Post on 21-Feb-2023
Seven lessons from 20 years of
follow-up of intensive careunit survivorsRichard D. Griffithsa and Christina Jonesb
Purpose of review
Through a personal narrative, the authors discuss the
lessons they have learned from 20 years of intensive care
follow-up and rehabilitation.
Recent findings
There is a greater understanding of the legacies of the
physical, psychological and cognitive problems after critical
illness, and new momentum toward developing and
delivering practical care to both survivors of intensive care
and their relatives.
Summary
The need and demand for care after critical illness is now
firmly established.
Keywords
cognitive dysfunction, critical illness, diaries, follow-up,
outcomes, rehabilitation
Curr Opin Crit Care 13:508–513. � 2007 Lippincott Williams & Wilkins.
aDivision of Metabolic and Cellular Medicine, School of Clinical Science,University of Liverpool, Liverpool and bCritical Care Unit, Whiston Hospital,Prescot, Liverpool, UK
Correspondence to Professor R.D. Griffiths, Professor of Medicine (Intensive Care),Division of Metabolic and Cellular Medicine, School of Clinical Science, Universityof Liverpool, Duncan Building, UCD, Daulby Street, Liverpool L69 3GA, UKTel: +44 151 706 4086; fax: +44 151 706 5802; e-mail: rdg@liverpool.ac.uk
Current Opinion in Critical Care 2007, 13:508–513
Abbreviations
ICU in
508
tensive care unit
PTSD p osttraumatic stress disorder� 2007 Lippincott Williams & Wilkins1070-5295
IntroductionThe development of intensive care has allowed the
survival of more patients with complex multiple organ
system failure, but the very nature of this disease process
leaves a legacy of problems that must be addressed
during recovery. For years, intensive care was merely
considered a ‘service stop-over’, and the anaesthetic
intensive care profession, with some exceptions, had little
concern for where the patients came from and went to on
discharge. Follow-up was usually performed by those
involved with the admitting diagnosis and, historically,
there was little impetus to explore whether patients had
specific problems after intensive care that needed atten-
tion during rehabilitation.
In 1985, one author (R.D.G.) was fortunate to join the
oldest medically founded general intensive care unit
(ICU) in the UK (around 1959) where there had been
a history of continuity of care of some medical admis-
sions. Anecdotal evidence suggested that other patients
might also benefit from follow-up, but outcome data
beyond ICU survival were lacking. In 1987, clinical
follow-up of selected patients was started so that in 1988,
in response to a request from the Kings Fund Panel [1],
we could undertake the first UK exploration of the costs
and 6-month morbidity and mortality outcomes from
adult intensive care [2]. Using quality of life measures,
we identified a significant degree of physical and psycho-
logical morbidity at 6 months that contributed to restric-
tion in daily activities and serious disability or distress in
40 and 20% of patients, respectively. These data also
confirmed the limitations associated with assessment of
ICU survival and outcome in isolation. A plethora of
questionnaire-based follow-up information has appeared
over the last two decades and, while showing the many
anticipated challenges facing post-ICU patients, the abil-
ity of these studies to identify unrealized or remediable
issues to improve patient care, was limited. In light of
this, and with coauthor C.J., we established a research-
based clinical follow-up and rehabilitation service in
1990, to develop tools to understand [3] the physical
and psychological sequelae of critical illness, and how
to effectively intervene [4]. Starting within ICU, we
followed the patients on the wards, and as outpatients
at 2, 6 and 12 months [5]. The ability to closely follow-up
the morbidity and mortality outcomes to 6 months also
allowed us to undertake a landmark nutrition study
during the mid-1990s [6].
Lessons from 20 years of follow-up Griffiths and Jones 509
Table 1 Seven lessons from 20 years of follow-up of ICU
survivors
(1) Physical weakness is profound, but recovery is impressive(2) Recall of the ICU and memory difficulties are a problem(3) Acute stress reaction, panic attacks and posttraumatic stress
disorder may be a consequence of memory deficits(4) The withdrawn patient in the ICU may not be depressed, but
may be delirious(5) We do not routinely recognize cognitive dysfunction(6) Relatives have problems too and need help and understanding(7) A prospective nurse and relative kept diary may be used as a
post-ICU therapy
ICU, intensive care unit.
The narrative review presented here describes the
lessons (see Table 1) we have learned over 20 years of
what we call ‘intensive care after-care’ [7,8].
Lesson 1: physical weakness is profound,but recovery is impressiveWe did not appreciate the extent of muscle wasting until
serial muscle biopsy data from the 1990s [9] showed
losses of muscle protein reaching 2%/day [10], and a
mean reduction in fibre area of 4% in the faster type 2
fibres and 3% for the slower type 1 fibres was observed in
ICU survivors [11]. Ultrasound studies confirmed the
masking effect of increased oedema and elucidated
why simple limb girth measurements fail to disclose
the true loss of contractile machinery [12]. Immobility
and absence of the normal stretch and stresses in the ICU
contributed to the muscle injury since passive stretching
alone in neuromuscularly paralysed ICU patients may
reduce protein loss and maintain muscle structure [13].
A large follow-up study of patients with acute respiratory
distress syndrome confirmed that muscle weakness is the
single greatest determinant of outcome and showed that
the time for recovery should be measured in months to
years rather than days to weeks [14].
Critical illness motor and sensory polyneuropathy, while
a marked challenge within ICU, may become a less
important clinical issue in the long-term patient after
critical illness if the muscle bulk rebuilds. Early descrip-
tions of the pathology of these lesions tended to focus on
electrophysiology [15]; however, time has shown that
both muscle and nerve pathology coexist with a spectrum
of tissue involvement [16–18]. Key to appreciating the
pathological changes has been the association with
inflammatory states and the evidence of a vasculopathy
with marked endothelial activation in both nerve [19] and
muscle [20], and the central role that membrane excit-
ability contributes to this dysfunction [21]. Similarities
with diabetic neuropathy has led to the observation that
tight glycaemic control in the critically ill not only
improves survival, but also reduces the incidence of
neuropathy [22].
Major physical mobility problems and the type of
physical aids required after critical illness are predicted
by the duration of mechanical ventilation and length of
stay in the ICU [23]. The recognition of these physical
problems and their management after the ICU requires
detailed follow-up and common sense [24]. For example,
in the most severely affected patients, weakness may
preclude safe swallowing and the ability of the patient to
feed him/herself may prove impossible. The not uncom-
mon clouding of consciousness, confusion and impaired
cognitive function may confound accurate clinical exam-
ination on the ward. Not until the tissue oedema has
resolved can the true extent of muscle wasting be deter-
mined and muscle power correctly referenced to avail-
able muscle bulk. Coexisting joint stiffness may further
limit assessment of power. The most useful clinical
assessments should consider the activities of daily living,
and include rising from the bed and the chair, and the
ability to stand and walk unassisted. Even in the absence
of obvious neurological impairment, profound muscle
wasting results in weakness of the postural muscles
which are crucial for recovery when stumbling. It is for
this reason that a most common complaint is difficulty
walking over rough ground and the provision of different
walking aids, especially in windy conditions, can be of
help. Similarly, patients must be warned at hospital
discharge that while they may have recovered sufficient
strength to climb the stairs, they may lack the strength for
a confident and controlled descent. Alternatively, they
may only have sufficient strength to climb the stairs once
in the day, making a stair assessment prior to hospital
discharge of little practical use.
Physical therapy is the mainstay of fostering recovery and
the principle of a patient-centred rehabilitation manual
that has demonstrated proven benefit in a randomized
controlled trial [25]. Physical rehabilitation should pre-
ferably start within intensive care and is safe to do even
while patients are still ventilated [26]. In very long stay
ICU patients, electromyographic evidence of chronic
denervation may be detected many years later, but very
few have corresponding clinical weakness or important
limitation in activities of daily living at that time point
[27]. Occasionally, some patients with critical illness
polyneuropathy show sensory deficits at 2 months after
ICU discharge; very few ICU patients remain troubled by
this at 6 months. Our anecdotal clinical experience in
follow-up suggests the incidence of severe critical illness
polyneuropathy is reduced compared with that reported
in the late 1980s and early 1990s, but further confirmatory
data are required to quantify this impression.
Exercise is central to the rebuilding of wasted muscle
so other clinical conditions need to be optimized to
foster mobility. Treatment of heart failure, angina, asthma
and joint disease must be complementary. Similarly,
510 Critical care outcomes
psychological problems, especially those that affect
adequate sleep, must be adequately treated. Only in a
very small proportion of patients without preexisting pul-
monary disease does persistent respiratory impairment
impede recovery. The well being of even the most
severely affected chronic obstructive pulmonary disease
patient is improved if they survive the ICU and our success
rate at smoking cessation with a rehabilitation programme
has been impressive [28]. While we were pleased with the
physical recovery in our ICU patients, we realized that the
psychological consequences of lack of memory and recall
were compromising outcomes and this gave us Lesson 2.
Lesson 2: recall of the intensive care unit andmemory difficulties are a problemWe soon realized that many patients do not have a recall
of their illness or ICU stay, and this results in a poor
understanding of their post-ICU physical state and why
they are so weak and easily fatigable. Patients have
commented that they cannot understand why those
around them say they look so good and are doing so well
when they feel so weak. Alteration in physical appearance
also has an important impact, and patients are distressed
by what they see in the mirror if they are not prewarned
and offered an explanation. The most minor of problems
(a new scar) can have great importance if they do not
understand why. Simple explanation of taste changes,
hair loss and skin markings are necessary. A careful
clinical review may identify more serious problems such
as osteoporotic fractures, ossification, joint stiffness,
specific neuropathies, small bladder syndrome and sexual
dysfunction, and each of these require education. Even
before any specific therapy is delivered, the act of provid-
ing an explanation is central. The lack of recall and a
failure to realize how weak they are, especially when
assisted by nurses and physiotherapists while in hospital,
gives patients falsely high expectations of their ability,
and it is often only when they fall or go home that the true
extent of their weakness becomes apparent.
In addition to the lack of appreciation of physical debility
related to their critical illness, we soon recognized that a
patient’s memory and recall of their ICU experience
was severely compromised, and that it may be harmful
to have absent memory for what happened [29]. Many of
the sickest patients have no real factual recall of their
illness or the events immediately preceding it. Major
trauma patients ventilated in intensive care can rarely
remember the accident and severe sepsis patients do not
recall their hospital admission. This memory loss is not
simply confined to the periods of deep sedation, but can
persist intermittently for some time. This loss of a real
factual recall of their illness experience means that they
have gaps in their understanding of what has happened to
both themselves and their family [30]. As a consequence
of this, their expectations for rate of recovery may be
unrealistic and may lead to disappointment, even when
recovery is proceeding well. Even while still in the ICU
and ostensibly awake and aware during recovery, many
patients may not remember faces or any information or
explanation given to them. Memories change with time
and great care must be taken in the interpretation of what
they recall. This latter point may represent an important
limitation in many questionnaire-based studies that use
single time points. In a large follow-up study in Portugal,
Granja et al. [31] obtained 6-month outcome data on
464 out of 1433 patients admitted. Despite some loss
to follow-up, they were able to show that 38% had no
recall of any of their ICU stay. Ninety-three percent of
those whose recall was more intact remembered it as a
calm and friendly environment. Unreal experiences can
be pleasant, unpleasant or sometimes frightening. Fifty-
one percent of patients experienced dreams and night-
mares during their ICU stay; of these, 14% were of such a
character to still disturb their life 6 months later. Dreams,
nightmares, and difficulties in concentrating and remem-
bering recent events were independently associated with
a reduced quality of life. Apart from the observation that
patients did not know what was done to them when they
were unable to give consent [32], we realized there was a
much deeper consequence of having a period of amnesia
replaced by false memories and false experiences [33],
and this led to Lesson 3.
Lesson 3: acute stress reaction, panic attacksand posttraumatic stress disorder may be aconsequence of memory deficitsWe realized that patients may have no real recall of
intensive care and their experience may be replaced
by delusional, often paranoid, memories [34], and that
anxiety and panic attacks were more frequent than we
appreciated [35]. It became apparent that those patients
who experienced uncontrolled nightmares after the ICU
were at greatest risk of converting acute stress and panic
to posttraumatic stress disorder (PTSD). While we recog-
nized that some patients may have only pleasurable
experiences, it was the content of their memories that
could have an impact on their emotions and that prior
experience probably contributed to this. For instance,
only patients of an age to have experienced the reality of
the Second World War had delusions containing military
themes when admitted over a period of intensive media
exposure of a bombing campaign in Kosovo [36]. Con-
trary to the established belief that it was the real factual
experiences of intensive care that were traumatic, we
developed the hypothesis that the traumatic memory
could be of a delusional nature and also demonstrated
that patients who sustain distressing delusional experi-
ence without any real, factual experience were at
increased risk of developing acute stress reactions that
may progress to PTSD [37]. The key to this was realizing
that the delusional experiences appear very real and
Lessons from 20 years of follow-up Griffiths and Jones 511
frightening while the absence of real experience denies
them the protective reassurance and feeling of safety
provided by a contact with a nurse or other ICU staff.
Procedures that we may think unpleasant and distressing
may not be recalled or their impact may not be considered
distressing because they are associated with human con-
tact, support or comfort (e.g. endotracheal suctioning).
We underestimated that there was a feeling of safety for a
patient to see a nurse around them frequently. It is
important to stress that particular delusional beliefs by
patients that something happened may be very strongly
held even if they can be shown to be completely ficti-
tious. In addition, many so-called real experiences may
be misinterpreted. The suggestion that being awake and
aware was in some way protective against PTSD was
suggested through a retrospective study of a subgroup of
patients who had undergone sedation breaks [38]. The
prevalence of PTSD is difficult to ascertain and varies
considerably across published studies (5%–63%) and this
may reflect patient case mix, and the use of different
PTSD symptom scores and diagnostic tools [39��]. In a
recent observational study involving five ICUs across four
countries in Europe, the rate of defined PTSD was 9.2%
(range 3.2–14.8%) [40��]. Independent of case mix and
illness severity, the factors found to be related to the
development of PTSD were recall of delusional mem-
ories, prolonged sedation, a history of preexisting psycho-
logical problems such as anxiety or depression and
physical restraint with no sedation. Curiously, those with
PTSD related to physical restraint had no recall of their
restraint, suggesting that it may be related to a state of
delirium. The incidence of delirium varied between units
and its development was more common in patients
receiving high daily doses of benzodiazepines or opiates.
We realized that we were under-recognizing delirium and
that led us to Lesson 4.
Lesson 4: the withdrawn patient in theintensive care unit may not be depressed, butmay be deliriousThe general belief that the withdrawn patient in the
ICU was depressed had never been formally tested, yet
antidepressants were being used liberally; however, the
extent of the memory problems coupled with delusional
experiences that had occurred in quiet withdrawn
patients made us appreciate that perhaps we were
missing patients with hypoactive delirium. This was
illustrated by a withdrawn yet cooperative patient who
suffered a Capgas delusion where, due to a failure of face
recognition, she developed the delusion that her family
and nurses had all been replaced by aliens [41]. It is now
recognized that using bedside screening tools [42], the
incidence of delirium in some groups of patients is as high
as 80% [43] and it is the hypoactive form that dominates,
particularly in the elderly [44��]. Assessing the incidence
of delirium is challenging and limited by the nature of the
screening tool and patient case mix. In a large mixed ICU
population, 31.8% of 764 patients developed delirium
[45��], and a history of hypertension, alcoholism, severity
of illness and sedative/analgesia use increased this risk.
The recognition that there is an association between the
presence of delirium and development of later cognitive
problems [46] attests to the central nervous system being
involved in multiple organ failure, and leads to Lesson 5.
Lesson 5: we do not routinely recognizecognitive dysfunctionIncreasingly, post-ICU cognitive deficits are being
described. In both a 1- and 2-year follow-up of acute
respiratory distress syndrome survivors, half (47%) had
neurocognitive impairment at 1 year and, despite some
improvement, this persisted to 2 years [47]. Strikingly
persistent deficits occurred in memory and attention,
such that patients had problems in making decisions
and quick processing leading to ‘slips of action’, e.g.
putting the kettle on without filling it with water. In
addition, deficits were noted in executive functioning. A
detailed study of 51 patients [48] demonstrated similar
defects in executive function at 3 and 9 months after
ICU discharge. At 3 months, one-third of the patients
were functioning at a level equivalent to or below
the lowest performing 5% of a normal population. At
9 months, 4% were so severely impaired that performance
was still below normal. The question of whether cogni-
tive dysfunction was adequately recognized and its
natural history once detected was studied in a cohort
of 150 general ICU patients (length of stay greater than
6 days) who were awake, ventilated through a tracheost-
omy and screened for delirium using the Confusion
Assessment Method for the Intensive Care Unit [49��].
Only 20% of these patients were found not to be delirious
and had sufficient attention to undertake the touch-
screen computerized Cambridge Neuropsychological
Test Automated Battery. These patients, however, still
showed significant problems with strategic thinking and
problem solving with scores below the 25 centile for
normal performance. These patients did not fulfil criteria
for delirium (as stated previously), had no obvious neuro-
logical signs and were not giving rise to any clinical
concern. One week post-ICU discharge, 20% still could
not solve any problems and half had memory deficits. At
2 months, 50% still demonstrated difficulties with pro-
blem solving, while a third remained below the 25 centile
for performance. The impact of neurocognitive dysfunc-
tion and the resultant dependence of ICU patients on
relatives for assistance became even more apparent, and
led us to Lesson 6.
Lesson 6: relatives have problems too andneed help and understandingThat relatives may be very stressed by their experience
during ICU is well recognized, but we realized that this
512 Critical care outcomes
had later consequences and might affect the caregivers’
ability to act as support during recovery [50]. A frequent
early observation from our group was that a conflict arises
during recovery between the patient who does not
appreciate the severity of the illness due to a limited
or distorted recall and the relative who is stressed by the
reality of the life-threatening illness and vivid recall of
events. This may result in the relative being frightened of
a recurrence of the critical illness, an inability to discuss
the events in ICU and the behaviour of being overly
protective to the point of compromising rehabilitation
[51]. We recognized early that relatives also need help to
cope, and designed the rehabilitation package to include
their participation and encourage their joint attendance at
clinic follow-up [25].
An additional problem for recovering patients is that
family members can also develop PTSD. During a reha-
bilitation study we observed that at 6 months a significant
proportion of relatives (49%) expressed very high levels
of the symptoms related to PTSD [52], and that there was
a close relationship between symptom levels in patients
and their relatives. This is not surprising considering the
extreme stress and life-threatening experience they
witness, but the increased incidence may also reflect
familial risks. Another study showed that a third of family
members interviewed 3 months after ICU exhibited
stress symptoms consistent with a risk of developing
PTSD [53]. We realized the importance of family invol-
vement at all stages and that they could do things to
benefit the patient, and this led us to our final lesson.
Lesson 7: a prospective nurse and relativekept diary may be used as a post-intensivecare unit therapyOne solution to ease the conflict in recall between the
patient and relative, and to enable them both to have a
common shared ownership of the experience, comes
through keeping a diary with photographs while the
patient is in the ICU. This idea originated from Sweden
[54]. The diary should be written prospectively by staff
and family, and is given to the patient afterwards when
they are ready. The language used is everyday and any
medical words are explained. Periods of confusion or
agitation are also written about with possible reasons
for these. A small pilot study showed that patients felt
that the diary helped them come to terms with their
illness and recall what had happened [55]. The ICU diary
helps fill in the lost time for those with poor recall of the
ICU stay. The experience of such diaries continues to be
encouraging and contribute to patients’ understanding,
goal setting during recovery, improved family communi-
cation and is a source of comfort for the bereaved [56].
During an observational study, we noticed that the pro-
vision of an ICU dairy may reduce the level of symptoms
of PTSD experienced by patients after critical illness
[57]. Currently, we are involved in a multicentre ran-
domized European study by the RACHEL group to
explore the application and timing of diary use as an
interventional therapy to improve neuropsychological
outcomes. The proposed mechanism for its benefit is
as a natural cognitive behavioural therapy where patients
read their diary over and over of their own accord, and in
doing so reduce the ability of their memories to cause
them distress. If proven, this may provide the ICU team
with a powerful tool to help patients come to terms with
their illness and participate in cognitive behavioural
therapy.
ConclusionIntensive care leaves a physical and neuropsychological
legacy for patients and relatives. Our 20-year experience
from patient and carer feedback suggests that active
support and rehabilitation for patients and family care-
givers is much needed following intensive care.
References and recommended readingPapers of particular interest, published within the annual period of review, havebeen highlighted as:� of special interest�� of outstanding interest
Additional references related to this topic can also be found in the CurrentWorld Literature section in this issue (p. 607).
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39
��Jackson JC, Hart RP, Gordon SM, et al. Posttraumatic stress disorder andposttraumatic stress symptoms following critical illness in medical ICUpatients: assessing the magnitude of the problem. Criti Care 2007; 11:R27.
A review of the very mixed and varied published evidence, concluding that whilePTSD is clearly a problem its true incidence is yet to be defined.
40
��Jones C, Backman C, Capuzzo M, et al. Precipitants of post-traumatic stressdisorder following intensive care: a hypothesis generating study of diversity incare. Intensive Care Med 2007; 33:978–985.
A new study from several European sites that explores the various precipitants ofPTSD, reflecting the differences in sedation and restraint practice within Europe.
41 Jones C, Griffiths RD, Humphris GM. A case of Capgras delusion followingcritical illness. Intensive Care Med 1999; 25:1183–1184.
42 Ely EW, Margolin R, Francis J, et al. Evaluation of delirium in critically illpatients: validation of the Confusion Assessment Method for the IntensiveCare Unit (CAM-ICU). Crit Care Med 2001; 29:1370–1379.
43 Ely EW, Gautam S, Margolin R, et al. The impact of delirium in the intensivecare unit on hospital length of stay. Intensive Care Med 2001; 27:1892–1900.
44
��Peterson JF, Pun BT, Dittus RS, et al. Delirium and its motoric subtypes:a study of 614 critically ill patients. J Am Geriatr Soc 2006; 54:479–484.
A large study that helpfully describes the forms of delirium we can expect to see.Reminds us that in the elderly the hypoactive form is much more common and withthe increasing numbers of elderly being admitted to ICU the incidence will onlyincrease.
45
��Ouimet S, Kavanagh BP, Gottfried SB, Skrobik Y. Incidence, risk factors andconsequences of ICU delirium. Intensive Care Med 2007; 33:66–73.
A very large population studied using a different screening tool that confirms riskfactors and associations, and that about one-third of patients will experiencedelirium.
46 Jackson JC, Hart RP, Gordon SM, et al. Six-month neuropsychologicaloutcome of medical intensive care unit patients. Crit Care Med 2003; 31:1226–1234.
47 Hopkins RO, Weaver LK, Pope D, et al. Neurophysiological sequelae andimpaired health status in survivors of severe acute respiratory distresssyndrome. Am J Respir Crit Care Med 1999; 160:50–56.
48 Sukantarat KT, Burgess PW, Williamson RCN, Brett SJ. Prolonged cognitivedysfunction in survivors of critical illness. Anaesthesia 2005; 60:847–853.
49
��Jones C, Griffiths RD, Slater T, et al. Significant cognitive dysfunction innondelirious patients identified during and persisting following critical illness.Intensive Care Med 2006; 32:923–926.
Tests used touch screen computer software and showed severe cognitivedysfunction in awake non sedated patients ventilated through tracheostomieswho were not delirious at the time of testing (although most likely had beendelirious at some stage since many had to be excluded from study due to ongoingdelirium).
50 Jones C, Hussey R, Griffiths RD. Social support in the intensive care unit. Br JIntensive Care 1991; 1:66–69.
51 Jones C, Griffiths RD. Social support and anxiety levels in relatives of criticallyill patients. Br J Intensive Care 1995; 5:44–47.
52 Jones C, Skirrow P, Griffiths RD, et al. Post-traumatic stress disorder-relatedsymptoms in relatives of patients following intensive care. Intensive Care Med2004; 30:456–460.
53 Azoulay E, Pochard F, Kentish-Barnes N, et al. Risk of posttraumatic stresssymptoms in family members of intensive care unit patients. Am J Respir CritCare Med 2005; 171:987–994.
54 Backmann CG, Walther SM. Use of a personal diary written on the ICU duringcritical illness. Intensive Care Med 2001; 27:426–429.
55 Bergbom I, Svensson C, Berggren E, Kamsula M. Patients’ and relatives’opinions and feelings about diaries kept by nurses in an intensive care unit:pilot study. Intensive Crit Care Nurs 1999; 15:185–191.
56 Combe D. The use of patient diaries in an intensive care unit. Nurs Crit Care2005; 10:31–34.
57 Jones C, Capuzzo M, Flaatten H, et al. ICU diaries may reduce symptoms ofposttraumatic stress disorder. Intensive Care Med 2006; 32 (Suppl 1):S144.