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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

* [email protected]

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

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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

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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

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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

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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.

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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

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The effect of SHIP training on primary care physician HIV testing

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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

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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

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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

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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

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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

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