silent aspiration: what do we know?
TRANSCRIPT
Silent Aspiration: What Do We Know?
Deborah Ramsey, MA, MRCP,1,2 David Smithard, BSc, MD, FRCP,2 and Lalit Kalra, MD, PhD, FRCP1
1Guy�s, King�s and St. Thomas� School of Medicine, King�s College, London, and 2Health Care of Older People Department, William Harvey
Hospital, Ashford, Kent, United Kingdom
Abstract. Although clinically evident aspiration iscommon in subjects with dysphagia, a significantproportion may aspirate silently, i.e., without anyoutward signs of swallowing difficulty. This articlereviews the literature on the prevalence, etiology, andprognostic significance of silent aspiration. An elec-tronic database search was performed using silentaspiration, aspiration, dysphagia, and stroke assearch terms, together with hand-searching of arti-cles. Silent aspiration has been described in manyconditions and subgroups of patients (includingnormal individuals), using a number of detectionmethods, making comparisons a challenge. The bestdata are for acute stroke, in which 2%–25% of pa-tients may aspirate silently. Mechanisms associatedwith silent aspiration may include central or localweakness/incoordination of the pharyngeal muscu-lature, reduced laryngopharyngeal sensation, im-paired ability to produce a reflexive cough, and lowsubstance P or dopamine levels. In terms of prog-nosis, silent aspiration has been associated with in-creased morbidity and mortality in many but not allstudies. However, some degree of silent aspiration atnight may be normal in healthy individuals. Thephenomenon of silent aspiration is poorly understoodand further research is needed to improve methods ofdetection and thereby better define its prevalence andprognostic significance.
Key words: Dysphagia — Aspiration — Deglutitiondisorders — Stroke.
Swallowing problems are common in a number ofdisorders and may increase morbidity and mortality.Patients with dysphagia are at increased risk ofaspiration, i.e., passage of food/fluid below the truevocal cords into the airways, increasing the risk ofpneumonia and associated problems. In recent yearsvarious studies have described aspiration which ap-pears to be silent [1]: Material is inhaled withoutcoughing or other difficulties apparent at the bedside.This article reviews the literature on silent aspiration,including what is known of its prevalence, etiology,and significance.
Search Strategy and Selection Criteria
Information was obtained from a literature search ofthree electronic databases: Medline, Embase, and theCochrane Library, using silent aspiration, dysphagia,aspiration, and stroke as search terms. The searchwas supplemented by extensive hand-searching ofreferences. Papers not in the English language wereincluded if an abstract was available in English andgave sufficient detail of the study to make it appro-priate for consideration of inclusion. No time limitwas placed on the search history.
Definitions/Descriptions of Silent Aspiration
The first description of silent aspiration probablyappeared in 1937 [2]. The author described intro-ducing a radiopaque agent into the mouths or naso-pharynges of sleeping or stuporose subjects andfinding it radiographically in the bronchial tree thefollowing day, the implication being that it wasaspirated silently during sleep. In 1951, Culver et al.
Correspondence to: D.J.C. Ramsey, MA, MRCP, Department of
Stroke Medicine, GKT Medical School, Bessemer Road, London,
SE5 9PJ, United Kingdom. E-mail: [email protected]
Dysphagia 20:218–225 (2005)DOI: 10.1007/s00455-005-0018-9
[3] introduced blue dye into the stomachs of patientsbefore anesthesia and described a group who did notvomit perioperatively but in whom dye was visiblebronchoscopically below the vocal cords aftersurgery, presumably secondary to silent aspirationduring the procedure. A few years later, Gardner [4]added barium to the diet of surgical inpatients andsubsequently demonstrated radiographically orbronchoscopically the presence of thoracic barium in10/94 patients. Subsequent work suggested that thishad probably followed aspiration while feeding; sev-eral patients were drowsy and unwell, and one wasnoted to cough during drinking, but in at least onecase aspiration was not suspected clinically andtherefore might be considered silent.
In 1983, Linden and Siebens [5] studied a smallgroup of dysphagic patients clinically and with vid-eofluoroscopy in an attempt to correlate clinicalobservations with radiologically demonstrated pene-tration/aspiration. They were the first workers to cointhe phrase ‘‘silent penetration’’ in describing patientswho had laryngeal penetration on videofluoroscopybut did not have any clinical manifestations of aspi-ration, such as cough. It is unclear from their articlewhether this group included all patients in whommaterial passed into the laryngeal vestibule (pene-tration) regardless of whether it passed below the truevocal cords, or whether it included only individuals inwhom material passed below the cords (aspiration asit is now understood).
Since then many studies of dysphagic patientshave used videofluoroscopy (VF). This is regarded bymany as the ‘‘gold standard’’ method of swallowassessment [6] despite problems with its reliability [7].Aspiration has been demonstrated on VF which waswithout accompanying cough or obvious distress;these occurrences were defined as silent aspiration[1,8–15]. Others have used endoscopic methods tostudy swallowing [16], i.e., fiberoptic endoscopicevaluation of swallowing (FEES). The technique hasbeen used to demonstrate both silent and overtaspiration [17,18] and is thought to be at least assensitive as VF at detecting swallowing difficulties [7].Scintigraphic techniques with radioactive tracer havealso been used to identify silent aspiration [19–23].Radioactive tracer is either delivered to the naso-pharynx during or just before sleep, or it is added to asoluble paste attached to the teeth before sleeping.The detection of tracer in the thoracic region thefollowing day has been used as an indicator of silentaspiration of the tracer during sleep, but these studiescannot determine unequivocally whether tracer wasrefluxed from the stomach, as demonstrated in otherscintigraphic studies [24], or directly aspirated from
the pharynx. In addition, apparent aspiration duringsleep may involve different mechanisms comparedwith silent aspiration occurring during activeswallowing, as demonstrated in other scintigraphicstudies [25].
A possible indirect method of detecting silentaspiration is by measuring desaturation on pulseoximetry during swallowing. Collins and Bakheit [13]suggested that desaturation of greater than 2% frombaseline during swallowing is indicative of aspiration.However, pulse oximetry may lack the sensitivity todetect such small changes reliably because the man-ufacturer�s error rate for the equipment is 2%. Otherstudies have suggested that marked desaturation maycorrelate better with penetration, regardless of whe-ther aspiration also occurs, rather than with aspira-tion alone [26,27]. Lim et al. [26] found thatdesaturation on drinking aliquots of water occurredin a group of probable silent aspirators (patients whopassed a bedside screen but subsequently aspirated onendoscopic testing), but pulse oximetry was not per-formed during the bedside assessment itself, pre-venting better assessment of the correlation betweenoximetry data and clinical findings.
If defined as aspiration without cough or othersign of distress, silent aspiration is reliant for itsdetection upon the use of techniques other than abedside clinical assessment, which, by definition,cannot detect it. Although a number of methods havebeen used to assess swallowing and aspiration (silentor otherwise) in diverse patient groups, VF andFEES, at present, are regarded as the best methodsdespite their known limitations [7]. Since aspirationrepresents a problem in the mechanisms of airwayprotection during the swallow, this article focuses onproblems related to the oropharyngeal phases ofswallowing rather than the esophageal phase.
Prevalence of Silent Aspiration
Most studies on silent aspiration in dysphagic pa-tients depend upon VF for detection. Linden andSiebens [5] described 9/11 patients with asymptomaticlaryngeal penetration, 4 of whom did not cough evenon bronchial penetration. However, 10/11 patientshad a wet-hoarse voice, which is now known to besuggestive of an unsafe swallow. Splaingard et al. [8]found that 20% of 107 dysphagic inpatients under-going rehabilitation aspirated silently on VF. Retro-spective studies on large numbers (n ‡ 1000) ofdysphagic patients who had undergone VF for vari-ous reasons showed that 25%–30% aspirated silently[9,10]. Leder et al. [17] studied swallow endoscopi-
D. Ramsey et al.: Silent aspiration: What Is Known? 219
cally and found that 28% of 400 dysphagic inpatientsaspirated silently.
Scintigraphic studies on small numbers ofsleeping patients have shown that 70% (7/10) of pa-tients with a depressed conscious level developedthoracic tracer [19] and 71% (10/14) of patients withacute community-acquired pneumonia developedpositive scans [21]. Four studies [19–21,23] have de-scribed signs of tracer in healthy individuals duringsleep using scintigraphic techniques which variedconsiderably. Results ranged from the presence ofthoracic tracer in all 12 control subjects in one study[23], to 45% (9/20) to 50% (5/10) of subjects in otherstudies [19,20], and were as low as 10% (1/10) in onestudy [21].
In contrast to these studies of sleeping healthysubjects, a scintigraphic study [25] of swallowing inawake dysphagic patients found positive results in 5/14 (36%) patients and indeterminate results (residualisotope in the neck region but not localizable specif-ically to the esophagus or the airway) in 7/14 patients.None of those with a positive scan had an absentcough, although it was delayed in one; the exacttiming relative to the swallow was not documented soit is hard to know whether this could represent silentaspiration.
Silent Aspiration in Stroke
Dysphagia and aspiration have been studied mostfrequently in stroke patients using VF, and silentaspiration has been described as an occurrence sep-arate from overt aspiration. Horner et al. [1,11] per-formed two small studies of clinical predictors ofaspiration in dysphagic stroke patients (mean 2–3months after stroke) that showed that 28%–38% pa-tients aspirated silently. Holas et al. [12] studiedmedical complications in dysphagic stroke patientsundergoing rehabilitation and found that 39% aspi-rated silently.
Collins and Bakheit [13] compared pulseoximetry with VF in the detection of aspiration indysphagic stroke patients and found that 15% of theirpatients aspirated silently on VF. A scintigraphicstudy in sleeping patients with acute pneumoniashowed that positive scans correlated with a historyof previous strokes [22]. Thoracic tracer was found inmore than 90% and more than 60% of patients withprevious bilateral and unilateral basal ganglia in-farcts, respectively, but in less than 20% of patientswho had no history of cerebral infarcts.
These studies are summarized in Table 1, to-gether with data from two of the larger studies ofdysphagic patients in which data for stroke patients
specifically are available [9,17]. The studies giveprevalence estimates for silent aspiration in subacutedysphagic stroke patients of 15–39%, with significantproportions of aspirators aspirating silently. How-ever, the time between stroke and testing was veryvariable and not always given. Other researchers [28–32] (Table 1) specifically investigated unselected acutestroke patients, often looking at the incidence andpredictors of aspiration or comparing methods ofswallow assessment. These workers described aspi-ration in 21%–42% of acute stroke patients, with 2%–25% aspirating silently. The studies were not designedto assess prevalence, and numbers of silent aspiratorswere generally small.
Silent Aspiration in Nonstroke Disease
Videofluoroscopy has been found to demonstrate si-lent aspiration in many disorders incidentally; e.g.,78% of subjects aspirated silently in a study of indi-viduals with severe motor and intellectual disabilities[33]. Arvedson et al. [14] retrospectively reviewed VFresults for 186 children with developmental dyspha-gia and found that 26% had aspirated (94% silently).Silent aspiration occurred on VF in 2/11 (18%) chil-dren with chronic gastroesophageal reflux [34] andhas also been described in neurologically normal in-fants without reflux [35].
Traumatic brain injury can cause dysphagiaand silent aspiration [36,37], and the prolongedendotracheal intubation/ventilation often required insuch patients may contribute [38]. Tracheostomytubes have also been associated with aspiration, bothovert and silent; Elpern et al. [15], for example, found50% of medically stable ventilated patients with tra-cheotomies aspirated on VF and 77% of aspirationswere silent. Another study [18] tested swallowingendoscopically and found that 33% of patients with arecent (last two months) tracheotomy aspirated, 82%silently. However, the causal link between tracheot-omy and aspiration remains to be established [39].
Silent aspiration has been documented fol-lowing cardiothoracic surgery [40], probably sec-ondary to perioperative cerebrovascular events. Riskfactors for silent aspiration included older age, pre-vious cerebrovascular disease, insulin-dependentdiabetes mellitus, previous myocardial infarction, andchronic obstructive pulmonary disease. Silent aspi-ration has also been demonstrated after treatment forhead/neck malignancies, with 22% of 49 previouslytreated patients aspirating silently on VF in one study[41]. Other conditions associated with silent aspira-tion include ataxia–telangiectasia [42], myastheniagravis [43], Parkinson�s disease [44], and Down
220 D. Ramsey et al.: Silent aspiration: What Is Known?
syndrome [45]. It has been described secondary tounilateral recurrent laryngeal nerve paralysis [46],after pulmonary transplantation [47], after abdomi-nal surgery [48], and possibly after oral contrastadministration for CT scanning [49]. Many of thesestudies describe very small numbers of silent aspira-tors, and again none of the work was designed tostudy prevalence.
Etiology of Silent Aspiration
Silent aspiration may result from weakness/incoor-dination of pharyngeal musculature [10], leading toabnormal pharyngeal initiation of swallowing ormotor response. Similar difficulties may underlie theassociation between prolonged endotracheal intu-bation and silent aspiration: Intubation may impairvocal fold motion [50], and tracheotomies may af-fect the laryngopharyngeal movements of swallow-ing and airway protection [15,51]. Centralneurological damage also seems important. In onestudy dysphasia and more recent cerebrovascularevents were more common in silent than in overtaspirators [8]. A scintigraphic study of elderly pa-tients with pneumonia [22] also found more positivescans and longer swallow latency responses in pa-tients with previous basal ganglia infarcts than inthose without.
Another possible factor predisposing to silentaspiration is reduced pharyngeal sensation [2], e.g.,desensitization of the airways by prolonged intra-tracheal intubation or tracheotomy [15]. Aviv et al.[52] found that 11/18 stroke patients with no clinicaldysphagia had laryngopharyngeal sensory deficitswhen tested with air pulses directed at mucosainnervated by the superior laryngeal nerve. Althoughthe reaction to food/fluid may differ from that to airpulses, pneumonia often developed in patients withgreater sensory deficits. Reduced local sensitivity hasalso been demonstrated with increasing age [53],perhaps contributing to the higher prevalence ofdysphagia in older patients; many studies have shownan association between silent aspiration and in-creased age [8,10,40].
Since ‘‘silent aspiration’’ describes aspirationwithout coughing or other obvious distress, etiologictheories must consider the integrity of the cough reflex,which may be affected by impaired local/central neu-romuscular control of diaphragmatic or chest wallfunction [2,54]. There are actually two distinct types ofreflexive, nonvoluntary cough with different underly-ing neurological mechanisms: a primary cough reflexoccurring at the level of the vocal folds, often referredT
able1.Prevalence
ofsilentaspirationin
stroke
Researchers
Totalpatient
numbersin
study
Characteristics
ofpatientgroup
%ofpatients
whoaspirated
%ofpatientswho
aspiratedsilently
%ofaspirators
whoaspiratedsilently
Garonetal.1996[9]
516a
Dysphagicstrokepatients(timingunknown)
60
16
42
Leder
etal.1998[I7]
87a
Dysphagicstrokepatients(timingunknown)
47
20
41
Horner
and
Massey
1988[1]
21
Dysphagicstrokepatients,mean2.8monthspoststroke
52
38
73
Horner
etal.1988[11]
47
Dysphagicstrokepatients,mean2.9monthspoststroke
51
28
54
Holasetal.1994[12]
114
Dysphagicstrokepatients,median4weeksfrom
event
54
39
72
CollinsandBakheit1997[13]
54
Dysphagicstrokepatients(timingunknown)
41
15
36
Nakagawaetal.1997[22]
45b
Previousstroke
15
bilateralbg
>90
15
unilateralbg
>60
15
nilprevious
<20
Kiddetal.1993[30]
60
Acutestrokes
(within
72hours)
42
820
Danielsetal.1998[29]
55
Acutestrokes
(within
5days)
38
25
67
Smithard
etal.1998[28]
94b
Acutestrokes
(within
3days)
21
11
50
Mannetal.2000[31]
128
Acutestrokes
(within
7days)
22
27
Stannersetal.1993[32]
41c
Acutestrokes
(within
2days)
24
15
60
aData
included
onlyforstrokepatients.
bbg=
basalgangliainfarcts.Exactnumbersofaspiratingpatientsnotprovided
inpaper.
cData
given
onlyforpatientswhounderwentVF.
D. Ramsey et al.: Silent aspiration: What Is Known? 221
to as the laryngeal cough reflex, and a deeper tra-cheobronchial cough reflex which tends to be delayedand less productive. Although most workers studying‘‘the cough reflex’’ do not differentiate between these,often both are tested by the same procedure (e.g., inlooking for a cough response on swallowing), and itseems likely that either or both reflexes may be affectedby stroke or similar neurological processes.
Many workers have demonstrated an associ-ation between impaired cough and dysphagia/aspi-ration in stroke [28,29,32,55–58]. Nakazawa et al. [59]demonstrated depressed cough and delayed swallowreflexes in patients with aspiration pneumonia. Niimiet al. (60) found persistently higher cough thresholdsto inhaled irritants in patients with recurrent unex-plained pneumonia than controls, suggesting that anattenuated cough reflex may impair defenses againstthe development of infections. Stephens et al. [61]found an intact laryngeal cough reflex in 30 patientswith acute cerebral infarcts, irrespective of side ofinfarct, despite an abnormal voluntary cough in 79%of the 14 patients with a left-sided infarct. No pa-tients developed aspiration pneumonia, and theauthors suggested that the laryngeal cough reflex ismore important for airway protection than the abilityto produce a voluntary cough. The occurrence of si-lent aspiration during normal sleep, and especially inassociation with a depressed conscious level [19], mayfollow suppression during sleep of protective reflexesinvolved in swallowing and airway protection, withgreater suppression in patients with impaired con-sciousness.
Sputum levels of the neurotransmitter sub-stance P are reduced in patients with aspirationpneumonia [62], and recent scintigraphic work hassuggested that silent aspiration after stroke mayrelate to low substance P levels. Arai et al. [63]demonstrated an apparent reduction in silent aspi-ration in hypertensive stroke patients, mediated viaincreasing serum substance P concentrations [64],following treatment with ACE (angiotensin-con-verting enzyme) inhibitors; these potentiate sub-stance P, which is otherwise degraded by ACE.Upper respiratory tract epithelium contains nerveplexuses using substance P, and the cough responseis attenuated by capsaicin, which abolishes sub-stance P in the airway [64]. Angiotensin II receptorantagonists seem less effective [65]. Dopaminergicmechanisms also appear important, either directlyor by affecting substance P synthesis: levodopaimproves the swallowing reflex [66], and antipar-kinsonian agents cabergoline and amantadine re-duce silent aspiration in elderly patients after strokeas efficiently as ACE inhibitors [67].
Prognostic Significance
It is possible that silent aspiration has outcomessimilar to overt aspiration [68]: gastric acid can causea chemical pneumonitis independent of bacterialinfection (Mendelson�s syndrome), characterized byacute respiratory distress and hypoxia. Alternatively,aspirated particles may mechanically obstruct, caus-ing acute or chronic respiratory distress andincreasing the risk of a secondary pneumonia.
Increased pulmonary complications andpoorer outcomes have been reported in surgical andventilated patients [40,69,70], but it is difficult todisentangle the specific contribution of silent aspi-ration. Pikus et al. [71] retrospectively reviewed pa-tients who had undergone VF and found that thosewith silent aspiration developed pneumonia moreoften than those with normal swallowing, althoughthere was significant potential for selection bias intheir patient group determination. One study ofintubation injuries related silent aspiration to sub-sequent pulmonary complications [50], and in thegroup of normal infants found to have silent aspi-ration [35], improvement of respiratory functionoccurred only after resolution of dysphagia. Anotherstudy in older, bed-bound, institutionalized patientsshowed reduced pyrexial days (presumed respiratoryinfections) by mouth-cleaning and maintenance ofan upright posture after meals [72] and concludedthat this had reduced silent aspiration of pharyngealsecretions.
Within stroke patients there are conflictingreports on the consequences of silent aspiration. Onereview [73] found that pneumonia was infrequent indysphagic patients diagnosed at the bedside, sug-gesting that silent aspiration (presumably undiag-nosed clinically and therefore untreated) wasunimportant. In contrast, the scintigraphic study thatdemonstrated silent aspiration in older patients afterstroke [22] found that pneumonia was more commonin patients developing positive scans, implying anincreased pneumonia risk from infarct-related silentaspiration. Mortality was highest in patients who hadpreviously had bilateral cerebral infarcts. One study[52] showed that 2/5 patients with bilateral laryngo-pharyngeal sensory deficits developed aspirationpneumonia compared with 0/13 patients with normalsensation or unilateral deficits. Holas et al. [12] founda fivefold increase in relative risk of pneumonia forsilently aspirating patients compared with overt/no-naspirators, but they did not compare silent aspira-tors with either group separately.
In contrast to studies that showed increasedrisk of pulmonary complications and poor outcome,
222 D. Ramsey et al.: Silent aspiration: What Is Known?
Garcia et al. [48] described apparent silent aspirationafter extubation in a patient undergoing gastric sur-gery several days after esophagogastroduodeno-graphy with barium, with no clinical repercussions.Garon et al. [9] have commented that individuals withcerebral palsy and severe lifelong aspiration appearonly rarely to develop pneumonia. More objectively,work by Langmore et al. [74] on independent pre-dictors of aspiration pneumonia suggests thatdysphagia and aspiration (presumably including si-lent aspiration) are necessary but not sufficient con-ditions for the development of pneumonia. This issupported by the observation that the occurrence ofsilent aspiration in at least some healthy subjectsduring sleep appears to have few common clinicalsequelae, suggesting either that it has minimal prog-nostic significance in itself, or that healthy individualsare better able to combat the organism load aspi-rated, physically and immunologically, or that thesilent aspiration apparently detected by scintigraphicstudies during sleep is a different phenomenon from(and not truly comparable with) silent aspiration thatoccurs during swallowing in dysphagic individuals.The lack of negative sequelae in healthy individualsmay simply reflect aspiration of secretions rather thanfood textures.
Conclusions
The heterogeneity of patient groups, techniques, andmethodology of studies on silent aspiration has re-sulted in considerable controversy on its prevalence,etiology, and clinical consequences. It appears thatsilent aspiration is a real phenomenon that probablyoccurs in healthy individuals during sleep and inmany disease states. Although the exact prevalenceremains unknown because of the size and method-ology of existing studies, the most reliable estimatesare for stroke, where it has been reported in 15%–39% of subacute dysphagic stroke patients and in2%–25% of acute unselected stroke patients. Mecha-nisms that may underlie the occurrence of silentaspiration include central or local weakness/incoor-dination of the pharyngeal musculature, reducedlaryngopharyngeal sensation, impaired ability toproduce a reflexive cough, and low substance P ordopamine levels. The consequences of silent aspira-tion are unknown. Although some studies suggestincreased frequency of chest infections and poorerclinical outcomes, other studies have shown no ad-verse effects in mostly healthy individuals.
These controversies need to be addressed toguide appropriate clinical management of patients at
risk of silent aspiration. Further studies looking atsilent aspiration should ideally develop methods ofdetection more widely available than VF or FEES,the techniques used most frequently to study it.Defining true silent aspiration as aspiration that oc-curs during swallowing, rather than during sleep,would define a clinically relevant population groupfor further study. Reliable methods of detectionwould allow safe review of the appropriateness oforal feeding after conditions such as stroke. Theuncertainty in management of silently aspirating pa-tients can be resolved only if its etiology and conse-quences are better understood.
Acknowledgment. The authors gratefully acknowledge support
from Action Medical Research and The Stroke Association.
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