Annotated Bibliography
RESEARCH ARTICLE
Long term effect of primary health care
training on HIV testing: A quasi-experimental
evaluation of the Sexual Health in Practice
(SHIP) intervention
Kamla Pillay 1 , Melissa Gardner
2,3 , Allon Gould
4 , Susan Otiti
5 , Judith Mullineux
6 ,
Till Bärnighausen 7,8,9,10
, Philippa Margaret Matthews 11,12*
1 Homerton Hospital, London, United Kingdom, 2 Sexual Health in Practice Community Interest Company,
London, United Kingdom, 3 Killick Street Health Centre, London, United Kingdom, 4 Whipps Cross Hospital,
London, United Kingdom, 5 Public Health, London Borough of Haringey, London, United Kingdom, 6 Sexual
Health Promotion, Birmingham, United Kingdom, 7 Africa Health Research Institute, Somkhele, South Africa,
8 Institute of Public Health, Heidelberg University, Heidelberg, Germany, 9 Infection and Population Health,
University College London, London, United Kingdom, 10 Department of Global Health and Population,
Harvard T.H. Chan School of Public Health, Boston, United States of America, 11 Division of Infection and
Immunity, University College London, London, United Kingdom, 12 Africa Health Research Institute,
Somkhele, South Africa
Abstract
Background
To examine the effect of Sexual Health in Practice (SHIP) training for general practitioners
(GPs) on HIV testing rates in Haringey, a deprived area of London, UK, with a population of
over 250,000 and HIV prevalence of 0.7% (in 2014). SHIP is an educational intervention
delivering peer-developed and peer-led face-to-face training to improve quality of sexual
and reproductive health (SRH) care.
Methods
We carried out a quasi-experimental study of intervention effects across 52 GP practices
(2008–2016). We used time variation in SHIP intervention exposure for effect estimation,
controlling for practice and calendar month fixed effects in panel analysis. From 2008–2010,
baseline data were collected, and in the subsequent six-year period, 78 GPs in Haringey
(approximately 40% of all GPs) were SHIP trained. 46 Haringey practices (of 52) had at
least one trained doctor. Outcome measures were monthly HIV tests and results by practice
(obtained from the hospital laboratories).
Results
SHIP significantly increased HIV testing; for every GP trained, practice HIV testing rates
increased by 16% (testing rate ratio (TRR) 1.16, 95% confidence interval (CI) 1.05–1.28,
p value 0.004). This significant effect was demonstrated using an 8-year observation period,
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 1 / 13
a1111111111
a1111111111
a1111111111
a1111111111
a1111111111
OPEN ACCESS
Citation: Pillay K, Gardner M, Gould A, Otiti S,
Mullineux J, Bärnighausen T, et al. (2018) Long
term effect of primary health care training on HIV
testing: A quasi-experimental evaluation of the
Sexual Health in Practice (SHIP) intervention. PLoS
ONE 13(8): e0199891. https://doi.org/10.1371/
journal.pone.0199891
Editor: Mary C Smith Fawzi, Harvard Medical
School, UNITED STATES
Received: October 11, 2017
Accepted: June 15, 2018
Published: August 1, 2018
Copyright: © 2018 Pillay et al. This is an open access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript and Supporting Information
files.
Funding: The authors received no specific funding
for this work.
Competing interests: Dr Gardner is a GP and also
clinical lead of SHIP Community Interest (not for
profit) Company (formed in 2017). No other
authors have competing interests. This does not
and was sustained over the post-intervention period. An average of 1.42% of HIV tests were
positive.
Conclusion
SHIP training produces a significant and sustained increase in HIV testing for each GP
trained. Compared with general population screening, HIV tests used in routine clinical care
have a high probability of detecting a positive person. Unlike an RCT, this evaluation is a
‘real life’ measure of the effect that commissioners of SHIP could expect in comparable
areas of the UK. The effectiveness of the SHIP training may be related to the programme
components not included in interventions that did not demonstrate an effect, such as peer-
led teaching, and use of approaches to communication and rapid risk assessment tailored
to the setting.
Introduction
Despite highly effective treatment, HIV remains a major public health issue. Of the estimated
101,200 people infected in the UK, 13% are thought to remain undiagnosed.[1] Late HIV diag-
nosis is associated with significant mortality and increased risk of transmission.[2–4] ‘Treat-
ment as prevention’ guidelines are considered unlikely to decrease HIV transmission in the
UK unless individuals living with HIV are aware of their serostatus.[5] There is evidence to
suggest that people with undiagnosed HIV visit their GPs, but that this opportunity for diagno-
sis may be missed.[6, 7] Primary health care therefore presents opportunities to increase
diagnosis.
Current clinical guidance in the UK [8–10] gives numerous strategies to increase HIV test-
ing in primary health care (S1 File). However the ‘implementation gap’, is well recognised and
guidelines alone will not bring changes to clinical practice[11], including in general practice.
[12] With respect to sexual health, the gap is harder to bridge[13–15] because of stigma.[16–
19] Clinician, patient and system factors have each been found to impede STI and HIV testing.
[16–19] However, educational interventions to increase GP chlamydia and HIV testing tend
to be ineffective.[20–22] An ongoing theme is that interventions fail to overcome barriers to
testing specific to this setting.[20]
Sexual Health in Practice (SHIP) is a peer-developed and -led educational intervention
closely tailored to general practice that aims for broad improvement in sexual health care. In
previous mixed methods evaluation of SHIP[23, 24] a range of effects were found. SHIP
appears to differ from other interventions by tackling the barriers unique to the setting (Fig 1)
by teaching specific verbal strategies and an approach to rapid risk assessment developed for
general practice.
This quasi-experimental observational study measures the effectiveness of SHIP training of
GPs in increasing HIV testing rates. We use practice fixed effects to control for both observed
and unobserved time-invariant confounders of the relationship between the number of SHIP
trained GPs and HIV testing. The effect of training differentiated by local HIV prevalence
within Haringey and response to training beyond 6 months can both be evaluated. The effect
of SHIP training of GPs and practice nurses is compared. We report positivity rates of HIV
tests in routine clinical use in general practice. Lastly, we identify components of SHIP that dif-
fer from other interventions that may possibly explain the mechanisms of effect.
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 2 / 13
alter our adherence to PLOS ONE policies on
sharing data and materials.
Methods
Study design and data collection
We used de-identified data on i) monthly practice-level exposure (SHIP trained GPs and
nurses) and ii) the outcome (the numbers of HIV tests carried out by each practice each
month). The dataset spans eight years (March 2008 to February 2016), meaning that two years
of baseline data were collected prior to the first SHIP training in March 2010. In total, we
observed 4374 practice-months of data across 46 practices and 96 months. Less than 1% of the
data (42 practice-months) were missing.
Intervention
The SHIP programme offers interactive training for general practice designed and led by GPs
and practice nurses. During two afternoons of training for GPs (and three for nurses) SHIP
focuses on providing essential knowledge and skills for HIV and sexual health care. The train-
ing updates factual knowledge of sexually transmitted infections and HIV.
SHIP is also designed to help attendees develop and apply relevant communication strate-
gies and rapid sexual health risk assessment skills appropriate to different primary care clinical
roles. Additional SHIP training in contraception for nurses is not reported on here.
SHIP had been conceived and initially developed in Birmingham, England, and was origi-
nally commissioned from the Heart of Birmingham National Health Service (NHS) Trust;
SHIP had not been implemented in London before. SHIP sessions are taught by GP and prac-
tice nurse peer-educators, using a variety of methods. SHIP training in Haringey was commis-
sioned intermittently during the 8 year observation period with two "fallow" periods, without
training, of 12 and 23 months (Table 1).
Fig 1. Barriers to HIV testing in primary health care.
https://doi.org/10.1371/journal.pone.0199891.g001
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 3 / 13
SHIP content outline is given in more detail in the S2 File. SHIP training centres on skills,
notably, communication skills, needed to overcome the barriers to care, including those to
HIV testing (Fig 1). These barriers have been elicited, collated and updated over more than a
decade of training with contributions from GPs, practice nurses and SHIP peer educators.
Measures
Our exposure was attendance at SHIP training. This was recorded on compulsory sign-in
sheets at each training event and collected the participant’s name, role (GP or nurse) and the
name of their practice. Our outcome measure was numbers of HIV tests by practice (number
of tests from local laboratories is not available by individual doctor or nurse). HIV testing was
chosen because it reflects a complex clinical behaviour, and is simple to measure, clinically
meaningful, and subject to significant barriers to change. Laboratory HIV test numbers are an
accurate measure of testing as rapid tests are not used by Haringey practices. It is near-impos-
sible to artificially inflate practice HIV testing rates. HIV testing data were obtained directly
from three laboratories responsible for processing all GP HIV test requests in Haringey (Whit-
tington, North Middlesex and Homerton Hospitals), via Haringey Public Health. Laboratory
staff removed duplicate positive results (same patient identifiers). We controlled for time and
practice factors such as location and catchment area. The fixed-effect design of our analysis
means that we did not need to collect observational data of our controls. This is further
explained in the statistical analysis section.
Statistical analysis
Our main outcome was the monthly count of HIV tests in each practice. We regressed this
outcome on SHIP training exposure in Poisson regression analyses, controlling for practice
fixed effects. The practice fixed effects controls for all time-invariant confounding factors at
the level of the practice—i.e., factors such as practice location, practice catchment area and
practice specialization.[25, 26] The month fixed effects control for time-varying factors affect-
ing HIV-testing that are shared by all practices—i.e., factors such as HIV testing campaigns or
changes in HIV testing guidelines, such as BHIVA and NICE guidelines in 2008 and 2011
respectively.[8–10] The control of time-invariant practice-level confounding, including those
confounders that have not been observed, is the main reason that fixed-effects analyses are cat-
egorically different from many other observational study designs, which can only control for
confounders that have been observed.[27, 28] The month fixed effects provide additional con-
trol for confounding time-varying factors. SHIP was commissioned in Haringey between
Table 1. GP and practice nurse attendance at SHIP training March 2010 to end 2015.
SHIP
Commissioning
Testing data
collection
Training period 1 FALLOW PERIOD 1
July 2012 to April
2013
Training period 2 FALLOW PERIOD 2
March 2014 to Nov
2015
Training
period 3
2008–2010 2010 2011 2012 2013 2015
Training round No training Mar May-
June
Jan-
Feb
Jun Sept-
Oct
Mar June Sep-
Oct
Oct-
Nov
Nov-Dec
Total attendees N/A 44 42 29 34 19 14 22 18 22 18
Cumulative:
GP completers N/A 11 14 11 8 5 0 6 6 11 88
Cumulative GP
completers
N/A 11 25 36 44 49 49 55 61 72 80
Practice nurse
completers
N/A 6 5 12 4 0 2 3 3 2 5
https://doi.org/10.1371/journal.pone.0199891.t001
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 4 / 13
March 2010 and December 2015, with two ‘fallow’ periods (Table 1). SHIP training is com-
prised of a total of two afternoons for GPs, and three for the nurses. 78 Haringey GPs and 42
practice nurses attended the training (estimated 40% and 30% of the total Haringey number,
respectively).
Results
Attendance at training
Fig 2 shows the average number of SHIP-trained GPs per practice per calendar month over
the 8-year observation period, including two fallow periods. The first two years preceded the
start of the SHIP intervention. By the final year an average of around two GPs per practice
were trained. The average monthly HIV tests per practice increased six-fold, from approxi-
mately one to six over the eight-year observation period.
On average, for each additional GP completing SHIP training monthly practice HIV testing
rates increased by 16% (Table 2). This effect was highly significant (p = 0.004). When we add
the number of nurses who were SHIP trained to the regressions, the GP effect did not change
substantially (testing rate ratio (TTR) 1.17, 95% confidence interval (CI) 1.06–1.29, p value
0.001); the nurse coefficient was not significant. When analysis was stratified by 2011 HIV
prevalence in practice catchment areas, we found the increase in testing was driven by
Fig 2. Average number of HIV tests and GPs trained per practice.
https://doi.org/10.1371/journal.pone.0199891.g002
Table 2. Effect of SHIP training on HIV testing rates. The unit of observation is practice-month. All regressions control for practice and month fixed effects. 95% CIs
are based on robust standard errors, which were adjusted for clustering on practice. IRR = HIV testing incidence rate ratio, CI = confidence interval.
Additional GP trained IRR 95% CI p value N Obser-vations N groups Wald χ2 Prob. χ2
All practices 1.16 1.05–1.28 0.004 4,374 46 44506 <0.001
Practices in catchment areas with HIV prevalence <2/1000 0.96 0.79–1.16 0.658 576 6 1599 <0.001
Practices in catchment areas with HIV prevalence �2/1000 1.16 1.06-1-27 0.002 3,798 40 5546 <0.001
https://doi.org/10.1371/journal.pone.0199891.t002
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 5 / 13
practices located in relatively high HIV prevalence areas ie >2 diagnosed per 1000 population
(TRR 1.16, 95% CI 1.06–1.27, p value 0.002). Practices in low prevalence areas did not contrib-
ute to the effect (TRR 0.96, 95% CI 0.79–1.16, p value 0.658). To test whether the GP (or
nurse) SHIP effects were decreasing or increasing with number of practice clinicians trained,
we added higher-order polynomials of the GP and nurse variables to the regressions. None of
these was significant; the relationship between SHIP-trained GPs and HIV testing rates was
approximately linear: on average, each additional GP trained increases HIV testing rates by
16%.
Testing for short-lived effects
The overall estimation of SHIP effects on HIV testing may be distorted by the greatest
increases being in the earliest period after training. This is plausible, for example if motivation
to adhere to training is highest shortly afterwards and then wanes over time. It is also possible
that effects of training take time to establish—for instance, because training reduces the num-
ber of days spent in the practice and because taught content needs to be translated into practice
processes. To test for such potential short term effects, we added an indicator variable to our
main regression capturing whether a GP in a practice had been trained in the past 3 months
(versus longer than 3 months ago). In a further distinct regression, we added an indicator vari-
able to our main regression capturing whether a GP in a practice had been trained in the past 6
months (versus longer than 6 months ago). Table 3 shows the results of these two analyses. In
both cases, the indicator variable for recent training was not significant and the coefficient size
was close to one. Thus, the main SHIP effect estimate (the effect of an “additional GP trained”),
remains nearly identical in both size and significant to the results without the variable control-
ling for short lived effects. Thus there is no evidence of any short term changes that differ
from, and so distort, the identified long term effect of training.
Detection of HIV-positive cases
Overall an average of 1.42% of HIV tests were positive (95% CI 0.99–1.96%). In sub-analyses,
we explored whether SHIP training increased this probability of diagnosis per test, as well as
the positive detection rate per practice. For this analysis we used a linear probability model.
This proportion did not increase significantly due to SHIP training and the GP SHIP training
effect was nearly zero (0.001, 95% CI -0.003–0.005, p value 0.515). In line with this finding, GP
SHIP training therefore increased the number of positive cases of HIV detected per practice
per month to about the same extent (by 17%) as it increased the number of HIV tests per prac-
tice per month (positive detection rate ratio 1.17, 95% CI 0.93–1.48, p value 0.168). This result
makes sense, because the positive detection rate is the product of the HIV testing rate and the
Table 3. Testing SHIP training for short term effects.
IRR 95% CI p value N Obser-vations N groups Wald χ2 Prob. χ2
Additional GP trained 1.16 1.04–1.28 0.006
GP trained in the last 3 months 0.99 0.76–1.29 0.934 4,374 46 40771 <0.001
Additional GP trained 1.16 1.05–1.29 0.004
GP trained in the last 6 months 0.95 0.75–1.20 0.658 4,374 46 33607 <0.001
The unit of observation is practice-month. All regressions control for practice and month fixed effects. 95% CIs are based on robust standard errors, which were
adjusted for clustering on practice. IRR = HIV testing incidence rate ratio, CI = confidence interval
https://doi.org/10.1371/journal.pone.0199891.t003
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 6 / 13
positive detection ratio. However, the result was not significant, which was most likely due to a
lack of power because positive HIV tests are, overall, rare events.
Discussion
We have demonstrated here that a complex educational intervention, the SHIP training of
GPs and nurses in London, had a highly significant, and sustained effect on practice HIV test-
ing rates. SHIP training of each additional GP increased HIV testing rates by 16%. These
results are plausible because in the SHIP training GPs identify opportunities to increase test-
ing, in particular during individual consultations and in response to both clinical presentations
and risk assessment. Our findings suggest that SHIP training is effective, both in terms of test-
ing and in terms of absolute number of positive individuals identified.
In contrast to the GP effect, SHIP training of nurses did not affect HIV testing rates. Likely
reasons for this finding include that GPs see more patients with symptomatic presentations,
some of which may be HIV-associated. Furthermore, whilst training aims to increase HIV test-
ing for asymptomatic patients found to be at risk, the workload of the nurses over-represents
women. Men, including those who have sex with men (one of the main HIV-affected groups),
are more likely to present to GPs rather than practice nurses. [29] In SHIP training for nurses,
there is a strong focus on chlamydia testing, management of vaginal discharge, sexual health
promotion and contraception. HIV testing rates are therefore unlikely to be the best outcome
measure to assess the effect of SHIP training on practice nurses. In addition, only a compara-
tively small group of nurses were trained which could partially explain this null finding. The
study team is currently collating data on testing and positives for much more common condi-
tions (chlamydia and viral hepatitis) for the same 8 years of study, which will help evaluate
whether nurse practice was affected.
One important finding of our SHIP evaluation is that increases in HIV testing were sus-
tained. We found that the overall long term effect was not due to short lived changes in testing,
such as those often observed in training interventions. [17, 20–22] In many training contexts,
the motivation to adhere to training instructions is highest shortly after training. Over time,
the training effects then wane because the people who were trained lose the motivation to
adhere to new practice and forget the training contained. In contrast, our results indicated that
the effect achieved in the periods (3, and also 6, months after training) are sustained in the
long term. This finding suggests that changed clinical behaviours became normalised. The
opportunity to measure effects over many years is rare for educational interventions, however
even for shorter periods of follow up,[20–22] and broadening beyond sexual health, we were
unable to find good evidence of the effect of educational interventions on clinical practice.
In stratified analysis, we found that the SHIP effects were largely explained by the effects in
high HIV prevalence areas. High prevalence areas were defined as �2 cases /1000 in 15–59
year olds in the UK throughout the study period.[1] That the effect on testing rates was pro-
vided by practices in these areas is plausible because the need to test in high prevalence areas is
emphasised by SHIP. We hypothesise that the range of strategies used by SHIP to help practi-
tioners to identify and respond to relevant symptoms and also identify and respond to individ-
uals at highest risk was of most relevance to practitioners in the high prevalence areas of the
borough. Furthermore, we hypothesise that if a GP made a new HIV diagnosis (more likely in
a high prevalence area), this would reinforce the changed clinical behaviours.
2015 Haringey GP HIV testing rates (by GP-registered population) compare favourably
with those given in a 2016 Public England report.[30] This report, drawing on data from
around half of all English practices in high prevalence areas, gives an average 64.9 tests per
10,000 registered population. In Haringey high prevalence areas this figure, for 2015, is 121.3
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 7 / 13
tests per 10,000 registered population (having increased from 21.5 in the first year of observa-
tion in 2008).
Another important finding of our study is that SHIP increased the positive detection rate to
about the same extent as it increased the HIV testing rate. The positivity rate was high in Har-
ingey, an average of 1.4%. By contrast, Health Protection England’s 2016 report on HIV test-
ing[1] found average positive detection ratios in high prevalence areas to be 0.45% for GP HIV
tests. We had expected that the positive detection ratio would decrease with increasing HIV
testing rates because of a dilution effect: as GPs increased the number of people they test each
month, positivity rates would decline. The sustained high positive detection ratio that is
instead found—ie, the protection of the positive detection ratio despite increased HIV testing
rates—may be due to a number of characteristics of the SHIP training which help GPs identify
both asymptomatic and symptomatic patients with HIV.
While the SHIP effect on the detection of positive cases is important, testing that leads to
the detection of HIV-negative individuals is also beneficial, in particular if it follows the deter-
mination of high HIV risk in a risk assessment (as opposed to population screening). Beyond
reassurance for the patient, it may bring opportunities for patient education, Hepatitis B
immunisation and referral for HIV pre-exposure prophylaxis (where available). In addition,
testing behaviour may become more normalised (for individuals and within social networks).
We hypothesise that the listed features of SHIP that distinguish it from comparable inter-
ventions (Results) are likely to account for the effects. SHIP training is grounded in educa-
tional theory including tailoring to individual role;[31] and addressing barriers to change,[32]
particularly those SHIP has identified that act in the consultation (Fig 1). When possible, per-
formance feedback[33] is given to attendees of their individual practice HIV testing rates.
SHIP has a strong focus on communication skills including verbal strategies to help over-
come the barriers to testing (Fig 1) and the use of rapid risk assessment to identify if testing is
needed and help manage result-giving. These time-efficient communication skills feature posi-
tively in new peer-educator feedback who report adopting them as a change of practice. For
further illustration of these please see the S4 File.
Our study design has a number of important strengths. First, the data we used were high
quality, laboratory data. Second, our data were generated through routine data collection
mechanisms and so the intervention and evaluation were carried out in a real-life setting.
Thus, the artificiality of study context introduced by prospective controlled intervention stud-
ies was avoided. Third, because this was an audit of an educational intervention, the partici-
pants did not know that they were in a study, thus avoiding artificial testing results (although
artificially inflated HIV testing rates are difficult to generate). The external validity of our find-
ings is likely high, and higher than for a randomised controlled trial (RCT).
Fourth, the 8-year observation period allowed us to assess the long-term effectiveness of
SHIP. Overall, the month fixed effects in our analysis control for all of time-varying confound-
ing, i.e., background time trends that are shared by all practices. The study also controlled for
in-practice spillover effect (e.g. if a colleague shared knowledge within their practice, the effect
of this would be captured). The approach is also efficient: the costs of this study are essentially
those of commissioning SHIP—as opposed to the much higher costs of implementing an RCT.
Our study also suffers from some important limitations. Firstly, training was offered on a
‘first-come-first-served’ basis, potentially limiting the generalisability to doctors that have (not
yet) been exposed to SHIP training. However, the vast majority of practices in Haringey partic-
ipated in this study, so that any selection effect threatening generalisability is likely small. Fur-
thermore, only around 30–40% of Haringey GPs took part in the training, though this, if
anything, is likely to result in an underestimation of the effect of the intervention. Secondly,
the data did not account for any HIV tests in patients who were already aware of their HIV
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 8 / 13
positive status, which could pose a threat to generalisability to geographical areas with lower or
higher diagnosed prevalence. A further limitation is the inability to control for the spill-over
effects which are not within the same practice, for example a trained doctor changing practice
in the area. Any effect this had, however, would lead to an underestimate of the effect of SHIP.
HIV testing rates are a narrow measure of the effect of SHIP training. A more thorough
evaluation would look for effect on testing for other STIs, including viral hepatitis and
chlamydia.
Comparison with equivalent interventions
We identified two educational interventions in sexual health in primary health care in the UK,
the ‘Sexually Transmitted Infection Foundation’ (STIF) course and ‘3Cs and HIV’ both aiming
to increase STI testing in the primary health care context. [21, 22] Similarly Joore describes a
(substantially longer) educational intervention aiming to increase GP HIV testing rates in the
Netherlands.[34] All of these interventions have published results showing they were relatively
ineffective.[20–22, 34] We reviewed this published evidence, including process evaluation with
hypotheses as to the lack of effect, where available. We also reviewed publicly available course
materials and descriptions. Through this comparison we aimed to identify the features of
SHIP that differ from the other interventions.
Features of SHIP that differ from comparable interventions
Based on both published [20–22, 34] and publicly available course information and materials,
we compared content of the SHIP intervention with others to identify differences that might
explain the varying levels of effectiveness. Other interventions with similar objectives to the
SHIP intervention and implemented in the UK also focused on relevant clinical content for
education interventions and included participatory methods. Financial incentives to test, used
in the ‘3Cs and HIV’ intervention (but not by SHIP), did not deliver change of practice.
Exploring the lack of effect of ‘3Cs and HIV’ on chlamydia testing (data on HIV testing have
not been published), several factors were identified.[20] These included poor adherence to
intervention content; trainer support remaining unused; and computer prompts either not
being applied or not appearing to have an effect. Finally, in 3Cs practices, chlamydia testing
kits intended for use were in fact not readily available and the intervention videos and posters
were not used. By comparison SHIP does not include many of these features including on-
going trainer support, although it may create local champions through development of peer-
educators; testing kits are not relevant to HIV testing based on venous sampling; and videos
and posters are not offered either (although some patient resources are). The set up and use of
computer prompts (promoted by ‘3Cs and HIV’) is mentioned only briefly in one nurse, but
not GP, SHIP session: computer prompts would not be expected to overcome many of the bar-
riers in Fig 1.
With respect to communication and verbal strategies the 3Cs intervention offered ‘model’
approaches to offer of a chlamydia test illustrated by video and recommended scripts (rather
than experiential approaches to communication skill development and practice). [20, 21] Pub-
lished information on 3Cs does not indicate it supports the use of routine brief sexual history
taking and rapid assessment of risk. Joore explicitly considers the GPs expressed desire to use
risk assessment to be a barrier, and to be discouraged. [17] This likely reflects Joore’s aim to
increase HIV population screening (as opposed to increasing testing within individual consul-
tations). By contrast the SHIP approach assumes that these skills are essential to help overcome
barriers to HIV testing in individual consultations and to deliver higher quality care. This is
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 9 / 13
illustrated in two brief clinical outlines the S4 File to illustrate how training may overcome
some barriers, and see also Fig 1.
Through this comparison of content we identified distinguishing features, included in and
central to SHIP training, that we hypothesise are important to change:
1. Taught, adaptable, communication skills for clinicians differentiating approaches for
symptomatic, and asymptomatic patients (see S4 File):
a. Verbal strategies, such as introducing the topic of HIV
b. Rapid risk assessment for STIs and blood borne viruses
2. Precise tailoring to the general practice setting including relevant clinical presentations;
clinical software support; primary care diagnostics and secondary service interface.
3. Separate teaching of GPs and practice nurses (as opposed to co-teaching)
4. Disguised repetition to enhance factual learning (eg individual HIV indicator conditions
are each encountered in a number of different exercises)
5. Specific identification and listing of barriers to HIV testing by participants and trainers,
with barriers crossed out if participants agree they have been addressed.
Additional factors not always commissioned / or deliverable in Haringey:
6. Performance feedback on individual practice testing rates
7. Invitation of HIV positive representatives to bring the ‘patient voice’
8. Support of training attendance with specific resources (such as locum payment).
SHIP can, and has been, replicated in different areas of the UK with funding and through
collaboration and co-training (as occurred in Haringey). Further information on SHIP train-
ing is published elsewhere [23, 24]. However no current detailed ‘SHIP Implementation Hand-
book’ has been commissioned. It is not possible, without research funding, to state if such a
handbook would be as efficacious as current approaches to implementation of SHIP which
include centralised quality control (evidence updates and annual trainer days). SHIP is cur-
rently a not-for-profit Community Interest Company.
Conclusion
SHIP is an educational intervention that produces a significant and sustained increase in
HIV testing in primary health care for each GP trained in a high prevalence area of the UK.
HIV tests used in routine clinical care in Haringey have a relatively high positivity. The find-
ing that the HIV testing rate increased with no concomitant decline in the positivity suggests
that SHIP training also contributed to the performance of GPs in detecting people with
HIV. Unlike a randomised controlled trial, this evaluation is a ‘real life’ measure of the effect
that commissioners of SHIP could expect should SHIP be implemented in a comparable
area of the UK. SHIP effectiveness is likely explained by the components of SHIP training
that distinguish it from interventions in the UK that did not demonstrate an effect of HIV
testing.
Further analysis, applying the methods used here, of the effect on Hepatitis B and C testing
rates and positives; diagnoses of chlamydia and gonorrhoea; and falls in use of the high vaginal
swab, will give a better picture of the effects of SHIP on clinical practice, particularly in relation
to nurses and to evaluate cost-effectiveness. Further, understanding of the mechanisms of
action of SHIP would be aided by thorough process evaluation when SHIP is introduced into a
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 10 / 13
new area. This may help identify the components of the training that have most effect on prac-
tice, and those that might be dropped.
Supporting information
S1 File. Key points in current UK clinical guidance on HIV testing that informs SHIP
teaching content.
(DOCX)
S2 File. SHIP content outline.
(DOCX)
S3 File. SHIP evaluation in Haringey 2012 publication.
(PDF)
S4 File. SHIP clinical outlines.
(DOCX)
S5 File. SHIP de-intentified data.
(XLSX)
Acknowledgments
We give thanks to all collaborators, including those at Whittington, North Middlesex and
Homerton laboratories who have been endlessly patient with our requests. Also, Haringey gen-
eral practitioners and practice nurses for their fantastic work during and after training. Finally,
a big thanks to the MEDFASH team, especially Emma Harvey.
Author Contributions
Conceptualization: Melissa Gardner, Judith Mullineux, Till Bärnighausen, Philippa Margaret
Matthews.
Data curation: Kamla Pillay, Allon Gould.
Formal analysis: Till Bärnighausen.
Funding acquisition: Susan Otiti, Judith Mullineux.
Investigation: Till Bärnighausen.
Methodology: Judith Mullineux, Till Bärnighausen, Philippa Margaret Matthews.
Project administration: Susan Otiti.
Resources: Susan Otiti.
Supervision: Susan Otiti, Philippa Margaret Matthews.
Validation: Till Bärnighausen.
Writing – original draft: Kamla Pillay, Melissa Gardner, Judith Mullineux, Till Bärnighausen,
Philippa Margaret Matthews.
Writing – review & editing: Melissa Gardner, Allon Gould, Susan Otiti, Judith Mullineux, Till
Bärnighausen, Philippa Margaret Matthews.
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 11 / 13
References 1. Kirwan PDC, C. Brown, A.E. Gill, O.N. Delpech, V.C. HIV in the UK—2016 Report. London: Public
Health England, 2016.
2. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, et al. Prevention of
HIV-1 infection with early antiretroviral therapy. The New England journal of medicine. 2011; 365
(6):493–505. Epub 2011/07/20. https://doi.org/10.1056/NEJMoa1105243 PMID: 21767103.
3. Rodger AJ, Cambiano V, Bruun T, Vernazza P, Collins S, van Lunzen J, et al. Sexual Activity Without
Condoms and Risk of HIV Transmission in Serodifferent Couples When the HIV-Positive Partner Is
Using Suppressive Antiretroviral Therapy. Jama. 2016; 316(2):171–81. Epub 2016/07/13. https://doi.
org/10.1001/jama.2016.5148 PMID: 27404185.
4. May M, Gompels M, Delpech V, Porter K, Post F, Johnson M, et al. Impact of late diagnosis and treat-
ment on life expectancy in people with HIV-1: UK Collaborative HIV Cohort (UK CHIC) Study. BMJ
(Clinical research ed). 2011; 343:d6016. Epub 2011/10/13. https://doi.org/10.1136/bmj.d6016 PMID:
21990260.
5. Brown AE, Nardone A, Delpech VC. WHO ’Treatment as Prevention’ guidelines are unlikely to decrease
HIV transmission in the UK unless undiagnosed HIV infections are reduced. AIDS (London, England).
2014; 28(2):281–3. Epub 2013/12/24. https://doi.org/10.1097/qad.0000000000000137 PMID:
24361685.
6. Ellis S, Curtis H, Ong EL. HIV diagnoses and missed opportunities. Results of the British HIV Associa-
tion (BHIVA) National Audit 2010. Clinical medicine (London, England). 2012; 12(5):430–4. Epub 2012/
10/30. PMID: 23101142.
7. Dorward J, Chinnaraj A, Garrett N, Apea V, Leber W. Opportunities for earlier diagnosis of HIV in gen-
eral practice. Sexually transmitted infections. 2012; 88(7):524. Epub 2012/11/01. https://doi.org/10.
1136/sextrans-2012-050712 PMID: 23112337.
8. HIV testing: increasing uptake in men who have sex with men. London: National Institution for Health
and Care Excellence (NICE), 2011.
9. HIV testing: increasing uptake in black Africans. London: National Institution for Health and Care Excel-
lence (NICE), 2011.
10. UK National Guidelines for HIV Testing 2008: British HIV Association, British Association of Sexual
Health and HIV, British Infection Society. London: The British HIV Association (BHIVA), 2008.
11. Ishii LE. Closing the clinical gap: translating best practice knowledge to performance with guidelines
implementation. Otolaryngology—head and neck surgery: official journal of American Academy of Oto-
laryngology-Head and Neck Surgery. 2013; 148(6):898–901. Epub 2013/03/07. https://doi.org/10.1177/
0194599813481203 PMID: 23462655.
12. Lau R, Stevenson F, Ong BN, Dziedzic K, Treweek S, Eldridge S, et al. Achieving change in primary
care—effectiveness of strategies for improving implementation of complex interventions: systematic
review of reviews. BMJ Open. 2015; 5(12). https://doi.org/10.1136/bmjopen-2015-009993 PMID:
26700290
13. Elmahdi R, Gerver SM, Gomez Guillen G, Fidler S, Cooke G, Ward H. Low levels of HIV test coverage
in clinical settings in the U.K.: a systematic review of adherence to 2008 guidelines. Sexually transmitted
infections. 2014; 90(2):119–24. Epub 2014/01/15. https://doi.org/10.1136/sextrans-2013-051312
PMID: 24412996.
14. Kristensen N, Nymann C, Konradsen H. Implementing research results in clinical practice- the experi-
ences of healthcare professionals. BMC health services research. 2016; 16:48. Epub 2016/02/11.
https://doi.org/10.1186/s12913-016-1292-y PMID: 26860594.
15. Rangachari P, Rissing P, Rethemeyer K. Awareness of evidence-based practices alone does not trans-
late to implementation: insights from implementation research. Quality management in health care.
2013; 22(2):117–25. Epub 2013/04/02. https://doi.org/10.1097/QMH.0b013e31828bc21d PMID:
23542366.
16. Davies C, Gompels M, May M. Public and healthcare practitioner attitudes towards HIV testing: review
of evidence from the United Kingdom (UK). Int STD Res Rev. 2015; 3(3):91–122.
17. Joore IK, van Roosmalen SL, van Bergen JE, van Dijk N. General practitioners’ barriers and facilitators
towards new provider-initiated HIV testing strategies: a qualitative study. International journal of STD &
AIDS. 2017; 28(5):459–66. Epub 2016/05/22. https://doi.org/10.1177/0956462416652274 PMID:
27207253.
18. Thornton AC, Rayment M, Elam G, Atkins M, Jones R, Nardone A, et al. Exploring staff attitudes to rou-
tine HIV testing in non-traditional settings: a qualitative study in four healthcare facilities. Sexually trans-
mitted infections. 2012; 88(8):601–6. Epub 2012/07/10. https://doi.org/10.1136/sextrans-2012-050584
PMID: 22773329.
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 12 / 13
19. Yeung A, Temple-Smith M, Fairley C, Hocking J. Narrative review of the barriers and facilitators to chla-
mydia testing in general practice. Australian journal of primary health. 2015; 21(2):139–47. Epub 2014/
08/15. https://doi.org/10.1071/PY13158 PMID: 25118823.
20. Allison R, Lecky DM, Town K, Rugman C, Ricketts EJ, Ockendon-Powell N, et al. Exploring why a com-
plex intervention piloted in general practices did not result in an increase in chlamydia screening and
diagnosis: a qualitative evaluation using the fidelity of implementation model. BMC family practice.
2017; 18(1):43. Epub 2017/03/23. https://doi.org/10.1186/s12875-017-0618-0 PMID: 28327096.
21. Town K, McNulty CA, Ricketts EJ, Hartney T, Nardone A, Folkard KA, et al. Service evaluation of an
educational intervention to improve sexual health services in primary care implemented using a step-
wedge design: analysis of chlamydia testing and diagnosis rate changes. BMC public health. 2016;
16:686. Epub 2016/08/04. https://doi.org/10.1186/s12889-016-3343-z PMID: 27484823.
22. Bailey AC, Dean G, Hankins M, Fisher M. Attending an STI Foundation course increases chlamydia
testing in primary care, but not HIV testing. International journal of STD & AIDS. 2008; 19(9):633–4.
Epub 2008/08/30. https://doi.org/10.1258/ijsa.2008.008110 PMID: 18725557.
23. Mullineux J, Firmstone V, Matthews P, Ireson R. Innovative Sexual Health Education for General Prac-
tice: An Evaluation of the Sexual Health in Practice (SHIP) Scheme. Education for Primary Care. 2008;
19(4):397–407.
24. Pillay TD, Mullineux J, Smith CJ, Matthews P. Unlocking the potential: longitudinal audit finds multiface-
ted education for general practice increases HIV testing and diagnosis. Sexually transmitted infections.
2013; 89(3):191–6. Epub 2012/10/10. https://doi.org/10.1136/sextrans-2012-050655 PMID: 23044438.
25. Broadbent J, Maisey S, Holland R, Steel N. Recorded quality of primary care for osteoarthritis: an obser-
vational study. The British journal of general practice: the journal of the Royal College of General Practi-
tioners. 2008; 58(557):839–43. Epub 2008/12/11. https://doi.org/10.3399/bjgp08X376177 PMID:
19068156.
26. General and Personal Medical Services England 2002–2012. London: The Health and Social Care
Information Centre—Workforce Directorate, 2013.
27. Barnighausen T, Oldenburg C, Tugwell P, Bommer C, Cara E, Barreto M, et al. Quasi-experimental
study designs series—Paper 7: assessing the assumptions. Journal of clinical epidemiology. 2017.
Epub 2017/04/04. https://doi.org/10.1016/j.jclinepi.2017.02.017 PMID: 28365306.
28. Barnighausen T, Tugwell P, Rottingen JA, Shemilt I, Rockers P, Geldsetzer P, et al. Quasi-experimental
study designs series—Paper 4: uses and value. Journal of clinical epidemiology. 2017. Epub 2017/04/
04. https://doi.org/10.1016/j.jclinepi.2017.03.012 PMID: 28365303.
29. Wang Y, Hunt K, Nazareth I, Freemantle N, Petersen I. Do men consult less than women? An analysis
of routinely collected UK general practice data. BMJ Open. 2013; 3(8). https://doi.org/10.1136/
bmjopen-2013-003320 PMID: 23959757
30. Ogaz DF, M. Connor, N. Gill, O.N. HIV testing in England: 2016 report. London: Public Health England,
2016.
31. Baker R, Camosso-Stefinovic J, Gillies C, Shaw EJ, Cheater F, Flottorp S, et al. Tailored interventions
to address determinants of practice. The Cochrane database of systematic reviews. 2015;(4):
Cd005470. Epub 2015/04/30. https://doi.org/10.1002/14651858.CD005470.pub3 PMID: 25923419.
32. How to Change Practice: Understand, Identify and Overcome barriers to change. London: National
Institution for Health and Care Excellence (NICE), 2007.
33. Ivers N, Jamtvedt G, Flottorp S, Young JM, Odgaard-Jensen J, French SD, et al. Audit and feedback:
effects on professional practice and healthcare outcomes. The Cochrane database of systematic
reviews. 2012;(6):Cd000259. Epub 2012/06/15. https://doi.org/10.1002/14651858.CD000259.pub3
PMID: 22696318.
34. Joore IK, van Bergen J, Ter Riet G, van der Maat A, van Dijk N. Development and evaluation of a
blended educational programme for general practitioners’ trainers to stimulate proactive HIV testing.
BMC family practice. 2018; 19(1):36. Epub 2018/03/09. https://doi.org/10.1186/s12875-018-0723-8
PMID: 29514596.
The effect of SHIP training on primary care physician HIV testing
PLOS ONE | https://doi.org/10.1371/journal.pone.0199891 August 1, 2018 13 / 13
Copyright of PLoS ONE is the property of Public Library of Science and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.