Dysmotility of the small intestine in achalasia

Dysmotility of the small intestine in achalasia

T. SCHMIDT, A. PFEIFFER, N. HACKELSBERGER, R. WIDMER, C. PEHL & H. KAESS

Department of Gastroenterology and Hepatology, StaÈdtisches Krankenhaus MuÈ nchen-Bogenhausen,

Akademisches Lehrkrankenhaus, Englschalkingerstrasse 77, D-81925 Munich, Germany

Summary During recent years there has been in-

creasing evidence for extraoesophageal dysfunction in

achalasia. The aim was to investigate whether motil-

ity of the small intestine is abnormal in achalasia.

Thirteen patients (eight men, ®ve women) aged 52 (33±

85) years were studied. They had all previously un-

dergone treatment with pneumatic balloon dilatation

and were free of dysphagia when examined. Ambula-

tory 24-h motility was recorded in the upper jejunum

under standardized caloric intake with a digital da-

talogger and catheter-mounted pressure transducers

located beyond the ligament of Treitz. Visual analysis

was performed by two observers and data underwent

quantitative analysis of phasic contractile events

using a computer program. Normal values were ob-

tained from 50 healthy controls. In the fasting state, a

complete loss of cyclic MMC activity (n � 2), an ab-

normally prolonged phase II (n � 2) and disturbances

in the aboral migration of phase III (n � 5) were ob-

served. Postprandial motor response was absent

(n � 2) or frequently showed a contraction frequency

below the normal range (n � 5). Further abnormali-

ties consisted in hypomotility during phase II (n � 3)

and in a reduced frequency of migrating clustered

contractions in the fasting (n � 2) or postprandial

state (n � 2). In addition, motor events not present in

any healthy subject, giant migrating contractions

(n � 5), retrograde clustered contractions (n � 6) and

repetitive retrograde contractions (n � 3) were iden-

ti®ed. Each patient exhibited ®ndings out of the range

of normal. Dysmotility of the proximal small intestine

is present in achalasia.

Keywords achalasia, small bowel manometry, small

bowel motility.

INTRODUCTION

Achalasia is a motor disorder of the oesophagus char-

acterized by a loss of peristaltic activity of the tubular

oesophagus and by a defective relaxation of an often

hypertensive lower oesophageal sphincter.1 Whatever

the pathogenetic process, it has long been assumed to

be con®ned to the oesophagus. However, in recent

years, there has been increasing evidence for extra-

oesophageal dysfunction in achalasia involving the

stomach,2±5 the gallbladder,3 the sphincter of Oddi6

and the autonomic nervous system.7,8 Abnormal small

bowel motility with a reduced occurrence and a dis-

turbed aboral migration of phase III of the migrating

motor complex (MMC) has been observed during 4-h

recordings with stationary perfused-tube manometry.9

In the last decade, the application of ambulatory long-

term manometry10±12 has resulted in a better under-

standing of the enormous variability of human small

bowel motility, and long-term recordings may allow

the MMC to be better characterized.13,14 Postprandial

motility has, to our knowledge, not been investigated

in achalasia. Therefore, the aim of the present study

was to study fasting and digestive motility in patients

with achalasia by ambulatory 24-h manometry.

MATERIALS AND METHODS

Patients and controls

The achalasia group comprised 13 patients (eight men,

®ve women) aged 52 (33±85) years. The mean duration

of the disease was 3 years, with a range from 3 months

to 20 years. The diagnosis of achalasia was made in all

patients by upper gastrointestinal radiology, endoscopy

and oesophageal manometry. All patients had been

treated with pneumatic dilatation (1±3 sessions) before

the motility studies. According to Vantrappen &

Hellemans,15 the clinical result was classi®ed as good

in ®ve patients or excellent in eight patients, respec-

tively. A barium swallow performed before the motil-

ity study did not reveal oesophageal retention. All

Address for correspondenceDr Thomas Schmidt, Department of Gastroenterology, Hos-pital Bogenhausen, Englschalkingerstrasse 77, D-81925 Mu-nich, Germany. Tel: 049 89 92702061; fax: 049 89 92702486.Received: 11 June 1997Accepted for publication: 4 August 1998

Neurogastroenterol. Mot. (1999) 11, 11±17

Ó 1999 Blackwell Science Ltd 11

patients were free of gastrointestinal symptoms when

studied. Except small bowel manometry, no extra-

oesophageal motility studies or autonomic function

tests were performed. No patient was taking any

medication known to affect gastrointestinal motility,

and no history of diabetes mellitus, neuropathy or

malignancy was present. Normal values for jejunal

motility were obtained in 50 healthy volunteers (28

men, 22 women), aged 26 (19±46) years. All controls

were `tube-naive' and were studied according to the

same protocol as reported previously.16,17

The study protocol was approved by the local ethics

committee and was in accordance with the updated

Declaration of Helsinki. Informed consent was ob-

tained from each subject.

Study protocol

After an overnight fast, intubation of the small intes-

tine was performed transnasally on day I. Using ¯uo-

roscopic control the recording catheter was positioned

with its proximal sensor at the ligament of Treitz.18

Subjects were ambulatory, and physical activity was

not restricted. Activities were documented in a diary.

At 18:00 h a standardized evening meal was ingested

consisting of bread, cheese, sausages and fruit yoghurt

(600 kcal; 40% proteins, 40% carbohydrate, 20% fat).

Intake of tap water was allowed ad libitum. Day II was

spent fasting, until manometry was stopped after a

total recording period of 24 h.

Digital recording system

Intraluminal pressure was recorded with two piezo-

resistive strain gauge transducers spaced at 15-cm in-

tervals in the distal part of a ¯exible polyurethane

catheter (OD 2.3 mm, Keller AG, Winterthur, Swit-

zerland). A catheter with six transducers spaced at 3-

cm intervals was used in three patients and 20 con-

trols, respectively. Calibration of the catheters was

performed in a water bath at 37 °C for 30 min before

each measurement. Pressure data were sampled from

each sensor at a rate of 3 Hz and were stored on a 2-

MByte portable data logger (PMT Megalogger, Dr Ul-

rich Hoppe, GoÈ ttingen, Germany).

Data analysis

Data were downloaded to a personal computer (486 DX

2, ESCOM Computers, Munich, Germany) without

any reduction. Both visual and computer-aided analysis

were undertaken. All visual analysis steps were per-

formed independently by two observers. For automated

analysis, a computer program described in detail else-

where19 was used.

According to the subject's diary, each recording pe-

riod was subdivided into a diurnal and a nocturnal

period (usually from 23:00 to 06:00 h) reference to the

waking (W) or sleeping (S) state of the subject and

marked by mouse operation as regions of interest. In a

similar way, fasting motility, its constituent phases

and postprandial activity were marked and stored on

separate computer ®les. Fasting motility was subdi-

vided into three phases.20 Phase I was de®ned as motor

quiescence.20 Phase II (irregular contractile activity)

was de®ned to start when the contractile activity at

any recording site exceeded more than two phasic

contractions per 10 min.21 Phase III was de®ned as a

rhythmic series of uninterrupted contractions at a

maximal rate of 10±12 min)1 and a duration of more

than 2 min followed by motor quiescence.20 Aboral

migration velocity phase III was determined visually by

dividing the length of the recording segment (15 cm) by

the time taken for the onset of phase III to traverse this

distance.20 MMC cycle length was de®ned as the time

period between the end of successive phase III activi-

ties at the distal recording site. Incomplete MMC cy-

cles were excluded from data analysis. Postprandial

motility was de®ned as the time period from the be-

ginning of the meal to the return of either phase III or

phase I.12

Phase II, III and postprandial contractile activity

underwent rejection of artefacts and quantitative au-

tomated analysis of contractions.19 Brie¯y, phasic

pressure events exceeding an amplitude of 9.7 mmHg,

a duration of 2.8 sec and an area under the curve of

18.4 sec ´ mmHg were considered by the algorithm as

a real contraction. From the data ®les of recognized

contractions, the mean values for contraction fre-

quency (min±1) and contraction amplitude (mmHg)

were calculated.

Finally, phase II and postprandial motility were

screened visually on separate occasions by two ob-

servers for special motor patterns, migrating clustered

contractions (MCCs), retrograde clustered contractions

(RCCs), giant migrating contractions (GMCs) and re-

petitive retrograde contractions. The observers used

the following de®nitions, and only motor events rec-

ognized by both observers were included in the data

analysis. A MCC was de®ned as a rhythmic series of 3±

10 phasic contractions occurring at a frequency of 10±

12 min)1 22 preceded and followed by at least 30 sec of

absent motor activity12 and showing aboral migration

through the whole recording segment of 15 cm. RCCs

were de®ned as MCCs exhibiting migration in an oral

direction. A GMC was de®ned as a single contraction

12 Ó 1999 Blackwell Science Ltd

T. Schmidt et al. Neurogastroenterology and Motility

with a duration of more than 10 sec and an amplitude

of at least 30 mmHg.23 The frequency (per h of phase II

and fed activity, respectively) and migration velocity

(cm sec)1) of MCCs, RCCs and GMCs were calculated.

Repetitive retrograde contractions were de®ned as

groups of single contractions being retropropagated

over at least two recording sites. Only the recordings

with six closely spaced pressure tranducers were

screened for this motor event.

Statistical analysis

Results of visual and computerized analysis were en-

tered into a preprogrammed database (Paradox 1.0;

Borland International Inc., Scotts Valley, CA, USA) for

further statistical workup. The replicate observations

within an individual over the 24-h recording period

[for example the duration of several phase II(W) epi-

sodes] were ®rst averaged to obtain a mean value for

each parameter [a mean duration of phase II(W) for

that individual]. Results were expressed as mean (of

the means) � SEM unless otherwise stated. For com-

parisons, the independent two-sample t-test was ap-

plied. Differences were considered signi®cant at

P < 0.05. For each parameter, the total range of the

values obtained in healthy controls was de®ned as

normal motility.

RESULTS

Fasting motility

MMC cycle In two patients, no phase III activity was

identi®ed over the 24-h period, and only isolated ap-

parently irregular contractions were recorded. The data

characterizing the MMC activity in the remaining 11

patients are shown in Table 1. In the waking (W) and

sleeping (S) state, there was a trend towards a longer

mean MMC cycle length in the patient group caused by

an increased duration of phase II (P < 0.05). In two

patients, both the MMC(W) and the MMC(S) cycle

length exceeded the upper limit of controls due to a

prolonged phase II(W).

Phase II The parameters characterizing phasic con-

tractile activity during phase II are summarized in

Table 2. For the group of achalasia patients, the mean

values for phase II contraction frequency and for the

frequency of migrating clustered contractions (MCCs)

were lower compared with normal subjects (P < 0.05).

In one patient, phase II(W) and phase II(S) contraction

frequency were below the normal range. Two other

patients exhibited hypomotility only during phase

II(W) together with an abnormally low MCC frequen-

cy.

Phase III Phase III activities with an aboral migration

did not differ between patients and controls in terms of

contraction frequency, contraction amplitude and ab-

oral migration velocity. In ®ve patients, disturbed ab-

oral migration of phase III was found, affecting

44 � 15% (range 14±100%) of all phase III activities

over the 24-h period. In these individuals, phase III was

Table 1 Characteristics of the MMC cycles recorded in thewaking (W) and sleeping (S) state in achalasia patients withpreserved MMC activity (n = 11) and healthy controls (n = 50).Values are means � SEM; t-test.

Achalasia Controls

MMC(W)Cycle length [min] 126 � 14* 101 � 5Phase I [min] 12 � 4 16 � 2Phase II [min] 110 � 12* 81 � 5Phase III [min] 3.7 � 0.4 4.4 � 0.2

MMC(S)Cycle length [min] 103 � 4* 85 � 3Phase I [min] 46 � 8 46 � 3Phase II [min] 52 � 6* 34 � 3Phase III [min] 5.0 � 0.2 5.4 � 0.2

*P < 0.05 vs controls.

Table 2 Parameters of phase IIactivity recorded in the waking(W) and sleeping (S) state inachalasia patients with preservedMMC activity (n = 11) and heal-thy controls (n = 50). Values aremeans � SEM; t-test.

Achalasia Controls

Phase II(W)Contraction frequency [min)1] 1.4 � 0.3* 2.0 � 0.1Contraction amplitude [mmHg] 24.3 � 1.9 23.0 � 0.5Migrating Clustered Contractions [h)1] 4.5 � 0.7* 7.5 � 0.6

Phase II(S)Contraction frequency [min)1] 0.7 � 0.3* 1.3 � 0.1Contraction amplitude [mmHg] 25.1 � 1.6 24.1 � 1.0Migrating clustered contractions [h)1] 3.9 � 1.0* 6.2 � 0.6

*P < 0.05 vs controls.


Volume 11, Number 1, February 1999 Jejunal motility in achalasia

either recorded simultaneously at adjacent recording

sites or exhibited a premature distal start and a si-

multaneous ending (Fig. 1).

Postprandial motility

The data on postprandial motility are summarized in

Table 3. After the standardized evening meal, both

patients with absent MMC activity did not show a

digestive motor response. For the group comprising the

remaining 11 patients, a reduced mean contraction

frequency (P < 0.001) was observed compared with

controls. In ®ve patients, the postprandial contraction

frequency was below the normal range.

In addition, the group of achalasics showed a ten-

dency towards a lower mean value for the occurrence

of MCCs compared with the mean value found in

controls (P < 0.05). In two patients, the MCC frequen-

cy was below the normal range.

The duration of digestive motility and the post-

prandial contraction amplitude were not different be-

tween patients and controls.

Special motor patterns

Motor events, not observed in any healthy subject,

were present during fasting and postprandial motility

in the patient group (Fig. 1). Giant migrating contrac-

tions were identi®ed in ®ve patients. They occurred

with a mean frequency (range) of 2.1 � 0.8 (0.2±7.0) h)1,

were characterized by an amplitude of 69 � 7 (48±

83) mmHg, a duration of 12.2 � 0.6 (11±14) sec and

were propagated aborally at a velocity of 4.3 � 0.7 (2.1±

6.0) cm sec)1. Six patients exhibited retrograde clus-

tered contractions. These clusters occurred with a fre-

quency of 1.9 � 0.6 (0.8±4.0) h)1 and showed migration

in an oral direction at a velocity of 1.3 � 0.3 (0.8±

2.3) cm sec)1. Repetitive retrograde contractions were

Figure 1 Upper tracings: disturbed aboral migration of phase III of the migrating motor complex in achalasia. Compressed view ofjejunal motility recordings obtained with two intraluminal pressure sensors located at the ligament of Treitz and 15 cm distally.Normal aboral migration of phase III in a healthy subject (left), simultaneous occurrence of phase III at both recording sites (middle)and premature distal start and simultaneous ending of phase III (right) in two achalasia patients. Lower tracings: expanded view offurther abnormal motor events in achalasia patients not present in any healthy subject. Motility was recorded with two intra-luminal pressure sensors at 15-cm intervals (left), and with six sensors at 3-cm intervals (middle and right tracing) distal to theligament of Treitz. Left: a giant migrating contraction, characterized by an increased amplitude and a prolonged duration comparedwith normal phasic small bowel contractions. Middle: clustered contractions with retrograde migration. Right: repetitive retro-grade contractions.



seen in all three patients who had been studied with six

closely spaced pressure sensors. The pattern consisted

of groups of 2±10 single contractions separated by in-

tercontractile intervals ranging from 11 to 22 sec. Each

single contraction was retropropagated over 2±4 re-

cording sites (3±9 cm) at a mean velocity of 1.2 � 0.2

(0.7±2.3) cm sec)1. Over the 24-h period, 1±3 episodes

of this motor pattern were identi®ed.

Summary of abnormal manometric ®ndings

In our 13 achalasia patients, 37 ®ndings not present in

the control group were observed (number of patients):

absent MMC activity (n � 2), prolonged MMC cycle

length/phase II (n � 2), disturbed aboral migration of

phase III (n � 5), hypomotility (n � 3) and reduced

migrating clustered contractions in phase II (n � 2),

absent postprandial motor response (n � 2), hypomo-

tility (n � 5) and reduced migrating clustered con-

tractions (n � 2) during postprandial motility, giant

migrating contractions (n � 5), retrograde clustered

contractions (n � 6), repetitive retrograde contractions

(n � 3). Each patient had at least one of these motor

abnormalities (Table 4).

DISCUSSION

In achalasia, a well-de®ned motor disorder of the oeso-

phagus, evidence for extraoesophageal dysfunction is

accumulating. Morphological studies have shown

fragmentation of parasympathetic nerves as well as

degeneration of ®bres in the vagal trunc.24±26 Further-

more, a reduction of cells and neuronal depigmentation

in the dorsal motor nuclei of the vagus nerve have been

observed.27,28 Functional studies have demonstrated, at

least in some patients, a reduced gastric acid secretion

during sham feeding or insulin-induced hypo-

glycaemia,29±31 as well as an alteration of gastric

emptying consisting in a more rapid emptying of liq-

uids2,3 and a delayed emptying of solids.5 The biliary

system may be affected by impaired gallbladder con-

tractility3 and sphincter of Oddi hypertension.6 Finally,

autonomic function studies have provided evidence for

impairment in the sympathetic and parasympathetic

nervous system.7,8

On the motor activity of the small intestine, only very

few observations are available. In 1983, Erckenbrecht

et al.9 studied nine achalasia patients with stationary

short-term duodenojejunal manometry. In ®ve of these

pateints no phase III activity was recorded over a fasting

Table 3 Parameters of post-prandial motility in achalasia pa-tients with preserved digestivemotor response (n = 11) andhealthy controls (n = 50). Valuesare means � SEM; t-test.

Achalasia Controls

Duration of postprandial motility [min] 255 � 18 263 � 13Contraction frequency [min)1] 1.4 � 0.3** 3.1 � 0.2Contraction amplitude [mmHg] 23.7 � 1.0 23.7 � 0.5Migrating clustered contractions [h)1] 6.2 � 1.3* 10.8 � 0.9

**P < 0.001 vs controls; *P < 0.05 vs controls.

Table 4 Summary of abnormal manometric ®ndings in the group of 13 achalasia patients

Pt.No.

Absentphase IIIactivity

ProlongedMMCcyclelength

Disturbedmigrationof phaseIII

Phase IIhypomotility*

ReducedMCCs in phase II

Absentpostprandialmotorresponse

Postprandialhypomotility*

ReducedMCCspost-prandialy GMCsz RCCs§ RRCs±

1 + +2 + + +3 +4 +5 + +6 + + + +7 + + + +8 + + +9 + +

10 +11 + + + + +12 + + + + + +13 + + +

*Contraction frequency below the normal range; ymigrating clustered contractions; zgiant migrating contractions; §retrogradeclustered contractions; ±repetitive retrograde contractions.



period of 4 h, and four patients had activity fronts which

occurred simultaneously at the duodenal and the jejunal

level. In 1990, Kellow et al.32 reported on an achalasia

patient with chronic painless diarrhoea due to small

bowel bacterial overgrowth. In a 24-h fasting recording,

no MMCs were seen in the duodenum and jejunum.

Our data con®rm and extend these observations in

that there are at least some patients with achalasia in

whom phase III activity is completely absent and re-

placed by a motor activity of single irregular contrac-

tions similar to that seen in the previous case report.32

Other patients seem to have alterations of the normal

aboral migration of phase III, either with a simulta-

neous occurrence, as observed by Erckenbrecht et al.,9

or with a premature distal start.

Futhermore, quantitative computer-aided analysis of

individual small bowel contractions, not available in

the previous studies,9,32 demonstrated that hypomo-

tility during phase II can be present in some patients as

another feature of abnormal fasting motility.

Postprandial motility has, to our knowledge, not

been investigated in achalasia. Our two patients with

absent MMC activity had no motor response to the

ingested meal. Five of the remaining 11 patients (45%)

showed postprandial hypomotility compared with

controls. A reduced occurrence of migrating clustered

contractions, a highly coordinated physiological motor

pattern12,16 which provides mixing and aboral trans-

port of luminal contents,33 was an additional abnor-

mality in some patients in the digestive period and

during phase II. Oesophageal stasis is unlikely to ex-

plain postprandial hypomotility. Since gastric empty-

ing and autonomic function tests were not performed

in our patients, we cannot exclude that disturbed gas-

tric emptying of solids5 and dysfunction of extraoeso-

phageal vagal ®bres34,35 could play a role.

The site and nature of the lesion responsible for the

observed motor abnormalites are unclear at present. In a

histological study by light microscopy of transmural

biopsies,4 normal neuronal densities in the jejunal

Auerbach's plexus were found, in contrast to the well-

known depletion of ganglion cells in the distal oesoph-

agus.25 This ®nding, however, does not exclude the

presence of dysfunction. As the initiation and aboral

migration of phase III are products of the enteric nervous

system,36,37 the absent or reduced MMC activity and

disturbances of phase III migration point to a neuro-

pathic process at the level of the myenteric plexus.

Similar manometric observations have been made in

patients with neuropathic pseudo±obstruction syn-

dromes38,39 and it is well known that achalasia-like

oesophageal motor disorders can be a manifestation of

more widespread visceral neuropathies with clinically

apparent pseudo-obstruction syndromes.40±42 Two oth-

er abnormalities in our patients, postprandial hypomo-

tility and reduced MCC activity, also point to an

underlying neuropathic process, as they have recently

been identi®ed as manometric features of diabetic

neuropathy.43

Finally what could be the consequences of our ®nd-

ings? Clinically, nonoesophageal gastrointestinal

symptoms seem to be less frequent in achalasia than in

patients with other oesophageal contraction abnor-

malities,44 and no symptoms attributable to disturbed

small bowel function were present in our patients.

Whether small intestinal hypomotiliy during phase II

or the digestive period changes small intestinal transit

is unknown at present. Gastrocecal transit in the

fasting state, assessed by the H2 lactulose breath test,

has been reported to be not signi®cantly different from

healthy controls,2 and no postprandial transit studies

have, to our knowledge, been performed. Owing to its

housekeeping function,45 the absent MMC or a re-

duced MMC activity can be associated with bacterial

overgrowth of the small intestine,20,23,46 as in the pa-

tient described by Kellow et al.32 Data on the rela-

tionship between abnormal motility and changes of the

intestinal micro¯ora, which have recently been ob-

tained in radiation enteropathy,23 are not available in

achalasia at present.

In summary, jejunal motility in achalasia is charac-

terized by disturbed generation and impaired aboral

migration of phase III, postprandial hypomotility and

several other motor abnormalities. We conclude that

disturbed motor function in achalasia is not limited to

the oesophagus, but also can involve the small intestine.

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Dysmotility of the small intestine in achalasia