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Occupational Medicine2014;64:483489Advance Access publication 7 July 2014 doi:10.1093/occmed/kqu094
The Author 2014. Published by Oxford University Press on behalf of the Society of Occupational Medicine.All rights reserved. For Permissions, please email: [email protected]
Risk factors for occupational acute mountain
sickness
D. Vinnikov1, N. Brimkulov2, V. Krasotski1, R. Redding-Jones1and P. D. Blanc3,4
1Medical Department, Kumtor Gold Company, Bishkek 720017, Kyrgyzstan, 2Chair of Internal Diseases, Kyrgyz State Medical
Academy, Bishkek 720020, Kyrgyzstan, 3Department, Division of Occupational and Environmental Medicine, University of
California San Francisco, San Francisco, CA 94143-0924, USA, 4Department of Occupational and Environmental Medicine,
University of Gothenburg, Gothenburg 40530, Sweden.
Correspondence to: D. Vinnikov, Medical Department, Kumtor Gold Company, Isanova Street, 25A, Bishkek 720017,
Kyrgyzstan. Tel: +996 772 864260; fax: +996 312 900740; e-mail: [email protected]
Background Studies of occupational acute mountain sickness (AMS) have not focused on the more severe end of
the spectrum to date.
Aims To examine risk factors associated with the development of occupational AMS severe enough to
receive treatment in a compression chamber.
Methods A nested case referent study in a cohort of high-altitude (4000 m) mine workers, comparing cases
of severe, chamber-treated AMS to matched referents. Using logistic regression, we tested potential
risk factors based on premorbid surveillance examinations, including cigarette smoking (current
smoking, smoking intensity and exhaled carbon monoxide [CO]).
Results There were 15 cases and 30 controls. In multivariate analysis including age, sex and place of resi-
dence, current smoking was associated with increased risk of severe AMS (odds ratio [OR] 10.0;
95% confidence interval [CI] 1.567.4), taking into account any prior, less severe AMS event, which
was also a potent risk factor (OR 33.3; 95% CI 2.8390). Smoking intensity (cigarettes per day) and
exhaled CO were also statistically significantly associated with severe AMS.
Conclusions Cigarette smoking is a strong, previously under-appreciated risk factor for severe AMS. Because
this is a modifiable factor, these findings suggest that workplace-based smoking cessation should be
tested as an intervention to prevent such morbidity.Key words Altitude; mining; mountain; occupation; smoking.
Introduction
Acute mountain sickness (AMS) is a common complica-
tion of hypobaric environmental stress [1,2]. It can be
associated with significant morbidity leading to compro-
mise in both physical and cognitive functioning. AMS
remains a persistent and even growing problem, despite
decades of research into the factors that may influence itsincidence and severity. Beyond the well-established AMS
risk factors such as degree of elevation, rate of ascent to
a given altitude [13] and level of exertion under hypo-
baric conditions [4], the identification of other poten-
tially modifiable variables remains elusive. Obesity and
migraine history have been shown to impart AMS risk
[5,6], but beyond that individual susceptibility is gen-
erally considered an idiosyncratic phenomenon [710].
Thus, risk profiling has focused on physiological charac-
teristics of an AMS-prone state, such as excessive desat-
uration under hypobaric conditions, a low ventilatory
response to exercise or variability in nitric oxide metabo-
lism [4,11].
It is unclear whether certain established or suspectedfactors are associated with an increased risk of severe
AMS. These factors include obesity, decrements in lung
function, hypertension and previous less severe AMS
episodes that have not led to chamber treatment. There
is also a need to assess whether current cigarette smok-
ing might be associated with AMS as smoking reduction
is an achievable workplace wellness intervention. We
have previously shown in a longitudinal analysis that a
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484 OCCUPATIONAL MEDICINE
secondhand smoke exposure reduction policy that was
successfully instituted at the mine site was temporally
associated with improved lung function [12]. We, there-
fore, carried out this study to examine AMS risk through
a retrospective analysis of cases in a population employed
at high altitude.
MethodsStudy data were extracted from the clinical illness case
files and baseline hire and annual surveillance exami-
nation records of the occupational health service for
an active gold mine operating at an altitude of 3800
4200 m. The mine is located in the Tyan Shan Mountains
of the Kyrgyz Republic, ~400 km from its capital, Bishkek.
This occupational cohort, provided a unique opportu-
nity to study AMS. First, this is a relatively large cohort
and AMS is an endemic problem in this setting. Second,
there is a medical service at the mine allowing easy iden-
tification of people with symptoms of AMS and on-site
use of a compression (hyperbaric) chamber for treat-ment of clinically severe cases. Finally, electronic medical
records including premorbid surveillance data facili-
tated the identification of cases as well as the selection
of matched referent mine workers without compression
chamber-treated AMS, permitting a nested casecontrol
study. Mineworkers generally work 2 week periods on-
site, with a 12 hour on, 12 hour off shift schedule while
at the mine. Mining personnel commute on buses from
their places of permanent residence either in the Issykul
Lake plateau area of Kyrgyzstan (1600 m elevation) or in
Bishkek and its environs (700 m).
All mine employees undergo pre-placement and
annual health surveillance screening in Bishkek, whichprovided the premorbid data for both cases and referents.
Although screening does select out individuals based on
the presence of selected health conditions, prior AMS
events are not considered an employment exclusion cri-
terion. The medical database includes all screening data
and test results for each employee as well as records
of any symptomatic mine clinic visits, with mandatory
entry of an associated diagnosis code. This includes sep-
arate coding options for mountain sickness (MS) and
AMS. Although distinct options, they are applied too
interchangeably in practice to allow their use as sepa-
rate distinct diagnostic entities for these purposes of this
investigation.We queried this database to identify all on-site mine
clinic intake visits involving a diagnosis of MS or AMS
during a period of 4 years, starting on 1 January 2009 and
ending on 31 December 2012. The calendar year 2009
marked the introduction of the medical electronic soft-
ware system. The MS or AMS codes are typically entered
when employees present with complaints that are con-
sistent with high-altitude syndromes and when another
aetiology for such symptoms is not readily apparent.
Management of AMS cases is based on conventional
assessment and management protocols, with cases des-
ignated as mild, moderate or severe [1,2]. Symptoms
that prompt the clinical diagnosis include persistent
headache (especially with a poor response to acetami-
nophen [paracetamol] or ibuprofen), dizziness, shortness
of breath, gastrointestinal complaints, sleep disturbance
and fatigue. Suspected MS/AMS is generally treated
empirically with acetazolamide 125 mg orally every 12
hours and with inhalation of supplementary oxygen for
at least 30 minutes, following which the patient is reas-
sessed clinically. In practice, systematic standard elicita-
tion of complaints that could yield Lake Louise Scoring
(LLS) is not recorded. This tool is a scoring system to
assess the presence and severity of AMS, which quanti-
fies headache with other symptoms of AMS [13].
The occupational medicine clinic on-site at the mine
is equipped with a fully functional multiplace hyper-
baric chamber (Southern Oceanic, Republic of South
Africa). Patients considered on clinical grounds to be suf-
fering from severe AMS are treated in the chamber. Werestricted the case definition of AMS to those persons who
were deemed ill enough to undergo compression chamber
treatment. We selected two referents for each case, one on
each side of a numeric sorting by employee identification
number. When annual surveillance data were missing (e.g.
when that employee was no longer in the workforce), we
selected the next listed employee. The mean time elapsed
from the screening examination until the incident AMS
event was 3.5 months among the cases and 4 months
among the incidence density-matched referent employees.
Annual screening data closest in date prior to the
event were used to derive demographics, place of per-
manent residence, physical examination and testing dataand duration of employment. Clinical data included
height and weight (yielding body mass index [BMI]),
blood pressure, findings of fundoscopic examination by
a trained ophthalmologist (a routine in the surveillance
protocol), pulmonary function test results (MicroLoop
portable spirometer with Spida5 software, FusionCare,
Hampshire, UK) and electrocardiogram (ECG) assess-
ment. The cigarette smoking status of each mine
employee is reassessed at every annual screening. Self-
reported daily smoking at the time of examination and
numbers of cigarettes smoked per day are elicited and
further assessed with an exhaled carbon monoxide (CO)
measurement by means of portable breath CO analyser(Smokerlyzer, Bedfont, UK).
Because the medical electronic record system did not
cover the earlier period between hire and the years of
our study, prior AMS events were identified through
review of hard copy medical files. From this data source,
the number and date of such episodes along with their
severity and treatment were extracted. We excluded any
potential referent with a record of prior chamber treat-
ment: this had occurred in only one potential referent
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D. VINNIKOV ET AL.: RISK FACTORS FOR OCCUPATIONAL AMS 485
and an employee with the closest adjacent identifica-
tion number was substituted. No previous chamber
treatments were identified among the cases prior to the
case-defining event.
We used logistic regression analysis to estimate the
relative odds of severe AMS (defined by compression
chamber treatment) using a hierarchical approach to
model building. In the first step, we compared cases and
referents in terms of two groups of variables: potential
study confounders and potential risk factors of pri-
mary study interest (t-test, Fishers exact test or 2*2
tables were used). For confounders, we assessed dif-
ferences between cases and referents in age, sex and
altitude of residence (because those dwelling at higher
altitude might be protected from AMS). Among risk
factors for disease, we were interested in obesity, lung
function, hypertension or its sequelae, previous MS/
AMS and cigarette smoking. The latter was of partic-
ular interest because it is potentially modifiable at the
workplace [12]. Moreover, in addition to self-reported
smoking status, we also had exhaled CO measurements.The characteristics of cases and referents are shown in
Table 1. We limited logistic regression modelling only
to those variables of primary study interest that dif-
fered between cases and referents (P< 0.20). We tested
each of these in bivariate models and then in multi-
variate models adjusted for age, sex and place of resi-
dence (Issykul plateau versus Bishkek and its environs).
We further explored the relationship between cigarette
smoking and AMS, taking into account previous AMS
events. To assess potential mediation and effect modera-
tion, we tested these models with and without a prior
AMS*smoking interaction term. These final models did
not include sex, age and residence. The study protocol
was reviewed and approved by the committee on bioeth-
ics of the Kyrgyz State Medical Academy.
Results
MS/AMS cases amounted to 216 in 2012, 388 in 2011,
350 in 2010 and 350 in 2009, a total of 1304. Of these,
15 (1%) underwent chamber pressurization treatment
with 7 treated in 2009, 1 in 2010, 3 in 2011 and 4 in
2012. As shown in Table 1, the study population was
predominantly male, but females were over-represented
among cases and cases were slightly younger than refer-
ents (P< 0.20, meeting criteria for model inclusion; see
Methods). Most saliently, a substantially greater propor-
tion of cases had experienced at least one prior episode
of less severe AMS compared with referents (53% ver-sus 7%; P < 0.001). Lung function parameters, blood
pressure and BMI were similar among cases and refer-
ents. Resting heart rates were marginally faster among
the cases compared with referents, but not at a level of
statistical significance. Cigarette smoking status differed
between cases and referents for each of the three meas-
ures studied: there were almost twice as many smokers
in the case group, they smoked twice as many cigarettes
Table 1. Initial risk factors of interest in cases and referents
Indicators Cases, n(%) Referents, n(%) P-value
N 15 30
Male/female 11/4 (73/27) 27/3 (90/10) NS
Issykul residents/lowland residents 9/6 (60/40) 17/13 (57/43) NS
Age in years, mean SD 33 7 36 9 NS
Employment duration in years, mean SD 5.9 3.1 8.6 4.3
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486 OCCUPATIONAL MEDICINE
per day and their exhaled CO level was higher compared
with referents (Table 1).
The clinical symptoms and treatment of the 15 cases
of severe AMS are summarized in Table 2. The most
prevalent symptom group was neurological, with at least
one of the following symptoms present: headache, diz-
ziness or numbness of the extremities. Gastrointestinal
and cardiopulmonary symptoms were less common. In
accordance with standard recommendations [13], all
cases were treated with acetazolamide and systemic cor-
ticosteroids were administered in all but two. By study
definition, all 15 cases underwent compression cham-
ber treatment. None evolved into more serious disease
requiring emergency transport to lower altitude (the
protocol for high-altitude pulmonary oedema or high-
altitude cerebral oedema).
Based on a prioricriteria, we tested six independent
variables as risk factors for AMS (based on their bivari-
ate associations inTable 1; see Methods). These analy-
ses are shown inTable 3, which presents the unadjusted
odds ratio (OR; consistent with the previous bivariatedata) and then the OR adjusted for age, sex and place
of residence. We chose to include age, sex and residence
in the multivariate model because they were potential
confounding variables. Work duration was negatively
associated with severe AMS, while increased heart rate
was positively associated, although neither factor was
statistically significant in these models. In contrast, both
previous AMS and current cigarette smoking (assessed
dichotomously or by intensity) were associated with
increased odds of severe AMS. Smoking adjusted for
age, sex and place of residence increased the odds for
severe AMS by 10 times, while any previous but less
severe AMS increased odds by an even greater margin
(Table 3). Smoking, ascertained both by the number
of cigarettes smoked per day and the concentration of
exhaled CO, was tested in separate multivariate mod-
els included both AMS and an AMS*smoking interac-
tion term for each of the smoking measures (Table 4).
The interaction terms were not statistically significant
in either model. Moreover, the effect estimates for ciga-
rettes per day and exhaled CO were similar with (Model
2) or without the interaction term (Model 1) in the
model, although the prior AMS effect estimate became
less stable with inclusion of the interaction term.
Discussion
We found that active cigarette smoking was a potent
risk factor for severe AMS. The cigarette smoking
exposure-response was noted both for self-reported
smoking quantities and exhaled CO and was robusteven after taking into account any prior AMS event.
Moreover, prior AMS risk, as anticipated and sup-
porting our study methodology, was a powerful inde-
pendent risk factor for recurrent AMS, consistent with
the findings of other epidemiological investigations
[3,8,10,1416].
The chief focus in investigations of AMS risk has been
on physiological variables that predispose to adverse out-
comes, such as rate of ascent [1417], obesity [5], oxygen
desaturation [9] and hypoxic tolerance [4]. One prospec-
tive cohort study of six different physiological measures
(oxygen desaturation, low heart rate and low ventilator
rate, each at rest and at exercise) found all predisposedto severe high-altitude-related illness [4].
The potential importance of cigarette smoking
in AMS varies with the population studied. Among
mountain climbing enthusiasts, the prevalence of
active cigarette smoking is generally low (e.g. 9% in
Table 2. Symptoms reported and treatment administered among
15 cases of AMS
n(%)
Symptoms
Neurological
Headache 11 (73)
Dizziness 7 (47)
Numbness of extremities 4 (27)
Any neurological symptom 15 (100)
Cardiopulmonary
Palpitations 3 (20)
Shortness of breath 1 (7)
Any cardiopulmonary symptom 4 (27)
Gastrointestinal Nausea 6 (40)
Vomiting 3 (20)
Any gastrointestinal symptom 7 (47)
Other
Disturbed sleep 3 (20)
Fatigue 2 (13)
Treatments
Acetazolamide 15 (100)
Dexamethasone 13 (87)
Compression chamber treatment (case definition) 15 (100)
Table 3. Logistic regression of selected variables for severe AMS
Variable OR unadjusted OR adjusted for
age, sex and place
of residence
OR 95% CI OR 95% CI
Duration of employment 0.8 0.71.0 0.9 0.71.1
Heart rate/10 beats
per minute
1.7 0.83.7 2.2 0.95.3
Previous AMS 25.4 2.7237 33.3 2.8390
Smoking 2.7 0.79.6 10.0 1.567.4
Cigarettes per day/
10 cigarettes
3.0 1.09.2 5.5 1.421.9
Exhaled CO/10 p.p.m. 2.2 0.95.7 4.0 1.213.1
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D. VINNIKOV ET AL.: RISK FACTORS FOR OCCUPATIONAL AMS 487
one such study [8] and 11% in another study [15]).
Cigarette smoking is, however, much more common
in occupational cohorts, tourists and military person-
nel assigned to high altitude. It is all the more notable,
therefore, that two relatively large studies of cohortsin which smoking is common have found that this
factor appears to be protective against AMS. One of
these analysed nearly 400 railway construction work-
ers in China, the highest worksite being at 4905 m
[18]. Current smokers had lower LLS values for AMS
compared with non-smokers, driven largely by head-
ache symptoms, yet conversely, smoking was associ-
ated with lung function and oxygenation deficits at
follow-up [18]. A second study from China found that
for military recruits taken to a high altitude, cigarette
smoking was also protective for LLS-defined AMS
[19]. Several other studies of AMS have also reported
an association suggestive of smoking being a protec-tive factor for AMS, albeit not a statistically significant
one [3,4,8,15]. Other data on carboxyhaemoglobin
or exhaled CO as a potential AMS risk derive from
an interest in potential exposure to CO from cooking
stoves in mountaineering. This has not been found to
be associated with risk, positively or negatively [20].
Cigarette smoking is associated with lower exhaled
NO [21] and may confound the association with AMS.
The analysis of Chinese military recruits noted above
paradoxically found higher pre-ascent exhaled NO
among the cases, even though smokers had lower lev-
els; no multivariate analysis was reported [19].
A key aspect of our study is that we defined AMS asepisodes severe enough on clinical grounds to undergo
compression chamber treatment. It may be that smok-
ing protects against certain symptoms that contribute to
LLS-defined illness but nonetheless conveys increased
risk of more severe illness. In that light, we believe that
our studys limitation of a lack of systematic LLS data
is counterbalanced by its ability to identify cases at the
severe end of the AMS disease spectrum. This also would
explain the lack of a reduction in the risk associated with
current smoking by prior, less severe AMS events when
tested in the same model. Were smoking to be strongly
associated with milder AMS, including such events on
the multivariate modelling should have affected smok-
ing-associated risk estimates.Ours was a relatively small sample, comprising only
15 cases of severe AMS. Thus, we lack statistical power
to detect modest associations (e.g. in the observed
trends of lower forced expiratory volume in 1 second/
forced vital capacity and in heart rate). Even though
there was no marked difference in occupation status
of cases and referents when grouped broadly (produc-
tion versus service work), we acknowledge that a far
larger study would be needed to identify or exclude
specific job tasks as risk factors for severe AMS. Our
initial choice of variables beyond smoking was based
on the findings of other studies. Most of the selected
physiological variables were extracted from an annualscreening prior to the event, a strength of the study,
but the analysis was therefore limited in its range of
selected variables. Inclusion of other variables might
have identified additional associations that could not
be studied in this study. Certain other factors simply
cannot be studied in our working population (e.g. rate
of ascent or number of nights at a given altitude before
final ascent) because our subjects are all transported
to the mine site by bus, a 7 hour trip. Symptom-driven
bias in subjects reports of their smoking status is not
relevant as this was assessed prior to the AMS event.
Treatment bias (selection for chamber treatment on the
grounds not of illness severity but of clinical concernover smoking status) is unlikely and notably our analy-
sis took place after the study period. Moreover, if smok-
ing were simply a risk factor for occult lung disease that
led to greater symptom severity we should have seen
a stronger association with impaired lung function.
Finally, this study involves intermittent high-altitude
exposure in well-acclimatized workers and thus should
not be generalized to others such as non-acclimatized
non-occupational populations.
Table 4. Prior AMS and smoking intensity tested in multivariate regression models of severe AMS
Model without interaction term Model with interaction term
OR 95% CI P OR 95% CI P
Model 1. Smoking intensity/AMS
Cigarettes per day/10 cigarettes 1.1 1.01.3
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Our analysis raises the question of whether an oth-
erwise fit for duty employee who has had one or more
episode of AMS should be targeted for additional meas-
ures to prevent recurrent and potentially more severe
events. Interestingly, national legislation in Kyrgyzstan,
which is otherwise fairly prescriptive in terms of man-
dated surveillance and even work restrictions, does not
identify a prior AMS episode as a contraindication for
employment. The potential advantages of workplace-
based smoking cessation efforts are more obvious.
Smoking cessation programmes should be a priority,
particularly targeting those with prior AMS for addi-
tional efforts, given that effective smoking cessation
strategies do exist [22]. This is no panacea however and
middle-aged working populations without severe smok-
ing complications may be one of the hardest in which to
achieve successful cessation [23].
In summary, this study demonstrates more severe
AMS may be associated with some risk factors that are
similar to and some that may differ from those for less
severe AMS. In conditions of intermittent exposure inwell-acclimatized workers, smoking appears to play a
potent role in severe AMS, suggesting that in such popu-
lations effective smoking cessation measures may reduce
AMS-associated morbidity.
Key points
Severe acute mountain sickness requiring com-pression treatment may be associated with risk fac-
tors that differ from those for less severe sickness,
in particular in terms of smoking-related risk.
Pre-employment evaluation of prospective employ-ees for high-altitude work should take into account
previous acute mountain sickness and smoking, as
both may identify individuals at higher risk.
Work-based smoking cessation interventionsfor high-altitude employees should consider the
potential added benefit of severe acute mountain
sickness prevention.
Acknowledgements
The study group would like to thank the management of
Kumtor Gold Company (Kumtor Operating Company) for
their support. Kumtor mine site and Bishkek doctors and
nurses have together made this study possible.
Conflicts of interest
D.V., V.K. and R.R. are employees of the Kumtor Gold
Company. P.D.B. is involved in other research, partially sup-
ported by Kumtor Gold Company. No authors received pay-
ment for this research.
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Fifty years ago: General practice and industrial
medicine in the United States
B. H. Pentney, Appointed Factory Doctor, Camberwelland Lambeth
Given at a meeting of the Association on 3 April 1964
I am an Appointed Factory Doctor, but it was as a gen-
eral practitioner that I received a Nuffield Travelling
Fellowship for 1963. I had chosen to study the type
and range of general practice and the place of the
general practitioner in industry. I was also to con-
sider what part the general practitioner could play in
a future occupational health service in this country.
The tour was started in July 1963 and most of the time
was spent in two places5 weeks in California and
11 weeks in Cincinnati. In North America there is alarge and growing body of whole-time industrial physi-
cians, and these are of a high order of knowledge and
efficiency. They are the experts. For the greater part
they are whole time employees of big industrial organ-
izations. They are responsible for the running of their
medical services and research, and set the standard of
occupational health throughout the country.
A very comprehensive Workmens Compensation
system is really the basis of the greater part of the work
of the general practitioner in industrial medicine, and
it is at first sight of immense value in the creation of
occupational health systems generally. Unfortunately,
during its development the emphasis seems to havealtered. The ideals, including fair reimbursement for
suffering and loss of earnings, and early rehabilita-
tion, have sometimes been submerged in the processes
of preparing a case for presentation to the Accident
Commission. The disability will be assessed most care-
fullypossibly using the standard Packard Thurber
systemto achieve some uniformity. Compensation
will be awarded strictly in accordance with a standard
scale, taking into consideration the patients age, the
exact anatomical site of the lesion, the percentage of
loss of movement and expectancy in that mans spe-cific trade. With these tremendously detailed assess-
ments, time is lost and it seemed to me that early and
adequate rehabilitation was impeded. I was surprised
at the wide range of disabilities accepted as industrial
in origin and shocked at the amount of compensation
awardedfor example, for bronchitis and coronary
disease.
Undoubtedly the general practitioner has an estab-
lished place in occupational health in the United
States. It is, however, fairly limited in its application.
Individual and group practitioners provide good casu-
alty and routine examination services for large and
small industries.Although to us it is clearly desirable that all fact-
ories should have medical services, occupational health
has not yet been completely sold to industry. There
industrial medical practitioners dealing mainly with
Workmens Compensation cases have not established
free access into plants, and they appear to have little
enthusiasm for, or encouragement to be interested in,
sick factories. Though splendid and growing centres
for environmental studies are available there is much
left to be achieved in terms of getting the proprietor or
management to want medical services. Post-graduate
training in the speciality is available, but on the whole
poorly attended, and it would seem that though thismust be made more attractive, the subject of occupa-
tional health ought to be a mandatory undergraduate
subject.
From: General practice and industrial medicine in the
United States. Trans Ass Industr Med Offrs(1964) 14,
89. Available at: Occup Med (Lond) 1964;14:8990.
doi:10.1093/occmed/14.1.89.
The full Occupational Medicinearchive can be accessed
online at http://occmed.oxfordjournals.org/.
http://occmed.oxfordjournals.org/http://occmed.oxfordjournals.org/