Population-based surveys on the frequency of common skin diseasesin adults—is there a risk of response bias?

D. Gill, K. Merlin, A. Plunkett, D. Jolley and R. MarksThe University of Melbourne, Department of Medicine (Dermatology), St Vincent’s Hospital, Melbourne; Skin and Cancer Foundation, Victoria, Australia

Summary Population-based surveys on the frequency of common skin diseases are important indetermining the health needs of a community. As they rely on voluntary presentation,there is a risk of response bias which may compromise the quality of the data obtained.The aim was to determine in what way and to what degree response bias may occur in apopulation-based survey on the frequency of common skin diseases in adults. A follow-up study was conducted on 1043 out of 2500 adults who did not attend for examinationas part of a randomized population-based survey on the frequency of common skindiseases amongst adults in Maryborough, Central Victoria, Australia. Nonrespondentswere more likely to be at the extremes of age, retired, unemployed and less likely toreport that they had a history of skin disease than the respondents. Subsequentexamination of a sample of the nonrespondents revealed they were more likely tohave skin cancers and Campbell de Morgan angiomas than the respondents. Thesedifferences cannot be fully explained on the basis of an age-related response bias alone.Response bias is a risk in population-based surveys of common skin diseases which relyon voluntary presentation. Some attempt should be made to sample the nonrespondentsin these surveys to determine the nature and extent of any bias and to adjust for it, ifnecessary.

Introduction

Community-based surveys of disease frequency can pro-vide valuable information to clinicians, the researchcommunity and policy-makers in the health field. Inepidemiological studies, particularly those that userandom sampling and rely on voluntary presentationto determine frequency of disease, nonresponse may posea problem.

The purpose of random sampling is to increase thelikelihood that the sample selected truly represents thewhole population. This allows smaller numbers to bestudied than would otherwise be necessary to obtain

information about the whole population. Nonrespondents(or even ‘late comers’) from a specified sample may exhibitexposures or outcomes which differ from those of respond-ents (or ‘early comers’)1 and can potentially affect theresults of surveys making them nonrepresentative of thecommunity as a whole.

Data obtained from these surveys must be carefullyexamined to determine whether there may be responsebias affecting the study and giving misleading results.2

Characteristics of this special group, the nonrespon-dents, need to be determined so they can be comparedwith the respondents. The possibility of any bias can thenbe identified and, if necessary, adjusted for when analys-ing the results of the survey. It is often extremely difficultto assess precisely the extent of the nonresponse bias butit is usually instructive to consider the likely direction ofits magnitude.3

The aim of this study was to examine and report oncharacteristics of nonrespondents in a community-based

Experimental dermatology • Original article

q 2000 Blackwell Science Ltd • Clinical and Experimental Dermatology, 25, 62–6662

Correspondence: R. Marks, The University of Melbourne, Department ofMedicine (Dermatology), St Vincent’s Hospital, 41 Victoria Parade, Fitzroy3065, Melbourne, Victoria, Australia. Tel: þ 03 9288 3332.Fax: þ03 9288 3292.

Accepted for publication 21 September 1999

survey on the frequency of common skin diseases inadults in Victoria, Australia.

Materials and methods

In September 1997, a cross-sectional survey was con-ducted to determine the prevalence of common skindiseases in an Australian population. A total of 2500people were randomly selected from the AustralianElectoral Roll for the City of Maryborough, Postcode3465, Central Victoria.

An information brochure and questionnaire (examin-ing demographic data and skin problems) were posted tothose selected inviting them to fill out the form andpresent for a skin examination. Those who did notrespond to the first invitation were contacted by tele-phone. If uncontactable by at least two telephone calls(which included a call outside work hours) a secondletter of invitation was sent and this was followed-up byat least two telephone calls by a doctor (DG).

A total of 1457 people (58.3%) presented during theinitial examination period (‘respondents’) and 1043(41.7%) did not. The 1043 people who did not attendare termed collectively ‘nonrespondents’. Of the non-respondents, 96 people gave consent to the skin exami-nation but did not attend and 431 people gave noconsent to the skin examination either through thepostal survey or follow-up telephone call(s).

The St. Vincent’s Hospital Human Research andEthics Committee gave approval to contact this lattergroup with a modified questionnaire requesting theperson’s date of birth, whether they had suffered froma skin condition in the past 2 weeks and offering them afurther opportunity to have a skin examination. Theywere also notified that they would be contacted bytelephone call from a doctor (DG) within 2 weeks torecord the above information and if they requested it, tomake a time for a skin examination. Fifty-three peoplefrom this group agreed to have a skin examination.These people will be termed ‘late participants’.

The 1043 nonrespondents fell into several groups:(A) late participants (53)–people who completed the

questionnaire and came for a skin examination afterinitially giving ‘no consent’; (B) partial participants(108)—people who filled out the questionnaire but didnot consent to a skin examination; (C) nonparticipants(623)—people who did not present for an examinationand did not fill out the questionnaire; (D) no contact(259)—people who could not be contacted by mail ortelephone (as outlined above).

Analysis

Statistical analysis was carried out with IntercooledStata 5 software.4 Bivariate analyses comparing respon-dents/nonrespondents were done using x2 analysis orFisher’s exact test. Logistic regression analysis was usedto calculate and compare the age and prevalence of skindisease in respondents and nonrespondents.

Results

Of the 623 nonparticipants, 223 people had moved outof the region and 18 were away at the time of theexaminations. Of the 259 people in the no contactgroup, 43 letters were returned to sender (unknown atthat address) and 64 people were confirmed deceased.We could find no evidence that the further 152 people inthis group were actually living in the area (and wereunable to confirm that they even existed).

The proportion of males and females was similar inthe respondents and nonrespondents (Table 1). Data ondate of birth were available for 708 of the 1043 non-respondents. Figures are given for comparison, but sig-nificance testing was not done on the deceased groupbecause of small numbers in each age group category.The nonrespondents differed throughout all age groupsto respondents except 30–39 years with a tendencytoward a greater difference at the extremes of the agegroups studied (x2 ¼ 89.5, d.f. ¼ 5, P<0.001). This isillustrated in Figs 1 and 2.

The questionnaire was completed by 161 nonrespon-dents (Groups A and B, Table 2). The late participants(Group A) and partial participants (Group B) have been

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Table 1 Comparison of sex and age between respondents and nonrespondents.

Nonrespondents Late participants Partial participants Nonparticipants DeceasedRespondents (Groups A,B,C,D) (Group A) (Group B) (Group C) (Group D)% % % % % %(n ¼ 1457) (n ¼ 848) (n ¼ 53) (n ¼ 108) (n ¼ 623) (n ¼ 64)

Male 46.0 47.9 43.3 40.7 48.0 62.5Female 54.0 52.1 56.7 59.3 52.0 37.5

analysed as a combined group and also individually asseparate groups. The late and partial participants(Groups A and B) were more likely to be retired/pen-sioners (particularly the late participants). The late andpartial participants were all more likely to have notstated their occupation whereas very few of the respon-dents failed to answer this question (Fig. 3). Overall, thelate and partial participants occupations differed fromthe respondents (x2 ¼ 92.7, d.f. ¼ 6, P <0.000).

The partial participants were less likely to reporthaving been treated for a previous skin cancer comparedwith the respondents. Self-reporting of eczema was lowerin the late participants group compared with the respond-ents. There were some slight differences in proportions ofother common skin diseases when Groups A and B werecompared with the respondents.

Each of the nonrespondents groups (excluding thedeceased) was questioned regarding whether they hadany skin conditions/rashes in the last 2 weeks. It should be

noted that the respondents and late and partial partici-pants (groups A and B) filled in a specific questionnairewhich asked about suffering from several common skindiseases (namely eczema/dermatitis, psoriasis, warts,acne and tinea) in the last week. The nonparticipantsgroup were only asked the question ‘Have you sufferedfrom any skin condition/problem or rash in the last 2weeks’ and were not prompted by specific names of skindiseases.

Data on 251 of the 623 nonrespondents was obtainedregarding any skin condition they had been suffering inthe last 2 weeks (Table 3). Respondents had a higherfrequency of positive response to these questions. Wehave no verification of these self-reports of diseasefrequency in the nonrespondents.

Table 4 illustrates the prevalence of common skindiseases recorded on examination for the respondentsand the late participants. Tinea pedis, combined skincancer [squamous cell carcinoma, basal cell carcinoma(BCC), melanoma], BCC alone, solar keratoses, seborrhoeic

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Figure 1 Age of respondents compared with nonrespondents.

Figure 2 Age of respondents compared with subgroups ofnonrespondents.

Table 2 Comparison of questionnaire data.

Respondents Late participants Partial participants% % %(n ¼ 1457) (n ¼ 53) (n ¼ 108)

Country of birth, Australia 91.9 93.3 92.0

History of skin diseaseSkin cancer 19.4 20.8 10.4Eczema 16.3 5.7 13.2Psoriasis 5.3 0 7.5Tinea 11.1 7.5 9.4Wart 14.8 7.5 10.4Acne 15.4 9.4 14.2

keratoses and Campbell de Morgan angiomas were sig-nificantly more frequent in the late participants com-pared with respondents. When controlled for agehowever, logistic regression analysis revealed only com-bined skin cancer [odds ratio (OR) ¼ 2.11; 95% confi-dence interval (CI), 1.03–4.34; R2 ¼ 0.0416; P ¼ 0.04]and Campbell de Morgan angiomas (OR ¼ 2.15; 95% CI,1.07–4.30; R2 ¼ 0.0448; P ¼ 0.031) had a significantlyhigher prevalence in late responders compared withresponders.

Discussion

Nonresponse bias can be difficult to estimate in a popula-tion survey. Even if an attempt is made to contact thenonrespondents the data still remain unavailable for alarge proportion of them.5 The various reasons for non-response usually makes the assessment of the extent ofsuch biases difficult or impossible.6 We experiencedsimilar difficulty assessing nonrespondents in oursurvey. The process was time consuming and eventhough we were able to obtain some data on variousdemographic details and skin conditions they were notcomplete for all nonrespondents.

Results from other surveys that have examined non-respondents reveal that nonresponse is a nonrandomaction.7 The nonrespondents in our survey differed torespondents in several ways. Nonrespondents weremuch more likely to be at the extremes of age which issimilar to previous findings.2,7,8 Nonrespondents werevery similar to respondents when comparing sex andcountry of birth. Although economic status was notassessed directly, nonrespondents were more likely tobe retired, unemployed or to have not stated theiroccupation, which is in keeping with findings of otherinvestigators.7,8

Some authors have concluded that nonresponse biascan be estimated by analysing responses from the late(or reluctant) respondents. They argue that becausewillingness to attend is a continuum, reluctant respond-ents are more likely to be similar to nonrespondents.5

This was illustrated by the late participants and partialparticipants in this study particularly when consideringage and self-reported presence of a skin condition. Thesetwo groups also showed a similar distribution to the ageof nonrespondents overall.

In our examination of the ‘late participants’ somedifferences between them and the respondents can partlybe explained by the over-representation of elderly peoplein the late participants group. Seborrhoeic keratoses,Campbell de Morgan lesions, BCC and solar keratoses areknown to increase steadily with age. Atopic eczema hasbeen shown to decrease with age and this is consistentwith lower prevalence rates for the late participants.

The decrease in the overall prevalence of self-report ofskin disease in respondents compared with combined lateand partial participants and the nonparticipants suggeststhe possibility of a positive response bias. Those peoplewho believed they were suffering from a skin disease mayhave been more likely to participate in the survey thanthose who did not. A previous report investigating non-response bias in a large population-based survey foundthat the presence of health problems that a personwished to discuss with a physician had the largestassociation with likelihood of presenting for examina-tion.2 This is presumably the phenomenon seen in thosepeople who suspect they have a skin disease. However,

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Figure 3 Occupation of respondents compared with non-respondents.

Table 3 Prevalence of self-reported skin disease.

Respondents Late participants Partial participants Nonparticipants(%) (Group A) (%) (Group B) (%) (Group C) (%)

Skin condition (n ¼ 1457) (n ¼ 53) (n ¼ 108) (n ¼ 251)

Self-reported 46.2 28.3 39.3 8.4Examination by doctor 84.4 50.9 NA NA

the late participants who were examined in our surveyhad over twice the likelihood of having a skin cancer(OR ¼ 2.11) compared with respondents, even when agedifferences between the two groups were taken intoaccount. Whether this is a real phenomena will dependon subsequent surveys specifically looking at this group.

It must be said that this does not necessarily mean thenonrespondents in our survey suffered from less skindisease in general than the respondents. There wasrelatively poor correlation between self-report of skindisease and true prevalence of skin disease detectedwhen examined by a physician. As reported above, thefrequency of some common skin diseases was actuallyhigher in the subgroup of nonrespondents, whereasmany others were similar.

In conclusion, this study demonstrates that response

bias can occur in population-based surveys of commonskin diseases in adults which rely on voluntary presenta-tion. Some assessment of the people who do not attendfor examination is important to determine whether theprevalence estimates are representative of the populationstudied and to allow comparisons between respondentand nonrespondent groups and, if appropriate, adjust-ment of prevalence rates if there is a systematic differ-ence found between those who respond and those whodo not.

Acknowledgements

The authors thank the following for their assistancethroughout the study. Clinicians: P. Fergin, D. Gin,P. Foley, L. Hale, T. Hall, J. Horton, A. Howard, M. Lee,C. McCormack, A. Mar, R. Nixon, D. Nurse, D. Orchard, H.Rotstein, R. Sinclair, B. Tate, B. Welsh and J. Yeatman.Nurses: L. Atkin, V. Bennett and C. Skinner. Administra-tive staff: B. Edwards, M. Kilkenny. B. Waixel and membersof the Maryborough District Health Service and themembers of Rotary, Maryborough who acted as volun-teers on the days of the examinations. Funding for thestudy included grants from the F & E Bauer Foundationand internal funds of the Department of Dermatology, StVincent’s Hospital. Finally, we wish to thank the people ofMaryborough without whose support and participationthe survey would not have been possible.

References

1 Sackett D. Bias in analytic research. J Chron Dis 1979; 32:51–63.

2 Forthofer RN. Investigation of nonresponse bias inNHANES II. Am J Epidemiol 1983; 117: 507–159.

3 Martin Bobak. Bias-The silent menace. In: Williams H,Strachan D, eds. The Challenge of Dermatoepidemiology. NewYork: CRC Press. 1997: 87–98.9999.

4 StataCorp. Stata Statistical Software: Release 5.0. College Sta-tion, TX: Stata Corp., 1997.

5 Herbert R, Bravo G, Korner-Bitensky N, Voyer L. Refusaland information bias associated with postal questionnairesand face-to-face interviews in elderly subjects. J Clin Epi-demiol 1996; 49: 373–81.

6 Benfante R, Reed D, MacLean Kagan A. Response bias inthe Honolulu Heart Program. Am J Epidemiol 1989; 130:1088–100.

7 Boyle F, Najman J, Vance J, Thearle M. Estimating non-participation bias in a longitudinal study of bereavement.Aust N Z J Public Health 1996; 20: 483–7.

8 Joseph Melton L, III, Dyck P, Karnes J et al. Non-responsebias in studies of diabetic complications. Rochester DiabeticNeuropathy Study 1993; 46: 341–8.

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Table 4 Comparison of respondents with late participants (Group A).

Respondents Late participants(%) (%)

Prevalence (n ¼ 1457) (n ¼ 53)

EczemaAtopic 6.4 1.9Seborrhoeic 9.3 3.8Asteatotic 9.7 5.7Contact 3.2 0Discoid 1.5 0Varicose/stasis 1.9 3.8

Psoriasis 6.8 1.9

Tinea PedisClinical diagnosis 37.7 50.9Mycological diagnosis 8.9 NA

Tinea UnguiumClinical diagnosis 28.4 28.3Mycological diagnosis 5.4 NA

Skin cancerOverall 7.9 20.8Melanoma 1.0 1.9Basal cell 5.8 15.1Squamous cell 1.4 3.8Solar keratosis 34.9 49.1

WartsCommon 5.6 9.4Plane 0.5 0Plantar 1.2 1.9

Acne 10.3 11.3

Seborrhoeic keratoses 62.8 71.7

Campbell de Morgan(cherry angiomas) 57.1 79.2

NA, Not available.