Comments on Selected Recent Dysphagia Literature

David W. Buchholz, MD and Stefanie Neumann, MA

Long-term Functional Outcome in Patients with Neu-rogenic DysphagiaBartolome G, Prosiegel M, Yassouridis ANeuroRehabilitation 9:195–204, 1997

Bartolome et al. conducted a questionnaire survey toevaluate long-term outcomes and to identify variablespredicting favorable outcomes among patients who pre-viously had received inpatient swallowing therapy forneurogenic dysphagia. Therapy had been of two types:(1) restitutional (preparatory stimuli and muscle exer-cises in an attempt to restore impaired function) and (2)compensatory techniques (head postures, diet alterations,and special techniques including supraglottic swallow-ing, the Mendelsohn maneuver, and double swallowing).The underlying neurologic diseases were primarilystroke and neoplasm. Pretreatment intervals (i.e., timefrom onset of illness until initiation of swallowingtherapy) had ranged from 1 to 104 weeks with a medianof 13 weeks.

Most patients had received both types of therapy.Inpatient treatment had lasted between 1 and 62 weekswith a median of 10 weeks. Swallowing therapy hadbeen conducted 4–5 days per week for 45 min/session.The duration of the posttreatment interval (i.e., the timefrom completion of swallowing therapy at discharge un-til the questionnaire follow-up) varied from 7 to 263weeks with a median of 83 weeks. Only 1 patient re-ceived outpatient swallowing therapy postdischarge.

Long-term outcome of therapy postdischarge wasrated by the following feeding status scale: (1) oral feed-ing without compensation, (2) oral feeding with compen-sation, (3) oral and tube feeding combined, and (4) totaltube feeding. Feeding status was determined by patients’responses to the questionnaire. The questionnaire alsoinquired about occurrence of pneumonia. Positive long-term outcome was indicated by a favorable change infeeding status posttreatment, such as shifting from oralfeeding with compensation to oral feeding without com-pensation.

Of the 82 patients to whom the questionnaire wassent, 68 responded within 3 weeks, and 5 were excludedfrom analysis for various reasons, leaving 63 patients inthe study.

Bartolome et al. found that 43% of patients re-ported positive outcomes in terms of feeding status, pri-marily related to shifts from oral feeding with compen-sation to oral feeding without compensation, during theposttreatment interval. At completion of swallowingtherapy, 87% of patients had been using restitutionalstrategies and 97% had been using compensatory meth-ods. When surveyed by questionnaire at a median ofapproximately 18 months later, only 30% reported stillusing restitutional techniques and 59% reported usingcompensations.

Logistic regression analysis revealed that amonga number of candidate variables the only pretreatmentvariables predicting positive long-term outcomes in theposttreatment period were decreasing pretreatment inter-val and low Barthel score. There was no occurrence ofpneumonia posttreatment.

In their discussion of apparent progress in theposttreatment interval, as suggested by patients shiftingfrom oral feeding with compensation to oral feedingwithout compensation, Bartolome et al. concede, ‘‘Wedo not know whether or not certain compensations wereunnecessary for some patients even before being dis-charged.’’

With regard to prediction of successful long-termoutcome by short pretreatment interval, they note thatthis finding might be explained by greater potential forspontaneous recovery among patients treated soonerrather than later after disease onset. Nonetheless, the au-thors conclude, ‘‘The analysis of predictive variablessuggests [5] early use of therapy to enhance the chancesof successful long-term outcome.’’

In reference to the statistical influence of a lowBarthel score on successful outcome, they state, ‘‘A fur-ther very simple explanation would be that a greatervariation is to be expected in the case of a low Barthel

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score than in the case of a relatively high Barthelscore. . . .’’

Finally, Bartolome et al. ‘‘advocate regular mul-tidisciplinary follow-up controls using videofluoroscopicand/or videoendoscopic examination.’’ They explain,‘‘This facilitates comparisons of a normal swallow [ac-tually, the patient’s disordered swallow without compen-satory intervention] with the efficacy of the applied tech-nique with the aim of reducing compensations as early aspossible.’’

CommentsLong-term outcome studies of swallowing therapy forneurogenic dysphagia are sorely needed. We agree withBartolome et al. that ‘‘the true long-term efficiency ofdysphagia management could only be determined by arandomized controlled trial, including a no-treatmentgroup.’’ Accordingly, the study reported by Bartolome etal. does not inform us as to whether or not swallowingtherapy is of long-term benefit.

For Bartolome et al. to regard shifts from oralfeeding with compensation to oral feeding without com-pensation as positive outcomes, i.e., indicating improve-ment in swallowing function, is questionable. Compen-sations are onerous, unnatural behaviors that are unlikelyto persist reliably when a patient leaves the structuredenvironment of swallowing therapy sessions and reentersthe real world. It is a leap of faith to assume that patientscontinue to employ compensatory methods, i.e.,unlesstheir swallowing function improves, postdischarge. It isas or more likely that posttreatment compliance withcompensatory techniques routinely erodes and that anyperceived improvement based on disposal of compensa-tions is illusory.

Among other questions, one wonders how pa-tients would be able to accurately assess improvementin swallowing function so as to conclude correctlythat compensation is no longer necessary? Bartolomeet al.’s advocation of ‘‘regular multidisciplinary follow-up controls using videofluoroscopic and/or videoendo-scopic examination . . . with the aim of reducing com-pensations as early as possible’’ is, in effect, acknowl-edgment of this quandary. If patients were reliable judgesof their need, or lack of need, for compensatory tech-niques—which is a basic premise of this report—whywould these recommended follow-up studies be neces-sary?

With regard to prediction of favorable long-termoutcomes on the basis of short pretreatment intervals andlow Barthel scores, these associations can be readily ex-plained by the fact that patients with these characteristicshad more time for spontaneous recovery and more roomfor improvement. The findings of this study do not jus-

tify the early use of swallowing therapy, as suggested bythe authors. Indeed, as the authors acknowledge, whetheror not swallowing therapy—early, late, or otherwise—iseffective in improving long-term outcome of neurogenicdysphagia remains to be determined.

Motor Innervation of the Cricopharyngeus Muscle bythe Recurrent Laryngeal NerveHammond DS, Davenport PW, Hutchison A, Otto RAJ Appl Physiol 83:89–94, 1997

Hammond et al. note, ‘‘Recurrent laryngeal nerve (RLN)dysfunction has been associated with laryngeal dysfunc-tion, although swallowing dysfunction in patients withRLN paresis has been reported’’ [1,2]. The authors ‘‘testthe hypothesis that the cricopharyngeus muscle (CPM)is, in part, anatomically and functionally innervated bythe RLN. . . . [Although] the CPM has been reported tobe innervated by the pharyngeal plexus, formed frombranches of the glossopharyngeal, vagus, and sympa-thetic nerves [3]. . . . anatomic studies [in human cadav-ers] have suggested that the RLN also supplies theCPM’’ [4,5].

Hammond et al. used a sheep model for swallow-ing ‘‘because of the anatomic and physiological similari-ties to humans.’’ Their investigations included (1) ana-tomic dissection of the RLN, (2) electrical stimulation ofthe RLN while recording electromyographic (EMG) ac-tivity of the CPM, and (3) recording CPM activity duringswallowing pre- and post-RLN section.

The results were as follows: (1) there is a nervebranch leading from the RLN to the CPM, (2) electricalstimulation of the RLN elicited EMG activity in the ip-silateral CPM, and (3) sectioning of the RLN resulted inloss of the early phases of swallow-related CPM electro-myographic activity, although late-phase activity per-sisted.

Hammond et al. conclude, ‘‘These findings dem-onstrate that RLN is one component of the innervation ofthe CPM and plays an important role in swallowing.’’They also note, ‘‘The retention of low level EMG activ-ity after RLN section demonstrates that the CPM hasother innervation, presumably from the superior laryn-geal nerve.’’

CommentsAlthough these important anatomic and physiologic datademonstrate substantial contribution of the RLN to thefunction of the CPM in sheep, it is unclear whether or notthis is relevant to dysphagia in humans. Setting asidepotential interspecies differences, the larger issue is:

186 D.W. Buchholz and S. Neumann: Recent Dysphagia Literature

Does RLN dysfunction alone cause dysphagia—and,specifically, aspiration—in humans?

In our opinion, despite the findings of Hammondet al., this question remains unanswered. Although theauthors speculate regarding potential clinical conse-quences of impaired RLN input leading to CPM dysfunc-tion, their data do not actually demonstrate dysphagia, letalone aspiration.

As for reports of RLN dysfunction associatedwith dysphagia and aspiration in humans, these patientsmay not have suffered from pure RLN dysfunction.Rather, they may have had neurologic diseases produc-ing not only RLN dysfunction but also other neurologicdysfunction affecting the pharynx and larynx, with thelatter, not the former, being responsible for dysphagia oraspiration.

References

1. Ekberg O, Lindgren S, Schultze T: Pharyngeal swallowing inpatients with paresis of the recurrent nerve.Acta Radiol Diag-nost 27:697–700, 1986

2. Shin T: Aspiration caused by recurrent laryngeal nerve paraly-sis.Otol Fukuoka 31:416–420, 1985

3. Snell RR:Clinical Anatomy for Medical Students,3rd ed. Bos-ton, MA: Little, Brown, 1986, p 732

4. Rustad WH, Morrison LF: Revised anatomy of the recurrentlaryngeal nerve. Surgical importance based on the dissection of100 cadavers.Laryngoscope 62:237–249, 1952

5. Steinberg JL, Khane GJ, Fernandes CMC, Nel JP: Anatomy ofthe recurrent laryngeal nerve: a redescription.J Laryngol Otol100:919–927, 1986

The Use of Percutaneous Endoscopic Gastrostomy(PEG) Feeding Tubes in Patients with NeurologicalDiseaseBritton JER, Lipscomb G, Mohr PD, Rees WD, Young ACJ Neurol 244:431–434, 1997

Britton et al. retrospectively reviewed the records of 32neurologic patients treated with percutaneous endoscopicgastrostomy (PEG) during a 31⁄2 year interval. The me-dian post-PEG follow-up period was 6 months (range1–36 months).

Twelve of the patients had motor neuron disease,12 had multiple sclerosis, and 8 had an assortment ofother neurologic disorders. Only 6 patients had video-fluoroscopic studies prior to PEG placement. The authorsreport, ‘‘in the majority aspiration was an obvious clini-cal problem, easily diagnosed at the bedside.’’ They add,‘‘A videofluoroscopy study did not change patient man-agement. . . .’’ There were minor but no major compli-cations of PEG. The median duration of feeding by PEGwas 183 days (range 3–1,271 days).

Britton et al. state, ‘‘In the 9 patients who re-

ported chest infections from the time of diagnosis therewere 45 separate episodes prior to PEG. . . . After PEGthere were only 7 episodes of infection in 7 patients . . . ,all of whom had continued to take food orally.’’ Amongthe 17 patients with data regarding weight, ‘‘All patientsgained weight after PEG tube-insertion with a meanweight gain of 9 kg (range 3.5–13.6 kg).’’

The authors interpret their findings to suggestthree indications for PEG. They state, ‘‘Those with ahistory of chest infection benefit the most. . . . thereduc-tion in frequency of chest infections shown in this studyrepresents a significant reduction in morbidity.’’

The authors continue, ‘‘The second group to ben-efit were patients with a decreased level of consciousnesswho were unlikely to recover or were in a persistentvegetative state. . . . the procedure greatly eased the careof such patients and was quickly accepted by nursingstaff and by the patients’ relatives and caregivers.’’

Britton et al. report, ‘‘A further indication forPEG is weight loss and inadequate nutrition. . . . PEGreleases the care-giver for other duties and improvesquality of life for the patient. In many cases, food maystill be taken orally after PEG insertion. . . .’’ They con-clude, ‘‘The improved quality of life offered by PEGfeeding is good value for the money.’’

CommentsThere is little doubt that PEG is effective for two of thethree indications suggested by Britton et al., namely, (1)unburdening caregivers of patients with decreased levelof consciousness or persistent vegetative state and (2)improving nutritional status when dysphagia leads toweight loss.

The issue of PEG to reduce chest infection isunsettled. These data of Britton et al. do not shed light onthis issue. Although there were 45 episodes of chest in-fection in 9 patients prior to PEG and 7 episodes in 7patients after PEG, the pre- and post-PEG time intervalsare not specified in the report and cannot be assumed tohave been comparable.

Of interest are ‘‘two patients who had videofluo-roscopic evidence of aspiration [and who] initially re-fused PEG and were able to live for 7 months and 2years, respectively, before agreeing to the procedure.’’Despite aspiration, and despite going without PEG for upto 2 years, these patients are not reported to have sus-tained chest infection.

We still do not know if PEG decreases, increases,or has no effect upon the incidence of chest infection inall comers, let alone defined populations of patients withspecific characteristics that might single them out as po-tential beneficiaries of PEG for this indication (see be-low).

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The Risk Factors and Impact on Survival of FeedingTube Placement in Nursing Home Residents with Se-vere Cognitive ImpairmentMitchell SL, Kiely DK, Lipsitz LAArch Intern Med 157:327–332, 1997

Mitchell et al. studied a cohort of 1,386 nursing homeresidents older than 65 years with recent progression tosevere cognitive impairment. The authors identified asubset of 135 patients (9.7%) who underwent placementof a feeding tube. Clinical characteristics and survivalduring a 24-month follow-up period were compared forresidents who were and those who were not tube fed.

Factors independently associated with a greaterlikelihood of feeding tube placement included ageyounger than 87 years, more intact functional and cog-nitive performance at baseline, recent weight loss, chew-ing and swallowing problems, recurrent lung aspiration,an unstable medical condition (pneumonia, stroke, ordiabetes), pressure ulcers, and no ‘‘do-not-resuscitate’’(DNR) order. The authors note, ‘‘Recurrent lung aspira-tion was the strongest risk factor for feeding tube place-ment,’’ although aspiration is not defined.

The key finding was that survival between resi-dents with and without feeding tubes did not differ. Thisfact held true even with multivariate analysis adjustingfor the above-listed independent risk factors for feedingtube placement.

Mitchell et al. report, ‘‘The factors that remainedsignificantly associated with poor survival were aspira-tion [undefined], chewing and swallowing problems, ageolder than 87 years, pressure ulcers, stroke, DNR status,and no diagnosis of dementia.’’

The authors state, ‘‘We also explored whetherfeeding tube status had an impact on survival in sub-groups of residents with stroke, aspiration [undefined],chewing or swallowing problems, no dementia, and ageyounger than 87 years. The mortality rate of the tube-fedsubjects in these strata did not differ significantly fromthose without feeding tubes.’’

Mitchell et al. comment, ‘‘This study supportsthe observation that nursing home residents with a po-tentially reversible component to their condition aremore likely to be tube fed. . . . Health care providers andfamilies may consider enteral support more readily for anacute neurological event rather than a progressive de-mentia. . . . A study of physicians’ and nurses’ attitudesregarding tube feeding in long-term care demonstrated apreference for tube feeding in residents who wereyounger, had more intact mental status, and were con-sidered happier by these professionals [1]. These prefer-ences were reflected in our findings in that younger age,no dementia, and less functional impairment were inde-

pendently associated with an increased likelihood offeeding tube placement.’’

The authors continue, ‘‘We found aspiration [un-defined] to be both an independent risk factor for feedingtube placement and for mortality in residents with severecognitive impairment. Aspiration was also a strong con-founder for the pneumonia variable in our analysis.Therefore, it is likely that aspiration was an importantcause of pneumonia in our population. . . . tube feeding,regardless of the specific device, does not necessarilyprotect the nursing home resident from aspirating andmay be a particularly ineffective intervention for the sub-set of patients with severe cognitive impairment.’’

Mitchell et al. discuss their finding ‘‘that pressureulcers are an independent risk factor for feeding tubeplacement.’’ They observe, ‘‘It is difficult to discernfrom our study whether the pressure ulcers were the rea-son for feeding tube placement or, in fact, a consequenceof having a feeding tube. The incidence of pressure soresis associated with restraint use, immobility, and fecalincontinence, all of which are potential complications oftube feeding’’ [2,3].

Mitchell et al. summarize, ‘‘This is the first in-vestigation known to us to include a control group with-out feeding tubes rigorously matched for recent progres-sion to severe cognitive impairment and where multivariatetechniques were used to adjust for comorbid conditions. . . .After adjusting for independent risk factors for receivinga feeding tube, feeding tube status was the least impor-tant determinant of survival in this frail population.’’

Reviewing pertinent literature, Mitchell et al. re-port, ‘‘One third of nursing home residents would chooseto be tube fed if they could no longer eat because ofimpaired cognition [4]. Prolonged survival was the mostcommon reason cited for accepting a feeding tube amongintact elderly patients presented with a hypothetical vi-gnette [5]. Therefore, our finding that feeding tube place-ment did not significantly affect the survival of nursinghome residents with severe cognitive impairment is criti-cal. If other putative benefits of feeding tubes such asprevention of aspiration in the healing of pressure soresare also questionable, then one must ask what are thegoals of tube feeding this frail population.’’

Mitchell et al. concede, ‘‘Ideally, a randomized,controlled, clinical trial would be needed to adequatelymatch the 2 groups [tube fed and not tube fed] prospec-tively. However, such a trial would be impossible toperform due to the ethical and emotional issues involvedin the decision to tube feed an elderly patient with severecognitive impairment.’’

CommentsFor reasons noted by Mitchell et al. in the final paragraphabove, their data may be as good as we will ever have

188 D.W. Buchholz and S. Neumann: Recent Dysphagia Literature

regarding decisions about feeding tube placement innursing home residents with severe cognitive impair-ment. It appears that this intervention is unjustifiable interms of demonstrable benefit to the patient with regardto mortality and morbidity including aspiration and pres-sure ulcers. Nonetheless, consideration of feeding tubeplacement in this population may be justifiable in rela-tion to benefits on behalf of individuals other than thepatient (that is, family and care-givers). It remains to bedetermined whether or not the findings of Mitchell et al.in terms of ineffectiveness of feeding tubes in prolongingsurvival in this specific population are generalizable toother populations of prospective feeding tube recipients.

References

1. Watts DT, Cassel CK, Hickam DH: Nurses’ and physicians’attitudes toward tube-feeding decisions in long-term care.J AmGeritr Soc 34:607–611, 1986

2. Peck A, Cohen CE, Mulvihill MN: Long-term enteral feeding ofaged demented nursing home patients.J Am Geritr Soc38:1195–1198, 1990

3. Allman RM, Goode PS, Patrick MM, Burst N, Bartolucci AA:Pressure ulcer risk factors among hospitalized patients with ac-tivity limitation. JAMA 273:865–870, 1995

4. O’Brien LA, Grisso JA, Maislin G, et al.: Nursing home resi-dents’ preferences for life-sustaining treatments.JAMA274:1775–1779, 1995

5. Ouslander JG, Tymchuk AJ, Krynski MD: Decisions about en-teral tube feeding among the elderly.J Am Geriatr Soc41:70–77, 1993

Survival Estimates for Patients with Abnormal Swal-lowing StudiesCowen ME, Simpson SL, Vettese TEJ Gen Intern Med 12:88–94, 1997

Cowen et al. set out ‘‘to better understand the life ex-pectancy of patients who have an abnormal videofluoro-scopic swallowing study’’ (VFSS). They reviewed chartsof 888 patients who had had a VFSS, and they selected149 patients who were advised to be nonoral feedersbased on VFSS findings. The criteria indicating recom-mendation for nonoral feeding included: (1) inability tosustain arousal for 30 min several times per day, com-bined with neurologic deficits or severe deconditioning;(2) inability to propel more than 25% of the bolus to thepharynx; (3) aspiration of more than one consistency, orfrank, gross aspiration of one consistency, with subopti-mal alertness; or (4) moderate-to-severe (greater than50% of bolus) stasis in the pharynx that could not becleared.

Most patients had serious comorbid conditionsincluding most frequently cerebrovascular accident

(56.4%), hemiplegia (41.6%), congestive heart failure(32.2%), and dementia (20.1%). Exclusionary criteria in-cluded oropharyngeal, thyroid or esophageal cancer orsurgery, neck irradiation, tracheostomy, and existing gas-trostomy. In effect, the 149 patients reviewed were can-didates for percutaneous endoscopic gastrostomy (PEG).

The 149 patients were divided into three catego-ries post-VFSS: (1) PEG tube placed (2) (n 4 80), PEGtube not placed because of rapid clinical improvement(‘‘improved’’ group, n 4 18), and (3) PEG tube notplaced because of other reasons including comfort con-siderations (‘‘comfort’’ group,n 4 51). The comfortgroup included patient/family refusal of tube feeding (n4 28), patients fed by nasogastric tube rather than gas-trostomy (n 4 10), patients who died before receivingPEG (n 4 12), and 1 patient who was transferred.

Median survival of the study population was159 days with 30-day mortality of 27% and 1-year mor-tality of 62%. Causes of death according to death cer-tificates were most commonly cardiac (29.8%) or cere-brovascular (18.3%); pneumonia and chronic obstructivelung disease were each listed on 5.8% of death certifi-cates.

Multivariate analysis revealed four variables thatwere independently associated with increased likelihoodof death: (1) advanced age, (2) reduced serum albumin,(3) disorientation to person, and (4) higher Charlson co-morbidity category [1].

Unadjusted median survival was 33 days for thecomfort group and 181 days for the PEG group. Afteradjusting for independent predictors of increased mortal-ity (advanced age, reduced serum albumin, disorientationto person, and higher comorbidity), patients with PEGtubes placed after VFSS survived twice as long as thosein the comfort group without PEG.

Cowen et al. conclude, ‘‘It appears that patientswho underwent PEG placement survived approximatelytwice as long as those who did not, after controlling forthe four mortality risk factors. It is likely the survivaladvantage was due to other prognostic factors that wereinfluencing the decision to place the PEG tube. However,these remain unidentified. We therefore cannot prove thebenefit of a PEG tube by this study design.’’

The authors continue, ‘‘It is important not tooverstate the applicability of our study to individual de-cision-making. . . . Quality of life, not addressed in ourstudy, must also be considered. . . . Further studies areneeded to provide clinicians, patients, and families withclearer guidelines for these difficult decisions.’’

Cowen et al. also note, ‘‘Such information couldbe obtained from a randomized, controlled trial of pa-tients having and not having PEG tubes. . . . Yet, to con-duct such a study would require the participants (and

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their families) to be sufficiently neutral toward tube feed-ings to allow randomization in the first place. At thispoint in time, enrolling such patients in the United Stateswould be difficult.’’

CommentsDespite this well-conceived and well-executed study byCowen et al., we remain in the dark as to what if any

benefit (or risk) is derived from PEG in terms of mor-tality.

Reference

1. Charlson ME, Pompei P, Ales KL, MacKenzie CR: A newmethod of classifying prognostic comorbidity in longitudinalstudies: development and validation.J Chron Dis 40:373–383,1987

190 D.W. Buchholz and S. Neumann: Recent Dysphagia Literature