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R983137983152983145983140 983139983151983149983149983157983150983145983139983137983156983145983151983150983155

Recent trends in gonorrhoea and syphilis epidemiologyin Sweden 2007 to 2011

I Velicko (ingavelickosmise)1 M Unemo2

1 Swedish Institute for Communicable Disease Control (Smittskyddsinstitutet) Department of Epidemiology Solna Sweden2 WHO Collaborating Centre for Gonorrhoea and other STIs National Reference Laboratory for Pathogenic NeisseriaDepartment of Laboratory Medicine Clinical Microbiology Oumlrebro University Hospital Oumlrebro Sweden

Citation style for this ar ticleVelicko I Unemo M Recent trends in gonorrhoea and syphilis epidemiology in Sweden 2007 to 2011 Euro Surveill 201217(29)pii=20223 Available online httpwwweurosurveillanceorgViewArticleaspxArticleId=20223

Article submitted on 10 July 2012 published on 19 July 2012

Gonorrhoea incidence in Sweden continued to increaseduring 2007ndash2011 while for syphilis there was a

very minor decrease but no clear trend Gonorrhoeaincidence increased most among heterosexuallyinfected men and women while for syphilis the majorburden was among men who have sex with men

Neisseria gonorrhoeae resistance to first-line antimi-crobials increased annually Surveillance of infectionand antimicrobial resistance along with continuousanalysis are needed to develop prevention activitiesto reduce risk behaviours

Recent reports from several European Union (EU) coun-tries have revealed increases in gonorrhoea incidence

particularly in populations with higher frequency ofspread of sexually transmitted infections (STIs) suchas men who have sex with men (MSM) and young het-erosexual individuals of both sexes (under 25 yearsof age) and stable or increasing syphilis incidence inMSM [1-4]

During the past couple of decades Sweden hasobserved an increased incidence of gonorrhoea (since1996) and syphilis (since 1999) [5-7] MSM have beenshown to be at increased risk of acquiring and spread-ing both gonorrhoea and syphilis [56] Heterosexuallyinfected men especially those aged 25ndash34 yearsalso have a high gonorrhoea incidence comparedwith women [6] During the last 10 years womenhave constituted only approximately 20ndash30 of allgonorrhoea and syphilis cases in the country [56]Disquietingly during the past five years gonorrhoeaand syphilis incidences in heterosexually infected menand women including those in younger age groups(under 25 years of age) have increased Furthermoreas observed worldwide antimicrobial resistance ofNeisseria gonorrhoeae in Sweden has increased annu-ally during this time including to the recommendedfirst-line cefixime and ceftriaxone [689] One instance

of treatment failure of pharyngeal gonorrhoea with cef-triaxone has been verified in Sweden [10]

In this report we describe the trends from 2007 to 2011for gonorrhoea including antimicrobial resistance and

syphilis in Sweden in order to identify recent changesin the epidemiology of the diseases and groups at risk

Surveillance of gonorrhoeaand syphilis in SwedenThe aetiologically based surveillance systems of themandatorily reported gonorrhoea and syphilis inSweden have been described elsewhere [56] The gon-orrhoea and syphilis case definitions used in Swedenare identical to those of the EU [11]

ItemGonorrhoea Syphilis

20 07 20 11 200 7 20 11

Total number of cases 642 951 239 206

Total incidence (number of casesper 100000 population)

71 100 26 22

Percentage of male casesamong all cases 80 69 82 82

Percentage of MSM amongall male cases

38 40 57 66

Percentage of adolescents andyoung adults of both sexes(aged 15ndash24 years) among all cases

34 41 8 11

Male-to-female case ratio 421 221 481 511

Percentage increasedecreaseobserved in heterosexual male casesin 2011 compared with 2007

+35 minus52

Percentage increasedecreaseobserved in MSM cases in 2011compared with 2007

+35 minus1

Percentage increasedecreaseobserved in female cases in 2011compared with 2007

+147 minus15

983156983137983138983148983141

Trends in gonorrhoea and syphilis in Sweden 2007 and2011

MSM men who have sex with men

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For this study all reported cases were extracted

from the national surveillance database SmiNet [12]which is maintained by the Swedish Institute forCommunicable Disease Control (SmittskyddsinstitutetSMI) Surveillance data since 1997 are also presentedas historical background of the gonorrhoea and syphi-lis incidences in Sweden Population data for Swedenfor the respective years were taken from StatisticsSweden [13]

Gonorrhoea in SwedenFrom 2007 to 2011 the number of gonorrhoea casesincreased by 48 (from 642 to 951 cases) reachingan incidence of 100 per 100000 population in 2011(Table) This increase was partly due to an increase (of147) in the number of cases among women (Figure1) We also observed an increase of 35 in the numberof cases among heterosexually infected men (Figure1) The proportion of cases who were heterosexu-ally infected men increased from 52 in 2007 to 57in 2011 while the proportion of MSM among casesremained relatively stable (38ndash40)

The increase among women was mostly observed in theage group 15ndash24 years where the incidence increasedby 154 (from 124 to 315 per 100000 population)

(Figure 2) During 2007 to 2011 a mean of 62 of allfemale cases was reported in this age group

Among male cases the largest increases were reported

in the age groups 15ndash24 and 25ndash34 years (Figure 2)which constituted a mean of 30 and 34 respec-tively of all male cases during 2007 to 2011 Duringthis time the incidence increased by 31 (from 233 to306 per 100000 population) in men in the age group15ndash24 years and by 23 (from 309 to 380 per 100000population) in men aged 25ndash34 years (Figure 2)

During 2007 to 2011 about 70 of all the cases becameinfected in Sweden a mean of 74 of the 15ndash24 year-olds and 70 of the 25ndash34 year-olds In the remainingage groups more than a mean of 50 were infectedabroad Of all cases infected abroad the countrieswhere the infection was most commonly acquired wereThailand Philippines Spain Denmark and GermanyWomen and MSM were more frequently infected inSweden (a mean of 79 and 80 of the respectivecases) than heterosexually infected men (a mean of50 of cases)

Neisseria gonorrhoeae resistanceto antimicrobialsResistance to the previous first-line antimicrobials forgonorrhoea treatment ampicillin (24ndash44 of isolateswere resistant) and ciprofloxacin (55ndash75) remained

high during 2007 to 2011 Azithromycin resistanceranged from 6 to 13 (11 in 2011) Decreasedsusceptibility or resistance to cefixime and ceftri-axone increased from less than 1 to 8 and 0

F983145983143983157983154983141 1

Gonorrhoea cases by route of transmission Sweden 1997ndash2011 (n=8626)a

a Cases with unknown or other transmission route were excluded (a total of 8924 cases were reported during this time)

0

50

100

150

200

250

300

350

400

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Year

Men who have sex with men

Heterosexually infected men

Women

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F983145983143983157983154983141 2

Gonorrhoea incidence by sex and age group (from 15 to 44 years) Sweden 2000ndash2011 (n=6933) a

a Of the 7908 cases reported during this time 6933 were aged 15ndash44 years

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Women

I n c i d e

n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o p u l a t i o n )

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Men

I n c i d e n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o

p u l a t i o n )

15ndash 24 years 25ndash34 years 35ndash44 years

Year

Year

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to 2 respectively All isolates were susceptible tospectinomycin

Syphilis in SwedenFrom 2007 to 2011 the total incidence of syphilisshowed a very minor decrease However due to thelow number of cases and the large fluctuations in the

number of cases annually (Figure 3) no clear trend insyphilis incidence could be observed Thus the syphilisincidence which started to increase in late-1990s maynow be stabilising From 2007 to 2011 172ndash277 caseswere reported annually (incidence 19ndash26 per 100000population) (Figure 3 Table) Most cases (a mean of79) were reported among men A slight decrease (of15) in incidence among women has been observedsince 2007 However for women in age group 25ndash34years incidence increased particularly between 2009and 2011 (by 94) Among all female syphilis casesduring 2007 to 2011 a mean of 41 were reported inthis age group (25ndash34-years) In all other age groups

the incidence in women decreased during 2007ndash2011

Among the male cases the largest increase in incidenceduring the study period occurred between 2009 and2011 and was mostly due to the increased incidencesin the age groups 35ndash44 (45 to 93 per 100000 popu-lation) and 55ndash64 years (25 to 38 per 100000 popula-tion) From 2007 to 2011 of all male cases those aged

25ndash34 years constituted a mean of 27 and those aged35ndash44 years a mean of 31

During 2007 to 2011 between 40 and 52 of allsyphilis cases became infected in Sweden a mean of51 of the 15ndash24 year-olds and a mean of 51 of the45ndash54 year-olds In the remaining age groups a mean

of more than 50 were infected abroad Of all casesinfected abroad the countries where the infection wasmost commonly acquired were Somalia Iraq ThailandGermany and Denmark Women and MSM were morefrequently infected in Sweden (a mean of 45 and 67of the respective cases) than heterosexually infectedmen (a mean of 34 of cases)

DiscussionThe incidences of gonorrhoea and syphilis have beenincreasing since the midlate-1990s in Sweden ashas also been observed in several other EU countrieswith well-functioning testing and surveillance sys-

tems [1-4] However the general trend in the EU whichcontains many diverse countries is a decline for bothinfections since the mid-2000s [1415] In Swedenfrom 2007 to 2011 gonorrhoea incidence substantiallyincreased among men (from both hetero- and homo-sexual transmission) in women the increase was evenmore striking (Table) Observations of increased gon-orrhoea (as well as syphilis) incidence in females and

F983145983143983157983154983141 3

Syphilis cases by route of transmission Sweden 1997ndash2011 (n=1647)a

a Cases with unknown or other transmission route were excluded (a total of 2078 cases were reported during this time)

0

20

40

60

80

100

120

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Men who have sex with men

Heterosexually infected men

Women

Year

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males (heterosexually infected and MSM) have alsobeen recently reported in some EU countries [1-3] InSweden since the late 1990s a general increase insyphilis incidence has been observed among hetero-and homosexual men and women However from 2007to 2011 the total incidence of syphilis showed a veryminor decrease but due to the low number of cases

and the large variation in the number of cases annu-ally no clear trend could be determined Neverthelessthe syphilis incidence in Sweden which started toincrease in late-1990s may now be stabilising

Many different factors might contribute to the diver-gent gonorrhoea and syphilis trends from 2007 to2011 in Sweden Firstly the increase in risky sexualbehaviour in young predominantly heterosexual indi-viduals such as increased number of sexual partnersover time increased number of new casual sexual part-ners and low level of condom use with casual sexualpartners [1617] has presumably contributed to the

increase in gonorrhoea in these highly sexually activeyoung people Gonorrhoea is also frequently importedfrom abroad by heterosexual men which allows furtherspread of the infection domestically

In these younger age groups of predominantly het-erosexual individuals syphilis remains relatively rareand does not have the same speed of spread as it ismostly spreading among MSM in Sweden In generalMSM are a group in which both gonorrhoea and syphi-lis are spread more easily due to more risky sexualbehaviour such as unprotected anal intercourse which

makes them more prone to acquire STIs [518] Somerecent surveys among MSM in Sweden have demon-strated that an increased number of sexual partnersduring last year unprotected anal intercourse duringthe last year last sexual contact with a casual part-ner and sexual contact with an HIV-positive man aresignificantly associated with being diagnosed withchlamydia gonorrhoea or syphilis during the last 12months [1819] However despite the large fluctuationsin the exact number of cases annually among MSMin Sweden the incidence of gonorrhoea and syphiliswhich both started to increase in midlate-1990s maynow be stabilising

Other possible reasons for the observed trends is theincreased awareness of healthcare workers in Swedenwhich has contributed to increased uptake of testingespecially by young individuals being screened both forchlamydial infection and gonorrhoea [7] (an increasingnumber of youth health clinics in Sweden are offeringscreening for chlamydia infection and gonorrhoea fromthe same biological samples using sensitive genetictests for diagnosis) Syphilis testing is routinely onlyoffered to new migrants MSM symptomatic patientspatients with unsafe sexual contacts with a syphilis-

positive patient and HIV-positive patients The epi-demiology of syphilis in Sweden is also substantiallyaffected by importation of the infection as a result ofsyphilis-positive individuals migrating from countries

with a higher syphilis prevalence than in Sweden aswell as importation of infection by Swedish travellersthis accounts for the large variation in reported casesannually [7]

The importation of gonorrhoea by heterosexuallyinfected Swedish men predominantly after travel

in Asia might also introduce multidrug-resistantN gonorrhoeae strains (defined in reference 8) inSweden Treatment failures with cefixime have beenverified in Norway [20] England [21] Austria [22]France [23] and Sweden (unpublished data) It is ofconcern that the first gonococcal strains with high-level resistance to ceftriaxone ndash the last remainingoption for single antimicrobial empirical treatment ofgonorrhoea ndash have been verified in Japan [24] France[23] and Spain [25] In addition ceftriaxone treatmentfailures of pharyngeal gonorrhoea have also been veri-fied in Europe in Sweden [10] and Slovenia [26] In thisemergent situation the World Health Organization

(WHO) has published a lsquoGlobal action plan to controlthe spread and impact of antimicrobial resistancein Neisseria gonorrhoeaersquo [2728] and the EuropeanCentre for Disease Prevention and Control (ECDC) haslaunched a response plan for the European Union [29]

Continuous monitoring and thorough analysis of trendsin sexually transmitted infections in general and insyphilis and gonorrhoea in particular including anti-microbial resistance should be maintained in order toidentify risk groups involved in transmission of theseinfections Ideally this analysis should include denom-

inators such as number of individuals tested (includ-ing also negative individuals) and diagnostic method(including specific tests) used More knowledge is cru-cial to better understand the changing epidemiologyof sexually transmitted infections and plan preventionactivities to better target particular populations at risk

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References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

17 Swedish Institute for Communicable Disease Control (SMI)Ungdomsbarometern 2011 Ungdomar och sexualitet 2011Specialrapport foumlr Smittskyddsinstitutet [Youth Barometer2011 Young people and sexuality 2011 Special report forthe Swedish Institute for Communicable Disease Control]Solna SMI 2011 Swedish Available from httpwwwsmittskyddsinstitutetseuploadPublikationerhivsexprevUngdomsbarometernUngdomsbarometern2011pdf

18 Tikkanen RH MSM-Enkaumlten Riskhandlingar hivtest ochpreventiva behov bland maumln som har sex med maumln [MSMsurvey Risk actions HIV testing and prevention needs among

men who have sex with men] Malmouml Malmouml houmlgskola 2010Swedish Available from httpdspacemahsebitstreamhandle204310523Fou_2010_4pdfsequence=1

19 Eriksson EL Berglund T Liljeros F Tikkanen RH Risk factorsfor self-reported STI analysed from a Swedish national MSMinternet survey Conference book of the Future of EuropeanPrevention among MSM (FEMP 2011) 10-11 November 2011Stockholm Sweden

20 Unemo M Golparian D Syversen G Vestrheim DF Moi HTwo cases of verified clinical failures using internationallyrecommended first-line cefixime for gonorrhoea treatmentNorway 2010 Euro Surveill 201015(47)pii=19721 Availablefrom httpwwweurosurveillanceorgViewArticleaspxArticleId=19721

21 Ison CA Hussey J Sankar KN Evans J Alexander SGonorrhoea treatment failures to cefixime and azithromycinin England 2010 Euro Surveill 201116(14)pii=19833Available from httpwwweurosurveillanceorgViewArticle

aspxArticleId=1983322 Unemo M Golparian D Stary A Eigentler A First Neisseria

gonorrhoeae strain with resistance to cefixime causinggonorrhoea treatment failure in Austria 2011 Euro Surveill201116(43)pii=19998 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19998

23 Unemo M Golparian D Nicholas R Ohnishi M Gallay ASednaoui P High-level cefixime- and ceftriaxone-resistantN gonorrhoeae in France novel penA mosaic allele in asuccessful international clone causes treatment failureAntimicrob Agents Chemother 201256(3)1273-80

24 Ohnishi M Golparian D Shimuta K Saika T Hoshina SIwasaku K et al Is Neisseria gonorrhoeae initiating a futureera of untreatable gonorrhea detailed characterizationof the first strain with high-level resistance to ceftriaxoneAntimicrob Agents Chemother 201155(7)3538-45

25 Caacutemara J Serra J Ayats J Bastida T Carnicer-Pont D Andreu A

et al Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in CataloniaSpain J Antimicrob Chemother 201267(8)1858-60

26 Unemo M Golparian D Potočnik M Jeverica S Treatmentfailure of pharyngeal gonorrhoea with internationallyrecommended first-line ceftriaxone verified in SloveniaSeptember 2011 Euro Surveill 201217(25)pii=20200Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=20200

27 World Health Organization (WHO) Global action plan to controlthe spread and impact of antimicrobial resistance in Neisseriagonorrhoeae Geneva WHO 2012 Available from httpwwwwhointreproductivehealthpublicationsrtis9789241503501

28 Ndowa F Lusti-Narasimhan M Unemo M The serious threat ofmultidrug-resistant and untreatable gonorrhoea the pressingneed for global action to control the spread of antimicrobialresistance and mitigate the impact on sexual and reproductivehealth Sex Transm Infect 201288(5)317-8

29 European Centre for Disease Prevention and Control (ECDC)Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe Stockholm ECDC 2012Available from httpwwwecdceuropaeuenpublicationsPublications1206-ECDC-MDR-gonorrhoea-response-planpdf

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For this study all reported cases were extracted

from the national surveillance database SmiNet [12]which is maintained by the Swedish Institute forCommunicable Disease Control (SmittskyddsinstitutetSMI) Surveillance data since 1997 are also presentedas historical background of the gonorrhoea and syphi-lis incidences in Sweden Population data for Swedenfor the respective years were taken from StatisticsSweden [13]

Gonorrhoea in SwedenFrom 2007 to 2011 the number of gonorrhoea casesincreased by 48 (from 642 to 951 cases) reachingan incidence of 100 per 100000 population in 2011(Table) This increase was partly due to an increase (of147) in the number of cases among women (Figure1) We also observed an increase of 35 in the numberof cases among heterosexually infected men (Figure1) The proportion of cases who were heterosexu-ally infected men increased from 52 in 2007 to 57in 2011 while the proportion of MSM among casesremained relatively stable (38ndash40)

The increase among women was mostly observed in theage group 15ndash24 years where the incidence increasedby 154 (from 124 to 315 per 100000 population)

(Figure 2) During 2007 to 2011 a mean of 62 of allfemale cases was reported in this age group

Among male cases the largest increases were reported

in the age groups 15ndash24 and 25ndash34 years (Figure 2)which constituted a mean of 30 and 34 respec-tively of all male cases during 2007 to 2011 Duringthis time the incidence increased by 31 (from 233 to306 per 100000 population) in men in the age group15ndash24 years and by 23 (from 309 to 380 per 100000population) in men aged 25ndash34 years (Figure 2)

During 2007 to 2011 about 70 of all the cases becameinfected in Sweden a mean of 74 of the 15ndash24 year-olds and 70 of the 25ndash34 year-olds In the remainingage groups more than a mean of 50 were infectedabroad Of all cases infected abroad the countrieswhere the infection was most commonly acquired wereThailand Philippines Spain Denmark and GermanyWomen and MSM were more frequently infected inSweden (a mean of 79 and 80 of the respectivecases) than heterosexually infected men (a mean of50 of cases)

Neisseria gonorrhoeae resistanceto antimicrobialsResistance to the previous first-line antimicrobials forgonorrhoea treatment ampicillin (24ndash44 of isolateswere resistant) and ciprofloxacin (55ndash75) remained

high during 2007 to 2011 Azithromycin resistanceranged from 6 to 13 (11 in 2011) Decreasedsusceptibility or resistance to cefixime and ceftri-axone increased from less than 1 to 8 and 0

F983145983143983157983154983141 1

Gonorrhoea cases by route of transmission Sweden 1997ndash2011 (n=8626)a

a Cases with unknown or other transmission route were excluded (a total of 8924 cases were reported during this time)

0

50

100

150

200

250

300

350

400

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Year

Men who have sex with men

Heterosexually infected men

Women

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F983145983143983157983154983141 2

Gonorrhoea incidence by sex and age group (from 15 to 44 years) Sweden 2000ndash2011 (n=6933) a

a Of the 7908 cases reported during this time 6933 were aged 15ndash44 years

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Women

I n c i d e

n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o p u l a t i o n )

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Men

I n c i d e n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o

p u l a t i o n )

15ndash 24 years 25ndash34 years 35ndash44 years

Year

Year

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4 wwweurosurveillanceorg

to 2 respectively All isolates were susceptible tospectinomycin

Syphilis in SwedenFrom 2007 to 2011 the total incidence of syphilisshowed a very minor decrease However due to thelow number of cases and the large fluctuations in the

number of cases annually (Figure 3) no clear trend insyphilis incidence could be observed Thus the syphilisincidence which started to increase in late-1990s maynow be stabilising From 2007 to 2011 172ndash277 caseswere reported annually (incidence 19ndash26 per 100000population) (Figure 3 Table) Most cases (a mean of79) were reported among men A slight decrease (of15) in incidence among women has been observedsince 2007 However for women in age group 25ndash34years incidence increased particularly between 2009and 2011 (by 94) Among all female syphilis casesduring 2007 to 2011 a mean of 41 were reported inthis age group (25ndash34-years) In all other age groups

the incidence in women decreased during 2007ndash2011

Among the male cases the largest increase in incidenceduring the study period occurred between 2009 and2011 and was mostly due to the increased incidencesin the age groups 35ndash44 (45 to 93 per 100000 popu-lation) and 55ndash64 years (25 to 38 per 100000 popula-tion) From 2007 to 2011 of all male cases those aged

25ndash34 years constituted a mean of 27 and those aged35ndash44 years a mean of 31

During 2007 to 2011 between 40 and 52 of allsyphilis cases became infected in Sweden a mean of51 of the 15ndash24 year-olds and a mean of 51 of the45ndash54 year-olds In the remaining age groups a mean

of more than 50 were infected abroad Of all casesinfected abroad the countries where the infection wasmost commonly acquired were Somalia Iraq ThailandGermany and Denmark Women and MSM were morefrequently infected in Sweden (a mean of 45 and 67of the respective cases) than heterosexually infectedmen (a mean of 34 of cases)

DiscussionThe incidences of gonorrhoea and syphilis have beenincreasing since the midlate-1990s in Sweden ashas also been observed in several other EU countrieswith well-functioning testing and surveillance sys-

tems [1-4] However the general trend in the EU whichcontains many diverse countries is a decline for bothinfections since the mid-2000s [1415] In Swedenfrom 2007 to 2011 gonorrhoea incidence substantiallyincreased among men (from both hetero- and homo-sexual transmission) in women the increase was evenmore striking (Table) Observations of increased gon-orrhoea (as well as syphilis) incidence in females and

F983145983143983157983154983141 3

Syphilis cases by route of transmission Sweden 1997ndash2011 (n=1647)a

a Cases with unknown or other transmission route were excluded (a total of 2078 cases were reported during this time)

0

20

40

60

80

100

120

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Men who have sex with men

Heterosexually infected men

Women

Year

892019 jurnal mengenai kulit

httpslidepdfcomreaderfulljurnal-mengenai-kulit 56

5wwweurosurveillanceorg

males (heterosexually infected and MSM) have alsobeen recently reported in some EU countries [1-3] InSweden since the late 1990s a general increase insyphilis incidence has been observed among hetero-and homosexual men and women However from 2007to 2011 the total incidence of syphilis showed a veryminor decrease but due to the low number of cases

and the large variation in the number of cases annu-ally no clear trend could be determined Neverthelessthe syphilis incidence in Sweden which started toincrease in late-1990s may now be stabilising

Many different factors might contribute to the diver-gent gonorrhoea and syphilis trends from 2007 to2011 in Sweden Firstly the increase in risky sexualbehaviour in young predominantly heterosexual indi-viduals such as increased number of sexual partnersover time increased number of new casual sexual part-ners and low level of condom use with casual sexualpartners [1617] has presumably contributed to the

increase in gonorrhoea in these highly sexually activeyoung people Gonorrhoea is also frequently importedfrom abroad by heterosexual men which allows furtherspread of the infection domestically

In these younger age groups of predominantly het-erosexual individuals syphilis remains relatively rareand does not have the same speed of spread as it ismostly spreading among MSM in Sweden In generalMSM are a group in which both gonorrhoea and syphi-lis are spread more easily due to more risky sexualbehaviour such as unprotected anal intercourse which

makes them more prone to acquire STIs [518] Somerecent surveys among MSM in Sweden have demon-strated that an increased number of sexual partnersduring last year unprotected anal intercourse duringthe last year last sexual contact with a casual part-ner and sexual contact with an HIV-positive man aresignificantly associated with being diagnosed withchlamydia gonorrhoea or syphilis during the last 12months [1819] However despite the large fluctuationsin the exact number of cases annually among MSMin Sweden the incidence of gonorrhoea and syphiliswhich both started to increase in midlate-1990s maynow be stabilising

Other possible reasons for the observed trends is theincreased awareness of healthcare workers in Swedenwhich has contributed to increased uptake of testingespecially by young individuals being screened both forchlamydial infection and gonorrhoea [7] (an increasingnumber of youth health clinics in Sweden are offeringscreening for chlamydia infection and gonorrhoea fromthe same biological samples using sensitive genetictests for diagnosis) Syphilis testing is routinely onlyoffered to new migrants MSM symptomatic patientspatients with unsafe sexual contacts with a syphilis-

positive patient and HIV-positive patients The epi-demiology of syphilis in Sweden is also substantiallyaffected by importation of the infection as a result ofsyphilis-positive individuals migrating from countries

with a higher syphilis prevalence than in Sweden aswell as importation of infection by Swedish travellersthis accounts for the large variation in reported casesannually [7]

The importation of gonorrhoea by heterosexuallyinfected Swedish men predominantly after travel

in Asia might also introduce multidrug-resistantN gonorrhoeae strains (defined in reference 8) inSweden Treatment failures with cefixime have beenverified in Norway [20] England [21] Austria [22]France [23] and Sweden (unpublished data) It is ofconcern that the first gonococcal strains with high-level resistance to ceftriaxone ndash the last remainingoption for single antimicrobial empirical treatment ofgonorrhoea ndash have been verified in Japan [24] France[23] and Spain [25] In addition ceftriaxone treatmentfailures of pharyngeal gonorrhoea have also been veri-fied in Europe in Sweden [10] and Slovenia [26] In thisemergent situation the World Health Organization

(WHO) has published a lsquoGlobal action plan to controlthe spread and impact of antimicrobial resistancein Neisseria gonorrhoeaersquo [2728] and the EuropeanCentre for Disease Prevention and Control (ECDC) haslaunched a response plan for the European Union [29]

Continuous monitoring and thorough analysis of trendsin sexually transmitted infections in general and insyphilis and gonorrhoea in particular including anti-microbial resistance should be maintained in order toidentify risk groups involved in transmission of theseinfections Ideally this analysis should include denom-

inators such as number of individuals tested (includ-ing also negative individuals) and diagnostic method(including specific tests) used More knowledge is cru-cial to better understand the changing epidemiologyof sexually transmitted infections and plan preventionactivities to better target particular populations at risk

892019 jurnal mengenai kulit

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6 wwweurosurveillanceorg

References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

17 Swedish Institute for Communicable Disease Control (SMI)Ungdomsbarometern 2011 Ungdomar och sexualitet 2011Specialrapport foumlr Smittskyddsinstitutet [Youth Barometer2011 Young people and sexuality 2011 Special report forthe Swedish Institute for Communicable Disease Control]Solna SMI 2011 Swedish Available from httpwwwsmittskyddsinstitutetseuploadPublikationerhivsexprevUngdomsbarometernUngdomsbarometern2011pdf

18 Tikkanen RH MSM-Enkaumlten Riskhandlingar hivtest ochpreventiva behov bland maumln som har sex med maumln [MSMsurvey Risk actions HIV testing and prevention needs among

men who have sex with men] Malmouml Malmouml houmlgskola 2010Swedish Available from httpdspacemahsebitstreamhandle204310523Fou_2010_4pdfsequence=1

19 Eriksson EL Berglund T Liljeros F Tikkanen RH Risk factorsfor self-reported STI analysed from a Swedish national MSMinternet survey Conference book of the Future of EuropeanPrevention among MSM (FEMP 2011) 10-11 November 2011Stockholm Sweden

20 Unemo M Golparian D Syversen G Vestrheim DF Moi HTwo cases of verified clinical failures using internationallyrecommended first-line cefixime for gonorrhoea treatmentNorway 2010 Euro Surveill 201015(47)pii=19721 Availablefrom httpwwweurosurveillanceorgViewArticleaspxArticleId=19721

21 Ison CA Hussey J Sankar KN Evans J Alexander SGonorrhoea treatment failures to cefixime and azithromycinin England 2010 Euro Surveill 201116(14)pii=19833Available from httpwwweurosurveillanceorgViewArticle

aspxArticleId=1983322 Unemo M Golparian D Stary A Eigentler A First Neisseria

gonorrhoeae strain with resistance to cefixime causinggonorrhoea treatment failure in Austria 2011 Euro Surveill201116(43)pii=19998 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19998

23 Unemo M Golparian D Nicholas R Ohnishi M Gallay ASednaoui P High-level cefixime- and ceftriaxone-resistantN gonorrhoeae in France novel penA mosaic allele in asuccessful international clone causes treatment failureAntimicrob Agents Chemother 201256(3)1273-80

24 Ohnishi M Golparian D Shimuta K Saika T Hoshina SIwasaku K et al Is Neisseria gonorrhoeae initiating a futureera of untreatable gonorrhea detailed characterizationof the first strain with high-level resistance to ceftriaxoneAntimicrob Agents Chemother 201155(7)3538-45

25 Caacutemara J Serra J Ayats J Bastida T Carnicer-Pont D Andreu A

et al Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in CataloniaSpain J Antimicrob Chemother 201267(8)1858-60

26 Unemo M Golparian D Potočnik M Jeverica S Treatmentfailure of pharyngeal gonorrhoea with internationallyrecommended first-line ceftriaxone verified in SloveniaSeptember 2011 Euro Surveill 201217(25)pii=20200Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=20200

27 World Health Organization (WHO) Global action plan to controlthe spread and impact of antimicrobial resistance in Neisseriagonorrhoeae Geneva WHO 2012 Available from httpwwwwhointreproductivehealthpublicationsrtis9789241503501

28 Ndowa F Lusti-Narasimhan M Unemo M The serious threat ofmultidrug-resistant and untreatable gonorrhoea the pressingneed for global action to control the spread of antimicrobialresistance and mitigate the impact on sexual and reproductivehealth Sex Transm Infect 201288(5)317-8

29 European Centre for Disease Prevention and Control (ECDC)Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe Stockholm ECDC 2012Available from httpwwwecdceuropaeuenpublicationsPublications1206-ECDC-MDR-gonorrhoea-response-planpdf

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892019 jurnal mengenai kulit

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3wwweurosurveillanceorg

F983145983143983157983154983141 2

Gonorrhoea incidence by sex and age group (from 15 to 44 years) Sweden 2000ndash2011 (n=6933) a

a Of the 7908 cases reported during this time 6933 were aged 15ndash44 years

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Women

I n c i d e

n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o p u l a t i o n )

0

5

10

15

20

25

30

35

40

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

Men

I n c i d e n c e ( n u m b e r o f c a s e s p e r 1 0 0 0

0 0 p o

p u l a t i o n )

15ndash 24 years 25ndash34 years 35ndash44 years

Year

Year

892019 jurnal mengenai kulit

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4 wwweurosurveillanceorg

to 2 respectively All isolates were susceptible tospectinomycin

Syphilis in SwedenFrom 2007 to 2011 the total incidence of syphilisshowed a very minor decrease However due to thelow number of cases and the large fluctuations in the

number of cases annually (Figure 3) no clear trend insyphilis incidence could be observed Thus the syphilisincidence which started to increase in late-1990s maynow be stabilising From 2007 to 2011 172ndash277 caseswere reported annually (incidence 19ndash26 per 100000population) (Figure 3 Table) Most cases (a mean of79) were reported among men A slight decrease (of15) in incidence among women has been observedsince 2007 However for women in age group 25ndash34years incidence increased particularly between 2009and 2011 (by 94) Among all female syphilis casesduring 2007 to 2011 a mean of 41 were reported inthis age group (25ndash34-years) In all other age groups

the incidence in women decreased during 2007ndash2011

Among the male cases the largest increase in incidenceduring the study period occurred between 2009 and2011 and was mostly due to the increased incidencesin the age groups 35ndash44 (45 to 93 per 100000 popu-lation) and 55ndash64 years (25 to 38 per 100000 popula-tion) From 2007 to 2011 of all male cases those aged

25ndash34 years constituted a mean of 27 and those aged35ndash44 years a mean of 31

During 2007 to 2011 between 40 and 52 of allsyphilis cases became infected in Sweden a mean of51 of the 15ndash24 year-olds and a mean of 51 of the45ndash54 year-olds In the remaining age groups a mean

of more than 50 were infected abroad Of all casesinfected abroad the countries where the infection wasmost commonly acquired were Somalia Iraq ThailandGermany and Denmark Women and MSM were morefrequently infected in Sweden (a mean of 45 and 67of the respective cases) than heterosexually infectedmen (a mean of 34 of cases)

DiscussionThe incidences of gonorrhoea and syphilis have beenincreasing since the midlate-1990s in Sweden ashas also been observed in several other EU countrieswith well-functioning testing and surveillance sys-

tems [1-4] However the general trend in the EU whichcontains many diverse countries is a decline for bothinfections since the mid-2000s [1415] In Swedenfrom 2007 to 2011 gonorrhoea incidence substantiallyincreased among men (from both hetero- and homo-sexual transmission) in women the increase was evenmore striking (Table) Observations of increased gon-orrhoea (as well as syphilis) incidence in females and

F983145983143983157983154983141 3

Syphilis cases by route of transmission Sweden 1997ndash2011 (n=1647)a

a Cases with unknown or other transmission route were excluded (a total of 2078 cases were reported during this time)

0

20

40

60

80

100

120

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Men who have sex with men

Heterosexually infected men

Women

Year

892019 jurnal mengenai kulit

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5wwweurosurveillanceorg

males (heterosexually infected and MSM) have alsobeen recently reported in some EU countries [1-3] InSweden since the late 1990s a general increase insyphilis incidence has been observed among hetero-and homosexual men and women However from 2007to 2011 the total incidence of syphilis showed a veryminor decrease but due to the low number of cases

and the large variation in the number of cases annu-ally no clear trend could be determined Neverthelessthe syphilis incidence in Sweden which started toincrease in late-1990s may now be stabilising

Many different factors might contribute to the diver-gent gonorrhoea and syphilis trends from 2007 to2011 in Sweden Firstly the increase in risky sexualbehaviour in young predominantly heterosexual indi-viduals such as increased number of sexual partnersover time increased number of new casual sexual part-ners and low level of condom use with casual sexualpartners [1617] has presumably contributed to the

increase in gonorrhoea in these highly sexually activeyoung people Gonorrhoea is also frequently importedfrom abroad by heterosexual men which allows furtherspread of the infection domestically

In these younger age groups of predominantly het-erosexual individuals syphilis remains relatively rareand does not have the same speed of spread as it ismostly spreading among MSM in Sweden In generalMSM are a group in which both gonorrhoea and syphi-lis are spread more easily due to more risky sexualbehaviour such as unprotected anal intercourse which

makes them more prone to acquire STIs [518] Somerecent surveys among MSM in Sweden have demon-strated that an increased number of sexual partnersduring last year unprotected anal intercourse duringthe last year last sexual contact with a casual part-ner and sexual contact with an HIV-positive man aresignificantly associated with being diagnosed withchlamydia gonorrhoea or syphilis during the last 12months [1819] However despite the large fluctuationsin the exact number of cases annually among MSMin Sweden the incidence of gonorrhoea and syphiliswhich both started to increase in midlate-1990s maynow be stabilising

Other possible reasons for the observed trends is theincreased awareness of healthcare workers in Swedenwhich has contributed to increased uptake of testingespecially by young individuals being screened both forchlamydial infection and gonorrhoea [7] (an increasingnumber of youth health clinics in Sweden are offeringscreening for chlamydia infection and gonorrhoea fromthe same biological samples using sensitive genetictests for diagnosis) Syphilis testing is routinely onlyoffered to new migrants MSM symptomatic patientspatients with unsafe sexual contacts with a syphilis-

positive patient and HIV-positive patients The epi-demiology of syphilis in Sweden is also substantiallyaffected by importation of the infection as a result ofsyphilis-positive individuals migrating from countries

with a higher syphilis prevalence than in Sweden aswell as importation of infection by Swedish travellersthis accounts for the large variation in reported casesannually [7]

The importation of gonorrhoea by heterosexuallyinfected Swedish men predominantly after travel

in Asia might also introduce multidrug-resistantN gonorrhoeae strains (defined in reference 8) inSweden Treatment failures with cefixime have beenverified in Norway [20] England [21] Austria [22]France [23] and Sweden (unpublished data) It is ofconcern that the first gonococcal strains with high-level resistance to ceftriaxone ndash the last remainingoption for single antimicrobial empirical treatment ofgonorrhoea ndash have been verified in Japan [24] France[23] and Spain [25] In addition ceftriaxone treatmentfailures of pharyngeal gonorrhoea have also been veri-fied in Europe in Sweden [10] and Slovenia [26] In thisemergent situation the World Health Organization

(WHO) has published a lsquoGlobal action plan to controlthe spread and impact of antimicrobial resistancein Neisseria gonorrhoeaersquo [2728] and the EuropeanCentre for Disease Prevention and Control (ECDC) haslaunched a response plan for the European Union [29]

Continuous monitoring and thorough analysis of trendsin sexually transmitted infections in general and insyphilis and gonorrhoea in particular including anti-microbial resistance should be maintained in order toidentify risk groups involved in transmission of theseinfections Ideally this analysis should include denom-

inators such as number of individuals tested (includ-ing also negative individuals) and diagnostic method(including specific tests) used More knowledge is cru-cial to better understand the changing epidemiologyof sexually transmitted infections and plan preventionactivities to better target particular populations at risk

892019 jurnal mengenai kulit

httpslidepdfcomreaderfulljurnal-mengenai-kulit 66

6 wwweurosurveillanceorg

References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

17 Swedish Institute for Communicable Disease Control (SMI)Ungdomsbarometern 2011 Ungdomar och sexualitet 2011Specialrapport foumlr Smittskyddsinstitutet [Youth Barometer2011 Young people and sexuality 2011 Special report forthe Swedish Institute for Communicable Disease Control]Solna SMI 2011 Swedish Available from httpwwwsmittskyddsinstitutetseuploadPublikationerhivsexprevUngdomsbarometernUngdomsbarometern2011pdf

18 Tikkanen RH MSM-Enkaumlten Riskhandlingar hivtest ochpreventiva behov bland maumln som har sex med maumln [MSMsurvey Risk actions HIV testing and prevention needs among

men who have sex with men] Malmouml Malmouml houmlgskola 2010Swedish Available from httpdspacemahsebitstreamhandle204310523Fou_2010_4pdfsequence=1

19 Eriksson EL Berglund T Liljeros F Tikkanen RH Risk factorsfor self-reported STI analysed from a Swedish national MSMinternet survey Conference book of the Future of EuropeanPrevention among MSM (FEMP 2011) 10-11 November 2011Stockholm Sweden

20 Unemo M Golparian D Syversen G Vestrheim DF Moi HTwo cases of verified clinical failures using internationallyrecommended first-line cefixime for gonorrhoea treatmentNorway 2010 Euro Surveill 201015(47)pii=19721 Availablefrom httpwwweurosurveillanceorgViewArticleaspxArticleId=19721

21 Ison CA Hussey J Sankar KN Evans J Alexander SGonorrhoea treatment failures to cefixime and azithromycinin England 2010 Euro Surveill 201116(14)pii=19833Available from httpwwweurosurveillanceorgViewArticle

aspxArticleId=1983322 Unemo M Golparian D Stary A Eigentler A First Neisseria

gonorrhoeae strain with resistance to cefixime causinggonorrhoea treatment failure in Austria 2011 Euro Surveill201116(43)pii=19998 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19998

23 Unemo M Golparian D Nicholas R Ohnishi M Gallay ASednaoui P High-level cefixime- and ceftriaxone-resistantN gonorrhoeae in France novel penA mosaic allele in asuccessful international clone causes treatment failureAntimicrob Agents Chemother 201256(3)1273-80

24 Ohnishi M Golparian D Shimuta K Saika T Hoshina SIwasaku K et al Is Neisseria gonorrhoeae initiating a futureera of untreatable gonorrhea detailed characterizationof the first strain with high-level resistance to ceftriaxoneAntimicrob Agents Chemother 201155(7)3538-45

25 Caacutemara J Serra J Ayats J Bastida T Carnicer-Pont D Andreu A

et al Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in CataloniaSpain J Antimicrob Chemother 201267(8)1858-60

26 Unemo M Golparian D Potočnik M Jeverica S Treatmentfailure of pharyngeal gonorrhoea with internationallyrecommended first-line ceftriaxone verified in SloveniaSeptember 2011 Euro Surveill 201217(25)pii=20200Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=20200

27 World Health Organization (WHO) Global action plan to controlthe spread and impact of antimicrobial resistance in Neisseriagonorrhoeae Geneva WHO 2012 Available from httpwwwwhointreproductivehealthpublicationsrtis9789241503501

28 Ndowa F Lusti-Narasimhan M Unemo M The serious threat ofmultidrug-resistant and untreatable gonorrhoea the pressingneed for global action to control the spread of antimicrobialresistance and mitigate the impact on sexual and reproductivehealth Sex Transm Infect 201288(5)317-8

29 European Centre for Disease Prevention and Control (ECDC)Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe Stockholm ECDC 2012Available from httpwwwecdceuropaeuenpublicationsPublications1206-ECDC-MDR-gonorrhoea-response-planpdf

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4 wwweurosurveillanceorg

to 2 respectively All isolates were susceptible tospectinomycin

Syphilis in SwedenFrom 2007 to 2011 the total incidence of syphilisshowed a very minor decrease However due to thelow number of cases and the large fluctuations in the

number of cases annually (Figure 3) no clear trend insyphilis incidence could be observed Thus the syphilisincidence which started to increase in late-1990s maynow be stabilising From 2007 to 2011 172ndash277 caseswere reported annually (incidence 19ndash26 per 100000population) (Figure 3 Table) Most cases (a mean of79) were reported among men A slight decrease (of15) in incidence among women has been observedsince 2007 However for women in age group 25ndash34years incidence increased particularly between 2009and 2011 (by 94) Among all female syphilis casesduring 2007 to 2011 a mean of 41 were reported inthis age group (25ndash34-years) In all other age groups

the incidence in women decreased during 2007ndash2011

Among the male cases the largest increase in incidenceduring the study period occurred between 2009 and2011 and was mostly due to the increased incidencesin the age groups 35ndash44 (45 to 93 per 100000 popu-lation) and 55ndash64 years (25 to 38 per 100000 popula-tion) From 2007 to 2011 of all male cases those aged

25ndash34 years constituted a mean of 27 and those aged35ndash44 years a mean of 31

During 2007 to 2011 between 40 and 52 of allsyphilis cases became infected in Sweden a mean of51 of the 15ndash24 year-olds and a mean of 51 of the45ndash54 year-olds In the remaining age groups a mean

of more than 50 were infected abroad Of all casesinfected abroad the countries where the infection wasmost commonly acquired were Somalia Iraq ThailandGermany and Denmark Women and MSM were morefrequently infected in Sweden (a mean of 45 and 67of the respective cases) than heterosexually infectedmen (a mean of 34 of cases)

DiscussionThe incidences of gonorrhoea and syphilis have beenincreasing since the midlate-1990s in Sweden ashas also been observed in several other EU countrieswith well-functioning testing and surveillance sys-

tems [1-4] However the general trend in the EU whichcontains many diverse countries is a decline for bothinfections since the mid-2000s [1415] In Swedenfrom 2007 to 2011 gonorrhoea incidence substantiallyincreased among men (from both hetero- and homo-sexual transmission) in women the increase was evenmore striking (Table) Observations of increased gon-orrhoea (as well as syphilis) incidence in females and

F983145983143983157983154983141 3

Syphilis cases by route of transmission Sweden 1997ndash2011 (n=1647)a

a Cases with unknown or other transmission route were excluded (a total of 2078 cases were reported during this time)

0

20

40

60

80

100

120

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

N u m b e r o f c a s e s

Men who have sex with men

Heterosexually infected men

Women

Year

892019 jurnal mengenai kulit

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5wwweurosurveillanceorg

males (heterosexually infected and MSM) have alsobeen recently reported in some EU countries [1-3] InSweden since the late 1990s a general increase insyphilis incidence has been observed among hetero-and homosexual men and women However from 2007to 2011 the total incidence of syphilis showed a veryminor decrease but due to the low number of cases

and the large variation in the number of cases annu-ally no clear trend could be determined Neverthelessthe syphilis incidence in Sweden which started toincrease in late-1990s may now be stabilising

Many different factors might contribute to the diver-gent gonorrhoea and syphilis trends from 2007 to2011 in Sweden Firstly the increase in risky sexualbehaviour in young predominantly heterosexual indi-viduals such as increased number of sexual partnersover time increased number of new casual sexual part-ners and low level of condom use with casual sexualpartners [1617] has presumably contributed to the

increase in gonorrhoea in these highly sexually activeyoung people Gonorrhoea is also frequently importedfrom abroad by heterosexual men which allows furtherspread of the infection domestically

In these younger age groups of predominantly het-erosexual individuals syphilis remains relatively rareand does not have the same speed of spread as it ismostly spreading among MSM in Sweden In generalMSM are a group in which both gonorrhoea and syphi-lis are spread more easily due to more risky sexualbehaviour such as unprotected anal intercourse which

makes them more prone to acquire STIs [518] Somerecent surveys among MSM in Sweden have demon-strated that an increased number of sexual partnersduring last year unprotected anal intercourse duringthe last year last sexual contact with a casual part-ner and sexual contact with an HIV-positive man aresignificantly associated with being diagnosed withchlamydia gonorrhoea or syphilis during the last 12months [1819] However despite the large fluctuationsin the exact number of cases annually among MSMin Sweden the incidence of gonorrhoea and syphiliswhich both started to increase in midlate-1990s maynow be stabilising

Other possible reasons for the observed trends is theincreased awareness of healthcare workers in Swedenwhich has contributed to increased uptake of testingespecially by young individuals being screened both forchlamydial infection and gonorrhoea [7] (an increasingnumber of youth health clinics in Sweden are offeringscreening for chlamydia infection and gonorrhoea fromthe same biological samples using sensitive genetictests for diagnosis) Syphilis testing is routinely onlyoffered to new migrants MSM symptomatic patientspatients with unsafe sexual contacts with a syphilis-

positive patient and HIV-positive patients The epi-demiology of syphilis in Sweden is also substantiallyaffected by importation of the infection as a result ofsyphilis-positive individuals migrating from countries

with a higher syphilis prevalence than in Sweden aswell as importation of infection by Swedish travellersthis accounts for the large variation in reported casesannually [7]

The importation of gonorrhoea by heterosexuallyinfected Swedish men predominantly after travel

in Asia might also introduce multidrug-resistantN gonorrhoeae strains (defined in reference 8) inSweden Treatment failures with cefixime have beenverified in Norway [20] England [21] Austria [22]France [23] and Sweden (unpublished data) It is ofconcern that the first gonococcal strains with high-level resistance to ceftriaxone ndash the last remainingoption for single antimicrobial empirical treatment ofgonorrhoea ndash have been verified in Japan [24] France[23] and Spain [25] In addition ceftriaxone treatmentfailures of pharyngeal gonorrhoea have also been veri-fied in Europe in Sweden [10] and Slovenia [26] In thisemergent situation the World Health Organization

(WHO) has published a lsquoGlobal action plan to controlthe spread and impact of antimicrobial resistancein Neisseria gonorrhoeaersquo [2728] and the EuropeanCentre for Disease Prevention and Control (ECDC) haslaunched a response plan for the European Union [29]

Continuous monitoring and thorough analysis of trendsin sexually transmitted infections in general and insyphilis and gonorrhoea in particular including anti-microbial resistance should be maintained in order toidentify risk groups involved in transmission of theseinfections Ideally this analysis should include denom-

inators such as number of individuals tested (includ-ing also negative individuals) and diagnostic method(including specific tests) used More knowledge is cru-cial to better understand the changing epidemiologyof sexually transmitted infections and plan preventionactivities to better target particular populations at risk

892019 jurnal mengenai kulit

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6 wwweurosurveillanceorg

References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

17 Swedish Institute for Communicable Disease Control (SMI)Ungdomsbarometern 2011 Ungdomar och sexualitet 2011Specialrapport foumlr Smittskyddsinstitutet [Youth Barometer2011 Young people and sexuality 2011 Special report forthe Swedish Institute for Communicable Disease Control]Solna SMI 2011 Swedish Available from httpwwwsmittskyddsinstitutetseuploadPublikationerhivsexprevUngdomsbarometernUngdomsbarometern2011pdf

18 Tikkanen RH MSM-Enkaumlten Riskhandlingar hivtest ochpreventiva behov bland maumln som har sex med maumln [MSMsurvey Risk actions HIV testing and prevention needs among

men who have sex with men] Malmouml Malmouml houmlgskola 2010Swedish Available from httpdspacemahsebitstreamhandle204310523Fou_2010_4pdfsequence=1

19 Eriksson EL Berglund T Liljeros F Tikkanen RH Risk factorsfor self-reported STI analysed from a Swedish national MSMinternet survey Conference book of the Future of EuropeanPrevention among MSM (FEMP 2011) 10-11 November 2011Stockholm Sweden

20 Unemo M Golparian D Syversen G Vestrheim DF Moi HTwo cases of verified clinical failures using internationallyrecommended first-line cefixime for gonorrhoea treatmentNorway 2010 Euro Surveill 201015(47)pii=19721 Availablefrom httpwwweurosurveillanceorgViewArticleaspxArticleId=19721

21 Ison CA Hussey J Sankar KN Evans J Alexander SGonorrhoea treatment failures to cefixime and azithromycinin England 2010 Euro Surveill 201116(14)pii=19833Available from httpwwweurosurveillanceorgViewArticle

aspxArticleId=1983322 Unemo M Golparian D Stary A Eigentler A First Neisseria

gonorrhoeae strain with resistance to cefixime causinggonorrhoea treatment failure in Austria 2011 Euro Surveill201116(43)pii=19998 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19998

23 Unemo M Golparian D Nicholas R Ohnishi M Gallay ASednaoui P High-level cefixime- and ceftriaxone-resistantN gonorrhoeae in France novel penA mosaic allele in asuccessful international clone causes treatment failureAntimicrob Agents Chemother 201256(3)1273-80

24 Ohnishi M Golparian D Shimuta K Saika T Hoshina SIwasaku K et al Is Neisseria gonorrhoeae initiating a futureera of untreatable gonorrhea detailed characterizationof the first strain with high-level resistance to ceftriaxoneAntimicrob Agents Chemother 201155(7)3538-45

25 Caacutemara J Serra J Ayats J Bastida T Carnicer-Pont D Andreu A

et al Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in CataloniaSpain J Antimicrob Chemother 201267(8)1858-60

26 Unemo M Golparian D Potočnik M Jeverica S Treatmentfailure of pharyngeal gonorrhoea with internationallyrecommended first-line ceftriaxone verified in SloveniaSeptember 2011 Euro Surveill 201217(25)pii=20200Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=20200

27 World Health Organization (WHO) Global action plan to controlthe spread and impact of antimicrobial resistance in Neisseriagonorrhoeae Geneva WHO 2012 Available from httpwwwwhointreproductivehealthpublicationsrtis9789241503501

28 Ndowa F Lusti-Narasimhan M Unemo M The serious threat ofmultidrug-resistant and untreatable gonorrhoea the pressingneed for global action to control the spread of antimicrobialresistance and mitigate the impact on sexual and reproductivehealth Sex Transm Infect 201288(5)317-8

29 European Centre for Disease Prevention and Control (ECDC)Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe Stockholm ECDC 2012Available from httpwwwecdceuropaeuenpublicationsPublications1206-ECDC-MDR-gonorrhoea-response-planpdf

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5wwweurosurveillanceorg

males (heterosexually infected and MSM) have alsobeen recently reported in some EU countries [1-3] InSweden since the late 1990s a general increase insyphilis incidence has been observed among hetero-and homosexual men and women However from 2007to 2011 the total incidence of syphilis showed a veryminor decrease but due to the low number of cases

and the large variation in the number of cases annu-ally no clear trend could be determined Neverthelessthe syphilis incidence in Sweden which started toincrease in late-1990s may now be stabilising

Many different factors might contribute to the diver-gent gonorrhoea and syphilis trends from 2007 to2011 in Sweden Firstly the increase in risky sexualbehaviour in young predominantly heterosexual indi-viduals such as increased number of sexual partnersover time increased number of new casual sexual part-ners and low level of condom use with casual sexualpartners [1617] has presumably contributed to the

increase in gonorrhoea in these highly sexually activeyoung people Gonorrhoea is also frequently importedfrom abroad by heterosexual men which allows furtherspread of the infection domestically

In these younger age groups of predominantly het-erosexual individuals syphilis remains relatively rareand does not have the same speed of spread as it ismostly spreading among MSM in Sweden In generalMSM are a group in which both gonorrhoea and syphi-lis are spread more easily due to more risky sexualbehaviour such as unprotected anal intercourse which

makes them more prone to acquire STIs [518] Somerecent surveys among MSM in Sweden have demon-strated that an increased number of sexual partnersduring last year unprotected anal intercourse duringthe last year last sexual contact with a casual part-ner and sexual contact with an HIV-positive man aresignificantly associated with being diagnosed withchlamydia gonorrhoea or syphilis during the last 12months [1819] However despite the large fluctuationsin the exact number of cases annually among MSMin Sweden the incidence of gonorrhoea and syphiliswhich both started to increase in midlate-1990s maynow be stabilising

Other possible reasons for the observed trends is theincreased awareness of healthcare workers in Swedenwhich has contributed to increased uptake of testingespecially by young individuals being screened both forchlamydial infection and gonorrhoea [7] (an increasingnumber of youth health clinics in Sweden are offeringscreening for chlamydia infection and gonorrhoea fromthe same biological samples using sensitive genetictests for diagnosis) Syphilis testing is routinely onlyoffered to new migrants MSM symptomatic patientspatients with unsafe sexual contacts with a syphilis-

positive patient and HIV-positive patients The epi-demiology of syphilis in Sweden is also substantiallyaffected by importation of the infection as a result ofsyphilis-positive individuals migrating from countries

with a higher syphilis prevalence than in Sweden aswell as importation of infection by Swedish travellersthis accounts for the large variation in reported casesannually [7]

The importation of gonorrhoea by heterosexuallyinfected Swedish men predominantly after travel

in Asia might also introduce multidrug-resistantN gonorrhoeae strains (defined in reference 8) inSweden Treatment failures with cefixime have beenverified in Norway [20] England [21] Austria [22]France [23] and Sweden (unpublished data) It is ofconcern that the first gonococcal strains with high-level resistance to ceftriaxone ndash the last remainingoption for single antimicrobial empirical treatment ofgonorrhoea ndash have been verified in Japan [24] France[23] and Spain [25] In addition ceftriaxone treatmentfailures of pharyngeal gonorrhoea have also been veri-fied in Europe in Sweden [10] and Slovenia [26] In thisemergent situation the World Health Organization

(WHO) has published a lsquoGlobal action plan to controlthe spread and impact of antimicrobial resistancein Neisseria gonorrhoeaersquo [2728] and the EuropeanCentre for Disease Prevention and Control (ECDC) haslaunched a response plan for the European Union [29]

Continuous monitoring and thorough analysis of trendsin sexually transmitted infections in general and insyphilis and gonorrhoea in particular including anti-microbial resistance should be maintained in order toidentify risk groups involved in transmission of theseinfections Ideally this analysis should include denom-

inators such as number of individuals tested (includ-ing also negative individuals) and diagnostic method(including specific tests) used More knowledge is cru-cial to better understand the changing epidemiologyof sexually transmitted infections and plan preventionactivities to better target particular populations at risk

892019 jurnal mengenai kulit

httpslidepdfcomreaderfulljurnal-mengenai-kulit 66

6 wwweurosurveillanceorg

References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

17 Swedish Institute for Communicable Disease Control (SMI)Ungdomsbarometern 2011 Ungdomar och sexualitet 2011Specialrapport foumlr Smittskyddsinstitutet [Youth Barometer2011 Young people and sexuality 2011 Special report forthe Swedish Institute for Communicable Disease Control]Solna SMI 2011 Swedish Available from httpwwwsmittskyddsinstitutetseuploadPublikationerhivsexprevUngdomsbarometernUngdomsbarometern2011pdf

18 Tikkanen RH MSM-Enkaumlten Riskhandlingar hivtest ochpreventiva behov bland maumln som har sex med maumln [MSMsurvey Risk actions HIV testing and prevention needs among

men who have sex with men] Malmouml Malmouml houmlgskola 2010Swedish Available from httpdspacemahsebitstreamhandle204310523Fou_2010_4pdfsequence=1

19 Eriksson EL Berglund T Liljeros F Tikkanen RH Risk factorsfor self-reported STI analysed from a Swedish national MSMinternet survey Conference book of the Future of EuropeanPrevention among MSM (FEMP 2011) 10-11 November 2011Stockholm Sweden

20 Unemo M Golparian D Syversen G Vestrheim DF Moi HTwo cases of verified clinical failures using internationallyrecommended first-line cefixime for gonorrhoea treatmentNorway 2010 Euro Surveill 201015(47)pii=19721 Availablefrom httpwwweurosurveillanceorgViewArticleaspxArticleId=19721

21 Ison CA Hussey J Sankar KN Evans J Alexander SGonorrhoea treatment failures to cefixime and azithromycinin England 2010 Euro Surveill 201116(14)pii=19833Available from httpwwweurosurveillanceorgViewArticle

aspxArticleId=1983322 Unemo M Golparian D Stary A Eigentler A First Neisseria

gonorrhoeae strain with resistance to cefixime causinggonorrhoea treatment failure in Austria 2011 Euro Surveill201116(43)pii=19998 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19998

23 Unemo M Golparian D Nicholas R Ohnishi M Gallay ASednaoui P High-level cefixime- and ceftriaxone-resistantN gonorrhoeae in France novel penA mosaic allele in asuccessful international clone causes treatment failureAntimicrob Agents Chemother 201256(3)1273-80

24 Ohnishi M Golparian D Shimuta K Saika T Hoshina SIwasaku K et al Is Neisseria gonorrhoeae initiating a futureera of untreatable gonorrhea detailed characterizationof the first strain with high-level resistance to ceftriaxoneAntimicrob Agents Chemother 201155(7)3538-45

25 Caacutemara J Serra J Ayats J Bastida T Carnicer-Pont D Andreu A

et al Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in CataloniaSpain J Antimicrob Chemother 201267(8)1858-60

26 Unemo M Golparian D Potočnik M Jeverica S Treatmentfailure of pharyngeal gonorrhoea with internationallyrecommended first-line ceftriaxone verified in SloveniaSeptember 2011 Euro Surveill 201217(25)pii=20200Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=20200

27 World Health Organization (WHO) Global action plan to controlthe spread and impact of antimicrobial resistance in Neisseriagonorrhoeae Geneva WHO 2012 Available from httpwwwwhointreproductivehealthpublicationsrtis9789241503501

28 Ndowa F Lusti-Narasimhan M Unemo M The serious threat ofmultidrug-resistant and untreatable gonorrhoea the pressingneed for global action to control the spread of antimicrobialresistance and mitigate the impact on sexual and reproductivehealth Sex Transm Infect 201288(5)317-8

29 European Centre for Disease Prevention and Control (ECDC)Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe Stockholm ECDC 2012Available from httpwwwecdceuropaeuenpublicationsPublications1206-ECDC-MDR-gonorrhoea-response-planpdf

Page 6: jurnal mengenai kulit

892019 jurnal mengenai kulit

httpslidepdfcomreaderfulljurnal-mengenai-kulit 66

6 wwweurosurveillanceorg

References

1 Health Protection Agency (HPA) Sexually transmittedinfections in men who have sex with men in the UK 2011report London HPA 2011 Available from httpwwwhpaorgukwebcHPAwebFileHPAweb_C1317131685989

2 Health Protection Agency (HPA) New data show sexuallytransmitted infection diagnoses on the rise in EnglandLondon HPA 31 May 2012 Press release Available fromhttpwwwhpaorgukwebwHPAwebampHPAwebStandardHPAweb_C1317134411572

3 Trienekens SC Koedijk FD van den Broek IV Vriend HJ Op deCoul EL van Veen MG et al Sexually transmitted infectionsincluding HIV in the Netherlands in 2011 Bilthoven NationalInstitute for Public Health and the Environment (RIVM) 2012RIVM report number 2010510012012 Available from httpwwwrivmnldsresourceobjectid=rivmp181418amptype=orgampdisposition=inline

4 Norwegian Institute of Public Health Gonoreacute og syf ilis iNorge 2011 [Gonorrhoea and syphilis in Norway 2011] OsloNorwegian Institute of Public Health Norwegian [Accessed 30June 2012] Available from httpwwwfhinoewaydefaultaspxpid=233amptrg=Area_5774ampMainArea_5661=5588015178710000ampMainLeft_5588=5774015178710000ampArea_5774=55449700015776100

5 Velicko I Arneborn M Blaxhult A Syphilis epidemiologyin Sweden re-emergence since 2000 primarily due tospread among men who have sex with men Euro Surveill200813(50)pii=19063 Available from httpwww

eurosurveillanceorgViewArticleaspxArticleId=190636 Velicko I Unemo M Increase in reported gonorrhoea cases

in Sweden 2001-2008 Euro Surveill 200914(34)pii=19315Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19315

7 Swedish Institute for Communicable Disease Control (SMI)Epidemiologisk aringrsrapport 2011 [Annual epidemiologicalreport 2011] Solna SMI 2012 Swedish Available fromhttpsmiseuploadPublikationerEpidemiologisk-arsrapport-2012-15-6pdf

8 Tapsall JW Ndowa F Lewis DA Unemo M Meeting thepublic health challenge of multidrug- and extensively drugresistant Neisseria gonorrhoeae Expert Rev Anti Infect Ther20097(7)821-34

9 Stoltey JE Barry PM The use of cephalosporins for gonorrheaan update on the rising problem of resistance Expert OpinPharmacother 201213(10)1411-20

10 Unemo M Golparian D Hestner A Ceftriaxone treatmentfailure of pharyngeal gonorrhoea verified by internationalrecommendations Sweden July 2010 Euro Surveill201116(6)pii=19792 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19792

11 European Commission Commission Decision of 28IV2008amending Decision 2002253EC laying down case definitionsfor reporting communicable diseases to the Communitynetwork under Decision No 211998EC of the EuropeanParliament and of the Council Official Journal of the EuropeanUnion Luxembourg Publications Office of the European Union1862008L 159 Available from httpeur-lexeuropaeuLexUriServLexUriServdouri=OJL200815900460090ENPDF

12 Swedish Institute for Communicable Disease Control (SMI)SmiNet ndash elektronisk anmaumllan av smittsamma sjukdomar[SmiNet - electronic system for notification of mandatoryreportable infections in Sweden] Solna SMI Swedish[Accessed 30 Jun 2012] Available from httpwwwsminetse

13 Statistics Sweden (SCB) Finding statisticsStatisticaldatabasePopulation Stockholm SCB [Accessed 30 Jun 2012]Available from httpwwwssdscbsedatabasermakroMainTableaspyp=rqexwrampxu=A4097001ampomradekod=BEampomradetext=Populationamplang=2amplangdb=2

14 Savage EJ Hughes G Ison C Lowndes CM the EuropeanSurveillance of Sexually Transmitted Infections (ESSTI)network Syphilis and gonorrhoea in men who havesex with men a European overview Euro Surveill200914(47)pii=19417 Available from httpwwweurosurveillanceorgViewArticleaspxArticleId=19417

15 European Centre for Disease Prevention and Control (ECDC)Sexually transmitted infections in Europe 1990ndash2010Stockholm ECDC 2012 Available from httpwwwecdceuropaeuenpublicationsPublications201206-Sexually-Transmitted-Infections-Europe-2010pdf

16 Tikkanen RH Abelsson J Forsberg M UngKAB09 -Kunskap attityder och sexuella handlingar bland unga[UngKAB09 - Knowledge attitudes and sexual practicesamong young people] Gothenburg Gothenburg University2011 Swedish Available from httpsgupeaubgusebitstream2077250172gupea_2077_25017_2pdf

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