 100,000 persons by age group for first-time surgical excisions of basal and squamous cell carcinomas (A), diagnostic biopsy procedures (B), and cryotherapy and serial curettage excision (C) of histologically confirmed malignant lesions for the time period 2000 through 2011.
increased from 1155 3 10 5 in 2000 to 3272 3 10 5 in 2011. Biopsy rates increased in all age groups older than 5 years (Fig 2, B), at an overall average of 8.0%
These analyses reveal a number of notable findings. Firstly, the significant increases in excision and biopsy rates for keratinocyte cancers overall underscore the burden of these cancers in Australia, with more than 1 million procedures performed annually in a population of 23 million. Secondly, and notwithstanding the overall increases, we observed that treatment rates of keratinocyte cancers declined significantly among younger adults. Thirdly, there has been a sizeable increase in the numbers of diagnostic biopsies for skin cancer, across all age groups, consistent with an overall heightened awareness of skin cancer in the population. The declines in excision rates for keratinocyte cancers in the younger age groups are particularly encouraging. These data, derived from a populationwide medical services register, are consistent with smaller surveys suggesting that skin cancer incidence might be declining among younger people.2,22,23 The most recent Australian study estimated BCC and SCC incidence trends by extrapolating data from 4 cross-sectional prevalence surveys conducted in 1985, 1990, 1995, and 2002.2 That study, which mostly preceded the observation period for our study, reported statistically significant trends of increasing skin cancer incidence in people older than 60 years contrasting with ‘‘stable’’ incidence rates in younger age groups. Our study extends the observation period, and suggests that skin cancer incidence trends for older and younger Australians have diverged further in the past 10 years. Such findings would accord with the anticipated effects of skin cancer prevention programs that have been prominent in Australia since the early 1980s5 and that
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would be most likely to benefit recent birth cohorts. Concerns have been expressed recently that skin cancer prevention campaigns may be losing their effectiveness in the light of recent population surveys demonstrating lower levels of sun protection than previously.24 It will therefore be important to monitor treatment rates among the post-1970 birth cohorts as they age to assess whether the declining rates are sustained into the future. Conversely, excision rates among people older than 45 years continued to increase steadily over the study period. Given the long latent period for sunlight-induced cancers25 and population aging, the burden of keratinocyte cancer is likely to remain substantial for some time to come. Skin biopsy rates increased substantially over the time period, raising the possibility that the increases in services to treat skin cancer among older Australians may partially reflect increased diagnostic scrutiny. To explore this issue further would require access to individual patient data that should be available in the future from large Australian cohorts currently in the field.26-28 Data on biopsy positivity rates in Australia are scant, but generally report moderate to high clinical accuracy,29-31 however such studies provide no insights into temporal trends in biopsy positivity rates. Few other population studies have reported trends for keratinocyte cancers separately for different age groups, because these cancers are not routinely collected by the majority of cancer registries. An analysis of the Swedish Cancer Registry reported increasing incidence trends for SCC between 1990 and 2005 of between 3.7% per annum for men and 8.5% per annum for women, with higher rates of increase above age 85 years than below age 85 years.14 A study in New Hampshire reported increases for BCC for all ages between 1979 and 1994.32 The comprehensive nature of Medicare lends credence to our findings. The Medicare database records all services performed by registered providers, with the exception of: (1) services provided by hospital doctors to public patients in public hospitals; and (2) services that qualify for a benefit under the Department of Veterans’ Affairs. Although approximately one third of hospital admissions for melanoma are thought to occur in the public hospital system,33 the vast majority of primary excisions for these cancers occur in outpatient settings.34 Data on patterns of care for keratinocyte cancer in Australia are scant, however the 2002 National Nonmelanoma Skin Cancer Survey reported that only 1.6% of skin cancers diagnosed in 2502 survey respondents were treated in hospital
Olsen, Williams, and Whiteman 5
settings; the highest proportion (51.1%) were treated by general practitioners, with a further 10.3% in skin cancer clinics, 17.6% by dermatologists, 5.9% by plastic surgeons, and 13.5% other/not stated.34 Thus, although the data presented here cannot be considered complete for the entire population, the degree of underestimation is likely to be very small and unlikely to account for the declines in excision rates we have observed in the younger age groups. Because we did not have access to unit record data, we could not enumerate the incidence of multiplicity of treatments. Previous reports have suggested that about one fourth of patients with skin cancer in Australia are given the diagnosis of more than 1 skin cancer per year.2 This could affect interpretation if the proportions of people undergoing multiple excisions for skin cancers changed over time and also differed by age group. We have no evidence that this occurred, but cannot exclude the possibility. The declining rates of treatment for keratinocyte cancers in younger people is not likely to be related to decreased diagnostic scrutiny given our finding of an increase in biopsy rates in all age groups older than 5 years (Fig 2, B). It might also be argued that the declining incidence in young people might reflect demographic changes in Australia; specifically increased intakes of migrants with darker skin types who have inherently lower rates of skin cancer. Again, the increased rate of biopsy in people younger than 45 years suggests that the change in ethnic profile cannot explain the decrease in rate of excisions for this age group. In summary, these analyses confirm that keratinocyte cancers continue to be a major public health problem in the Australian population, with a steadily increasing clinical toll during the past decade. Some grounds for guarded optimism are warranted however, with the emergence of significant declines in treatments for skin cancer among younger generations. It is too early yet to attribute these emerging trends to any single factor, but we anticipate continued scrutiny of these and other data to determine the efficacy of interventions intended to turn the rising tide of skin cancer. REFERENCES 1. AIHW. Cancer in Australia 2001. Canberra: Australian Institute of Health and Welfare and Australian Association of Cancer Registries; 2004. 2. Staples MP, Elwood M, Burton RC, Williams JL, Marks R, Giles GG. Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985. Med J Aust 2006;184: 6-10.
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3. Australian Institute of Health and Welfare. Health system expenditures on cancer and other neoplasms in Australia, 2000-01. Canberra: Australian Institute of Health and Welfare; 2005. 4. Fransen M, Karahalios A, Sharma N, English DR, Giles GG, Sinclair RD. Non-melanoma skin cancer in Australia. Med J Aust 2012;197:565-8. 5. Montague M, Borland R, Sinclair C. Slip! Slop! Slap! and SunSmart, 1980-2000: skin cancer control and 20 years of population-based campaigning. Health Educ Behav 2001;28: 290-305. 6. Marks R. Skin cancer control in the 1990’s, from Slip! Slop! Slap! To sun smart. Australas J Dermatol 1990;31:1-4. 7. Dobbinson S, Peipers A, Reading D, Sinclair C. A national approach to skin cancer prevention: the national SunSmart schools program. Med J Aust 1998;169:513-4. 8. Stratigos AJ, Forsea AM, van der Leest RJ, de Vries E, Nagore E, Bulliard JL, et al. Euromelanoma: a dermatology-led European campaign against nonmelanoma skin cancer and cutaneous melanoma; past, present and future. Br J Dermatol 2012; 167(Suppl):99-104. 9. Broadwater C, Heins J, Hoelscher C, Mangone A, Rozanas C. Skin and colon cancer media campaigns in Utah. Prev Chronic Dis 2004;1:A18. 10. Rivers JK, Gallagher RP. Public education projects in skin cancer: experience of the Canadian Dermatology Association. Cancer 1995;75:661-6. 11. Jensen AO, Olesen AB, Dethlefsen C, Sorensen HT. Do incident and new subsequent cases of non-melanoma skin cancer registered in a Danish prospective cohort study have different 10-year mortality? Cancer Detect Prev 2007;31:352-8. 12. Stefoski Mikeljevic J, Johnston C, Adamson PJ, Wright A, Bishop JA, Batman P, et al. How complete has skin cancer registration been in the UK? A study from Yorkshire. Eur J Cancer Prev 2003;12:125-33. 13. Lomas A, Leonardi-Bee J, Bath-Hextall F. A systematic review of worldwide incidence of nonmelanoma skin cancer. Br J Dermatol 2012;166:1069-80. 14. Hussain SK, Sundquist J, Hemminki K. Incidence trends of squamous cell and rare skin cancers in the Swedish national cancer registry point to calendar year and age-dependent increases. J Invest Dermatol 2010;130:1323-8. 15. Rogers HW, Weinstock MA, Harris AR, Hinckley MR, Feldman SR, Fleischer AB, et al. Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch Dermatol 2010; 146:283-7. 16. de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW. Predictions of skin cancer incidence in The Netherlands up to 2015. Br J Dermatol 2005;152:481-8. 17. Taylor MJ, Horey D, Livingstone C, Swerissen H. Decline with a capital D: long-term changes in general practice consultation patterns across Australia. Med J Aust 2010;193:80-3. 18. Australian Government Department of Health Services. Item selection guide: removal of skin lesions. Canberra: Department of Human Services; 2013.
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19. Askew DA, Wilkinson D, Schluter PJ, Eckert K. Skin cancer surgery in Australia 2001-2005: the changing role of the general practitioner. Med J Aust 2007;187:210-4. 20. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 2000;19:335-51. 21. Kim HJ, Fay MP, Yu B, Barrett MJ, Feuer EJ. Comparability of segmented line regression models. Biometrics 2004;60: 1005-14. 22. Marks R, Staples M, Giles GG. Trends in non-melanocytic skin cancer treated in Australia: the second national survey. Int J Cancer 1993;53:585-90. 23. Staples M, Marks R, Giles G. Trends in the incidence of non-melanocytic skin cancer (NMSC) treated in Australia 1985-1995: are primary prevention programs starting to have an effect? Int J Cancer 1998;78:144-8. 24. Makin JK, Warne CD, Dobbinson SJ, Wakefield MA, Hill DJ. Population and age-group trends in weekend sun protection and sunburn over two decades of the SunSmart program in Melbourne, Australia. Br J Dermatol 2013;168: 154-61. 25. Armstrong BK, Kricker A. The epidemiology of UV induced skin cancer. J Photochem Photobiol B 2001;63:8-18. 26. Brown WJ, Bryson L, Byles JE, Dobson AJ, Lee C, Mishra G, et al. Women’s Health Australia: recruitment for a national longitudinal cohort study. Women Health 1998;28:23-40. 27. Banks E, Redman S, Jorm L, Armstrong B, Bauman A, Beard J, et al. Cohort profile: the 45 and up study. Int J Epidemiol 2008; 37:941-7. 28. Olsen CM, Green AC, Neale RE, Webb PM, Cicero RA, Jackman LM, et al. Cohort profile: the QSkin sun and health study. Int J Epidemiol 2012;41:929-i. 29. Heal CF, Raasch BA, Buettner PG, Weedon D. Accuracy of clinical diagnosis of skin lesions. Br J Dermatol 2008;159: 661-8. 30. Youl PH, Baade PD, Janda M, Del Mar CB, Whiteman DC, Aitken JF. Diagnosing skin cancer in primary care: how do mainstream general practitioners compare with primary care skin cancer clinic doctors? Med J Aust 2007;187:215-20. 31. Moffatt CR, Green AC, Whiteman DC. Diagnostic accuracy in skin cancer clinics: the Australian experience. Int J Dermatol 2006;45:656-60. 32. Karagas MR, Greenberg ER, Spencer SK, Stukel TA, Mott LA. Increase in incidence rates of basal cell and squamous cell skin cancer in New Hampshire, USA: New Hampshire skin cancer study group. Int J Cancer 1999;81:555-9. 33. AIHW. Australian hospital statistics 2008-2009. Canberra: Australian Institute of Health and Welfare; 2010. 34. National Cancer Control Initiative (NCCI) Non-melanoma Skin Cancer Working Group (2002). The 2002 National non-melanoma skin cancer survey. Melbourne. A report by the National Cancer Control Initiative Non-melanoma Skin Cancer Working Group for the state and territory cancer councils. Melbourne, Victoria, Australia: National Cancer Control Initiative; 2003.
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Appendix I. Medicare Australia item numbers for relevant skin cancer treatments Procedure
Surgical excision Benign lesions (8 items) BCC and SCC, first surgical excision (8 items) Residual and recurrent BCC and SCC, previously treated surgically (24 items) Residual and recurrent BCC and SCC, previously treated nonsurgically Mohs micrographic surgery Biopsy Other treatment (cryotherapy or serial curettage) Benign lesion Premalignant lesion Malignant lesion (5 items) BCC, Basal cell carcinoma; SCC, squamous cell carcinoma.
Item numbers
31205, 31210, 31215, 31220, 31225, 31230, 31235, 31240 31255, 31260, 31265, 31270, 31275, 31280, 31285, 31290 31256, 31261, 31266, 31271, 31276, 31281, 31286, 31291, 31257, 31262, 31267, 31272, 31277, 31282, 31287, 31292, 31258, 31263, 31268, 31273, 31278, 31283, 31288, 31293 31295 31000, 31001, 31002 30071 30195 30192 30196, 30197, 30202, 30203, 30205
ARTICLE
Turning the tide? Changes in treatment rates for keratinocyte cancers in Australia 2000 through 2011 Catherine M. Olsen, PhD,a Patricia F. Williams, MD,b and David C. Whiteman, MBBS, PhDa Queensland, Australia, and Richmond, Virginia Background: Keratinocyte cancers (basal cell carcinoma, squamous cell carcinoma) are the commonest cancers in human beings. Population data on incidence trends are scant because few jurisdictions reliably record diagnoses or treatments. Objective: We sought to examine temporal trends of treating keratinocyte cancers in Australia. Methods: We analyzed Medicare Australia data relating to the diagnosis and treatment of keratinocyte skin cancer between 2000 and 2011. We examined counts and rates for each procedure, and the average annual percentage rate of change. Results: There were significant increases in excision rates for keratinocyte cancers (3.3% per annum for men and 2.2% per annum for women), however temporal trends differed significantly by age group. Although annual increases in excision rates were highest for men aged 75 to 84 years (8.6% per annum), they declined significantly for men and women younger than 45 years. Skin biopsy rates increased substantially in all age groups over the study period, suggesting no lessening in skin cancer surveillance in any age group. Limitations: The Medicare data do not include services provided in public hospitals, however fewer than 2% of skin cancers are treated in these settings. Conclusions: Although overall treatment rates for keratinocyte cancers have increased substantially during the past decade, excision rates are declining in younger Australians. ( J Am Acad Dermatol http:// dx.doi.org/10.1016/j.jaad.2014.02.011.) Key words: basal cell carcinoma; skin cancer; squamous cell carcinoma.
A
ustralia has the highest incidence of keratinocyte cancers (basal cell carcinoma [BCC], squamous cell carcinoma [SCC]) in the world.1 Each year, almost 2% of the population is estimated to develop BCC or SCC,2 and the costs of treating these cancers are higher than for any other cancer in Australia.3,4 In response, campaigns to reduce population sun exposure have been implemented with the goal of reducing the incidence of keratinocyte cancers.5 Commencing in the 1980s with the Slip! Slop! Slap! Campaign in Queensland,6
these strategies evolved into the comprehensive SunSmart program in the 1990s,7 which has continued to the present day. Primary prevention programs with similar intent have been enacted in other populations around the world.8-10
From the Cancer Control Group, Population Health Department, QIMR Berghofer Medical Research Institute,a and Virginia Commonwealth University Dermatology Residency Program.b Drs Olsen and Williams contributed equally to this manuscript and are recognized as equal first authors. Dr Whiteman is a Future Fellow of the Australian Research Council. Dr Williams was supported by the Virginia Commonwealth University School of Medicine. Conflicts of interest: None declared.
Accepted for publication February 5, 2014. Reprint requests: Catherine M. Olsen, PhD, QIMR Berghofer Medical Research Institute, Post Office Royal Brisbane Hospital, Q 4029 Australia. E-mail: Catherine.Olsen@ qimrberghofer.edu.au. Published online March 28, 2014. 0190-9622/$36.00 Ó 2014 by the American Academy of Dermatology, Inc. http://dx.doi.org/10.1016/j.jaad.2014.02.011
Abbreviations used: AAPC: BCC: SCC:
average annual percentage rate of change basal cell carcinoma squamous cell carcinoma
1
2 Olsen, Williams, and Whiteman
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To gauge the impact of prevention programs, it is and thus for which the relevant period was 2006 necessary to monitor incidence rates over time. through 2011. Population-based data for keratinocyte cancers are For each item number, we obtained the number of scarce,11,12 but the available data suggest that inciprocedures performed for each Australian state and dence rates have been increasing in all populations territory for every year of the past decade from the where reliable records exist,13 including in statistics page of the Medicare World Wide Web Sweden,14 the United States,15 The Netherlands,16 site (https://www.medicareaustralia.gov.au/statistics/ and Australia.2 mbs_item.shtml). We queried Medicare is Australia’s ‘‘counts,’’ and ‘‘counts per CAPSULE SUMMARY universal health care system, capita’’ of services, stratified which subsidizes virtually all by calendar year from Population data to monitor performance medical services outside of January 2000 to December of prevention programs for keratinocyte the public hospital system for 2011. All data were imported cancers are scant. all citizens and permanent into Microsoft Excel In Australia, between 2009 through 2011, residents, regardless of age (Microsoft, Redmond, WA) there was a significant decline in excision or other factors; the total for analysis. For first surgical rates for keratinocyte cancers among Medicare-registered populatreatment of keratinocyte those younger than 45 years. tion closely approximates cancer, cryotherapy and the total estimated resident serial curettage or excision Continued monitoring will determine population.17 The near comof histologically confirmed whether these declines are sustained malignant lesions and also plete uptake of Medicare into the future. diagnostic biopsy proceservices, coupled with site-, dures, we examined the size-, and histology-specific data stratified by sex and age group (5-year age item codes for skin conditions, makes it possible to groups). estimate the national incidence of procedures for To assess whether trends identified in treatment diagnosing and treating keratinocyte cancers in the services were specific for keratinocyte cancers or Australian population, and to examine trends over reflected broader trends in dermatologic practice, we time. also collected data on the surgical and nonsurgical By analyzing these data,18 we sought to describe the treatment of benign skin lesions and melanomas, and trends in clinical diagnosis and treatment of BCC and the nonsurgical treatment of premalignant skin leSCC in Australia during the period 2000 through 2011. sions. We plotted the counts and counts per capita of services by year to identify trends. We calculated the average annual percentage rate of change (AAPC) for METHODS counts per capita for the period 2000 through 2011 We obtained all data from the Medicare Australia using the Joinpoint Regression Program, Version 4.0.4. World Wide Web site (http://www.medicareaustralia. May 2013 (Statistical Research and Applications gov.au; accessed between May-June, 2012). We Branch, National Cancer Institute, Bethesda, MD).20 identified all item numbers representing procedures All but 1 of the 25 item numbers relating to residual and for the diagnosis and treatment of skin cancers using recurrent disease were first designated in 2005. Upon the Medicare Benefits Schedule Book of Therapeutic review, we excluded data for these 24 items for the Procedures, Category 3, operating from May 1, 201218 year 2005 as unreliable, as indicated by very low (item numbers are summarized in Appendix I). procedure counts in this first year of implementation, Surgical excision is the recommended treatment for and there were insufficient time points to calculate the all primary melanoma and most keratinocyte skin AAPC for this group of items. To test for differences in cancers, although various nonsurgical treatments are AAPC by sex, we used the pairwise comparison option appropriate for some lesions.19 For the item codes in the Joinpoint Regression Program (Statistical relating to cryotherapy, curettage, and excision, Research and Applications Branch, National Cancer Medicare Australia requires that the diagnosis of Institute), which uses a classic approximate F-test to malignancy is proven by histopathology or compare 2 sets of trend data.21 confirmed by specialist opinion before benefits are claimed. All of the item numbers analyzed in this report were unchanged for the entire study period RESULTS 2000 through 2011, except for the 24 items relating to The past decade has seen substantial increases ‘‘surgical removal of a BCC or SCC that was initially in the number of services to diagnose and treat treated surgically,’’ which were introduced in 2005 keratinocyte cancers in Australia. Table I presents the d
d
d
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Olsen, Williams, and Whiteman 3
Table I. Counts and counts per capita with average annual percent rate of change for specific procedures Counts per 100,000 persons
Counts Procedure
2000*
2011
Surgical excision Benign lesions (8 items) 535,106 541,793 BCC and SCC, first surgical 329,850 552,098 treatment (8 items) 19,886 23,834 Residual and recurrent BCC and SCC, previously treated surgically* (24 items) Mohs micrographic surgery 3385 10,536 Total 888,227 1,128,261 Biopsy 228,264 738,067 Other treatment (cryotherapy or serial curettage) Benign lesion 90,910 175,493 Premalignant lesion 390,535 614,843 Malignant lesion (5 items) 129,386 201,513 Total 839,095 1,729,916 Grand total 1,727,322 2,858,177
2000*
2011
2709 1671
2402 2448
95
106
17 4492 1155
47 5003 3272
460 1977 654 4246 8738
778 2726 895 7671 12,674
AAPC, % (95% CI) Women
1.3 (e2.0 to 2.2 (1.6-2.8)
Men
0.6)
0.8 (e1.5 to 3.3 (2.6-4.0)
9.3 (7.9-10.6)
11.7 (10.3-13.1)
7.3 (5.2-9.4)
8.0 (5.5-10.6)
3.1 (0.7-5.6) 1.4 (e0.1 to 2.8) 1.6 (0.7-2.6)
4.5 (2.2-6.9) 2.9 (1.3-4.6) 3.3 (2.3-4.3)
Py
0.1) \.001 \.001
\.001 .001
\.001 \.001 .004
AAPC, Average annual percentage rate of change; BCC, basal cell carcinoma; CI, confidence interval; SCC, squamous cell carcinoma. *Residual and recurrent BCC and SCC surgical treatment were itemized for the first time in 2005 and there were insufficient data points to calculate the AAPC. y For pairwise comparison between men and women.
counts and rates for the years 2000 and 2011 with the AAPC over the decade for skin cancer treatment and diagnosis. To assess whether these trends were specific for keratinocyte cancers, we generated equivalent data for excisions for melanoma. Surgical treatment of skin cancer Temporal trends in rates of first-time excisions of keratinocyte cancers are presented in Fig 1 and Table I. The AAPC for first-time excisions of keratinocyte cancer was 3.3% per annum for men and 2.2% for women and the difference between the sexes, for all age groups, was significant (P \.001). There were marked differences in the AAPC for skin cancer surgery by age group. For BCC and SCC, the excision rates declined significantly for both men and women younger than 45 years between 2000 and 2011. In contrast, the highest rates of change for BCC and SCC excisions were for men aged 75 to 84 years (8.6% per annum) and for women aged 85 and older (5.6%) (Fig 2, A). For melanoma excisions the trends were similar to those observed for BCC and SCC excisions; that is, trends of increasing excision rates among older men and women but significantly declining rates of excision for both men and women younger than 35 years (data not shown). Although a relatively uncommon approach to skin cancer treatment in Australia, Mohs procedures have increased dramatically over the time period (AAPC
Fig 1. Basal cell carcinoma (BCC )/squamous cell carcinoma (SCC ) excision rate for the time period 2000 through 2011. Number of first-time surgical excisions of BCC and SCC per 100,000 persons. See item codes in Appendix I.
9.3% per annum for women and 11.7% per annum for men) (Table I). The rates of Mohs procedures among those younger than 45 years was very low, and was highest among men aged 75 to 84 years. Diagnostic procedures for skin cancer Skin biopsies have increased more than any other skin cancererelated procedure during the past decade; in absolute terms, the skin biopsy rate
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4 Olsen, Williams, and Whiteman
per annum for men and 7.3% for women. The number of excisions for benign skin lesions, including those conducted to exclude a diagnosis of melanoma, has fluctuated over the past decade without a steady trend of increase or decrease (Table I). Nonsurgical treatment of skin cancer Other skin cancer treatments (including cryotherapy and serial curettage) are also presented in Table I. Overall numbers of these treatments for benign, premalignant, and malignant lesions all increased over the time period. In accord with the trend for surgical treatments, other treatments of histologically confirmed keratinocyte cancers over the time period declined significantly for women younger than 45 years and men younger than 55 years (Fig 2, C ).
DISCUSSION
Fig 2. Average annual percentage rate of change (APC ) of counts per 100,000 persons by age group for first-time surgical excisions of basal and squamous cell carcinomas (A), diagnostic biopsy procedures (B), and cryotherapy and serial curettage excision (C) of histologically confirmed malignant lesions for the time period 2000 through 2011.
increased from 1155 3 10 5 in 2000 to 3272 3 10 5 in 2011. Biopsy rates increased in all age groups older than 5 years (Fig 2, B), at an overall average of 8.0%
These analyses reveal a number of notable findings. Firstly, the significant increases in excision and biopsy rates for keratinocyte cancers overall underscore the burden of these cancers in Australia, with more than 1 million procedures performed annually in a population of 23 million. Secondly, and notwithstanding the overall increases, we observed that treatment rates of keratinocyte cancers declined significantly among younger adults. Thirdly, there has been a sizeable increase in the numbers of diagnostic biopsies for skin cancer, across all age groups, consistent with an overall heightened awareness of skin cancer in the population. The declines in excision rates for keratinocyte cancers in the younger age groups are particularly encouraging. These data, derived from a populationwide medical services register, are consistent with smaller surveys suggesting that skin cancer incidence might be declining among younger people.2,22,23 The most recent Australian study estimated BCC and SCC incidence trends by extrapolating data from 4 cross-sectional prevalence surveys conducted in 1985, 1990, 1995, and 2002.2 That study, which mostly preceded the observation period for our study, reported statistically significant trends of increasing skin cancer incidence in people older than 60 years contrasting with ‘‘stable’’ incidence rates in younger age groups. Our study extends the observation period, and suggests that skin cancer incidence trends for older and younger Australians have diverged further in the past 10 years. Such findings would accord with the anticipated effects of skin cancer prevention programs that have been prominent in Australia since the early 1980s5 and that
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would be most likely to benefit recent birth cohorts. Concerns have been expressed recently that skin cancer prevention campaigns may be losing their effectiveness in the light of recent population surveys demonstrating lower levels of sun protection than previously.24 It will therefore be important to monitor treatment rates among the post-1970 birth cohorts as they age to assess whether the declining rates are sustained into the future. Conversely, excision rates among people older than 45 years continued to increase steadily over the study period. Given the long latent period for sunlight-induced cancers25 and population aging, the burden of keratinocyte cancer is likely to remain substantial for some time to come. Skin biopsy rates increased substantially over the time period, raising the possibility that the increases in services to treat skin cancer among older Australians may partially reflect increased diagnostic scrutiny. To explore this issue further would require access to individual patient data that should be available in the future from large Australian cohorts currently in the field.26-28 Data on biopsy positivity rates in Australia are scant, but generally report moderate to high clinical accuracy,29-31 however such studies provide no insights into temporal trends in biopsy positivity rates. Few other population studies have reported trends for keratinocyte cancers separately for different age groups, because these cancers are not routinely collected by the majority of cancer registries. An analysis of the Swedish Cancer Registry reported increasing incidence trends for SCC between 1990 and 2005 of between 3.7% per annum for men and 8.5% per annum for women, with higher rates of increase above age 85 years than below age 85 years.14 A study in New Hampshire reported increases for BCC for all ages between 1979 and 1994.32 The comprehensive nature of Medicare lends credence to our findings. The Medicare database records all services performed by registered providers, with the exception of: (1) services provided by hospital doctors to public patients in public hospitals; and (2) services that qualify for a benefit under the Department of Veterans’ Affairs. Although approximately one third of hospital admissions for melanoma are thought to occur in the public hospital system,33 the vast majority of primary excisions for these cancers occur in outpatient settings.34 Data on patterns of care for keratinocyte cancer in Australia are scant, however the 2002 National Nonmelanoma Skin Cancer Survey reported that only 1.6% of skin cancers diagnosed in 2502 survey respondents were treated in hospital
Olsen, Williams, and Whiteman 5
settings; the highest proportion (51.1%) were treated by general practitioners, with a further 10.3% in skin cancer clinics, 17.6% by dermatologists, 5.9% by plastic surgeons, and 13.5% other/not stated.34 Thus, although the data presented here cannot be considered complete for the entire population, the degree of underestimation is likely to be very small and unlikely to account for the declines in excision rates we have observed in the younger age groups. Because we did not have access to unit record data, we could not enumerate the incidence of multiplicity of treatments. Previous reports have suggested that about one fourth of patients with skin cancer in Australia are given the diagnosis of more than 1 skin cancer per year.2 This could affect interpretation if the proportions of people undergoing multiple excisions for skin cancers changed over time and also differed by age group. We have no evidence that this occurred, but cannot exclude the possibility. The declining rates of treatment for keratinocyte cancers in younger people is not likely to be related to decreased diagnostic scrutiny given our finding of an increase in biopsy rates in all age groups older than 5 years (Fig 2, B). It might also be argued that the declining incidence in young people might reflect demographic changes in Australia; specifically increased intakes of migrants with darker skin types who have inherently lower rates of skin cancer. Again, the increased rate of biopsy in people younger than 45 years suggests that the change in ethnic profile cannot explain the decrease in rate of excisions for this age group. In summary, these analyses confirm that keratinocyte cancers continue to be a major public health problem in the Australian population, with a steadily increasing clinical toll during the past decade. Some grounds for guarded optimism are warranted however, with the emergence of significant declines in treatments for skin cancer among younger generations. It is too early yet to attribute these emerging trends to any single factor, but we anticipate continued scrutiny of these and other data to determine the efficacy of interventions intended to turn the rising tide of skin cancer. REFERENCES 1. AIHW. Cancer in Australia 2001. Canberra: Australian Institute of Health and Welfare and Australian Association of Cancer Registries; 2004. 2. Staples MP, Elwood M, Burton RC, Williams JL, Marks R, Giles GG. Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985. Med J Aust 2006;184: 6-10.
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3. Australian Institute of Health and Welfare. Health system expenditures on cancer and other neoplasms in Australia, 2000-01. Canberra: Australian Institute of Health and Welfare; 2005. 4. Fransen M, Karahalios A, Sharma N, English DR, Giles GG, Sinclair RD. Non-melanoma skin cancer in Australia. Med J Aust 2012;197:565-8. 5. Montague M, Borland R, Sinclair C. Slip! Slop! Slap! and SunSmart, 1980-2000: skin cancer control and 20 years of population-based campaigning. Health Educ Behav 2001;28: 290-305. 6. Marks R. Skin cancer control in the 1990’s, from Slip! Slop! Slap! To sun smart. Australas J Dermatol 1990;31:1-4. 7. Dobbinson S, Peipers A, Reading D, Sinclair C. A national approach to skin cancer prevention: the national SunSmart schools program. Med J Aust 1998;169:513-4. 8. Stratigos AJ, Forsea AM, van der Leest RJ, de Vries E, Nagore E, Bulliard JL, et al. Euromelanoma: a dermatology-led European campaign against nonmelanoma skin cancer and cutaneous melanoma; past, present and future. Br J Dermatol 2012; 167(Suppl):99-104. 9. Broadwater C, Heins J, Hoelscher C, Mangone A, Rozanas C. Skin and colon cancer media campaigns in Utah. Prev Chronic Dis 2004;1:A18. 10. Rivers JK, Gallagher RP. Public education projects in skin cancer: experience of the Canadian Dermatology Association. Cancer 1995;75:661-6. 11. Jensen AO, Olesen AB, Dethlefsen C, Sorensen HT. Do incident and new subsequent cases of non-melanoma skin cancer registered in a Danish prospective cohort study have different 10-year mortality? Cancer Detect Prev 2007;31:352-8. 12. Stefoski Mikeljevic J, Johnston C, Adamson PJ, Wright A, Bishop JA, Batman P, et al. How complete has skin cancer registration been in the UK? A study from Yorkshire. Eur J Cancer Prev 2003;12:125-33. 13. Lomas A, Leonardi-Bee J, Bath-Hextall F. A systematic review of worldwide incidence of nonmelanoma skin cancer. Br J Dermatol 2012;166:1069-80. 14. Hussain SK, Sundquist J, Hemminki K. Incidence trends of squamous cell and rare skin cancers in the Swedish national cancer registry point to calendar year and age-dependent increases. J Invest Dermatol 2010;130:1323-8. 15. Rogers HW, Weinstock MA, Harris AR, Hinckley MR, Feldman SR, Fleischer AB, et al. Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch Dermatol 2010; 146:283-7. 16. de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW. Predictions of skin cancer incidence in The Netherlands up to 2015. Br J Dermatol 2005;152:481-8. 17. Taylor MJ, Horey D, Livingstone C, Swerissen H. Decline with a capital D: long-term changes in general practice consultation patterns across Australia. Med J Aust 2010;193:80-3. 18. Australian Government Department of Health Services. Item selection guide: removal of skin lesions. Canberra: Department of Human Services; 2013.
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19. Askew DA, Wilkinson D, Schluter PJ, Eckert K. Skin cancer surgery in Australia 2001-2005: the changing role of the general practitioner. Med J Aust 2007;187:210-4. 20. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 2000;19:335-51. 21. Kim HJ, Fay MP, Yu B, Barrett MJ, Feuer EJ. Comparability of segmented line regression models. Biometrics 2004;60: 1005-14. 22. Marks R, Staples M, Giles GG. Trends in non-melanocytic skin cancer treated in Australia: the second national survey. Int J Cancer 1993;53:585-90. 23. Staples M, Marks R, Giles G. Trends in the incidence of non-melanocytic skin cancer (NMSC) treated in Australia 1985-1995: are primary prevention programs starting to have an effect? Int J Cancer 1998;78:144-8. 24. Makin JK, Warne CD, Dobbinson SJ, Wakefield MA, Hill DJ. Population and age-group trends in weekend sun protection and sunburn over two decades of the SunSmart program in Melbourne, Australia. Br J Dermatol 2013;168: 154-61. 25. Armstrong BK, Kricker A. The epidemiology of UV induced skin cancer. J Photochem Photobiol B 2001;63:8-18. 26. Brown WJ, Bryson L, Byles JE, Dobson AJ, Lee C, Mishra G, et al. Women’s Health Australia: recruitment for a national longitudinal cohort study. Women Health 1998;28:23-40. 27. Banks E, Redman S, Jorm L, Armstrong B, Bauman A, Beard J, et al. Cohort profile: the 45 and up study. Int J Epidemiol 2008; 37:941-7. 28. Olsen CM, Green AC, Neale RE, Webb PM, Cicero RA, Jackman LM, et al. Cohort profile: the QSkin sun and health study. Int J Epidemiol 2012;41:929-i. 29. Heal CF, Raasch BA, Buettner PG, Weedon D. Accuracy of clinical diagnosis of skin lesions. Br J Dermatol 2008;159: 661-8. 30. Youl PH, Baade PD, Janda M, Del Mar CB, Whiteman DC, Aitken JF. Diagnosing skin cancer in primary care: how do mainstream general practitioners compare with primary care skin cancer clinic doctors? Med J Aust 2007;187:215-20. 31. Moffatt CR, Green AC, Whiteman DC. Diagnostic accuracy in skin cancer clinics: the Australian experience. Int J Dermatol 2006;45:656-60. 32. Karagas MR, Greenberg ER, Spencer SK, Stukel TA, Mott LA. Increase in incidence rates of basal cell and squamous cell skin cancer in New Hampshire, USA: New Hampshire skin cancer study group. Int J Cancer 1999;81:555-9. 33. AIHW. Australian hospital statistics 2008-2009. Canberra: Australian Institute of Health and Welfare; 2010. 34. National Cancer Control Initiative (NCCI) Non-melanoma Skin Cancer Working Group (2002). The 2002 National non-melanoma skin cancer survey. Melbourne. A report by the National Cancer Control Initiative Non-melanoma Skin Cancer Working Group for the state and territory cancer councils. Melbourne, Victoria, Australia: National Cancer Control Initiative; 2003.
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Appendix I. Medicare Australia item numbers for relevant skin cancer treatments Procedure
Surgical excision Benign lesions (8 items) BCC and SCC, first surgical excision (8 items) Residual and recurrent BCC and SCC, previously treated surgically (24 items) Residual and recurrent BCC and SCC, previously treated nonsurgically Mohs micrographic surgery Biopsy Other treatment (cryotherapy or serial curettage) Benign lesion Premalignant lesion Malignant lesion (5 items) BCC, Basal cell carcinoma; SCC, squamous cell carcinoma.
Item numbers
31205, 31210, 31215, 31220, 31225, 31230, 31235, 31240 31255, 31260, 31265, 31270, 31275, 31280, 31285, 31290 31256, 31261, 31266, 31271, 31276, 31281, 31286, 31291, 31257, 31262, 31267, 31272, 31277, 31282, 31287, 31292, 31258, 31263, 31268, 31273, 31278, 31283, 31288, 31293 31295 31000, 31001, 31002 30071 30195 30192 30196, 30197, 30202, 30203, 30205
