Commentary from the Italian Association

Sleep Medicine

journalhomepage:www.elsevier.com/locate/sleep

SPECIAL SECTION

Commentary from the Italian Association of Sleep Medicine on the AASM manual for the scoring of sleep and associated events: For debate and discussion q

Liborio Parrino a,*,1

, Raffaele Ferri d,1 , Marco Zucconi , Francesco Fanfulla

b,1

c,1

b Sleep Disorders Center, Department of Neurosciences, University of Parma, Italy Sleep Research Center, Department of Neurology I.C., Oasi Institute for Research on Mental Retardation and Brain Aging (IRCCS), Troina, Italy

d Sleep Disorders Center, Department of Neurology, Scientific Institute and University Ospedale San Raffaele, Vita-Salute University, Milan, Italy Sleep Center, Pulmonary Division, Istituto Scientifico di Pavia, Fondazione S. Maugeri, IRCCS, Italy

article info

abstract

Article history: In 2007, the American Academy of Sleep Medicine (AASM) completed a new manual for the scoring of Received 24 October 2008

sleep and associated events. The AASM manual is divided into separate sections relative to the parame- Received in revised form 16 May 2009

ters reported for polysomnography. The present commentary, accomplished by a Task Force of the Italian Accepted 22 May 2009

Available online 28 June 2009 Association of Sleep Medicine, focuses on sleep scoring data, arousal rules, movement and respiratory events. Comparisons with the previous Rechtschaffen and Kales system are detailed and a number of

Keywords: methodological weaknesses are pointed out. Major comments address the 30-s scoring epochs, the

restrictive approach to arousals and EEG activating patterns, the incomplete quantification of motor Sleep

Scoring rules events and the thresholds for the definition of hypopnea. Since the new AASM manual is an iterative pro- Arousals

cess, proposals for discussion and re-examination of the agreed criteria with other national and interna- CAP

tional organizations are encouraged.

Sleep-related movements Ó 2009 Elsevier B.V. All rights reserved. Respiratory events

1. Prologue process which broadly represents current knowledge and expertise in the field. Besides the rules for sleep staging and arousals, agree-

In June 2007, the American Academy of Sleep Medicine (AASM) ment was acheived for cardiac, movement and respiratory events, completed a new manual for the scoring of sleep and associated

and for the first time, criteria for sleep in children were detailed. events [1] . The manual, presented during the 21st Annual Meeting

The rules and specifications in the visual scoring, however, re- of the Associated Professional Sleep Societies, was preceded by the

tain much of the framework of Rechtschaffen and Kales (R&K) rules March 2007 issue of the Journal of Clinical Sleep Medicine compris-

[3] , and this reverberates negatively upon the entire arrangement ing seven evidence-based review articles [2] . Each article was orga-

of the manual. Software and hardware companies have been in- nized to provide a historical perspective, a review and evidence

volved in polysomnography data acquisition and scoring, but sleep grading the validity or reliability of measures and a discussion of fu-

is still interpreted as a discontinuous process artificially divided in ture areas for research. Over 1500 total articles were reviewed

discrete standardized epochs. This approach is different from pub- reflecting the PubMed literature on human studies published in Eng-

lished material and clinical evidence, which in the past decades has lish between 1968 and 2004. Under the overall supervision of a

emphasized the necessity to use alternative scoring methods. Re- steering committee, the task force members developed a consensus

cently, Schulz [4] published a contribution provocatively entitled ‘‘Rethinking sleep analysis.” In this perspective, the Italian school has always supported the R&K stage definition approach, which,

q In order to generate a healthy discussion and debate to promote scientific however, needs to be implemented by analysis of the continuity progress we are inviting comments from the readership as Letters to the Editor

and consolidation of sleep to recover most of the information ne- which will be published in subsequent issues of the journal after appropriately editing the contents.

glected by the conventional scoring measures. A more dynamic ap- * Corresponding author. Address: Clinica Neurologica – Centro di Medicina del

proach is not limited to arousals and cyclic EEG patterns during Sonno, Università deglI Studi, Via Gramsci, 14, 43100 Parma, Italia. Tel./fax: +11 39

sleep, but also includes motor and respiratory events, which have 521 287913.

been demonstrated to undergo ordered sequences in a number of 1 E-mail address: liborio.parrino@unipr.it (L. Parrino).

pathological conditions such as periodic limb movements and Task Force on the AASM Manual for the Scoring of Sleep and Associated Events on

sleep apnea syndrome.

behalf of the Governing Board of the Italian Association of Sleep Medicine: Franco

Ferrillo (President), Gian Luigi Gigli (Vice-President), Liborio Parrino (Secretary), Since the new AASM scoring manual is an iterative process, Alberto Braghiroli (Treasurer).

future editions of the manual will undoubtedly require a 1389-9457/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.sleep.2009.05.009

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

re-examination of evidence to include additional elements and ad- according to the AASM standard compared with those obtained dress the rapidly evolving science of the metrics of examining

from R&K rules. These authors have shown that inter-rater reliabil- sleep. The present commentary, carried out by an ad hoc task force

ity was higher for scorings according to the AASM standard only for of the Italian Association of Sleep Medicine, was written in a per-

stages W, N1 and R, with only a small increase, even if statistically spective of acknowledgement and integration.

significant; inter-rater reliability was essentially the same for N3/ SWS. On the contrary, inter-rater reliability for N2/S2, the stage

2. Sleep stages: the unsolved problem in which both normal controls and patients usually spend the majority of their time asleep, was decreased with the new AASM

The standardized R&K criteria for sleep staging set up in 1968 rules compared to that obtained from R&K rules. Moreover, these [3] have constituted the only internationally accepted system for

results were obtained in conditions potentially able to inflate the sleep scoring for almost 40 years, and an enormous body of data

AASM scoring agreement when compared to R&K, as the same has been produced and published in the scientific literature with

authors also express in their paper. The reasons considered to be this system. The new AASM manual [1] has the scope to revise

at the basis of the decrease in inter-rater reliability for N2/S2 are R&K sleep staging and to address digital methodology as well as

likely to be connected with the low inter-rater reliability which the scoring of arousals, respiratory events, sleep related movement

characterizes the detection of arousals [7] , events that have as- disorders, and cardiac abnormalities, with consideration of pediat-

sumed a crucial role in determining the end of N2 in the new AASM ric and geriatric age groups. The work accompanying the decisions

rules but still with a poor definition (see below). Regarding the on the new rules showed that, using the R&K system, inter-rater

introduction of a frontal derivation in the EEG channel set needed accuracy was highest for REM sleep, followed by stage 2 sleep,

for sleep scoring, the inter-rater reliability for N3/SWS has not and lowest for stage 1 sleep, while reliability for wake and slow

changed, probably because of the persisting rule of the 75 l V

wave sleep (SWS) was moderate. Accordingly, scoring rules for amplitude for slow waves, a merely conventional value not based stage 1 and SWS required reassessment [5] . Table 1 compares

on any physiologically sound basis. Finally, it should be noted that, the major sleep staging rules in the two systems.

even if inter-rater reliability for N1 was significantly increased, it Compared to the R&K system, the AASM rules extend the

still remained far below that obtained for other sleep stages, indi- recording requirements with specifications that take into full ac-

cating a disappointing ‘‘moderate” degree of agreement. count the current standard techniques for recording and storing

Silber et al. [5] stated, ‘‘Scoring rules for stage 1 and SWS sleep biological signal. The visual scoring of sleep now needs to be per-

needed reassessment”; based on the considerations and results re- formed on at least three EEG channels, including frontal and occip-

ported above, we can affirm that the reassessment proposed by the ital derivations, besides the classical EOG and EMG channels. This

AASM has not been followed by the expected improvement in in- corrects the single central derivation number of channels indicated

ter-rater reliability of these stages.

in the R&K rules and allows a more extensive coverage of scalp In the new AASM system, the distinction between wakefulness areas where significant sleep/wake rhythms and waveforms are

(W), non-REM sleep (N) and REM sleep (R) is maintained, but the better represented, such as K-complexes and delta waves. Even if

non-REM stages are reduced to three: N1 (previous stage 1), N2 this choice keeps the costs of polysomnography low to favor its

(previous stage 2), N3 (previous stages 3 + 4). The new rules are use in large clinical populations, this minimal set of EEG deriva-

meant to have a major impact on everyday clinical and research tions surely does not satisfy research purposes. An alternative with

practice and will play a topical role in the field of sleep medicine

a higher number of EEG channels might have been indicated, with in the next years. Nevertheless, they have been established on a the advantage of standardizing at least some research applications

low degree of evidence. This evidence was not present in the scien- of polysomnography.

tific literature, and a more convincing way to proceed, before the It is interesting to notice that each rule of the new AASM man-

final establishment of rules, should have included a careful multi- ual is accompanied by a recommendation level ([RECOMMENDED],

center statistical validation. Without these premises, the new rules [ALTERNATIVE], or [OPTIONAL]), and each recommendation is

are simply a stab in the dark and very unlikely to provide better associated with a procedural note classified into 4 classes, depend-

performance; more importantly, they do not support or facilitate ing on the five levels of evidence contained in the publications

a more reliable automatic computer implementation compared which were taken into account to establish each rule [1] . The four

to the R&K criteria. The sleep medicine community needs to be classes are [STANDARD] – recommendation based on level 1 evi-

supported by new, statistically driven data and procedures which dence or overwhelming level 2 evidence; [GUIDELINE] – recom-

should probably be set in new, large studies that are somewhat mendation based on level 2 evidence or a consensus of level 3

free from the errors of the past. Considering studies essentially evidence; [CONSENSUS] – recommendation with less evidence

based on a single system carries the serious danger of creating a vi- than guideline for which agreement was reached in a standardized

cious circle which generates self-similar products (with the same consensus process based on available information; and [ADJUDI-

errors), prohibiting new ideas to break through. CATION] – recommendation from the steering committee based

Alternative sleep state classification systems have been pro- on all available information; adjudication was only performed (a)

posed in the literature, such as those proposed by Steriade and when there was insufficient evidence and no consensus agreement

McCarley [8] and further refined by Hobson et al. [9] and Massa- or (b) in conjunction with task force leaders on issues regarding

quoi and McCarley [10] , or the older proposal by Koella [11] , which minor clarifications and additions to rules. For the visual scoring

started from a neurophysiological model of sleep rather than its of sleep, 29 rules were established with only three supported by

simple polygraphic pattern (see [4] for a thoughtful comment on

a recommendation based on a [STANDARD] level procedure, none this topic). These systems, however, have never seen a wide-scale was classified as [GUIDELINE], the vast majority was supported

application or been evaluated by independent experts for their by a [CONSENSUS] procedure, one was classified as [CONSENSUS/

eventual validity in sleep clinical and research applications. None- ADJUDICATION] and only two reached [ADJUDICATION] level. In

theless, for all the reasons above, the comment on the new visual this section of the manual, these levels seem to be very low and

rules is essentially negative, and the application of these new rules fuel the concerns of the impact of these new rules on the major

does not seem to be supported by a sufficient degree of evidence. problem of visual scoring, i.e., inter-rater and intra-rater variabil-

A second problem is the compatibility of the enormous amount ity. This concern is confirmed by a very recent report by Danker-

of data produced in the past with the results of new analyses based Hopfe et al. [6] on inter-rater reliability of the expert scorings

on the AASM rules. Are we ready and willing to disregard all this

801 Table 1

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

Sleep stage scoring rules (simplified). Rechtschaffen and Kales [3]

Waking 50% of the page (epoch) consists of alpha (8 13 Hz) activity or low voltage, mixed (2 7 Hz) frequency activity Stage 1

50% of the epoch consists of relatively low voltage mixed (2 7 Hz) activity, and <50% of the epoch contains alpha activity. Slow rolling eye movements lasting several seconds often seen in early stage 1

Stage 2 Appearance of sleep spindles and/or K-complexes and <20% of the epoch may contain high voltage (>75 l V, <2 Hz) activity. Sleep spindles and K-complexes each must last >0.5 s Stage 3

20 50% of the epoch consists of high voltage (>75 l V), low frequency (<2 Hz) activity Stage 4

>50% of the epoch consists of high voltage (>75 l

V) <2 Hz delta activity

Stage REM Relatively low voltage mixed (2 7 Hz) frequency EEG with episodic rapid eye movements and absent or reduced chin EMG activity

Iber et al. [1] Stage W

A. Score epochs as stage W when more than 50% of the epoch has alpha rhythm over the occipital region B. Score epochs without visually discernable alpha rhythm as stage W if any of the following are present

(1) Eye blinks at a frequency of 0.52 Hz (2) Reading eye movements (3) Irregular conjugate rapid eye movements associated with normal or high chin muscle tone

Stage N1 A. In subjects who generate alpha rhythm, score stage N1 if alpha rhythm is attenuated and replaced by low amplitude, mixed frequency activity for more than 50% of the epoch B. In subjects who do not generate alpha rhythm, score stage N1 commencing with the earliest of any of the following phenomena (1) Activity in the range 4–7 Hz with slowing of background frequencies by P1 Hz from those of stage W (2) Vertex sharp waves (3) Slow eye movements

Stage N2 A. The following rule defines the start of a period of stage N2 sleep (1) Begin scoring stage N2 (in absence of criteria for N3) if l or both of the following occur during the first half of that epoch or the last half of the previous epoch a. One or more K-complexes unassociated with arousals b. One or more trains of sleep spindles

B. The following rule defines continuation of a period of stage N2 sleep (1) Continue to score epochs with low amplitude, mixed frequency EEG activity without K-complexes or sleep spindles as stage N2 if they are preceded by (a) K-complexes unassociated with arousals or (b) sleep spindles

(1) End stage N2 sleep when 1 of the following events occurs a. Transition to stage W b. An arousal (change to stage N I until a K-complex unassociated with an arousal or a sleep spindle occurs) c. A major body movement followed by slow eye movements and low amplitude mixed frequency EEG without non-arousal associated K-

complexes or sleep spindles d. Transition to stage N3 e. Transition to stage R

Stage N3 Score N3 when 20% or more of an epoch consists of slow wave activity (waves of frequency 0.5–2 Hz and peak-to-peak amplitude >75 l V, measured over the frontal regions), irrespective of age Stage R

A. Score stage R sleep in epochs with all the following phenomena a. Low amplitude, mixed frequency EEG b. Low chin EMG tone c. Rapid eye movements

B. The following rule defines the continuation of a period of stage R sleep Continue to score stage R sleep, even in the absence of rapid eye movements. For epochs following 1 or more epochs of stage R as defined in A above, if the EEG continues to show low amplitude, mixed frequency activity without K-complexes or sleep spindles and the chin EMG tone remains low

C. The following rule defines the end of a period of stage R sleep (1) Stop scoring stage R sleep when 1 or more of the following occur a. There is a transition to stage W or N3 b. An increase in chin EMG tone above the level of stage R is seen and criteria for stage N1 are met c. An arousal occurs followed by low amplitude, mixed frequency EEG and slow eye movements d. A major body movement followed by slow eye movements and low amplitude mixed frequency EEG without non-arousal associated K-

complexes or sleep spindles e. One or more non-arousal associated K-complexes or sleep spindles are present in the first half of the epoch in the absence of rapid eye movements, even if chin EMG tone remains low D. Score epochs at the transition between stage N2 and stage R as follows (1) In between epochs of definite stage N2 and definite stage R, score an epoch with a distinct drop in chin EMG in the first half of the epoch to the level seen in stage R as stage R if all of the following criteria are met, even in the absence of rapid eye movements a. Absence of non-arousal associated K-complexes b. Absence of sleep spindles

(2) In between epochs of definite stage N2 and definite stage R, score an epoch with a distinct drop in chin EMG in the first half of the epoch to the level seen in stage R as stage N2 if all of the following criteria are met a. Presence of non-arousal associated K-complexes or sleep spindles b. Absence of rapid eye movements

(3) In between epochs of definite stage N2 with minimal chin EMG tone and definite stage R without further drop in chin EMG tone, score epochs as stage R if all of the following are met, even in the absence of rapid eye movements a. Absence of non-arousal associated K-complexes b. Absence of sleep spindles

information stored in our databases? Are we really ready to throw sleep architecture follow-up study? Rescoring old recordings is the baby away with the bath water? Is this information really use-

now impossible if we have not recorded at least one frontal, one less now? Should we now wait long before we can have a serious

central and one occipital channel; thus the new rules limit the

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

use of previous recordings, and completely new databases need to power of the EEG delta band [23] . Instead of including enriching

be collected. Preliminary studies show significant differences be- information on the power of the EEG signal, the adopted solution tween sleep parameters derived from visual sleep scoring on the

is a reductive simplification of the previous sleep stages; obliterat- basis of the R&K rules and those based on the new AASM criteria.

ing the exponential profile of process ‘‘S,” the restorative function In particular, the time spent in N1 and N3 increases, while N2 de-

of slow wave sleep and its direct relationship with the waking creases significantly. Moreover, wake after sleep onset is pro-

activities are shadowed.

longed, while sleep latency, REM latency, total sleep time and The presentation of arousal confirms the definition established sleep efficiency seem to be little affected [12] .

in 1992 by the American Sleep Disorders Association (ASDA; since Finally, it is necessary to spend some words on the effects of

named the AASM) [24] . According to the original framework, sleep fragmentation into epochs. It has been clear for years that

arousals are markers of sleep disruption representing a detrimen- each sleep epoch of 30 s encompasses several short-time events

tal and harmful feature for sleep. For this reason they were ex- which carry important information not showing up in the classical

cluded from the conventional staging procedures. Several papers sleep staging reports. These features (K-complexes, sleep spindles,

have been written in the last 16 years, since the scoring rules for delta bursts, etc.) have been grouped under the label of sleep pha-

arousal were established [24] , but no substantial update has been sic events, and the most comprehensive method for their analysis

provided.

and report is the so-called Cyclic Alternating Pattern (CAP) [13] .

A number of studies have established that spontaneous arousals CAP cannot be measured without having scored sleep stages in ad-

are natural guests of sleep and undergo a linear increase along the vance; however, it is not limited to epoch fragmentation and spans

life span following the profile of maturation and aging [25–27] . over long periods of NREM sleep. Perhaps the sleep community is

Moreover, the spectral composition of arousals [28] and their seeking a breath of fresh air with a serious discussion on alterna-

ultradian distribution throughout the sleep cycles reveal that tive methods which overcome the boundaries of rigid epochs.

arousals are endowed within the texture of physiological sleep The new system should start from the consideration that sleep is

[29–31] under the biological control of REM-on and REM-off mech-

a continuous function [4,13] , including stages and cycles, but with-

anisms [32] .

out restricting a complex dynamic process into a static sequence of According to these indications, arousal scoring is now consid- 30-s artificial segments.

ered a fundamental process in staging classification as well as spin- There are many studies in the literature attempting to over-

dles and K-complexes. However, in the R&K system [3] , a K- come the limitations of the fixed-length epoch segmentation based

complex, with or without an arousal, was unmistakably a marker on different approaches, such as those proposing to represent

of sleep stage 2. According to the AASM manual, if a K-complex NREM sleep with a continuous function [14–16] and those based

is associated with an arousal the epoch is scored as N1. In other on variable-length segmentation techniques and followed by clus-

words, the R&K approach privileged the role of EEG synchrony in ter analysis [17–22] . Again, none of these methods has ever been

the scoring process, while the AASM manual enhances the impact tested in large numbers of sleep recordings and cannot be consid-

of EEG desynchrony.

ered as valid alternatives until this type of validation is carried out; If the brain is able to produce a K-complex this means that sleep however, it is also important to reemphasize here that the newly

has reached the threshold of what is arbitrarily classified as stage proposed AASM rules are not supported by any validation study.

2. A K-complex can be followed by other K-complexes, and, in that Thus, it seems reasonable to propose that the new AASM rules

case, stage 2 tends towards consolidation; or it can be followed by should not be used for sleep staging in replacement of the R&K

an arousal which reflects a regression towards a shallower neuro- rules because they have failed to introduce significant improve-

physiological condition. Most arousals (87%), however, are pre- ments, and, for this reason, they do not justify the necessary tech-

ceded by a K-complex or delta burst [28] , indicating that sleep nical, economic, clinical and scientific sacrifices that are needed to

can become transiently lighter without necessarily changing stage. pass from one system to the other. This does not imply that the

This is exactly what happens with major body movements, which R&K system should be kept for a long time, but points to the urgent

are scored by the AASM manual as N2 if the previous epoch is N2 need for serious international effort for a reliable, neurophysiologi-

and there are no slow eye movements [1] . The methodological cally-based, data-driven, computer-compatible system for sleep

weakness of the AASM system is confirmed by the lack of scoring scoring.

instructions on the occurrence of an arousal in an epoch with at least 20% of slow wave activity. Shall such an epoch be classified

3. Arousal rule: is something missing? as N3 or N1? Perhaps, a simple distinction between consolidated and unstable sleep would have been a more appropriate solution

It must be recognized that the new AASM manual dedicates

extensive attention to REM sleep. An epoch can be scored as R only Further problems are raised by the definition [1] : ‘‘Begin scoring with the following coexisting phenomena: low amplitude mixed

N2 if one or more K-complexes not associated with arousals occur frequency EEG, low chin EMG tone, and rapid eye movements.

during the first half of the epoch or the last half of the previous After a clear cut onset of REM sleep, the following epochs are

epoch.” The split of each epoch in first half and second half frankly scored as R if the EEG remains unmodified and muscle tone is

appears as an arbitrary time-consuming procedure, which proba- not restored in the first half of the epoch regardless of the occur-

bly tries to attenuate the rigid division in 30 s segments. rence of rapid eye movements. This definition seems to overcome

Finally, the original scoring of an arousal during REM sleep re- some of the previous constraints, such as the 3-min absence of ra-

quired a concurrent increase in submental EMG amplitude. In the pid eye movements (the period of time between 2 spindles or K-

new AASM manual [1] , the increase in submental EMG amplitude complexes with a low voltage mixed EEG was previously scored

must last for at least one second. This is because EMG increase can as stage 2 if the interval was <3 min and without rapid eye move-

provide better scoring reliability during all sleep stages, particu- ments [3] ).

larly comparing REM sleep vs. light sleep [34] . But data were In contrast, the role of the homeostatic process ‘‘S” is unexpect-

collected from OSA patients where the respiratory-driven muscle edly omitted in the new methodological framework. Stages 3 and 4

activation in REM sleep can differ from normal conditions. are now lumped together in a single stage N3, in contrast to the

The approach to arousals during sleep would be better nocturnal development of the process ‘‘S,” characterized by

conceived not as static single events but rather as a dynamic decreasing peaks across the night, according to the decreasing

process in which activating phenomena of different intensity and

803 morphology can be organized into sequences [35] . This extensive

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

movements. Besides periodic limb movements (PLMs), scoring cri- interpretation of arousals and their non-random distribution into

teria have also been established for the more frequent bruxism, periodic sequences converges on CAP, which represents a struc-

REM sleep Behavior Disorder (RBD), and Rhythmic Movement Dis- tured organization of sleep beyond the static stage setting

order (RMD), and for other less common movement disturbances, [36,37] . In the review chapter on the scoring of the AASM manual

such as Alternating Leg Movement Activation (ALMA), Hypnagogic [7] , the authors state that ‘‘reliable scoring of arousals is a difficult

Foot Tremor (HFT), and Excessive Fragmentary Myoclonus (EFM). and time-consuming process.” Nevertheless, identification of arousals has become mandatory in the new classification. In the

4.1. Limb movements

same chapter, the authors state that ‘‘measurement of CAP is more time consuming than scoring of ASDA arousals,” although ‘‘it can

The R&K manual [3] contained only rules for sleep stage scoring.

be argued that the statistical relationship between certain sub- In 1993, in sleep medicine’s pre-computer era, the Atlas Task Force of types of CAP activity and the occurrence of ASDA arousals makes

the American Sleep Disorders Association [45] established some cri- those measures similar.” Indeed, a highly significant correlation

teria, reassembling some previous data collected by Coleman et al. in (p < 0.0001) has been ascertained between subtypes A2 and A3 of

1982 [46] and based on a group of polysomnographic studies re- CAP and ASDA-scored arousals [38] , and a Kendall W inter-rater

corded on paper, and it never changed over the years. The new crite- coefficient of concordance value of 0.90 for various CAP parameters

ria indicated for PLMs have been mostly advocated from the in normal adults has also been reported [39] . The over 120 PubMed

standards for recording and scoring PLMs in sleep (PLMS) and wake- articles published on CAP suggest that this scoring method could

fulness (PLMW) developed by World Association of sleep Medicine provide integrative information to what is supplied by the simple

(WASM) and International Restless Legs Syndrome Study Group counting of arousals ( Table 2 ) because CAP is not a measure of

(IRLSSG) [47] . Briefly, the definition of minimum and maximum sleep fragmentation, but quantifies the amount of unstable, non-

duration, amplitude onset and offset of a leg movement (LM) event, consolidated sleep. Moreover, the CAP framework not only recov-

minimum number of consecutive LMs with a period length to define ers all the information provided in NREM sleep by AASM arousals,

a PLM series, as well as the criteria to determine bilateral or unilate- but also integrates single or repetitive arousals with other EEG

ral LM have been detailed. The novelties are the inclusion of longer events endowed with activation properties [26,38] . A number of

LM (from 0.5 to 10 s in duration), the shorter inter-movement inter- studies have shown that both K-complex sequences and delta

val (offset-to-onset 0.5 s) to determine the separation between LMs, bursts (either evoked or spontaneous) are regularly accompanied

despite the fact that clinical scoring for the minimum period length by activation of autonomic functions, i.e., heart rate, blood pres-

to include them in a PLM series remains 5 s, and the separation of less sure, muscle sympathetic activity [40] , which are generally weaker

than 5 s to determine the bilaterality of two LMs (and counted as a compared to what accompanies an AASM arousal, but may be

single LM). Also the relationship with other events (arousals and equally effective [41–43] . In a recent investigation carried out in

respiratory events), as well as calibration, detection and recording normotensive subjects with chronic insomnia, higher night time

criteria have been settled according to the recommendations and blood pressure and blunted blood pressure dipping was associated

standards coming from a detailed statistical analysis of computer- with brain cortical activation during sleep in the absence of arousal

ized sleep recordings in patients with RLS-PLMS, controls and differ- rate changes [44] . This implies that scoring of single arousal events

ent pathologies presenting with PLMs [48–50] . The criteria for can be enriched by integrative sleep parameters, including the

considering LMs associated with respiratory events and arousals more general concept of oscillating activation. Moreover, in an

have been established in detail. These events are not discarded from era that has overcome most of the time-consuming constraints

the motor activity report but, tabulated and scored apart, should be due to paper recording and that can rely on computer-assisted

considered different from the other ‘‘true” PLMS. memory attention, can be extended beyond the static framework

The new AASM rules stem from a process of review and analysis of 30-s epochs in search of boundless EEG patterns.

of different studies and of the WASM/IRLSSG standards, in particu- lar, reaching a high level of agreement with these standards be-

4. Movement thresholds: time for computer-assisted cause of the fact that the scoring of PLMS has evolved and moved quantification

towards more advanced procedures and because there is some le- vel of evidence for these new criteria and their reliability when

For the first time, the new AASM Manual has introduced, in a

used by experts [51] .

comprehensive manner, the scoring criteria for different types of Unfortunately, the new atlas rules miss some important charac- teristics of PLMs, such as PLMW which are sometimes as sensitive

Table 2 and specific as PLMS [51] , the Suggested Immobilization Test (SIT), Major clinical applications of CAP.

generally used in clinical trials of drugs for RLS-PLMS and thought to be a sensitive indicator of RLS severity [49,52] , and the relation-

rate and of subtypes A1 and A2 following acute drug treatment) ship with CAP [53] . Sleep recordings of patients affected by Rest- less Legs Syndrome, PLMS or other conditions generally contain a significant amount of non-periodic LMs [54–57] , and LM activity

motor events related to phase A) during wakefulness in the same patients is essentially non-periodic reduction of subtypes A1, respiratory events related to phase B; decrease of

[57] . Perhaps, the new AASM rules should have better defined this CAP rate, reduction of subtypes A3 and partial recovery of subtypes A1 fol-

type of activity and how to evaluate it, differentiating isolated LMs lowing treatment with CPAP)

from those occurring with intervals shorter or longer than PLMs, as these types of activities seem to be represented in different amounts in different groups of patients. Adopting the entire WASM/IRLSSG

decrease of CAP rate during night sleep recovery) standards [47] would probably be simpler and clearer. The next step, not mentioned in this Atlas, should be a better system and software to automatically analyze the candidates for LMs and PLMs and to use a computerized scoring method that

phase A) may provide reliability, variability and validity as good as visual

analysis, with less effort and better accuracy [47] .

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

4.2. REM sleep Behavior Disorder The addition of masseter EMG recordings is left (as a note) at the discretion of examiners. This may be a limit, because when the

Among the other sleep-related movement disorders or para- clinical/anamnestic relevance is unknown, this type of recording somnias, the scoring rules for bruxism, RBD and RMD reached

allows the detection and recognition of subtle forms of bruxism, the ‘‘recommended” level. For RBD, it is the first time that rules

with persistence in different sleep stages, and permits the differen- are written in a formal consensus setting with semiquantitative

tiation from other similar EMG activities, i.e., rhythmic masticatory definition, although they still reflect relatively old criteria, based

muscle activity and oro-mandibular myoclonus [62] . on the visual analysis of polysomnography [58] . During REM sleep the 30-s epochs are considered for both tonic and phasic activities,

4.4. Rhythmic Movement Disorder

while a division in 3-s mini-epochs is recommended for the phasic activity. Either or both the features must be present for the poly-

The scoring criteria for RMD are very simple and clear because somnographic scoring of RBD, together with the audio-video docu-

all the studies are case series or case reports with no controlled mentation of motor episodes or the typical clinical history.

data. The rules do not clarify whether the movements have to be Although the reliability of these criteria is still not completely ex-

exclusively present during sleep, rather than during wakefulness plored and validated [51] , they are a step towards the use of poly-

or in sleep-wake transition, but in the notes is it specified that vi- somnographic criteria in clinical practice to diagnose both clinical

deo-polysomnography is necessary for the diagnosis. This should and instrumental RBD, starting from the seminal paper of Lapierre

be better defined, since RMD are often present both in wakefulness and Montplaisir in 1992 [58] and applying the ICSD-2 indications

and sleep (NREM and REM) and also because the movements dur- [59] . Thus, despite the crucial relevance of increased chin EMG

ing wake periods may interfere with sleep duration and quality. activity for the diagnosis of RBD, the reliability of polysomnograph- ic criteria for REM without atonia is probably largely unexplored

4.5. Hypnagogic Foot Tremor, Excessive Fragmentary Myoclonus, because of the use of paper recordings in sleep research for dec-

Alternating Leg Muscle Activation

ades. In these studies, no clear mathematical and quantitative def- initions, in terms of amplitude and duration, have been provided

For the scoring of the other movement-related phenomena dur- for the elements taken into account: atonia, phasic and tonic

ing sleep, such as HFT, EFM and ALMA, criteria and rules are de- EMG activations. This is also reflected in the notes of the new scor-

fined as ‘‘optional.” Perhaps, in order to go more deeply into the ing rules for RBD: it is difficult to quantitatively differentiate tran-

definition and detection of these motor events and understand bet- sient normal muscle activities and twitching in small or large

ter their clinical significance (if any), we should wait for more data groups of muscles during REM sleep from the pathological twitch-

to be produced. So far, we have no real evidence that these move- ing and phasic activities of RBD without a cut-off threshold. More-

ment disorders are separate nosological and clinical entities. In over, the absolute amplitude of EMG activity is a very difficult

particular, for HFT and ALMA, the few reports available are obser- quantity to pick up visually because of its continuous intraindivid-

vational or brief case series coming from a few sleep labs describ- ual changes and its very large interindividual variability; again, a

ing them as possible variations of PLMs or RLS. Frequently in computer-analysis with quantitative data of digital EMG recording

clinical practice it is possible to encounter patients with PLMs that is more than welcome for their real quantification, overcoming the

have, during the recording night, periods of different periodic leg or semiquantitative data obtained by the currently used visual

foot movements, such as ALMA or HFT, but without specific clinical scoring.

correlates and without particular anamnestic features. Practically, a quantification of the whole sleep period (with the exclusion of very few artefact epochs) and the use of mini-epochs

5. Respiratory events

long enough to allow a reliable estimation of the background EMG mean amplitude and short enough to point out short-lasting phasic

The AASM Manual for the Scoring of Sleep and Associated activities could be useful, as well as an index of atonia to better cat-

Events introduces a systematic approach and scoring criteria for egorize differences of muscle atonia during REM sleep in controls

evaluating different types of respiratory events [1] . Previous scor- and RBD patients [60] .

ing criteria, in both the 1999 [63] and 2005 [64] versions, raised

a number of clinical problems, mainly due to different methods

4.3. Bruxism used to measure or identify the ‘‘target reduction” in respiratory signals and the definition of hypopnea and respiratory-effort-re-

The scoring rules for bruxism have been established as mini- lated arousals (RERA). In particular, two different definitions of mum burst amplitude, duration and interval criteria to correctly

hypopnea were proposed, one for the clinical setting and the other classify most of bruxers and controls, as tested in a limited number

for research purposes. Worldwide, however, many other defini- of controlled studies [61] : a minimal number of three elevations of

tions of hypopnea have been presented in the scientific literature chin EMG burst activity in a regular sequence or sustained eleva-

tion of chin EMG activity longer than 2 s (separated by a stable The new AASM rules represent a significant step towards EMG activity of at least 3 s) constitutes the minimal criteria to de-

resolving these problems and enable a common background for fine an episode of bruxism. Also in this case, it is the first time that

analyzing clinical and research data. The manual dedicates much rules for bruxism scoring are written, based on a few studies inves-

attention to the technical issues involved in obtaining valid, repro- tigating reliability and sensitivity/specificity of these criteria.

ducible traces. Alternative methods to obtain valid respiratory sig- Among these studies we have to recognize the expertise and effort

nals are extensively described, with the aim of minimizing of the group led by Lavigne in Montreal, who quantified and deter-

technical problems that may limit the validity of single studies mined specific polysomnographic features to recognize sleep brux-

and improving the diagnostic approach in individual patients. ism, based not just on video or audio recordings, (considered no

For the first time, the rules for event duration, for both apnea longer sufficient to diagnose sleep bruxism if used alone) [51] .

and hypopnea, are precisely described, with specific recommenda- With respect to previous criteria for scoring bruxism during

tions on the beginning and end of events, so that the intra-scorer, sleep, the novelty of the Atlas resides in the possibility to score this

inter-scorer, and night-to-night reliability should be improved. movement disorder by combining audio recording with polysom-

There are, however, still some concerns, as well as some previ- nography (at least two audible tooth grinding episodes per night).

ously unrecognized problems.

L. Parrino et al. / Sleep Medicine 10 (2009) 799–808

2 portable monitors. The identification of respiratory events in practice, however, may be more complicated. Indeed, Cracowski As in the 2005 AASM practice parameters, two definitions of

5.1. Definition of hypopnea

et al. [73] performed a study in a population of patients with mod- hypopnea are still proposed [64] . It is not clearly specified why

erate to severe OSAS with the aim of characterizing the proportion one definition should be used rather than the other. Data reported

of different types of obstructive non-apneic events (hypopneas and in many studies, extensively reviewed by the AASM Task Force on

RERAs) using the AASM 1999 criteria [63] . They found that 61.8% of Respiratory Scoring, showed that the inter-scorer, intra-scorer and

these events were hypopneas (>30% reduction of baseline flow) night-to-night reliability is good when hypopnea is defined by any

with associated cortical arousal, but desaturation was <3%; 14.8% oxyhemoglobin desaturation. The reliability is, however, lower

did not precisely fulfill the criteria for both hypopneas and RERAs. when using arousals in the event definition or when events are

As a consequence, the new criteria for hypopnea may lower the scored without regard to associated desaturation or when more

sensitivity of the diagnostic test or may result in an underestima- subtle flow limitation is used for event identification [65] .

tion of AHI. Indeed, Ruehland et al. recently demonstrated that As reported by the Task Force, using discernible amplitude cri-

using different standard hypopnea (including the new AASM stan- teria with a criterion of 3% desaturation provides an estimate of

dards) leads to marked differences in AHI in patients who under- AHI equivalent to that obtained using a 50% amplitude reduction,

went polysomnographic evaluation for clinical suspect of OSA [74] . irrespective of desaturation, but it is more reliable and reproduc-

The longitudinal data on progression of sleep apnea over time, ible. However, the level of associated desaturation used in the rec-

albeit scarce, have shown that sleep disordered breathing worsens ommended definition of hypopnea is P4%, so fewer episodes of

progressively [75,76] . Consequently, the question is: Is it better to hypopnea will be recorded. The decision to use 4% rather than 3%

quickly identify patients with nocturnal or daytime complaints and was essentially based on cross-sectional data obtained in the Sleep

a hypopnea with 3% desaturation, or to wait a long time, until the Heart Health Study, showing that AHI (hypopneas defined as dis-

OSA worsens and the degree of sleep hypoxia is greater? cernible reductions in amplitude plus a P4% desaturation) is sig-

The problem of sensitive and specific criteria for identifying nificantly associated with blood pressure, cardiovascular disease,

hypopnea, mainly obstructive, has not been adequately assessed, sleepiness and impaired quality of life [65] . Recently, Punjabi

especially when portable monitors are used instead of standard et al., analyzing data from the Sleep Heart Health Study to deter-

polysomnography. As stated by the AASM, portable monitors mine the definition of hypopneas that would be best correlated

should only be used for the diagnosis of OSA in adulthood in pa- with cardiovascular disease, found that hypopneas with a 4% or

tients with a high pre-test probability of moderate to severe OSA. more decrease in oxyhemoglobin saturation are associated with

But very recently, while analyzing differences in clinical features prevalent cardiovascular disease [66] . But from a clinical point of

between patients with upper airway resistance syndrome, pri- view, differences in odds ratios for prevalent cardiovascular dis-

mary snoring and OSA (hypopnea defined using the so-called eases derived for using the hypopnea index with P4% or P3%

‘‘Chicago Criteria”), Stoohs et al. found that the patients with desaturation thresholds were minimal.

upper airway resistance syndrome had the greatest impairment On the other hand, the clinical setting is quite different from the

of daily functioning and worst perception of sleep quality [77] . epidemiological point of view. The above mentioned studies

In other words, patients with upper airway resistance syndrome showed an increasing risk of cardiovascular diseases in subjects

do not differ clinically from patients with OSAS. As a conse- with very low AHI values, independently of daytime symptoms re-

quence, using portable monitors without EEG channels leads to lated to sleep-disordered breathing. In routine practice, we usually

a high risk of performing in-lab polysomnography for patients evaluate patients who are being investigated to explain the signs

with upper airway resistance syndrome and ‘‘detectable hypopne- and symptoms they experience. Thus, a more sensitive definition

as,” but with desaturation <4%.

of hypopnea is needed since most of the events may not be prop- Finally, two different diagnostic aspects must be resolved in the erly classified until the related desaturation is below 4%. The de-

clinical setting: first, the diagnosis must be made, and, secondly, gree of desaturation is, however, dependent on many factors,

the severity of the disease must be determined. This second aspect such as the duration of apnea, lung volumes, deranged lung

is relevant since the therapeutic algorithm is based on quite a dif- mechanics, presence of sub-clinical pulmonary hypertension, pre-

ferent definition of events from that currently proposed. existing lung diseases, age, obesity, control of breathing, etc., which suggest the use of such a lower cut-off in the clinical setting. On the

5.2. Identification of respiratory events during O 2 -therapy other hand, repetitive episodes of hypopnea, even in the absence of relevant desaturations, may determine other morbidities such as

Polysomnography is usually performed in a clinical setting in cognitive dysfunction, insomnia, depression and others, as stated

patients suffering from diseases other than OSA that may require in the ‘‘Diagnostic and Coding Manual of the International Classifi-

O 2 -therapy (patients with respiratory or thoracic diseases, patients cation of Sleep Disorders” [59] .

with chronic heart failure, etc.). No rules are available for the iden- Cross-sectional epidemiological data and follow-up studies

tification of hypopnea in these patients. have shown that OSA is a strong risk factor for death and cardio- vascular diseases in younger patients [67–69] . CPAP-treated pa-

5.3. Identification of respiratory events during CPAP therapy tients who were compliant with treatment had mortality rates similar to those recorded in the general population [70] , whereas

No mention is made in the manual or in the recent guidelines an excess of fatal cardiovascular events occurred in patients aged

for CPAP titration of the criteria to identify hypopnea during CPAP