Reserch Bettin Kjær Kristinsen, Berit Andersen, Flemming Bro, Hns Svnholm nd Peter Vedsted Impct of GP reminders on follow-up of bnorml cervicl cytology: before fter study in Dnish generl prctice Abstrct Bckground Dysplsi my progress becuse of loss to follow-up fter n bnorml cervicl cytology. Approximtely 18% of Dnish women postpone the recommended follow-up, which depends on the cytology results. Aim To investigte if reminder to the GP bout missed follow-up could reduce the proportion of women who fil to ct on recommended follow-up, nd to nlyse the effect on sociodemogrphic nd generl prctice vritions. Design nd setting A ntionl electronic GP reminder system ws lunched in Denmrk in 2012 to trget missed follow-up fter screening, opportunistic testing, or surveillnce indiction. The uthors compred follow-up proportions in ntionl observtionl before fter study. Method From ntionl registries, 1.5 million cervicl cytologies (from 2009 to 2013) were eligible for inclusion. Approximtely 10% hd recommendtion for follow-up. The proportion of cervicl cytologies without follow-up ws clculted t different time points. Results were strtified by follow-up recommendtions nd sociodemogrphic chrcteristics, nd chnges in prctice vrition for follow-up were nlysed. Results Fewer women with recommendtion for follow-up missed follow-up 6 months fter GP reminder. Follow-up improved in ll investigted sociodemogrphic groups (ge, ethnicity, eduction, nd cohbittion sttus). Interction ws found for ge nd cohbittion sttus. Vrition between prctices in loss to follow-up ws significntly reduced. Conclusion An electronic GP reminder system showed potentil to improve the qulity of cervicl cncer screening through reduced loss to follow-up. Keywords erly detection of cncer; generl prctice; mss screening; qulity of helth cre; uterine cervicl neoplsms. INTRODUCTION Successful prevention of cervicl cncer depends on follow-up of bnormlities fter cervicl cytology testing. 1,2 Nevertheless, women without follow-up re persisting problem in mny Western countries. 3 5 Lck of follow-up hs been ssocited with both ptient- 6 8 nd system-relted brriers. 3,9,10 In Denmrk, GP is usully involved in securing follow-up. 5,11 Consequently, since 2012, GPs hve received n electronic reminder if pproprite follow-up ws not duly registered. 11 Four other studies hve ddressed the effect of GP reminder s single intervention in cervicl cncer screening follow-up. However, two of the studies lcked control group, 12,13 nd before fter study did not find more women with follow-up when compring before nd fter in n undjusted nlysis, though the study my hve been underpowered. 14 A Dutch intervention study improved follow-up. However, in this setting it ws necessry to generte GP reminder for 45% of ll women in need of follow-up nd, despite this, 19% of intervention women missed followup 1 yer fter cervicl cytology requisition. 15 In Denmrk, 18% of women with cervicl cytology nd recommendtion for followup re without follow-up 12 weeks fter recommended follow-up. 5,11 This number is reltively low compred with studies in other countries. 3 Therefore, evidence bout the B Kjær Kristinsen, MHSc, PhD, reserch fellow, Reserch Unit for Generl Prctice, nd Reserch Centre for Cncer Dignosis in Primry Cre; F Bro, MD, professor, Reserch Unit for Generl Prctice; P Vedsted, MD, professor, Reserch Centre for Cncer Dignosis in Primry Cre, Deprtment of Public Helth, Arhus University, Arhus, Denmrk. B Andersen, MD, executive consultnt, ssocite professor, Deprtment of Public Helth Progrms; H Svnholm, MD, pthologist, Deprtment of Public Helth Progrms, nd Deprtment of Pthology, Rnders Regionl Hospitl, Rnders, Denmrk. effects of GP reminder in clinicl setting with better follow-up is needed. It could be expected tht the remining 18% of women without follow-up my fce more complex brriers nd could thus be more reluctnt to ttend follow-up. 16 Additionlly, no studies hve described the effect of GP reminders on socil inequlity 17 or vrition mong GP prctices. The uthors imed to evlute the effect of GP reminders on women without followup, on sociodemogrphic differences, nd on vrition between GP prctices. METHOD In lrge observtionl study, the uthors compred the proportions of follow-up before nd fter the implementtion of ntionl electronic reminder system for GPs. Setting All Dnish women ged 23 50 yers re invited to cervicl cncer screening every third yer, nd women ged 50 64 yers re invited every fifth yer. The women re identified through ntionl dtbses nd re encourged to book n ppointment free of chrge with their generl prctice. All smples re sent to pthology deprtment for dignosis. If necessry, recommendtion for follow-up is lso pplied tht is, either within 3 months (referrl to gynecologist) or in 3, 6, or 12 months, depending on the Address for correspondence Bettin Kjær Kristinsen, Reserch Unit for Generl Prctice, Arhus University, Brtholins Alle 2, DK-8000 Arhus, Denmrk. Emil: b.kristinsen@ph.u.dk Submitted: 15 Jnury 2017; Editor s response: 15 Februry 2017; finl cceptnce: 12 April 2017. British Journl of Generl Prctice This is the full-length rticle (published online 18 Jul 2017) of n bridged version published in print. Cite this version s: Br J Gen Prct 2017; DOI: https://doi.org/10.3399/bjgp17x691913 1 British Journl of Generl Prctice, Online First 2017
How this fits in A review found tht up to 12% of cncers rise due to filure in follow-up, nd is the third most common reson for cncer development. Strtegies to improve followup re thus crucil. As the smple tker, the GP plys pivotl role in securing follow-up. This study found tht GP reminder lmost hlved the proportion of women without follow-up, hd effect cross sociodemogrphic groups, nd decresed the vrition in loss to follow-up mong GPs. cytology or histology ws registered in the DPDB 1 month fter the follow-up ws due. Cytology results with recommendtion of follow-up in 3, 6, or 12 months generted reminder 3 months fter recommended dte of follow-up. It ws nticipted tht, fter receiving the electronic reminder from the DPDB, GPs would initite contct with the womn, nd encourge her to return for the required follow-up. However, there ws no protocol for how or when GPs should ct on reminders nd no dditionl resources were given to the GPs. Figure 1. Flow chrt of number of cervicl cytologies. Women without unique Dnish civil registrtion number. b Unknown dignosis or potentil uncertinty bout follow-up recommendtions. c Dignosis formed ccording to informtion vilble from the uthors upon request. current nd former cervicl cytology results. Results nd follow-up recommendtion re trnsferred to the electronic ptient record in the generl prctice. GPs convey results to women either fce-to-fce, or by phone, or by e-mil. 11 Before the implementtion of GP reminders, no other ntionl system inititives were performed in Denmrk to support women or GPs in remembering follow-up. 11 Approximtely 99% of ll Dnish women re listed with specific GP prctice. 18 Intervention The reminder system ws lunched ntionwide in Denmrk on 18 Jnury 2011 under the uspices of the Dnish Pthology Dt Bnk (DPDB). The reminder system ws fully opertionl on 2 Februry 2012 fter run-in period. 4 Cervicl cytologies with recommendtion of follow-up within 3 months (referrl to gynecologist) generted GP reminder if no new cervicl Study prticipnts All cervicl cytology smples (Systemtized Nomenclture of Medicine [SNOMED code: T8X310]) performed during 1 Jnury 2009 to 5 August 2013 for women with follow-up recommendtion were identified, regrdless of test indiction (screening, opportunistic testing, or surveillnce for erlier bnormlity). The uthors imed to study follow-up dherence 6 months fter the reminder (tht is, 7 months fter recommendtion for followup within 3 months, nd 9 months fter recommendtions for follow-up in 3, 6, or 12 months), s the reminder ws generted 1 or 3 months fter the dte of recommended follow-up. Dt regrding follow-up were retrieved on 30 My 2014. Therefore, the uthors only included cervicl cytologies with recommended follow-up dte 7 or 9 months erlier thn 30 My 2014. The uthors excluded cytologies of women with unknown dignosis or crcinom, women who died or emigrted from Denmrk in Cervicl cytologies (T8X310) with follow-up recommendtion for women ged 23 64 yers n = 152 551 Before Reminder dte before 18 Jul 2010 n = 34 147 Trnsition Reminder dte 19 Jul 2010 to 2 Feb 2012 n = 54 049 After Reminder dte fter 3 Feb 2012 n = 64 355 Exclusions: 13 Ptient identifiction error 98 Unknown dignosis b,c 41 Crcinom c 975 Women died or emigrted in the observtion period for follow-up Exclusions: 19 Ptient identifiction error 164 Unknown dignosis b,c 59 Crcinom c 1444 Women died or emigrted in the observtion period for follow-up Exclusions: 18 Ptient identifiction error 1955 Women in intervention study 127 Unknown dignosis b,c 60 Crcinom c 1470 Women died or emigrted in the observtion period for follow-up Before n = 33 020 Trnsition n = 52 363 After n = 60 725 British Journl of Generl Prctice, Online First 2017 2
Tble 1. Chrcteristics of the 146 108 cervicl cytologies nd the 124 244 women before, in the trnsition period, nd fter implementtion of GP reminders Before, Trnsition, After, n (%) n (%) n (%) Totl number of cervicl cytologies 33 020 52 363 60 725 Totl number of generl prctices 2093 2174 2176 10 th 90 th centile in number of cytologies per prctice 2 36 3 56 3 68 Number of generl prctices with >4 cytologies 1692 1943 Totl number of women 29 978 (100) 44 285 (100) 49 981 (100) Number of women with 1 cytology 27 044 (90) 36 779 (83) 40 098 (80) Number of women with 2 cytologies 2828 (9) 6964 (16) 9085 (18) Number of women with 3 cytologies 106 (0) 542 (1) 798 (2) Dignosis Norml 4237 (13) 16 248 (31) 17 182 (28) Indequte 10 308 (31) 11 240 (21) 11 440 (19) ASC-US, ASC-H, AGC 8034 (24) 10 840 (21) 12 367 (20) LSIL 6399 (19) 9720 (19) 14 730 (24) HSIL, AIS 4042 (12) 4315 (8) 5006 (8) Follow-up recommendtion Before 3 months (reminder fter 4 months) 11 957 (36) 13 887 (27) 17 673 (29) 3 months (reminder fter 6 months) 10 222 (31) 10 817 (21) 10 854 (18) 6 months (reminder fter 9 months) 6986 (21) 8890 (17) 9683 (16) 12 months (reminder fter 15 months) 3855 (12) 18 769 (36) 22 515 (37) Region Cpitl Region of Denmrk 6297 (19) 8532 (16) 10 868 (18) Region Zelnd 7134 (22) 11 872 (22) 13 048 (21) Centrl Denmrk Region 9527 (29) 15 247 (29) 16 848 (28) North Denmrk Region 3462 (10) 6837 (13) 8656 (14) Region of Southern Denmrk 6598 (20) 9875 (19) 11 305 (19) Missing 2 0 0 Medin ge of women (25th 75th centile) b 36 (29 44) 36 (29 44) 36 (29 45) Ethnicity b Dnish 27 493 (93) 40 764 (93) 45 891 (93) Western immigrnts/descendnts 684 (2) 991 (2) 1289 (3) Non-Western immigrnts/descendnts 1266 (4) 1892 (4) 2139 (4) Missing 535 638 662 Cohbittion sttus b Mrried/cohbiting 18 308 (62) 27 058 (62) 29 601 (60) Living lone 11 140 (38) 16 596 (38) 19 724 (40) Missing 530 631 656 Eduction (yers) b 10 5689 (20) 8349 (19) 9219 (19) >10 to <15 15 624 (54) 22 888 (53) 25 318 (53) >15 7663 (26) 11 658 (27) 13 656 (28) Missing 1002 1390 1788 Numbers per cervicl cytology. b Numbers per women t time of first cervicl cytology. AGC = typicl glndulr cells. AIS = denocrcinom in situ. ASC-H = typicl squmous cells of undetermined significnce. ASC- US = typicl cells of undetermined significnce. HSIL = high-grde squmous intrepithelil lesion. LSIL = lowgrde squmous intrepithelil lesion. the study period, women with identifiction errors, nd women who prticipted in the intervention rm of rndomised study trgeted to improve follow-up. Before fter exposure groups The uthors clculted GP reminder dte for ll included cervicl cytologies. They divided the study popultion into before group (with simulted reminder dte before ctivtion of the reminder system) nd n fter group (with n ctul reminder dte fter ctivtion). The before group consisted of women with simulted reminder dte before 18 July 2010 (tht is, 6 months before the system ws lunched on 18 Jnury 2011). The fter group consisted of women with reminder dte fter 2 Februry 2012 (when the system ws fully opertionl). The trnsition group consisted of women with GP reminder dte generted during the run-in period (between 19 July 2010 nd 2 Februry 2012). This period ensured fully functioning reminder system in the fter group nd gve the GPs time to dpt to the new procedures. Dt Dt regrding cervicl cytology nd histology were retrieved from the ntionwide DPDB. This register contins records on dignosis nd dtes of ll pthologicl mteril evluted in Denmrk since 1997, from ll settings nd regrdless of indiction. All cytologies re ssigned codes from the Dnish version of the SNOMED. 19 Ntionl stndrds from 2007 prescribe clssifiction of results in ccordnce with the Bethesd Clssifiction for Cervicl Cytology 2001 nd encourge inclusion of follow-up recommendtion (specific SNOMED codes). 20,21 Informtion on sociodemogrphic chrcteristics ws obtined through Sttistics Denmrk (on 1 Jnury in the yer preceding the cytology), nd ll dt were linked using the unique Dnish civil registrtion number of ech womn. Eductionl level ws ctegorised, ccording to the UNESCO clssifiction, s low ( 10 yers), middle (11 15 yers), or higher eduction (>15 yers). 22 Cohbittion ws ctegorised s mrried/cohbiting or living lone. Ethnicity ws ctegorised ccording to the definition pplied by Sttistics Denmrk s: Dnish; immigrnt or descendnt from Western countries; or immigrnt or descendnt from non- Western countries. 23 Age ws clculted by subtrcting the womn s dte of birth from the cytology requisition dte. Sttisticl nlysis Follow-up proportions were clculted for ech follow-up recommendtion (tht is, within 3, or in 3, 6, or 12 months) with 3 British Journl of Generl Prctice, Online First 2017
Tble 2. Associtions (odds rtios) of cervicl cytologies without follow-up, strtified by follow-up recommendtion Before After After versus % without % without before (ref) follow-up follow-up OR (95% CI) Recommended follow-up in 12 months, n 3855 22 515 At recommended follow-up dte 78.0 72.8 0.87 (0.83 to 0.91) 3 months fter recommended follow-up b 48.8 48.0 1.00 (0.96 to 1.06) 6 months fter recommended follow-up 36.0 18.6 0.54 (0.50 to 0.58) 9 months fter recommended follow-up 28.4 11.7 0.44 (0.39 to 0.50) Recommended follow-up in 6 months, n 6986 9683 At recommended follow-up dte 64.8 62.0 0.94 (0.90 to 0.97) 3 months fter recommended follow-up b 28.4 28.0 0.99 (0.96 to 1.03) 6 months fter recommended follow-up 18.5 10.9 0.73 (0.69 to 0.76) 9 months fter recommended follow-up 14.8 7.0 0.62 (0.56 to 0.69) Recommended follow-up in 3 months, n 10 222 10 854 At recommended follow-up dte 62.6 60.1 0.94 (0.90 to 0.97) 3 months fter recommended follow-up b 34.3 32.4 0.94 (0.91 to 0.98) 6 months fter recommended follow-up 25.5 15.0 0.64 (0.59 to 0.70) 9 months fter recommended follow-up 21.5 10.6 0.60 (0.55 to 0.67) Recommended follow-up within 3 months, n 11 957 17 673 At recommended follow-up dte 16.3 16.2 0.99 (0.95 to 1.02) 1 month fter recommended follow-up b 9.7 10.4 1.04 (0.99 to 1.08) 4 months fter recommended follow-up 4.4 3.9 0.93 (0.88 to 0.99) 7 months fter recommended follow-up 3.3 2.5 0.87 (0.81 to 0.94) Multilevel mixed-effect logistic regression, with correction for rndom-effect clusters t the level of GPs nd women. b The dte GP reminder ws generted for the fter group. CI = confidence intervl. OR = odds rtio. Ref = reference. ll women needing follow-up s the denomintor t four time points. Followup proportions in before-nd-fter groups were compred through odds rtios (OR) for the likelihood of not hving follow-up, nd strtified ccording to type of follow-up recommendtion. The unit of nlysis ws the individul cervicl cytology. The uthors clculted ORs using multilevel mixed-effects logistic regression with rndom effects to correct for clustering of mesurements within ech womn, nd for clustering of women within GP prctices. 24 Kpln Meier plots displyed the time from dte of initil cervicl cytology to dte of follow-up, or censoring due to missed follow-up, t the end of the observtion period, whichever cme first. To determine if the GP reminder effect ws modified by the sociodemogrphic chrcteristics of the women, followup proportions 7 or 9 months fter the recommended dte of follow-up (tht is, 6 months fter reminder for the fter group) between before nd fter groups were compred in strtified nlysis. Associtions between follow-up sttus nd sociodemogrphic fctors were estimted s described bove nd djusted for ge (s continuous vrible) nd type of followup recommendtion. Effect on GP prctice vrition ws explored by clculting followup proportions 7 or 9 months fter the recommended dte of follow-up (tht is, 6 months fter reminder for the fter group) for ech prctice before nd fter implementtion of the reminder system. To ensure high sttisticl precision, only GP prctices with four or more cervicl cytologies in need of follow-up were included. The proportions were listed ccording to order of prctice proportions in sctterplots, nd the interqurtile rnge ws estimted. Pitmn s test for compring vrinces of follow-up proportions of pired GP prctices ws dditionlly used (Stt commnd: sdpir). 25 Only prctices tht were ctive both before nd fter were included in this test. All sttisticl nlyses were conducted using Stt version 14. RESULTS In the study period, 1 487 155 cervicl cytologies were performed in generl prctice. Of these, 1 321 846 (88.9%) hd no follow-up recommendtion, nd 12 758 (0.8%) hd less thn 6 months to observe follow-up dherence fter the GP reminder. This left 152 551 (10.3%) eligible women in the study period. The uthors included 33 020 cervicl cytologies British Journl of Generl Prctice, Online First 2017 4
Follow-up recommendtion in 12 months Follow-up recommendtion in 6 months Proportion without follow-up 0 0.25 0.5 0.75 1.0 0 0.25 0.5 0.75 1.0 0 5 10 15 20 0 5 10 15 Follow-up recommendtion in 3 months Gynecologicl follow-up within 3 months Proportion without follow-up 0 0.25 0.5 0.75 1.0 0 0.25 0.5 0.75 1.0 0 Before After 5 10 15 0 2 4 6 8 10 Months from cytology requisition to follow-up Figure 2. Proportion of cervicl cytologies without follow-up before nd fter implementtion of reminders, strtified by follow-up recommendtion. First verticl line is the time point for recommended follow-up. Second verticl line is the time point when reminder ws generted for the fter group. Followup recommendtions within 3 months (needing to consult gynecologist) hd GP reminder 1 month fter recommended dte of follow-up (tht is, fter 4 months), wheres recommendtions for follow-up in 3, 6, or 12 months hd GP reminder 3 months fter dte of recommended follow-up (tht is, fter 6, 9, or 15 months). (from 29 978 women) before, nd 60 725 cytologies (from 49 981 women) fter the implementtion in the nlyses (Figure 1). Tble 1 shows the bseline chrcteristics of the included women nd cytologies. Follow-up recommendtions nd types of dignosis differed between the before nd fter groups. Tble 2 presents the likelihood of not being followed-up, strtified by type of follow-up recommendtion. Follow-up recommendtions roughly corresponded to certin dignoses. As indictions for follow-up recommendtions might hve chnged over time, sensitivity nlyses were performed with djustments for dignoses, but this did not chnge the results substntilly (further informtion is vilble from the uthors on request). Figure 2 shows mrked temporl reduction in no follow-up when GP reminder ws generted for the fter group, most mrkedly for those with recommendtion of follow-up in 12 months, nd less mrkedly for those with recommendtion of follow-up within 3 months. Tble 3 shows tht follow-up ws most complete for women 35 yers, ethnic Dnes, nd women who re highly educted. The proportion without follow-up decresed significntly from before to fter implementtion in ll sociodemogrphic groups. The effect ws lowest mong younger women (ged 23 34 yers) nd women living lone. The interqurtile intervl of follow-up proportions mong GP prctices in the before group rnged from 79% to 94% (interqurtile rnge [IQR] 15). Comprble estimtes for the fter group were 88% to 100% (IQR 12). The vrition between followup proportions decresed significntly from before to fter mong the 1527 pired prctices (rtio of stndrd devitions 0.67, 95% confidence intervl [CI] = 0.63 to 0.70), visulised by more horizontl fter line compred with the before line (Figure 3). DISCUSSION Summry The proportion of women without followup ws lmost hlved following the implementtion of the reminder system. It hd positive effect in ll sociodemogrphic groups nd reduced the vrition in followup proportions mong GP prctices. The qulity of the screening progrmme ws thus improved. However, 2.5% to 11.7% of cervicl cytologies hd no follow-up 6 months fter GP reminder, depending on the type of follow-up recommendtion. Strengths nd limittions The risk of selection bis ws reduced s the uthors used prospectively collected ntionl dt from the DPDB. These records hve been lmost complete since 5 British Journl of Generl Prctice, Online First 2017
Tble 3. Assocition (odds rtios) between no follow-up nd sociodemogrphic sttus Before After After versus before (ref) n (% without n (% without follow-up) b OR (95% CI) c follow-up) b OR (95% CI) c OR (95% CI) c P d Age group, yers 23 34 15 650 (14.8) 1 (ref) 27 905 (9.2) 1 (ref) 0.53 (0.49 to 0.57) 35 44 9793 (14.1) 0.79 (0.72 to 0.85) 17 588 (7.5) 0.63 (0.57 to 0.70) 0.44 (0.40 to 0.48) 0.001 45 54 5227 (12.7) 0.66 (0.59 to 0.74) 10 207 (6.5) 0.49 (0.43 to 0.55) 0.43 (0.37 to 0.48) 0.003 55 64 2350 (15.5) 0.79 (0.69 to 0.89) 5025 (7.2) 0.56 (0.48 to 0.66) 0.36 (0.30 to 0.43) 0.005 Ethnicity Non-Western 1374 (22.0) 1 (ref) 2507 (12.6) 1 (ref) 0.46 (0.36 to 0.55) Western 746 (18.1) 0.86 (0.67 to 1.11) 1548 (10.7) 0.87 (0.66 to 1.14) 0.48 (0.34 to 0.62) 0.833 Dnish 30 323 (13.7) 0.58 (0.49 to 0.68) 55 937 (7.7) 0.50 (0.42 to 0.59) 0.47 (0.44 to 0.49) 0.644 Eduction, yers <10 6267 (17.3) 1 (ref) 11 072 (10.3) 1 (ref) 0.47 (0.42 to 0.53) >10 to <15 17 321 (13.6) 0.72 (0.66 to 0.79) 30 970 (7.3) 0.60 (0.54 to 0.66) 0.44 (0.40 to 0.47) 0.301 >15 8348 (12.6) 0.66 (0.60 to 0.74) 16 592 (7.1) 0.59 (0.52 to 0.66) 0.47 (0.42 to 0.52) 0.962 Cohbittion Living lone 12 450 (12.8) 1 (ref) 24 441 (7.8) 1 (ref) 0.52 (0.48 to 0.57) Mrried/cohbiting 19 999 (15.0) 1.03 (0.95 to 1.11) 35 559 (8.1) 0.93 (0.86 to 1.01) 0.44 (0.41 to 0.47) 0.002 Follow-up proportions were studied 6 months fter GP reminder tht is, 7 months fter recommended dte of follow-up for women with recommendtion for gynecologicl follow-up within 3 months, nd 9 months fter dte of recommended follow-up for women with recommendtion for follow-up in 3, 6, or 12 months. b Numbers per cervicl cytology. Numbers vry due to missing dt. c Adjusted for type of follow-up recommendtion. Ethnicity, eduction, nd cohbitting sttus lso djusted for ge. d Test for interction showing if effects of reminders were modified by sociodemogrphic fctors. CI = confidence intervl. OR = odds rtio. Ref = reference. 2005. 26 The study enjoyed high sttisticl precision from the lrge number of included cervicl cytologies nd generl prctices. Misclssifiction due to mbiguous or imprecise coding ws minimised s ntionl stndrds for SNOMED coding of dignoses nd follow-up were dopted in Denmrk in 2007. A wekness of this observtionl study is the before fter design, s other chnges my hve cused the effects. For instnce, smll improvements were observed for the fter group even before the introduction of the reminders, but the lrgest effects begn to show t the exct time of the reminder introduction. The uthors excluded women with identifiction errors s it ws not possible in registries to study their follow-up. However, these women my be t greter risk of not returning for follow-up, therefore prevlence of followup proportions my be underestimted, though the uthors do not expect it to ffect the ssocitions. Differences in the distribution of followup recommendtions persisted between before nd fter groups. This ws expected, becuse of the design of the study. In prticulr, cytologies with lte followup recommendtion were more likely to receive reminder (nd be included in the fter group) thn those with short follow-up recommendtion. Therefore, ll nlysis of follow-up proportions were strtified by type of follow-up recommendtion. Distribution of dignoses lso differed from before to fter within ech type of follow-up recommendtion group (further informtion is vilble from the uthors upon request). This my hve been consequence of introducing humn ppillom virus (HPV) trige nd chnge to liquid-bsed screening techniques in pthology deprtments during the study period. 11,20 Even though djusting for dignosis did not lter ssocitions much, confounding my persist (further informtion is vilble from the uthors upon request). Comprison with existing literture Other studies found vrying improvement in follow-up using GP reminders, 13 15 but these did not investigte effects on sociodemogrphic vritions. In this study, the reminder improved follow-up in ll socil groups. However, 6.5% to 12.6% of the women were not followed up, prticulrly younger nd low-educted women with non-western ethnicity. Other studies hve found similr inequlities. 6,27 Inequlities persisted with reminders, nd s the reminders hd smller reltive effect mong women living lone nd younger women, reltive inequlities my thereby increse, even though the bsolute differences in these groups were reduced. The most profound effect of reminders British Journl of Generl Prctice, Online First 2017 6
Figure 3. GP vritions in cervicl cytology follow- up proportions. Proportions of 1692 GP prctices before, nd 1943 GP prctices fter, listed ccording to proportion of women with follow-up. Observtion of follow-up dherence ended 6 months fter GP reminder ws generted to the fter group. This entiled 7 months fter recommended dte of follow-up for women with recommendtion for follow-up within 3 months, nd 9 months for women with recommendtion for follow-up in 3, 6, or 12 months. Proportion with follow-up 0.2 0.4 0.6 0.8 1.0 Before After 0 20 40 60 80 100 Proportion of GPs Funding The study ws finncilly supported by the Dnish foundtion TrygFonden (grnt number: 7.12.0836), the Helth Science Reserch Foundtion of the Centrl Denmrk Region, nd the Helth Foundtion (grnt number: 20128125). Ethicl pprovl None required. Provennce Freely submitted; externlly peer reviewed. Competing interests The uthors hve declred no competing interests. Discuss this rticle Contribute nd red comments bout this rticle: bjgp.org/letters ws found for cervicl cytologies with recommendtion of follow-up in 12 months. Approximtely 80% of these cytologies were norml but still needed follow-up, for exmple, due to surveillnce for erlier dysplsi (further informtion is vilble from the uthors upon request). Norml test results re generlly excluded from studies on follow-up, 13 15 even though it is ssumed tht 8% of women develop new pre-cncerous dysplsi fter cone biopsy tretment, nd 80% within 2 yers. 28 Additionlly, incidence rte rtios of cervicl cncer re incresed for up to 15.5 yers fter n bnorml cytology. 29 Some of these women re followed in generl prctice. 11 A smller, significnt effect ws found mong women with recommendtion of follow-up within 3 months. Approximtely 30% of these hve high-grde squmous intrepithelil lesion (HSIL) dignosis (further informtion is vilble from the uthors upon request). However, s lmost 30% of women with cervicl squmous intrepithelil neoplsi (CIN) III re expected to receive cncer dignosis if no subsequent dequte tretment is performed, 30 even smll improvements for this group my be importnt. For women with recommendtion for followup in 3 months, 95% nd 99% of results were indequte in the before nd fter study popultions, respectively (further informtion is vilble from the uthors upon request). Women with this type of follow-up recommendtion lso improved follow-up, but do not necessrily hve n incresed risk of cncer. Implictions for prctice Reminders improved the follow-up of women prticipting in cervicl cncer screening, regrdless of sociodemogrphic chrcteristics. The effect ws seen in helthcre system with reltively high follow-up rte, which proves tht the GP reminder intervention delivers strong results. However, chllenges with followup nd socil inequlities persist, nd this finding needs further considertion. Electronic reminders re currently sent to the generl prctice tht performed the cytology nd thus not necessrily to the womn s current GP. In Denmrk, 23% of the popultion ged 18 30 yers chnge GP prctice ech yer, wheres the corresponding figure is only 4% for women ged 50. 31 Thus, reminders my ddress socil inequlity mong the young if sent to the womn s current GP or to the womn herself. The intervention decresed the vrition in follow-up proportions between GPs. This implies tht the GP reminder served s supportive tool for GPs, s follow-up of women now depends to lesser extent on individul GPs. 7 British Journl of Generl Prctice, Online First 2017
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Is chnge of generl prctitioners more frequent mong ptients dignosed with cncer or other serious diseses? [In Dnish]. Ugeskr Leger 2003; 165(27): 2743 2746. British Journl of Generl Prctice, Online First 2017 8