Available via license: CC BY 4.0
Content may be subject to copyright.
ORIGINAL ARTICLE
https://doi.org/10.1007/s12471-018-1153-x
Neth Heart J
Persistent foramen ovale closure in divers with a history of
decompression sickness
R. Koopsen1·P.R.Stella
2·K.M.Thijs
3·R.Rienks
2,4
© The Author(s) 2018
Abstract
Objective To study the effect of percutaneous patent foramen ovale (PFO) closure in divers with a history of decompression
sickness (DCS).
Study design (1) Retrospective study of patient records and (2) telephonic follow-up. Patients with unexplained decom-
pression sickness, who were referred to a cardiologist with a focus on diving medicine between 2000 and 2017, were
included in the study
Results A total of 62 divers with DCS were included. In all cases transoesophageal echocardiography (TEE) was per-
formed, showing 29 PFOs and 6 atrial septum defects (ASDs) in total n= 35 (56%). The highest prevalence was found in
divers with cutaneous and vestibular DCS. At follow-up (mean follow-up duration 6.8 years), 21 PFOs/ASDs were closed
using a percutaneous procedure. One diver was lost to follow-up. One diver quit diving. The remaining divers were able
to resume unrestricted diving; there was no recurrence of major DCS. Of the divers with an open PFO or ASD, 14 were
included of whom 7 are currently diving. All (except one diver with a small PFO) divers are using a conservative diving
profile to reduce nitrogen load and the appearance of venous nitrogen bubbles. There was no recurrence of major DCS in
this group.
Conclusion Percutaneous PFO closure may be an effective and safe treatment for divers who have suffered a major DCS to
return to unrestricted diving. Alternatively, conservative treatment seems safe when divers refrain from unrestricted diving
and use a conservative technique in order to reduce nitrogen load.
Keywords Patent foramen ovale · Decompression sickness · Diving
What’s new?
●Vestibular DCS and cutis marmorata are frequently asso-
ciated with PFO.
●PFO closure in divers with a history of DCS is a safe
and effective treatment for divers to return to unrestricted
diving.
●If the diver refrains from PFO closure, a restrictive diving
profile seems safe and could be recommended.
R. Koopsen
r.koopsen@students.uu.nl
1Utrecht University, Utrecht, The Netherlands
2Department of Cardiology, University Medical Center,
Utrecht, The Netherlands
3Department of Sports Medicine, University Medical Center,
Utrecht, The Netherlands
4Central Military Hospital, Utrecht, The Netherlands
Introduction
Decompression illness (DCI) is a major medical problem
among scuba divers. As a diver descends and breathes air
under increased pressure, the tissues become loaded with
increased quantities of nitrogen. During ascent, but espe-
cially after the dive, this nitrogen is released into the blood
which can lead to bubble formation. The volume and loca-
tion of these bubbles determine whether symptoms occur
[1].
Decompression illness (DCI) comprises both arterial gas
embolism (AGE) and decompression sickness (DCS). AGE
usually occurs directly after surfacing and is caused by lung
problems (bullae or blebs) or a provocative diving profile
(rapid ascent with breath holding), causing overstretching
and tearing of the alveoli leading to air bubbles in the pul-
monary veins and subsequently into the arterial system (pul-
monary barotrauma).
DCS is caused by nitrogen bubbles. The nitrogen that has
been stored in the tissues during the dive disappears by dif-
Neth Heart J
fusion into the venous system. It is subsequently transported
to the lungs and exhaled. When the pressure decreases dur-
ing ascent, and especially after the dive, there may be bub-
ble formation in the tissue and in the veins. This occurs
when the nitrogen concentration exceeds the capacity of the
tissue and the venous system to remove the nitrogen. Local
bubble formation usually results in ‘type 1’ DCS whereas
venous bubble formation may result in ‘type 2’ DCS in
the presence of a right-to-left shunt. DCS usually develops
from about 20 min after surfacing.
‘Minor decompression illness’, or type 1 manifests as
musculoskeletal and cutaneous symptoms, such as pain
around the joint, skin rash and pruritus. ‘Major decompres-
sion illness’, or type 2 causes neurological, vestibular or
pulmonary symptoms [2].
Recently it was hypothesised that cutis marmorata,
which had previously been classified under type 1 DCS,
may be better classified under type 2 DCS, because of its
postulated neurogenic origin [3,4].
When DCI occurs when diving safety limits have been
violated it is considered to be ‘deserved’ DCI. However,
in half of the cases, DCI is ‘undeserved’ i.e. it occurs de-
spite compliance with the standardised decompression pro-
cedures. In cases of undeserved DCI, it is warranted to
look for a right-to-left shunt facilitating the transition of
nitrogen bubbles from the venous to the arterial circulation.
The most frequent cause of a right-to-left shunt is patent
foramen ovale (PFO). Although PFO is present in a quar-
ter to one-third of the general population, the risk of having
a DCI event is low and has been reported to be 2.5 in 10,000
divers. However it is five times higher in divers with a PFO
than in those without a PFO [5]. It is suggested that a small
PFO may not contribute to DCI, and a large PFO (diameter
>10 mm) may [6].
There are few data on the recurrence of decompression
sickness after the first event. In a group of 50 recreational
divers with neurological DCS, neurological DCS reoccurred
in 48% of the divers [7]. A prospective study in 104 scuba
divers (divided into 3 groups: no PFO, closed PFO and
open PFO) performing 18,394 dives over a period of 5 years
showed major DCI events mainly in the open PFO group,
suggesting a protective effect of PFO closure [8]. Another
study comparing divers with a PFO to divers treated with
catheter-based PFO closure showed complete elimination
of arterial bubbles after simulated dives [9].
Percutaneous closure of PFO has been used to reduce the
risk of DCI and has been shown to be safe and allow most
patients to return to unrestricted diving [10]. However, the
effect of closure on the rate of recurrence of DCI has not
been properly established. Our study observed the clinical
course of patients who had suffered a DCS, whether or not
after PFO closure.
Methods
This retrospective study was conducted at the University
Medical Center Utrecht. Patients with unexplained decom-
pression sickness, who were referred to a cardiologist with
a focus on diving medicine between 2000 and 2017, were
included in the study.
Data were retrieved from our electronic patient file. At
time of presentation, a detailed description of the diving
accident, timetable of occurrence of symptoms, treatment,
medical history and diving experience were obtained.
A DCS event was classified into different types of DCS:
musculoskeletal, skin bends, cutis marmorata, neurological
or vestibular.
Analysis at presentation included transoesophageal
echocardiography (TEE) with contrast and using the Val-
salva manoeuver for detecting right-to-left shunts, com-
puted tomography (CT) scan of the thorax and magnetic
resonance imaging (MRI) of the cerebrum.
A telephone questionnaire was used to gather informa-
tion about current diving activities. The divers were asked if
they were currently diving, if they had changed their diving
profile focusing on reduction of venous bubble load (use of
nitrox, restrictions on the depth of the dive, strict adherence
to decompression tables, no repetitive dives during a single
day and reduced rate of ascent) and if they had experienced
any diving-related problems such as DCS.
All PFO and atrial septal defects (ASD) closures were
performed using a standardised procedure as has been de-
scribed previously [11]. The PFO/ASD was closed under
local anaesthesia with intracardiac echocardiography (ICE)
guidance. In almost 90% of the cases a Figulla Flex PFO oc-
cluder was used (Occlutech) while the remaining 10% was
closed with an Amplatzer PFO occluder (ABBOTT). Post-
procedural thrombosis prophylaxis consisted of 6 months of
treatment with carbasalate calcium and 3 months of clopi-
dogrel. The advice was given to resume diving six months
after the procedure. At that time, the antiplatelet therapy
was discontinued because it is presumed that full endothe-
lialisation of the atrial wall has taken place [12].
Results
A total of 77 divers were referred to our hospital between
2000 and 2017 for cardiac analyses after a decompression
illness. Ten divers were excluded because decompression
illness was unlikely, one diver did not attend the exam-
ination. Another four divers were excluded because they
suffered from arterial gas embolism (AGE); 62 divers were
analysed with a history of decompression sickness.
In all cases, a transoesophageal echocardiography (TEE)
was performed, showing 29 PFOs and 6 haemodynamically
Neth Heart J
Tab le 1 Patient characteristics and analysis of type of DCS and prevalence of PFO
DCS Total
(n= 62)
PFO/ASD absent
(n= 27)
PFO/ASD present
(n= 35)
PFO/ASD closed
(n= 21)
PFO/ASD not
closed
(n= 14)
Male (%) 58.1 66.7 51.4 57.1 42.9
Mean age (years, range) 38.3 (20–61) 33.0 (20–55) 42.3 (25–61) 44.7 (25–61) 38.8 (30–61)
Typ e 1
Musculoskeletal 2 2 0 0 0
Skin bends 8 3 5 2 3
Typ e 2
Cutis marmorata 15 3 12 10 2
Neurological 26 17 9 3 6
Vestibular 11 2 9 6 3
ASD atrial septum defect, DCS decompression sickness, PFO patent foramen ovale
Fig. 1 Clinical follow-up
0
2
4
6
8
10
12
14
16
PFO/ASD absent
(N=27)
PFO/ASD not closed
(N=14)
PFO/ASD closed
(N=21)
Number of divers
Quit diving
Connued unrestricted diving
Connued restricted diving
Not allowed to dive yet
Minor DCS
Major DCS
not significant ASDs (n= 35 in total: 56%). No other right-
to-left shunts were found. The echocardiographic data are
presented in Tab. 1. We found a high prevalence of PFO
in the subgroup of divers with cutis marmorata (80%) and
vestibular DCS (82%). A PFO or ASD was only found in
35% of divers with neurological DCS.
The mean follow-up duration was 6.8 years (range
0.5–11.6 years). At follow-up, there were 14 divers with an
open PFO. Two of them were lost to follow-up. Four divers
chose to change their diving profile instead of PFO clo-
sure in order to reduce venous bubble load, and continued
diving. In two divers, closure of the PFO was not offered
because they had a history of skin bends, which was later
not considered to be an indication for percutaneous clo-
sure of an PFO. They continued restricted diving as well.
Three divers had other strict contraindications for diving
such as pulmonary bullae or pulmonary emphysema, which
made closing of the PFO irrelevant. One diver decided
to quit diving. One diver, with a minor PFO, continued
unrestricted diving. No recurrence of major DCS occurred.
Two divers experienced minor DCS during follow-up, one
with an unrestricted diving profile and one with restrictions
(Fig. 1).
In 21 divers the PFO or ASD was closed, one of whom
was lost to follow-up. Out of 20 divers, 17 continued div-
ing. Three had changed their diving profile additionally.
In two divers the PFO had been closed recently and they
were not yet allowed to dive. None of the divers experi-
enced recurrence of major DCS after the PFO was closed.
However, one diver experienced minor DCS/skin bends af-
ter PFO closure. Four divers spontaneously reported that,
when looking retrospectively, they might have experienced
multiple minor DCS in the past as well, before the PFO was
closed, which they had not recognised as such at the time.
One diver was no longer diving despite successful closure
of a PFO.
In one diver, paroxysmal atrial fibrillation occurred di-
rectly after closure of the PFO. A TTE with contrast, at
4-month follow-up, did not show any residual shunts among
the treated divers.
Neth Heart J
Fig. 2 Clinical decision making
Patient with
unexplained DCS
TTE shows no ASD
or PFO
TTE shows
haemodynamically
insignificant ASD or
PFO
Patient has no
problem with a
conservative
diving profile or
refrains from
ASD/PFO closure
Patient wishes to
continue
unrestricted
diving, agrees to
ASD/PFO closure
and has no
contraindications
against ASD/PFO
closure
Patient
continues
unrestricted
diving
Conservative
diving profile ASD/PFO
closure
Most divers with no cardiac pathology continued diving
without adjusting their diving profile (55%). In one subject,
recurrence of DCS occurred.
Discussion
This study attempted to establish the efficacy of PFO clo-
sure in patients with a history of DCS. In 20 divers with
a closed PFO, major DCS did not reoccur. All divers were
able to go back to unrestricted diving, although three divers
preferred to continue their diving activities more conserva-
tively. As the present study is descriptive and there is no
comparison group, the efficacy of PFO closure could not
be statistically quantified.
Conservative or restricted diving is generally based on
common-sense advice with regard to decompression safety.
Clear guidelines on restricted diving are lacking. Kling-
mann et al. observed a significant reduction of DCS af-
ter providing the following recommendations: use of nitrox
with decompression times calculated on air tables, no deep
dives ( >25 meters), no repetitive dives, min imisation of Val-
salva manoeuvres, no decompression dives and a 5-minute
safety stop at 3 msw [13].
Currently, the most frequent indication for PFO closure
is the increased risk of cryptogenic stroke, migraine and
vascular headache. The safety and efficacy of percutaneous
closure of PFO has been the subject of several studies.
Three multicentre studies comparing PFO closure to an-
tiplatelet therapy have shown the safety of PFO closure.
These trials found a significantly higher rate of (transient)
atrial fibrillation in the PFO group than in the comparison
group but no differences in serious adverse events [14–16].
In our population, paroxysmal atrial fibrillation occurred in
one patient.
Since the majority of the group with an open PFO either
quit diving or changed to a more conservative diving profile,
it is not possible to compare the group with an open PFO
to the group with a closed PFO with respect to unrestricted
diving. However, in this group no recurrence of major DCS
was seen either.
In the group without PFO or ASD, major DCS reoc-
curred in one subject, which was later attributed to the
complications of sinusitis.
Billinger et al. found no recurrences of major DCI during
long-term follow-up in 26 divers (1,208 dives) who under-
went percutaneous closure of their PFO, which is consistent
with our findings. Yet, a case report has been published
which describes a diver who redeveloped cutaneous DCI
after treatment with a PFO occluder four years earlier [17].
The overall prevalence of right-to-left shunts in this pop-
ulation of divers with undeserved DCS is 56%. This is
higher than expected in the general population (approxi-
mately 27%) [5]. We found a high prevalence of right-to-
Neth Heart J
left shunts in both divers with cutis marmorata (80%) and
in divers with vestibular DCS (82%).
In the present patient group, initially skin bends and cutis
marmorata were considered equally as ‘cutaneous DCS’,
and thus ‘minor DCS’. There is increasing interest in the
aetiology of cutaneous DCS. Kemper et al. proposed that
cutis marmorata may be cerebrally mediated, as they found
an association between cutis marmorata and cardiac right-
to-left shunts [4]. This is consistent with our high preva-
lence of shunts in this population. Also, this new insight
can explain why originally no clear policy was followed
regarding PFO closure in patients with a history of skin
bends. At first, the PFOs of two divers were closed, later
two divers were advised to use a more conservative diving
profile.
In comparison to cutis marmorata and vestibular DCS,
we found a relatively low prevalence of right-to-left shunts
in patients with a neurological DCS (38%). A likely expla-
nation may be that patients with unspecific symptoms such
as fatigue, weakness, nausea, headache and disorientation
were all classified as neurological DCS. However, we did
not find a high prevalence of PFO/ASD in the patients with
more specific neurological symptoms. In our population, no
cases of paralysis or paraplegia occurred.
Conclusion
For divers who had suffered a major DCS, percutaneous
PFO closure may be an effective and safe treatment to re-
turn to unrestricted diving. Alternatively, a restrictive diving
profile seems safe and could be recommended for divers
who refrain from PFO closure (Fig. 2).
Conflict of interest R. Koopsen, P.R. Stella, K.M. Thijs and R. Rienks
declare that they have no competing interests.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
References
1. Baratt DM, Harch PG, Van Meter K. Decompression illness in
divers: a review of the literature. Neurologist. 2002;8:186–202.
2. Lynch JH, Bove AA. Diving medicine: a review of current evi-
dence. J Spec Oper Med. 2009;9:72–9.
3. Wilmshurst PT, Pearson MJ, Walsh KP, Morrison WL, Bryson P.
Relationship between right-to-left shunts and cutaneous decom-
pression illness. Clin Sci. 2001;100:539–42.
4. Kemper TC, Rienks R, van Ooij PJ, van Hulst RA. Cutis marmorata
in decompression illness may be cerebrally mediated: a novel hy-
pothesis on the aetiology of cutis marmorata. Diving Hyperb Med.
2015;45:84–8.
5. Torti SR, Billinger M, Schwerzmann M, et al. Risk of decompres-
sion illness among 230 divers in relation to the presence and size of
patent foramen ovale. Eur Heart J. 2004;25:1014–20.
6. Wilmshurst PT, Morrison WL, Walsh KP. Comparison of the size
of persistent foramen ovale and atrial septal defects in divers with
shunt-related decompression illness and in the general population.
Diving Hyperb Med. 2015;45:89–93.
7. Gempp E, Louge P, Blatteau JE, Hugon M. Risks factors for recur-
rent neurological decompression sickness in recreational divers: a
case-control study. J Sports Med Phys Fitness. 2012;52:530–6.
8. Billinger M, Zbinden R, Mordasini R, et al. Patent foramen ovale
closure in recreational divers: effect on decompression illness
and ischaemic brain lesions during long-term follow-up. Heart.
2011;97:1932–7.
9. Honˇ
ek J, Srámek M, Sefc L, et al. Effect of catheter-based patent
foramen ovale closure on the occurrence of arterial bubbles in scuba
divers. JACC Cardiovasc Interv. 2014;7:403–8.
10. Pearman A, Bugeja L, Nelson M, Szantho GV, Turner M. An audit
of persistent foramen ovale closure in 105 divers. Diving Hyperb
Med. 2015;45:94–7.
11. Wilmshurst P, Walsh K, Morrison L. Transcatheter closure of patent
foramen ovale using the Amplatzer septal occluder to prevent re-
currence of neurological decompression illness in divers. Heart.
1999;81:257–61.
12. Sigler M, Jux C. Biocompatibility of septal defect closure devices.
Heart. 2007;93:444–9.
13. Klingmann C, Rathmann N. Hausmann et al. Lower risk of decom-
pression sickness after recommendation of conservative decom-
pression practices in divers with and without vascular right-to-left
shunt. Diving Hyperb Med. 2012;42:146–50.
14. Mas J, Derumeaux G, Guillon B. Patent foramen ovale closure
or anticoagulation vs. antiplatelets after stroke. N Engl J Med.
2017;377:1011–21.
15. Sondergaard L, Kasner S, Rhodes J, et al. Patent foramen ovale
closure or antiplatelet therapy for cryptogenic stroke. N Engl J Med.
2017;377:1033–42.
16. Saver J, Carroll J, Thaler D, et al. Long-term outcomes of patent
foramen ovale closure or medical therapy after stroke. N Engl J
Med. 2017;377:1022–32.
17. Vande Eede M. Recurrent cutaneous decompression illness after
PFO device implantation: a case report. Undersea Hyperb Med.
2016;43:841–5.
