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Rawre J, Agrawal S, Dhawan B. Sexually transmitted infections: Need for extragenital screening. Indian J Med Microbiol 2018; 36:1-7. [PMID: 29735819 DOI: 10.4103/ijmm.ijmm_18_46] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/30/2022]
Abstract
Extragenital infections can occur concurrently with simultaneous urogenital infections. Extragenital sites are believed to serve as hidden reservoirs and play a critical role in their transmission. The etiological relationship of the most widespread Sexually transmitted diseases (STD) pathogen to reproductive tract has long been established, but the distribution to extragenital sites appears to be infrequent and its correlation with the sexual practice still requires to be investigated. Optimal-screening strategies for extragenital infections are largely unknown. However, there is a lack of data on clinical outcomes and optimal treatment regimens for rectal and pharyngeal extragenital infections. Further studies are needed in settings other than reproductive health and STD clinics, especially in primary care clinics and resource-limited settings.
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Affiliation(s)
- Jyoti Rawre
- Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
| | - Sonu Agrawal
- Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
| | - Benu Dhawan
- Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
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Dukers-Muijrers NHTM, Schachter J, van Liere GAFS, Wolffs PFG, Hoebe CJPA. What is needed to guide testing for anorectal and pharyngeal Chlamydia trachomatis and Neisseria gonorrhoeae in women and men? Evidence and opinion. BMC Infect Dis 2015; 15:533. [PMID: 26576538 PMCID: PMC4650297 DOI: 10.1186/s12879-015-1280-6] [Citation(s) in RCA: 79] [Impact Index Per Article: 7.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2015] [Accepted: 11/12/2015] [Indexed: 11/10/2022] Open
Abstract
Background Anorectal and pharyngeal infections with Chlamydia trachomatis (CT) and Neisseria gonorrheae (NG) are commonly observed in men who have sex with men (MSM). There is increasing evidence that such infections at extra-genital sites are also common in women. In both sexes, these infections are largely overlooked as they are not routinely tested for in regular care. Testing based on sexual behavior or symptoms would only detect half of these extra-genital infections. This paper elucidates the differences and similarities between women and MSM, regarding the epidemiology of extra-genital CT and NG. It discusses the clinical and public health impact of untested extra-genital infections, how this may impact management strategies, and thereby identifies key research areas. Discussion Extra-genital CT is as common in women as it is in MSM; NG in women is as common at their extra-genital sites as it is at their genital sites. The substantial numbers of extra-genital CT and NG being missed in women and MSM indicate a need to test and treat more patients and perhaps different choices in treatment and partner management strategies. Doing so will likely contribute to reduced morbidity and transmission in both sexes. However, in our opinion, it is clear that there are several knowledge gaps in understanding the clinical and public health impact of extra-genital CT and NG. Key research areas that need to be addressed concern associated morbidity (anorectal and reproductive morbidity due to extra-genital infections), ‘the best’ management strategies, including testing and treatment for extra-genital CT, extra-genital treatment resistance, transmission probabilities between partners and between anatomic sites in a woman, and impact on transmission of other infections. Data are also lacking on cost-effectiveness of pharyngeal testing, and of NG testing and anorectal CT testing in women. Gaps in the management of extra-genital CT and NG may also apply for other STIs, such Mycoplasma genitalium. Summary Current management strategies, including testing, to address extra-genital CT and NG in both sexes are suboptimal. Comparative data on several identified key themes in women and MSM are lacking and urgently needed to guide better management of extra-genital infections.
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Affiliation(s)
- Nicole H T M Dukers-Muijrers
- Department of Sexual Health, Infectious Diseases and Environmental Health, South Limburg Public Health Service, Geleenbeeklaan 2, 6166, GR Sittard-Geleen, The Netherlands. .,Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands.
| | - Julius Schachter
- Department of Laboratory Medicine, University of California, San Francisco, CA, USA
| | - Genevieve A F S van Liere
- Department of Sexual Health, Infectious Diseases and Environmental Health, South Limburg Public Health Service, Geleenbeeklaan 2, 6166, GR Sittard-Geleen, The Netherlands.,Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands
| | - Petra F G Wolffs
- Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands
| | - Christian J P A Hoebe
- Department of Sexual Health, Infectious Diseases and Environmental Health, South Limburg Public Health Service, Geleenbeeklaan 2, 6166, GR Sittard-Geleen, The Netherlands.,Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht University Medical Centre (MUMC+), Maastricht, The Netherlands
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Rönn M, Hughes G, Simms I, Ison C, Alexander S, White PJ, Ward H. Challenges Presented by Re-Emerging Sexually Transmitted Infections in HIV Positive Men who have Sex with Men: An Observational Study of Lymphogranuloma Venereum in the UK. JOURNAL OF AIDS & CLINICAL RESEARCH 2014; 5:1000329. [PMID: 26301124 PMCID: PMC4544700 DOI: 10.4172/2155-6113.1000329] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 12/05/2022]
Abstract
BACKGROUND United Kingdom has reported the largest documented outbreak of lymphogranuloma venereum (LGV), a re-emerging sexually transmitted infection (STI) which is primarily seen in HIV-positive men who have sex with men (MSM). A diagnostic service was established in response to the outbreak linked to a voluntary LGV Enhanced Surveillance system. We examined the performance of this novel surveillance system to identify utility in tracking a re-emerging infection. METHODS We described laboratory data on samples and surveillance data from case reports for LGV from 2004-2010. We performed a cross-sectional analysis comparing clinical and behavioural characteristics of HIV-positive and HIV-negative/unknown LGV cases diagnosed in MSM using multivariable logistic regression models with generalised estimating equations to control for repeat infections. RESULTS LGV Surveillance data were available for 87% (1,370/1,581) of LGV cases (after de-duplication). There were 1,342 episodes in 1,281 MSM, most of whom were known to be HIV-positive (1,028/1,281, 80.2%,). HIV-positive men reported a shorter duration of symptoms (aOR 0.5; 95%CI 0.3, 0.8 for reporting more than a week compared to a week or less) in comparison to HIV-negative/unknown MSM, and were more likely to report unprotected receptive anal intercourse (aOR 2.7; 95% CI 1.3, 5.8). CONCLUSION The surveillance identified the population at greater risk of infection based on higher levels of risk behaviour in HIV-positive LGV cases. However, there was diagnostic bias towards HIV-positive LGV cases who presented with a shorter duration of symptoms when compared to HIV-negative/unknown LGV cases.
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Affiliation(s)
- Minttu Rönn
- Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK
| | - Gwenda Hughes
- STI Section at the Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK
| | - Ian Simms
- STI Section at the Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK
| | - Cathy Ison
- Sexually Transmitted Bacteria Reference Unit, Public Health England, London, UK
| | - Sarah Alexander
- Sexually Transmitted Bacteria Reference Unit, Public Health England, London, UK
| | - Peter J White
- MRC Centre for Outbreak Analysis and Modelling and NIHR Health Protection Research Unit in Modelling Methodology, Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK
- Modelling and Economics Unit, Centre for Infectious Disease Surveillance and Control, Public Health England, London, UK
| | - Helen Ward
- Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK
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Macdonald N, Sullivan AK, French P, White JA, Dean G, Smith A, Winter AJ, Alexander S, Ison C, Ward H. Risk factors for rectal lymphogranuloma venereum in gay men: results of a multicentre case-control study in the U.K. Sex Transm Infect 2014; 90:262-8. [PMID: 24493859 PMCID: PMC4033107 DOI: 10.1136/sextrans-2013-051404] [Citation(s) in RCA: 33] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022] Open
Abstract
Objective To identify risk factors for rectal lymphogranuloma venereum (rLGV) in men who have sex with men (MSM). Design A case-control study at 6 UK hospitals compared MSM with rLGV (cases) with rLGV-negative controls: MSM without potential rLGV symptoms (CGa) and separately, MSM with such symptoms (CGs). Methods Between 2008 and 2010, there were 90 rLGV cases, 74 CGa and 69 CGs recruited. Lifestyles and sexual behaviours in the previous 3 months were reported using internet-based computer-assisted self-interviews. Logistic regression was used to investigate factors associated with rLGV. Results Cases were significantly more likely to be HIV-positive (89%) compared with CGa (46%) and CGs (64%). Independent behavioural risks for rLGV were: unprotected receptive anal intercourse (adjusted OR (AOR)10.7, 95% CI 3.5 to 32.8), fisting another (AOR=6.7, CI 1.8 to 25.3), sex under the influence of gamma-hydroxybutyrate (AOR=3.1, CI 1.3 to 7.4) and anonymous sexual contacts (AOR=2.7, CI 1.2 to 6.3), compared with CGa; unprotected insertive anal intercourse (AOR=4.7, CI 2.0 to 10.9) and rectal douching (AOR=2.9 CI 1.3 to 6.6), compared with CGs. An incubation period from exposure to symptoms of 30 days was indicated. Conclusions Unprotected receptive anal intercourse is a key risk factor for rectal LGV with the likelihood that rectal-to-rectal transmission is facilitated where insertive anal sex also occurs. The association between HIV and rLGV appears linked to HIV-positive men seeking unprotected sex with others with the same HIV status, sexual and drug interests. Such men should be targeted for frequent STI screening and interventions to minimise associated risks.
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Affiliation(s)
- N Macdonald
- Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK
| | - A K Sullivan
- Chelsea and Westminster NHS Foundation Trust, London, UK
| | - P French
- Mortimer Market Centre, Central and North West London NHS Foundation Trust, London, UK
| | - J A White
- Guy's and St Thomas' NHS Foundation Trust, London, UK
| | - G Dean
- Brighton & Sussex University Hospitals NHS Trust, Brighton, UK
| | - A Smith
- Jefferiss Wing Centre for Sexual Health, Imperial College Healthcare NHS Trust, London, UK
| | - A J Winter
- Sandyford Sexual Health Services, Glasgow, UK
| | - S Alexander
- Sexually Transmitted Bacterial Reference Unit, Public Health England, London, UK
| | - C Ison
- Sexually Transmitted Bacterial Reference Unit, Public Health England, London, UK
| | - H Ward
- Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK
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The efficacy of clinic-based interventions aimed at increasing screening for bacterial sexually transmitted infections among men who have sex with men: a systematic review. Sex Transm Dis 2012; 39:382-7. [PMID: 22504605 DOI: 10.1097/olq.0b013e318248e3ff] [Citation(s) in RCA: 42] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
Abstract
BACKGROUND In many countries, the prevalence of bacterial sexually transmitted infections (STIs) among men who have sex with men (MSM) is high. We undertook a systematic review to identify clinic-based strategies for increasing screening and detection of bacterial STIs among MSM. METHODS We reviewed studies that compared screening for or detection of gonorrhea, chlamydia, and syphilis in the presence and the absence of an intervention. The primary end points were STI screening, rescreening, or detection rates. RESULTS Of 1809 studies identified, 8 fulfilled the inclusion criteria; of these, 4 studies demonstrated significant increases in screening rates for gonorrhea and chlamydia using different strategies (odds ratio range, 1.4-1.9). These included the following: use of a computer alert on an electronic medical record; the introduction of clinic guidelines on STI screening; and short text messaging reminders for repeat STI screening. A further 4 studies demonstrated increases in syphilis testing (odds ratio range, 2.3-21.4), with increased detection of asymptomatic early syphilis in 2 studies. Strategies used included regular serological screening for syphilis during routine human immunodeficiency virus (HIV) care, syphilis serology included with blood tests performed as part of HIV monitoring, use of a computer alert on an electronic medical record, and an electronic medical record system to enhance syphilis retesting after syphilis treatment. CONCLUSIONS A range of interventions has been used, including the application of newer technologies targeting clinicians and patients that appear to be efficacious at increasing screening of MSM for bacterial STIs. Wider application of such interventions could improve STI screening and control in this high-risk population.
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Gallegos M, Bradly D, Jakate S, Keshavarzian A. Lymphogranuloma venereum proctosigmoiditis is a mimicker of inflammatory bowel disease. World J Gastroenterol 2012; 18:3317-21. [PMID: 22783058 PMCID: PMC3391771 DOI: 10.3748/wjg.v18.i25.3317] [Citation(s) in RCA: 20] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/07/2011] [Revised: 05/17/2011] [Accepted: 05/12/2012] [Indexed: 02/06/2023] Open
Abstract
There has been an increasing prevalence of lymphogranuloma venereum (LGV) or Chlamydia trachomatis (C. trachomatis) cases among the men who have sex with men (MSM) population, particularly in Europe and North America. These cases may present with an incomplete or undisclosed history and proctosigmoiditis without characteristic adenopathy syndrome. During the initial evaluation and colonoscopy, there is a strong clinical and endoscopic suspicion of inflammatory bowel disease (IBD) by virtue of presentation and endoscopic and histological findings. The diagnosis of IBD is subsequently modified to LGV proctosigmoiditis when one or more of the following transpire: (1) there is failure of response to IBD therapy; (2) additional components of history (MSM/travel) may be identified; (3) return of initially performed Chlamydia antibody test is positive; and (4) response to antibiotics effective against Chlamydia. We describe three such cases initially suspected to be an inflammatory bowel disease and subsequently identified as C. trachomatis proctosigmoiditis.
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Elgalib A, Alexander S, Tong CYW, White JA. Seven days of doxycycline is an effective treatment for asymptomatic rectal Chlamydia trachomatis infection. Int J STD AIDS 2011; 22:474-7. [DOI: 10.1258/ijsa.2011.011134] [Citation(s) in RCA: 28] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
There are no evidence-based guidelines for the specific management of rectal Chlamydia trachomatis (CT) infection. All men who have sex with men (MSM) diagnosed with asymptomatic rectal CT by nucleic acid amplification test (NAAT) at a large London genitourinary (GU) medicine clinic between September 2006 and September 2009 were offered oral doxycycline 100 mg twice daily for seven days and invited for a test of cure (TOC) by CT NAAT four weeks after treatment. A total of 487 asymptomatic rectal CT infections were diagnosed and analysis was restricted to 165 TOCs from men whose only treatment had been doxycycline for seven days. The median time post-treatment for TOC was 45 days (interquartile range [IQR], 34–88). Only two patients tested CT-positive at follow-up. One had taken doxycycline only for three days; the other attended for TOC 240 days after the completion of doxycycline treatment and at this time presented with new symptoms in the context of ongoing high sexual risk. Our findings show that doxycycline 100 mg twice daily for seven days is highly effective treatment for asymptomatic rectal CT infection, achieving clearance of CT in 98.8% (163/165; 95% CI 95.4–99.9%) of cases. We advocate doxycycline for seven days as first-line therapy for asymptomatic rectal CT.
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Affiliation(s)
- A Elgalib
- Department of Genitourinary Medicine, Guy's and St Thomas' Hospitals NHS Foundation Trust
| | - S Alexander
- Sexually Transmitted Bacteria Reference Laboratory, Health Protection Agency
| | - C Y W Tong
- Department of Infection, Guy's and St Thomas' Hospitals NHS Foundation Trust, London, UK
| | - J A White
- Department of Genitourinary Medicine, Guy's and St Thomas' Hospitals NHS Foundation Trust
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Lanjouw E, Ossewaarde JM, Stary A, Boag F, van der Meijden WI. 2010 European guideline for the management of Chlamydia trachomatis infections. Int J STD AIDS 2011; 21:729-37. [PMID: 21187352 DOI: 10.1258/ijsa.2010.010302] [Citation(s) in RCA: 62] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
This guideline aims to provide comprehensive information regarding the management of infections caused by Chlamydia trachomatis in European countries. The recommendations contain important information for physicians and laboratory staff working with sexually transmitted infections (STIs) and/or STI-related issues. Individual European countries may be required to make minor national adjustments to this guideline as some of the tests or specific local data may not be accessible, or because of specific laws.
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Affiliation(s)
- E Lanjouw
- Department of Dermatology, Erasmus MC, Rotterdam, Netherlands.
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Tipple C, Hill SC, Smith A. Is screening for pharyngeal Chlamydia trachomatis warranted in high-risk groups? Int J STD AIDS 2011; 21:770-1. [PMID: 21187360 DOI: 10.1258/ijsa.2010.009494] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
Abstract
A recent survey reported that 36% of UK genitourinary medicine clinics offer testing for pharyngeal Chlamydia trachomatis (CT). Screening at this site is targeted at high-risk groups attending our centre, including female sex workers (FSWs) and male sex workers (MSWs). A total of 2406 patients were screened between November 2006 and October 2007. A retrospective case-note review was performed for positive cases. The prevalence of pharyngeal CT was 1.9% in both men and women. The mean number of sexual partners reported in the preceding three months was 168 and 56 for FSWs and MSWs, respectively. Lack of consistent condom use and high numbers of sexual partners identify this population as potential core transmitters of infection. While the British Association of Sexual Health and HIV (BASHH) guidelines do not recommend routine screening for pharyngeal CT, there may be a role in selected high-risk populations.
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Affiliation(s)
- C Tipple
- The Jefferiss Wing Centre for Sexual Health, St Mary's Hospital, Imperial College Healthcare NHS Trust, London, UK.
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Sethupathi M, Blackwell A, Davies H. Rectal Chlamydia trachomatis infection in women. Is it overlooked? Int J STD AIDS 2009; 21:93-5. [PMID: 19917639 DOI: 10.1258/ijsa.2008.008406] [Citation(s) in RCA: 27] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022]
Abstract
Screening for rectal chlamydia was not routinely offered in our department until we had a local outbreak of lymphogranuloma venereum (LGV) in men who have sex with men (MSM) in 2004/2005. We later decided to extend the screening to high-risk women (women who had receptive anal sex, contacts of gonorrhoea, women, with anorectal symptoms, women who had been sexually assaulted). A retrospective study of 152 women from whom 160 rectal chlamydia swabs were taken was carried out. Twenty (12.5%) swabs were positive, 19 of which were also positive at the cervix. All were non-LGV serovars. The groups at greatest risk were high-risk women aged less than 20 years and women with proven gonococcal infection where the prevalence was 22.6% and 30%, respectively. We conclude that rectal chlamydial infection in women may be common and further studies are needed to elucidate its importance.
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Affiliation(s)
- M Sethupathi
- Department of Genitourinary Medicine, Singleton Hospital, Sketty Lane, Swansea SA28QA, UK.
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Abstract
PURPOSE OF REVIEW This review was prompted by a sustained outbreak of lymphogranuloma venereum that has been observed among men who have sex with men (MSM) worldwide since 2004. Recent developments in the epidemiology, diagnosis and management of the infection are summarized. RECENT FINDINGS Between the early 1980s and 2003, lymphogranuloma venereum was rarely seen in the developed world. In 2003, a cluster of cases was seen in the Netherlands occurring mostly in HIV-positive MSM with high levels of sexual risk. With the assistance of novel molecular diagnostic techniques, more than a thousand cases of Chlamydia trachomatis L2 serovar disease have now been reported in MSM worldwide. Almost all have presented with rectal infection, usually manifesting as severe proctitis, with ulcer adenopathy syndrome seldom seen. Oral doxycycline remains the recommended treatment and has proven effective in the recent outbreak. Conflicting data exist regarding the prevalence of asymptomatic infection, and our understanding of the exact modes of transmission remains incomplete. SUMMARY Lymphogranuloma venereum appears to have reestablished endemicity among MSM populations in many industrialized nations. In the relative absence of recent publications from its traditional endemic regions it can be assumed that these populations remain afflicted by the infection as well.
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Ward H, Alexander S, Carder C, Dean G, French P, Ivens D, Ling C, Paul J, Tong W, White J, Ison CA. The prevalence of lymphogranuloma venereum infection in men who have sex with men: results of a multicentre case finding study. Sex Transm Infect 2009; 85:173-5. [PMID: 19221105 PMCID: PMC2683989 DOI: 10.1136/sti.2008.035311] [Citation(s) in RCA: 68] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 01/23/2009] [Indexed: 11/26/2022] Open
Abstract
OBJECTIVE To determine the prevalence of lymphogranuloma venereum (LGV) and non-LGV associated serovars of urethral and rectal Chlamydia trachomatis (CT) infection in men who have sex with men (MSM). DESIGN Multicentre cross-sectional survey. SETTING Four genitourinary medicine clinics in the United Kingdom from 2006-7. SUBJECTS 4825 urethral and 6778 rectal samples from consecutive MSM attending for sexual health screening. METHODS Urethral swabs or urine and rectal swabs were tested for CT using standard nucleic acid amplification tests. Chlamydia-positive specimens were sent to the reference laboratory for serovar determination. MAIN OUTCOME Positivity for both LGV and non-LGV associated CT serovars; proportion of cases that were symptomatic. RESULTS The positivity (with 95% confidence intervals) in rectal samples was 6.06% (5.51% to 6.66%) for non-LGV CT and 0.90% (0.69% to 1.16%) for LGV; for urethral samples 3.21% (2.74% to 3.76%) for non-LGV CT and 0.04% (0.01% to 0.16%) for LGV. The majority of LGV was symptomatic (95% of rectal, one of two urethral cases); non-LGV chlamydia was mostly symptomatic in the urethra (68%) but not in the rectum (16%). CONCLUSIONS Chlamydial infections are common in MSM attending for sexual health screening, and the majority are non-LGV associated serovars. We did not identify a large reservoir of asymptomatic LGV in the rectum or urethra. Testing for chlamydia from the rectum and urethra should be included for MSM requesting a sexual health screen, but serovar-typing is not indicated in the absence of symptoms. We have yet to identify the source of most cases of LGV in the UK.
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Affiliation(s)
- H Ward
- Imperial College London, London, UK.
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