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Skin and subcutaneous tissue infections are a heterogeneous group of superficial bacterial infections, most commonly caused by opportunistic skin pathogens: Staphylococcus aureus and Streptococcus pyogenes.1While these infections are usually effectively treated within the primary care setting, several international studies have recognised an increase in the number of cases serious enough to require hospitalisation.2-4 This subset of more significant cases has been termed serious skin infections.In New Zealand (NZ) the increase has been particularly marked, with the rate of cellulitis double that of Australia and the United States of America.5 Between the years 1990 and 2007 the national incidence rate almost doubled,6,7 making these infections one of the most common reasons for childhood hospitalisation.8Within NZ significant inter-regional variation in the incidence of serious skin infections has been noted; these differences are hypothesised to be multi-factorial and in part reflect the distribution of population groups who are known to experience higher disease rates, notably M ori and Pacific children, children from lower socioeconomic backgrounds, and children less than 5 years old.5-10The Tairawhiti (Gisborne) region and District Health Board (DHB) is a geographically isolated area of 45 000 people on the East Coast of NZs North Island. The region is unique for its warm climate, large M ori population (47.3% of the total population and 58.0% of the 0-14 year old population), youthfulness (26.2% of people are aged less than 15 years old),11 and high level of deprivation (the region has the largest proportion of highly-deprived residents in the country).12In Tairawhiti, skin infections present a major challenge in both primary and secondary level care; recent research by the authors found that between 1990 and 2007 Tairawhiti District Health had the highest incidence of childhood serious skin infections out of all NZ DHBs.6This study aimed to describe the incidence and epidemiology of serious skin infections in children in the Tairawhiti region over the period 1990-2007, to compare these local patterns to equivalent national data, and to determine whether the infection incidence observed in the Tairawhiti region is greater than that which is expected given the high-risk population composition.Methods Case selection and data extractionHospital discharge data were obtained from the NZ Ministry of Health for all children aged 0-14 years, admitted at least overnight to a NZ public hospital between 1 January 1990 and 31 December 2007, with a principal or additional discharge diagnosis from a defined list of serious skin infection International Classification of Disease (ICD) codes (see Appendix 1 at the end of this article). Cases after July 1999 were identified using ICD-10 diagnostic codes, and cases prior to this date by ICD-9 codes which were forward and backward mapped from ICD-10. This case definition was developed in recent work which found the validity of the former definition was markedly improved by including categories of skin infections previously overlooked in epidemiological analyses. With the addition of skin infections of atypical anatomical sites, those secondary to either primary skin disease or trauma, and those recorded as additional diagnoses (see Appendix), the sensitivity of the case definition increased from 61.0% to 98.9% with little loss in specificity.13 Each discharge record included a unique patient identifier (encrypted National Health Index number) enabling transfers and readmissions within 30 days with the same principal diagnosis code to be removed. To ensure a better match with the census population, overseas visitors were excluded. Day cases were excluded from the case definition due to inconsistencies in the recording of these events between regions and over time. Patient variables including age, prioritised ethnicity, gender and home domicile code and admission variables such as the season, year, DHB, duration and outcome of admission were recorded and collated. Due to the small numbers of Pacific and other non-M ori ethnic groups in the Tairawhiti region, prioritised ethnicity used only two categories, M ori and non-M ori, with non-M ori including NZ European, Pacific, Asian and all other non-M ori ethnic groups. Assigning levels of socioeconomic deprivation used the New Zealand Deprivation Index (NZDep) and was based on the home domicile census area units (CAUs) of cases. The NZDep is based on nine variables extracted from census data;14 NZDep 1 indicates least deprivation and 10 indicates highest deprivation. In 2.21% of cases domicile codes could not be linked to CAUs due to retired codes and addresses outside of classification. To reduce the impact of these missing CAUs, retired domicile codes were linked to new codes using files from the Ministry of Health and Statistics NZ (R. Bishop, Statistics New Zealand, personal communication; CAU changes 1991-2006, Wellington, 2009; C. Lewis, New Zealand Health Information Service, personal communication; Domicile code mapping, Wellington, 2009). Data analysisThe data were analysed using Microsoft Excel 00ae and SAS 00ae. Denominators in rate calculations were derived from usually resident population counts from the 1991, 1996, 2001, and 2006 censuses. Counts from each census were used to approximate the population in the preceding and subsequent two years. Age adjustment used the World Health Organisation (WHO) standard population. Trends between populations were explored by the calculation of rate ratios (RRs) with 95% confidence intervals (95% CIs) calculated using the log-transformation method.15 Significant differences in RRs were indicated by a two-tailed p-value <0.05. Indirect standardisationThe final part of this analysis used indirect standardisation to adjust for variables in the Tairawhiti population that could affect disease rates, and hence establish whether the observed incidence (or crude incidence) of serious skin infections in the region was in line with the incidence expected after taking into account the high-risk age, ethnicity and deprivation composition of the population. Typically, direct standardisation is used to validly compare two or more groups that differ in health determinants, however this method requires a large population to ensure age, deprivation and ethnicity-specific rates remain stable. Due to the small numbers in some subgroups in the Tairawhiti population, direct standardisation could not be used. Age/ethnicity/deprivation-specific rates were calculated using interpolated usually resident population counts by CAU from the 1991, 1996, 2001, and 2006 censuses. Indirect standardisation was used to standardise each variable, both individually and in combination, across two time periods (1990-1999 and 2000-2007) with NZ in total (including Tairawhiti) used as the standard population. Expected discharge numbers for each age/ethnicity/deprivation group were calculated by multiplying the national rates for that stratum by the usually resident population for that stratum in the Tairawhiti region. Five cases with unknown deprivation scores were excluded from this analysis. The ratio of observed to expected (O:E) cases was then calculated. An O:E of 1 denoted the observed number of discharges was the same as the expected number, an O:E less than 1 indicated the observed number was less than the expected number and conversely an O:E greater than 1 indicated the observed number was greater than the expected number. Statistical significance was determined by calculating 95% confidence intervals for these ratios. Results Selection of cases, incidence and impactIn the Tairawhiti region a total of 1976 hospitalisations met the case definition. From this total, 10 (0.5%) overseas visitors, 50 (2.5%) transfers, 166 (8.4%) day cases, and 39 (2.0%) readmissions were excluded. This left 1711 (86.6%) cases of childhood serious skin infection for further analysis. Of these cases, 1 patient was reported to have been discharged dead from hospital (case fatality of 0.06%). Hospitalisation data recorded a total of 6459 hospital days over the study period. The median and mean lengths of stay were 2 and 3.8 days respectively. In New Zealand during the same period there were a total of 82 408 hospitalisations which met the case definition. From this, 213 (0.3%) private hospital admissions, 955 (1.2%) overseas visitors, 3109 (3.8%) transfers, 12 353 (15.0%) day cases, and 1210 (1.5%) readmissions were excluded. Of the remaining 64 568 cases, 29 were reported to have been discharged dead from hospital (case fatality 0.04%). Hospitalisation data recorded a total of 213 141 hospital days over the study period. The mean and median lengths of stay were 2 and 3.3 respectively. Table 1 shows the incidence of childhood serious skin infections in both the Tairawhiti region and NZ during 1990-1999 (ICD-9) and 2000-2007 (ICD-10). As recommended by the previous work developing the case definition, these data are disaggregated by category and level of diagnosis.13 During the earlier time period, 1990-1999, the age-adjusted total incidence of infections in Tairawhiti was 641.1/100 000 while the total NZ incidence was slightly over half this rate at 354.3/100 000. By 2000-2007 the incidence in Tairawhiti had increased by over 50% to 988.4/100 000, while that in NZ had increased by a similar proportion to 531.7/100,000. A more detailed version of this table is provided in the Appendix. Table 1. The incidence of serious skin infections in children aged 0-14 years in Tairawhiti and NZ, disaggregated by category and level of diagnosis, between 1990-1999 (ICD-9) and 2000-2007 (ICD-10) Category Level of diagnosis Tairawhiti region New Zealand 1990-1999 2000-2007 1990-1999 2000-2007 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 Serious skin infections of typical sites (previously used case definition) Principal All level 352 456 284.5 368.5 431 580 453.8 610.7 13541 17074 166.3 209.7 18177 24086 264.9 351.0 Serious skin infections of atypical anatomical sites Principal All level 72 100 58.2 80.8 37 45 39.0 47.4 3170 5233 38.9 64.3 1866 2270 27.2 33.1 Serious skin infections secondary to primary skin disease Principal All level 81 194 65.5 156.8 82 212 86.3 223.2 1406 5364 17.3 65.9 1909 6170 27.8 89.9 Serious skin infections secondary to external trauma Principal All level 25 48 20.2 38.8 15 76 15.8 80.0 635 1270 7.8 15.6 420 3101 6.1 45.2 Crude total serious skin infections Principal All level 530 798 428.3 644.9 565 913 594.9 961.4 18752 28941 230.3 355.4 22372 35627 326.0 519.2 Age-adjusted total serious skin infections All level 641.1 988.4 354.3 531.7 ICD: international classification of disease. 2020Total number of cases during time period. 2021Average annual incidence per 100 000 (based on usually resident population counts from NZ Census). Incidence by year and season, 1990-2007Figures 1 and 2 illustrate the incidence of serious skin infections in the Tairawhiti region and in the whole of NZ during each of the 18 years studied. Results are presented for incidence by category and in total. Between the years 1990 and 2007 the incidence of infections more than doubled in the Tairawhiti region (from 423.6/100 000 in 1990 to 952.6/100 000 in 2007), while the NZ incidence increased by just under double (from 298.0/100 000 to 547.3/100 000). In both settings the increasing infection incidence was a direct reflection of increases in the incidence of serious skin infections of typical sites, along with a small contribution from infections secondary to primary skin trauma. Infections secondary to primary skin disease increased less, and those of atypical sites declined over this period. Figure 1. The incidence of serious skin infections in 0-14-year-old children in the Tairawhiti region by category and year, 1990-2007 Figure 2. The incidence of serious skin infections in 0-14-year-old children in NZ by category and year, 1990-2007 Table 2 shows the seasonal variation in the incidence of serious skin infections. In NZ, the crude incidence of infections was significantly higher during summer and autumn compared to winter (RR 1.12 for both). This trend was less distinct in Tairawhiti, with no significant difference in the seasonal incidence of infections. There was, however, no statistically significant difference in this trend between Tairawhiti and NZ. Table 2. The crude incidence of serious skin infections in 0-14 year old children by season, gender, age group, ethnicity and deprivation level for the Tairawhiti region and NZ, 1990-2007 Variable Category

Summary

Abstract

Aim

Serious skin infections are an increasing problem for New Zealand children with the highest national incidence in the Gisborne (Tairawhiti) region on the East Coast of New Zealand's North Island. This study aimed to describe the epidemiology of serious skin infections in children in this region, and make comparisons with equivalent national data to identify factors that might be contributing to elevated infection rates.

Method

Hospitalisation data were reviewed for 0-14-year-old children in the Tairawhiti region discharged from hospital with a serious skin infection between 1990 and 2007. A range of demographic variables were compared to equivalent data for New Zealand cases over the same period. The ratio of observed to expected discharges was calculated after indirectly standardising the Tairawhiti population age, ethnicity and deprivation composition to that of the total New Zealand population.

Results

In Tairawhiti the age-adjusted incidence of serious skin infections increased from 641.1/100 000 in 1990-1999 to 988.4/100 000 in 2000-2007, while the New Zealand incidence increased from 354.3/100 000 to 531.7/100 000. Preschool-aged children, M ori children, and those living in deprived neighbourhoods had the highest infection rates in all regions. The disparity between M ori and non-M ori children was significantly greater in Tairawhiti than nationally. The standardised ratio of observed to expected discharges in Tairawhiti compared with New Zealand was 1.42 (95%CI 1.32-1.52) in 1990-1999 and 1.28 (95%CI 1.19-1.36) in 2000-2007.

Conclusion

Serious skin infections are an increasing problem for all New Zealand children, but incidence rates in the Tairawhiti region are consistently greater than average national trends, with significantly larger ethnic disparities. The population composition of this region only partly accounts for the difference, suggesting the involvement of other unknown aetiological factors; these warrant further research.

Author Information

Cathryn OSullivan, Masters of Medical Sciences Student, Department of Public Health, University of Otago, Wellington; Michael Baker, Associate Professor, Department of Public Health, University of Otago, Wellington; Jane Zhang, Data Analyst. Department of Public Health, University of Otago, Wellington; Anna Davies*, Senior Advisor (Epidemiology), Health & Disability Intelligence Unit, Ministry of Health, Wellington; Geoffrey Cramp, Public Health Physician and Medical Officer of Health, Te Puna Waiora, Tairawhiti District Health, Gisborne, * Anna Davies is an employee of the New Zealand Ministry of Health. The views expressed in this paper are the authors own and do not represent the views or policies of the Ministry of Health. The paper was submitted for publication with the permission of the Deputy Director-General, Health and Disability Systems Strategy.

Acknowledgements

This work was supported by initial funding from Tairawhiti District Health as part of a larger piece of work made possible by a grant from the Ministry of Health Reducing Inequalities Budget.

Correspondence

Associate Professor Michael Baker, Department of Public Health, University of Otago Wellington, PO Box 7343, Wellington South, New Zealand. Fax: +64 (0)4 3895319

Correspondence Email

michael.baker@otago.ac.nz

Competing Interests

None declared.

Sladden MJ, Johnston GA. Common skin infections in children. BMJ. 2004;29:95-99.Koning S, Mohammedamin RSA, Van Der Wouden JC, et al. Impetigo: Incidence and treatment in Dutch general practice in 1987 and 2001-Results from two national surveys. Br J Dermatol. 2006;154:239-243.Loffeld A, Davies P, Lewis A, Moss C. Seasonal occurrence of impetigo: a retrospective 8-year review (1996-2003). Clin Exp Dermatol. 2005;30:512-514.Hersh AL, Chambers HF, Maselli JH, Gonzales R. National Trends in Ambulatory Visits and Antibiotic Prescribing for Skin and Soft-Tissue Infections. Arch Intern Med. 2008;168:1585-1591.Hunt D. Assessing and Reducing the Burden of Serious Skin Infections in Children and Young People in the Greater Wellington Region [Internet]. Wellington: Capital and Coast DHB, Hutt Valley DHB, Regional Public Health; 2004 [cited June 2009]. Available from: http://www.skininfections.co.nz/documents/Serious_Skin_Infections_Nov2004.pdfOSullivan C, Baker M, Zhang J. 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Skin and subcutaneous tissue infections are a heterogeneous group of superficial bacterial infections, most commonly caused by opportunistic skin pathogens: Staphylococcus aureus and Streptococcus pyogenes.1While these infections are usually effectively treated within the primary care setting, several international studies have recognised an increase in the number of cases serious enough to require hospitalisation.2-4 This subset of more significant cases has been termed serious skin infections.In New Zealand (NZ) the increase has been particularly marked, with the rate of cellulitis double that of Australia and the United States of America.5 Between the years 1990 and 2007 the national incidence rate almost doubled,6,7 making these infections one of the most common reasons for childhood hospitalisation.8Within NZ significant inter-regional variation in the incidence of serious skin infections has been noted; these differences are hypothesised to be multi-factorial and in part reflect the distribution of population groups who are known to experience higher disease rates, notably M ori and Pacific children, children from lower socioeconomic backgrounds, and children less than 5 years old.5-10The Tairawhiti (Gisborne) region and District Health Board (DHB) is a geographically isolated area of 45 000 people on the East Coast of NZs North Island. The region is unique for its warm climate, large M ori population (47.3% of the total population and 58.0% of the 0-14 year old population), youthfulness (26.2% of people are aged less than 15 years old),11 and high level of deprivation (the region has the largest proportion of highly-deprived residents in the country).12In Tairawhiti, skin infections present a major challenge in both primary and secondary level care; recent research by the authors found that between 1990 and 2007 Tairawhiti District Health had the highest incidence of childhood serious skin infections out of all NZ DHBs.6This study aimed to describe the incidence and epidemiology of serious skin infections in children in the Tairawhiti region over the period 1990-2007, to compare these local patterns to equivalent national data, and to determine whether the infection incidence observed in the Tairawhiti region is greater than that which is expected given the high-risk population composition.Methods Case selection and data extractionHospital discharge data were obtained from the NZ Ministry of Health for all children aged 0-14 years, admitted at least overnight to a NZ public hospital between 1 January 1990 and 31 December 2007, with a principal or additional discharge diagnosis from a defined list of serious skin infection International Classification of Disease (ICD) codes (see Appendix 1 at the end of this article). Cases after July 1999 were identified using ICD-10 diagnostic codes, and cases prior to this date by ICD-9 codes which were forward and backward mapped from ICD-10. This case definition was developed in recent work which found the validity of the former definition was markedly improved by including categories of skin infections previously overlooked in epidemiological analyses. With the addition of skin infections of atypical anatomical sites, those secondary to either primary skin disease or trauma, and those recorded as additional diagnoses (see Appendix), the sensitivity of the case definition increased from 61.0% to 98.9% with little loss in specificity.13 Each discharge record included a unique patient identifier (encrypted National Health Index number) enabling transfers and readmissions within 30 days with the same principal diagnosis code to be removed. To ensure a better match with the census population, overseas visitors were excluded. Day cases were excluded from the case definition due to inconsistencies in the recording of these events between regions and over time. Patient variables including age, prioritised ethnicity, gender and home domicile code and admission variables such as the season, year, DHB, duration and outcome of admission were recorded and collated. Due to the small numbers of Pacific and other non-M ori ethnic groups in the Tairawhiti region, prioritised ethnicity used only two categories, M ori and non-M ori, with non-M ori including NZ European, Pacific, Asian and all other non-M ori ethnic groups. Assigning levels of socioeconomic deprivation used the New Zealand Deprivation Index (NZDep) and was based on the home domicile census area units (CAUs) of cases. The NZDep is based on nine variables extracted from census data;14 NZDep 1 indicates least deprivation and 10 indicates highest deprivation. In 2.21% of cases domicile codes could not be linked to CAUs due to retired codes and addresses outside of classification. To reduce the impact of these missing CAUs, retired domicile codes were linked to new codes using files from the Ministry of Health and Statistics NZ (R. Bishop, Statistics New Zealand, personal communication; CAU changes 1991-2006, Wellington, 2009; C. Lewis, New Zealand Health Information Service, personal communication; Domicile code mapping, Wellington, 2009). Data analysisThe data were analysed using Microsoft Excel 00ae and SAS 00ae. Denominators in rate calculations were derived from usually resident population counts from the 1991, 1996, 2001, and 2006 censuses. Counts from each census were used to approximate the population in the preceding and subsequent two years. Age adjustment used the World Health Organisation (WHO) standard population. Trends between populations were explored by the calculation of rate ratios (RRs) with 95% confidence intervals (95% CIs) calculated using the log-transformation method.15 Significant differences in RRs were indicated by a two-tailed p-value <0.05. Indirect standardisationThe final part of this analysis used indirect standardisation to adjust for variables in the Tairawhiti population that could affect disease rates, and hence establish whether the observed incidence (or crude incidence) of serious skin infections in the region was in line with the incidence expected after taking into account the high-risk age, ethnicity and deprivation composition of the population. Typically, direct standardisation is used to validly compare two or more groups that differ in health determinants, however this method requires a large population to ensure age, deprivation and ethnicity-specific rates remain stable. Due to the small numbers in some subgroups in the Tairawhiti population, direct standardisation could not be used. Age/ethnicity/deprivation-specific rates were calculated using interpolated usually resident population counts by CAU from the 1991, 1996, 2001, and 2006 censuses. Indirect standardisation was used to standardise each variable, both individually and in combination, across two time periods (1990-1999 and 2000-2007) with NZ in total (including Tairawhiti) used as the standard population. Expected discharge numbers for each age/ethnicity/deprivation group were calculated by multiplying the national rates for that stratum by the usually resident population for that stratum in the Tairawhiti region. Five cases with unknown deprivation scores were excluded from this analysis. The ratio of observed to expected (O:E) cases was then calculated. An O:E of 1 denoted the observed number of discharges was the same as the expected number, an O:E less than 1 indicated the observed number was less than the expected number and conversely an O:E greater than 1 indicated the observed number was greater than the expected number. Statistical significance was determined by calculating 95% confidence intervals for these ratios. Results Selection of cases, incidence and impactIn the Tairawhiti region a total of 1976 hospitalisations met the case definition. From this total, 10 (0.5%) overseas visitors, 50 (2.5%) transfers, 166 (8.4%) day cases, and 39 (2.0%) readmissions were excluded. This left 1711 (86.6%) cases of childhood serious skin infection for further analysis. Of these cases, 1 patient was reported to have been discharged dead from hospital (case fatality of 0.06%). Hospitalisation data recorded a total of 6459 hospital days over the study period. The median and mean lengths of stay were 2 and 3.8 days respectively. In New Zealand during the same period there were a total of 82 408 hospitalisations which met the case definition. From this, 213 (0.3%) private hospital admissions, 955 (1.2%) overseas visitors, 3109 (3.8%) transfers, 12 353 (15.0%) day cases, and 1210 (1.5%) readmissions were excluded. Of the remaining 64 568 cases, 29 were reported to have been discharged dead from hospital (case fatality 0.04%). Hospitalisation data recorded a total of 213 141 hospital days over the study period. The mean and median lengths of stay were 2 and 3.3 respectively. Table 1 shows the incidence of childhood serious skin infections in both the Tairawhiti region and NZ during 1990-1999 (ICD-9) and 2000-2007 (ICD-10). As recommended by the previous work developing the case definition, these data are disaggregated by category and level of diagnosis.13 During the earlier time period, 1990-1999, the age-adjusted total incidence of infections in Tairawhiti was 641.1/100 000 while the total NZ incidence was slightly over half this rate at 354.3/100 000. By 2000-2007 the incidence in Tairawhiti had increased by over 50% to 988.4/100 000, while that in NZ had increased by a similar proportion to 531.7/100,000. A more detailed version of this table is provided in the Appendix. Table 1. The incidence of serious skin infections in children aged 0-14 years in Tairawhiti and NZ, disaggregated by category and level of diagnosis, between 1990-1999 (ICD-9) and 2000-2007 (ICD-10) Category Level of diagnosis Tairawhiti region New Zealand 1990-1999 2000-2007 1990-1999 2000-2007 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 Serious skin infections of typical sites (previously used case definition) Principal All level 352 456 284.5 368.5 431 580 453.8 610.7 13541 17074 166.3 209.7 18177 24086 264.9 351.0 Serious skin infections of atypical anatomical sites Principal All level 72 100 58.2 80.8 37 45 39.0 47.4 3170 5233 38.9 64.3 1866 2270 27.2 33.1 Serious skin infections secondary to primary skin disease Principal All level 81 194 65.5 156.8 82 212 86.3 223.2 1406 5364 17.3 65.9 1909 6170 27.8 89.9 Serious skin infections secondary to external trauma Principal All level 25 48 20.2 38.8 15 76 15.8 80.0 635 1270 7.8 15.6 420 3101 6.1 45.2 Crude total serious skin infections Principal All level 530 798 428.3 644.9 565 913 594.9 961.4 18752 28941 230.3 355.4 22372 35627 326.0 519.2 Age-adjusted total serious skin infections All level 641.1 988.4 354.3 531.7 ICD: international classification of disease. 2020Total number of cases during time period. 2021Average annual incidence per 100 000 (based on usually resident population counts from NZ Census). Incidence by year and season, 1990-2007Figures 1 and 2 illustrate the incidence of serious skin infections in the Tairawhiti region and in the whole of NZ during each of the 18 years studied. Results are presented for incidence by category and in total. Between the years 1990 and 2007 the incidence of infections more than doubled in the Tairawhiti region (from 423.6/100 000 in 1990 to 952.6/100 000 in 2007), while the NZ incidence increased by just under double (from 298.0/100 000 to 547.3/100 000). In both settings the increasing infection incidence was a direct reflection of increases in the incidence of serious skin infections of typical sites, along with a small contribution from infections secondary to primary skin trauma. Infections secondary to primary skin disease increased less, and those of atypical sites declined over this period. Figure 1. The incidence of serious skin infections in 0-14-year-old children in the Tairawhiti region by category and year, 1990-2007 Figure 2. The incidence of serious skin infections in 0-14-year-old children in NZ by category and year, 1990-2007 Table 2 shows the seasonal variation in the incidence of serious skin infections. In NZ, the crude incidence of infections was significantly higher during summer and autumn compared to winter (RR 1.12 for both). This trend was less distinct in Tairawhiti, with no significant difference in the seasonal incidence of infections. There was, however, no statistically significant difference in this trend between Tairawhiti and NZ. Table 2. The crude incidence of serious skin infections in 0-14 year old children by season, gender, age group, ethnicity and deprivation level for the Tairawhiti region and NZ, 1990-2007 Variable Category

Summary

Abstract

Aim

Serious skin infections are an increasing problem for New Zealand children with the highest national incidence in the Gisborne (Tairawhiti) region on the East Coast of New Zealand's North Island. This study aimed to describe the epidemiology of serious skin infections in children in this region, and make comparisons with equivalent national data to identify factors that might be contributing to elevated infection rates.

Method

Hospitalisation data were reviewed for 0-14-year-old children in the Tairawhiti region discharged from hospital with a serious skin infection between 1990 and 2007. A range of demographic variables were compared to equivalent data for New Zealand cases over the same period. The ratio of observed to expected discharges was calculated after indirectly standardising the Tairawhiti population age, ethnicity and deprivation composition to that of the total New Zealand population.

Results

In Tairawhiti the age-adjusted incidence of serious skin infections increased from 641.1/100 000 in 1990-1999 to 988.4/100 000 in 2000-2007, while the New Zealand incidence increased from 354.3/100 000 to 531.7/100 000. Preschool-aged children, M ori children, and those living in deprived neighbourhoods had the highest infection rates in all regions. The disparity between M ori and non-M ori children was significantly greater in Tairawhiti than nationally. The standardised ratio of observed to expected discharges in Tairawhiti compared with New Zealand was 1.42 (95%CI 1.32-1.52) in 1990-1999 and 1.28 (95%CI 1.19-1.36) in 2000-2007.

Conclusion

Serious skin infections are an increasing problem for all New Zealand children, but incidence rates in the Tairawhiti region are consistently greater than average national trends, with significantly larger ethnic disparities. The population composition of this region only partly accounts for the difference, suggesting the involvement of other unknown aetiological factors; these warrant further research.

Author Information

Cathryn OSullivan, Masters of Medical Sciences Student, Department of Public Health, University of Otago, Wellington; Michael Baker, Associate Professor, Department of Public Health, University of Otago, Wellington; Jane Zhang, Data Analyst. Department of Public Health, University of Otago, Wellington; Anna Davies*, Senior Advisor (Epidemiology), Health & Disability Intelligence Unit, Ministry of Health, Wellington; Geoffrey Cramp, Public Health Physician and Medical Officer of Health, Te Puna Waiora, Tairawhiti District Health, Gisborne, * Anna Davies is an employee of the New Zealand Ministry of Health. The views expressed in this paper are the authors own and do not represent the views or policies of the Ministry of Health. The paper was submitted for publication with the permission of the Deputy Director-General, Health and Disability Systems Strategy.

Acknowledgements

This work was supported by initial funding from Tairawhiti District Health as part of a larger piece of work made possible by a grant from the Ministry of Health Reducing Inequalities Budget.

Correspondence

Associate Professor Michael Baker, Department of Public Health, University of Otago Wellington, PO Box 7343, Wellington South, New Zealand. Fax: +64 (0)4 3895319

Correspondence Email

michael.baker@otago.ac.nz

Competing Interests

None declared.

Sladden MJ, Johnston GA. Common skin infections in children. BMJ. 2004;29:95-99.Koning S, Mohammedamin RSA, Van Der Wouden JC, et al. Impetigo: Incidence and treatment in Dutch general practice in 1987 and 2001-Results from two national surveys. Br J Dermatol. 2006;154:239-243.Loffeld A, Davies P, Lewis A, Moss C. Seasonal occurrence of impetigo: a retrospective 8-year review (1996-2003). Clin Exp Dermatol. 2005;30:512-514.Hersh AL, Chambers HF, Maselli JH, Gonzales R. National Trends in Ambulatory Visits and Antibiotic Prescribing for Skin and Soft-Tissue Infections. Arch Intern Med. 2008;168:1585-1591.Hunt D. Assessing and Reducing the Burden of Serious Skin Infections in Children and Young People in the Greater Wellington Region [Internet]. Wellington: Capital and Coast DHB, Hutt Valley DHB, Regional Public Health; 2004 [cited June 2009]. Available from: http://www.skininfections.co.nz/documents/Serious_Skin_Infections_Nov2004.pdfOSullivan C, Baker M, Zhang J. Increasing hospitalisations for serious skin infections in New Zealand children, 1990-2007. Epidemiol Infect. 2010;15:1-11.Craig E, Jackson C, Han DY, NZCYES Steering Committee. Monitoring the Health of New Zealand Children and Young People: Indicator Handbook [Internet]. Auckland: Paediatric Society of New Zealand, New Zealand Child and Youth Epidemiology Service; 2007 [cited June 2009]. Available from: http://www.paediatrics.org.nz/files/Indicator%20Handbook%20Version%2008.3.pdfLawes C. Paediatric cellulitis hospital discharges in the Auckland Region. Auckland: Public Health Protection Service, Auckland Healthcare; 1998.Finger F, Rossaak M, Umstaetter R, et al. Skin infections of the limbs of Polynesian children. N Z Med J. 2004;117:U847. http://journal.nzma.org.nz/journal/117-1192/847/content.pdfMorgan C, Selak V, Bullen C. Glen Innes Serious Skin Infection Prevention Project: Final Report 1 February 2003-31 January 2004 [Internet]. Auckland: Auckland Regional Public Health Services; 2004 [cited June 2009]. Available from:http://www.arphs.govt.nz/Publications_Reports/archive/GlenInnesSkinProject.pdfDepartment of Statistics. New Zealand census of population and dwellings [Internet]. Wellington: Statistics New Zealand; 2006 [cited September 2009]. Available from: http://www.stats.govt.nzSalmond C, Crampton P, Atkinson J. NZDep2006 Index of Deprivation [Internet]. Wellington: Ministry of Health; 2007 [cited August 2009]. Available from:http://www.uow.otago.ac.nz/academic/dph/research/NZDep/NZDep2006%20research%20report%2004%20September%202007.pdfOSullivan C, Baker M. Proposed epidemiological case definition for serious skin infection in children. J Paediatr Child Health. 2010;46:176-183.Salmond C, Crampton P, Atkinson J. NZDep2006 Index of Deprivation: Users Manual [Internet]. Wellington: Ministry of Health; 2007 [cited November 2009]. Available from: http://www.moh.govt.nz/moh.nsf/Files/phi-users-manual/$file/phi-users-manual.pdfClayton D, Hills M. Statistical Methods in Epidemiology Oxford: Oxford University Press; 1993, p80-82.Baker MG, Telfar Barnard L, Kvalsvig A, et al. Increasing incidence of serious infectious diseases and inequalities in New Zealand: a national epidemiological study. Lancet. 2012 Feb 17. [Epub ahead of print].Baker M, McNicholas A, Garrett N, et al. Household crowding a major risk factor for epidemic meningococcal disease in Auckland children. Pediatr Infect Dis J. 2000;19:983-990.Grant CC, Scragg R, Tan D, et al. Hospitalization for pneumonia in children in Auckland, New Zealand. J Paediatr Child Health. 1998;34:355-359.Malcolm L. Inequities in access to and utilisation of primary medical care services for M ori and low income New Zealanders. N Z Med J. 1996;109:356-358.Brabyn L, Barnett R. Population need and geographical access to general practitioners in rural New Zealand. N Z Med J. 2004;117:U996. http://journal.nzma.org.nz/journal/117-1199/996/content.pdfBailie RS, Stevens MR, McDonald E, et al. Skin infection, housing and social circumstances in children living in remote Indigenous communities: testing conceptual and methodological approaches. BMC Public Health. 2005;5:128.Kakar N, Kumar V, Mehta G, et al. Clinico-bacteriological study of pyodermas in children. J Derm. 1999;26:288-93.Masawe A, Nsanzumuhire H, Mhalu F. Bacterial skin infections in preschool and school children in costal Tanzania. Arch Derm. 1975;111:1312-6.Dajani A, Ferrieri P, Wannamaker L. Endemic superficial pyoderma in children. Arch Dermatol 1973;108:517-522.Taplin D, Lansdell L, Allen A, et al. Prevalence of streptococcal pyoderma in relation to climate and hygiene. Lancet. 1973;1:501-3.Rogers M, Dorman D, Gapes M, Ly J. A three-year study of impetigo in Sydney. Med J Aust. 1987;147:63-65.Kristensen JK. Scabies and pyoderma in Lilongwe, Malawi. Prevalence and seasonal fluctuation. Int J Dermatol. 1991;30:699-702.Elliot AJ, Cross KW, Smith GE, et al. The association between impetigo, insect bites and air temperature: A retrospective 5-year study (1999-2003) using morbidity data collected from a sentinel general practice network database. Fam Pract. 2006;23:490-496.Lake R, Adlam B, Perera S. Acute gastrointestinal illness (AGI) study: final study report [Internet]. Christchurch: Institute of Environmental Science and Research Limited; 2007 [cited June 2010]. Available from:http://www.nzfsa.govt.nz/science/research-projects/gastrointestinal-report/Final_Report.pdf

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Skin and subcutaneous tissue infections are a heterogeneous group of superficial bacterial infections, most commonly caused by opportunistic skin pathogens: Staphylococcus aureus and Streptococcus pyogenes.1While these infections are usually effectively treated within the primary care setting, several international studies have recognised an increase in the number of cases serious enough to require hospitalisation.2-4 This subset of more significant cases has been termed serious skin infections.In New Zealand (NZ) the increase has been particularly marked, with the rate of cellulitis double that of Australia and the United States of America.5 Between the years 1990 and 2007 the national incidence rate almost doubled,6,7 making these infections one of the most common reasons for childhood hospitalisation.8Within NZ significant inter-regional variation in the incidence of serious skin infections has been noted; these differences are hypothesised to be multi-factorial and in part reflect the distribution of population groups who are known to experience higher disease rates, notably M ori and Pacific children, children from lower socioeconomic backgrounds, and children less than 5 years old.5-10The Tairawhiti (Gisborne) region and District Health Board (DHB) is a geographically isolated area of 45 000 people on the East Coast of NZs North Island. The region is unique for its warm climate, large M ori population (47.3% of the total population and 58.0% of the 0-14 year old population), youthfulness (26.2% of people are aged less than 15 years old),11 and high level of deprivation (the region has the largest proportion of highly-deprived residents in the country).12In Tairawhiti, skin infections present a major challenge in both primary and secondary level care; recent research by the authors found that between 1990 and 2007 Tairawhiti District Health had the highest incidence of childhood serious skin infections out of all NZ DHBs.6This study aimed to describe the incidence and epidemiology of serious skin infections in children in the Tairawhiti region over the period 1990-2007, to compare these local patterns to equivalent national data, and to determine whether the infection incidence observed in the Tairawhiti region is greater than that which is expected given the high-risk population composition.Methods Case selection and data extractionHospital discharge data were obtained from the NZ Ministry of Health for all children aged 0-14 years, admitted at least overnight to a NZ public hospital between 1 January 1990 and 31 December 2007, with a principal or additional discharge diagnosis from a defined list of serious skin infection International Classification of Disease (ICD) codes (see Appendix 1 at the end of this article). Cases after July 1999 were identified using ICD-10 diagnostic codes, and cases prior to this date by ICD-9 codes which were forward and backward mapped from ICD-10. This case definition was developed in recent work which found the validity of the former definition was markedly improved by including categories of skin infections previously overlooked in epidemiological analyses. With the addition of skin infections of atypical anatomical sites, those secondary to either primary skin disease or trauma, and those recorded as additional diagnoses (see Appendix), the sensitivity of the case definition increased from 61.0% to 98.9% with little loss in specificity.13 Each discharge record included a unique patient identifier (encrypted National Health Index number) enabling transfers and readmissions within 30 days with the same principal diagnosis code to be removed. To ensure a better match with the census population, overseas visitors were excluded. Day cases were excluded from the case definition due to inconsistencies in the recording of these events between regions and over time. Patient variables including age, prioritised ethnicity, gender and home domicile code and admission variables such as the season, year, DHB, duration and outcome of admission were recorded and collated. Due to the small numbers of Pacific and other non-M ori ethnic groups in the Tairawhiti region, prioritised ethnicity used only two categories, M ori and non-M ori, with non-M ori including NZ European, Pacific, Asian and all other non-M ori ethnic groups. Assigning levels of socioeconomic deprivation used the New Zealand Deprivation Index (NZDep) and was based on the home domicile census area units (CAUs) of cases. The NZDep is based on nine variables extracted from census data;14 NZDep 1 indicates least deprivation and 10 indicates highest deprivation. In 2.21% of cases domicile codes could not be linked to CAUs due to retired codes and addresses outside of classification. To reduce the impact of these missing CAUs, retired domicile codes were linked to new codes using files from the Ministry of Health and Statistics NZ (R. Bishop, Statistics New Zealand, personal communication; CAU changes 1991-2006, Wellington, 2009; C. Lewis, New Zealand Health Information Service, personal communication; Domicile code mapping, Wellington, 2009). Data analysisThe data were analysed using Microsoft Excel 00ae and SAS 00ae. Denominators in rate calculations were derived from usually resident population counts from the 1991, 1996, 2001, and 2006 censuses. Counts from each census were used to approximate the population in the preceding and subsequent two years. Age adjustment used the World Health Organisation (WHO) standard population. Trends between populations were explored by the calculation of rate ratios (RRs) with 95% confidence intervals (95% CIs) calculated using the log-transformation method.15 Significant differences in RRs were indicated by a two-tailed p-value <0.05. Indirect standardisationThe final part of this analysis used indirect standardisation to adjust for variables in the Tairawhiti population that could affect disease rates, and hence establish whether the observed incidence (or crude incidence) of serious skin infections in the region was in line with the incidence expected after taking into account the high-risk age, ethnicity and deprivation composition of the population. Typically, direct standardisation is used to validly compare two or more groups that differ in health determinants, however this method requires a large population to ensure age, deprivation and ethnicity-specific rates remain stable. Due to the small numbers in some subgroups in the Tairawhiti population, direct standardisation could not be used. Age/ethnicity/deprivation-specific rates were calculated using interpolated usually resident population counts by CAU from the 1991, 1996, 2001, and 2006 censuses. Indirect standardisation was used to standardise each variable, both individually and in combination, across two time periods (1990-1999 and 2000-2007) with NZ in total (including Tairawhiti) used as the standard population. Expected discharge numbers for each age/ethnicity/deprivation group were calculated by multiplying the national rates for that stratum by the usually resident population for that stratum in the Tairawhiti region. Five cases with unknown deprivation scores were excluded from this analysis. The ratio of observed to expected (O:E) cases was then calculated. An O:E of 1 denoted the observed number of discharges was the same as the expected number, an O:E less than 1 indicated the observed number was less than the expected number and conversely an O:E greater than 1 indicated the observed number was greater than the expected number. Statistical significance was determined by calculating 95% confidence intervals for these ratios. Results Selection of cases, incidence and impactIn the Tairawhiti region a total of 1976 hospitalisations met the case definition. From this total, 10 (0.5%) overseas visitors, 50 (2.5%) transfers, 166 (8.4%) day cases, and 39 (2.0%) readmissions were excluded. This left 1711 (86.6%) cases of childhood serious skin infection for further analysis. Of these cases, 1 patient was reported to have been discharged dead from hospital (case fatality of 0.06%). Hospitalisation data recorded a total of 6459 hospital days over the study period. The median and mean lengths of stay were 2 and 3.8 days respectively. In New Zealand during the same period there were a total of 82 408 hospitalisations which met the case definition. From this, 213 (0.3%) private hospital admissions, 955 (1.2%) overseas visitors, 3109 (3.8%) transfers, 12 353 (15.0%) day cases, and 1210 (1.5%) readmissions were excluded. Of the remaining 64 568 cases, 29 were reported to have been discharged dead from hospital (case fatality 0.04%). Hospitalisation data recorded a total of 213 141 hospital days over the study period. The mean and median lengths of stay were 2 and 3.3 respectively. Table 1 shows the incidence of childhood serious skin infections in both the Tairawhiti region and NZ during 1990-1999 (ICD-9) and 2000-2007 (ICD-10). As recommended by the previous work developing the case definition, these data are disaggregated by category and level of diagnosis.13 During the earlier time period, 1990-1999, the age-adjusted total incidence of infections in Tairawhiti was 641.1/100 000 while the total NZ incidence was slightly over half this rate at 354.3/100 000. By 2000-2007 the incidence in Tairawhiti had increased by over 50% to 988.4/100 000, while that in NZ had increased by a similar proportion to 531.7/100,000. A more detailed version of this table is provided in the Appendix. Table 1. The incidence of serious skin infections in children aged 0-14 years in Tairawhiti and NZ, disaggregated by category and level of diagnosis, between 1990-1999 (ICD-9) and 2000-2007 (ICD-10) Category Level of diagnosis Tairawhiti region New Zealand 1990-1999 2000-2007 1990-1999 2000-2007 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 No. 2020 Rate 2021 Serious skin infections of typical sites (previously used case definition) Principal All level 352 456 284.5 368.5 431 580 453.8 610.7 13541 17074 166.3 209.7 18177 24086 264.9 351.0 Serious skin infections of atypical anatomical sites Principal All level 72 100 58.2 80.8 37 45 39.0 47.4 3170 5233 38.9 64.3 1866 2270 27.2 33.1 Serious skin infections secondary to primary skin disease Principal All level 81 194 65.5 156.8 82 212 86.3 223.2 1406 5364 17.3 65.9 1909 6170 27.8 89.9 Serious skin infections secondary to external trauma Principal All level 25 48 20.2 38.8 15 76 15.8 80.0 635 1270 7.8 15.6 420 3101 6.1 45.2 Crude total serious skin infections Principal All level 530 798 428.3 644.9 565 913 594.9 961.4 18752 28941 230.3 355.4 22372 35627 326.0 519.2 Age-adjusted total serious skin infections All level 641.1 988.4 354.3 531.7 ICD: international classification of disease. 2020Total number of cases during time period. 2021Average annual incidence per 100 000 (based on usually resident population counts from NZ Census). Incidence by year and season, 1990-2007Figures 1 and 2 illustrate the incidence of serious skin infections in the Tairawhiti region and in the whole of NZ during each of the 18 years studied. Results are presented for incidence by category and in total. Between the years 1990 and 2007 the incidence of infections more than doubled in the Tairawhiti region (from 423.6/100 000 in 1990 to 952.6/100 000 in 2007), while the NZ incidence increased by just under double (from 298.0/100 000 to 547.3/100 000). In both settings the increasing infection incidence was a direct reflection of increases in the incidence of serious skin infections of typical sites, along with a small contribution from infections secondary to primary skin trauma. Infections secondary to primary skin disease increased less, and those of atypical sites declined over this period. Figure 1. The incidence of serious skin infections in 0-14-year-old children in the Tairawhiti region by category and year, 1990-2007 Figure 2. The incidence of serious skin infections in 0-14-year-old children in NZ by category and year, 1990-2007 Table 2 shows the seasonal variation in the incidence of serious skin infections. In NZ, the crude incidence of infections was significantly higher during summer and autumn compared to winter (RR 1.12 for both). This trend was less distinct in Tairawhiti, with no significant difference in the seasonal incidence of infections. There was, however, no statistically significant difference in this trend between Tairawhiti and NZ. Table 2. The crude incidence of serious skin infections in 0-14 year old children by season, gender, age group, ethnicity and deprivation level for the Tairawhiti region and NZ, 1990-2007 Variable Category

Summary

Abstract

Aim

Serious skin infections are an increasing problem for New Zealand children with the highest national incidence in the Gisborne (Tairawhiti) region on the East Coast of New Zealand's North Island. This study aimed to describe the epidemiology of serious skin infections in children in this region, and make comparisons with equivalent national data to identify factors that might be contributing to elevated infection rates.

Method

Hospitalisation data were reviewed for 0-14-year-old children in the Tairawhiti region discharged from hospital with a serious skin infection between 1990 and 2007. A range of demographic variables were compared to equivalent data for New Zealand cases over the same period. The ratio of observed to expected discharges was calculated after indirectly standardising the Tairawhiti population age, ethnicity and deprivation composition to that of the total New Zealand population.

Results

In Tairawhiti the age-adjusted incidence of serious skin infections increased from 641.1/100 000 in 1990-1999 to 988.4/100 000 in 2000-2007, while the New Zealand incidence increased from 354.3/100 000 to 531.7/100 000. Preschool-aged children, M ori children, and those living in deprived neighbourhoods had the highest infection rates in all regions. The disparity between M ori and non-M ori children was significantly greater in Tairawhiti than nationally. The standardised ratio of observed to expected discharges in Tairawhiti compared with New Zealand was 1.42 (95%CI 1.32-1.52) in 1990-1999 and 1.28 (95%CI 1.19-1.36) in 2000-2007.

Conclusion

Serious skin infections are an increasing problem for all New Zealand children, but incidence rates in the Tairawhiti region are consistently greater than average national trends, with significantly larger ethnic disparities. The population composition of this region only partly accounts for the difference, suggesting the involvement of other unknown aetiological factors; these warrant further research.

Author Information

Cathryn OSullivan, Masters of Medical Sciences Student, Department of Public Health, University of Otago, Wellington; Michael Baker, Associate Professor, Department of Public Health, University of Otago, Wellington; Jane Zhang, Data Analyst. Department of Public Health, University of Otago, Wellington; Anna Davies*, Senior Advisor (Epidemiology), Health & Disability Intelligence Unit, Ministry of Health, Wellington; Geoffrey Cramp, Public Health Physician and Medical Officer of Health, Te Puna Waiora, Tairawhiti District Health, Gisborne, * Anna Davies is an employee of the New Zealand Ministry of Health. The views expressed in this paper are the authors own and do not represent the views or policies of the Ministry of Health. The paper was submitted for publication with the permission of the Deputy Director-General, Health and Disability Systems Strategy.

Acknowledgements

This work was supported by initial funding from Tairawhiti District Health as part of a larger piece of work made possible by a grant from the Ministry of Health Reducing Inequalities Budget.

Correspondence

Associate Professor Michael Baker, Department of Public Health, University of Otago Wellington, PO Box 7343, Wellington South, New Zealand. Fax: +64 (0)4 3895319

Correspondence Email

michael.baker@otago.ac.nz

Competing Interests

None declared.

Sladden MJ, Johnston GA. Common skin infections in children. BMJ. 2004;29:95-99.Koning S, Mohammedamin RSA, Van Der Wouden JC, et al. Impetigo: Incidence and treatment in Dutch general practice in 1987 and 2001-Results from two national surveys. Br J Dermatol. 2006;154:239-243.Loffeld A, Davies P, Lewis A, Moss C. Seasonal occurrence of impetigo: a retrospective 8-year review (1996-2003). Clin Exp Dermatol. 2005;30:512-514.Hersh AL, Chambers HF, Maselli JH, Gonzales R. National Trends in Ambulatory Visits and Antibiotic Prescribing for Skin and Soft-Tissue Infections. Arch Intern Med. 2008;168:1585-1591.Hunt D. Assessing and Reducing the Burden of Serious Skin Infections in Children and Young People in the Greater Wellington Region [Internet]. Wellington: Capital and Coast DHB, Hutt Valley DHB, Regional Public Health; 2004 [cited June 2009]. Available from: http://www.skininfections.co.nz/documents/Serious_Skin_Infections_Nov2004.pdfOSullivan C, Baker M, Zhang J. Increasing hospitalisations for serious skin infections in New Zealand children, 1990-2007. Epidemiol Infect. 2010;15:1-11.Craig E, Jackson C, Han DY, NZCYES Steering Committee. Monitoring the Health of New Zealand Children and Young People: Indicator Handbook [Internet]. Auckland: Paediatric Society of New Zealand, New Zealand Child and Youth Epidemiology Service; 2007 [cited June 2009]. Available from: http://www.paediatrics.org.nz/files/Indicator%20Handbook%20Version%2008.3.pdfLawes C. Paediatric cellulitis hospital discharges in the Auckland Region. Auckland: Public Health Protection Service, Auckland Healthcare; 1998.Finger F, Rossaak M, Umstaetter R, et al. Skin infections of the limbs of Polynesian children. N Z Med J. 2004;117:U847. http://journal.nzma.org.nz/journal/117-1192/847/content.pdfMorgan C, Selak V, Bullen C. Glen Innes Serious Skin Infection Prevention Project: Final Report 1 February 2003-31 January 2004 [Internet]. Auckland: Auckland Regional Public Health Services; 2004 [cited June 2009]. Available from:http://www.arphs.govt.nz/Publications_Reports/archive/GlenInnesSkinProject.pdfDepartment of Statistics. New Zealand census of population and dwellings [Internet]. Wellington: Statistics New Zealand; 2006 [cited September 2009]. Available from: http://www.stats.govt.nzSalmond C, Crampton P, Atkinson J. NZDep2006 Index of Deprivation [Internet]. Wellington: Ministry of Health; 2007 [cited August 2009]. Available from:http://www.uow.otago.ac.nz/academic/dph/research/NZDep/NZDep2006%20research%20report%2004%20September%202007.pdfOSullivan C, Baker M. Proposed epidemiological case definition for serious skin infection in children. J Paediatr Child Health. 2010;46:176-183.Salmond C, Crampton P, Atkinson J. NZDep2006 Index of Deprivation: Users Manual [Internet]. Wellington: Ministry of Health; 2007 [cited November 2009]. Available from: http://www.moh.govt.nz/moh.nsf/Files/phi-users-manual/$file/phi-users-manual.pdfClayton D, Hills M. Statistical Methods in Epidemiology Oxford: Oxford University Press; 1993, p80-82.Baker MG, Telfar Barnard L, Kvalsvig A, et al. Increasing incidence of serious infectious diseases and inequalities in New Zealand: a national epidemiological study. Lancet. 2012 Feb 17. [Epub ahead of print].Baker M, McNicholas A, Garrett N, et al. Household crowding a major risk factor for epidemic meningococcal disease in Auckland children. Pediatr Infect Dis J. 2000;19:983-990.Grant CC, Scragg R, Tan D, et al. Hospitalization for pneumonia in children in Auckland, New Zealand. J Paediatr Child Health. 1998;34:355-359.Malcolm L. Inequities in access to and utilisation of primary medical care services for M ori and low income New Zealanders. N Z Med J. 1996;109:356-358.Brabyn L, Barnett R. Population need and geographical access to general practitioners in rural New Zealand. N Z Med J. 2004;117:U996. http://journal.nzma.org.nz/journal/117-1199/996/content.pdfBailie RS, Stevens MR, McDonald E, et al. Skin infection, housing and social circumstances in children living in remote Indigenous communities: testing conceptual and methodological approaches. BMC Public Health. 2005;5:128.Kakar N, Kumar V, Mehta G, et al. Clinico-bacteriological study of pyodermas in children. J Derm. 1999;26:288-93.Masawe A, Nsanzumuhire H, Mhalu F. Bacterial skin infections in preschool and school children in costal Tanzania. Arch Derm. 1975;111:1312-6.Dajani A, Ferrieri P, Wannamaker L. Endemic superficial pyoderma in children. Arch Dermatol 1973;108:517-522.Taplin D, Lansdell L, Allen A, et al. Prevalence of streptococcal pyoderma in relation to climate and hygiene. Lancet. 1973;1:501-3.Rogers M, Dorman D, Gapes M, Ly J. A three-year study of impetigo in Sydney. Med J Aust. 1987;147:63-65.Kristensen JK. Scabies and pyoderma in Lilongwe, Malawi. Prevalence and seasonal fluctuation. Int J Dermatol. 1991;30:699-702.Elliot AJ, Cross KW, Smith GE, et al. The association between impetigo, insect bites and air temperature: A retrospective 5-year study (1999-2003) using morbidity data collected from a sentinel general practice network database. Fam Pract. 2006;23:490-496.Lake R, Adlam B, Perera S. Acute gastrointestinal illness (AGI) study: final study report [Internet]. Christchurch: Institute of Environmental Science and Research Limited; 2007 [cited June 2010]. Available from:http://www.nzfsa.govt.nz/science/research-projects/gastrointestinal-report/Final_Report.pdf

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