80 THE BRITISH JOURNAL OF SURGERY

rapidly restore the blood-pressure there seems little cases in which this was done a good result was
doubt that immediate exploration of the great vessels recorded. Ligature or thrombosis of the iliac vein,
is the only measure which gives the patient any hope however, is likely to be followed by Edema of the
of survival. leg, which may be troublesome.
Thirteen cases (including 2 described in this paper) In the 8 further cases reconstructive operations
of arteriovenous fistula following an operation for were performed, though in 3 of these it was necessary
prolapsed intervertebral disk have now been described to introduce an arterial graft. Excellent results
in the literature. In 3 cases the records do not give followed in all the recorded cases in which this was
any account of the symptoms and signs which done.
followed the disk operation. In 3 cases there seems
to have been no indication of bleeding at the time of SUMlMARY
the operation, but in the other 7 there was either It is possible to damage the great vessels during an
moderate external bleeding, severe surgical shock, operation for prolapsed intervertebral disk, and the
or both. ease with which the accident may happen is
Early post-operative signs that an arteriovenous emphasized.
fistula has resulted include ileus and interference with The previously reported cases have been reviewed
micturition. Deep abdominal tenderness and the and z additional cases are described.
development of a murmur and thrill were noted early
in nearly all cases. I wish to express my thanks to Dr. D. H. Davies
The time of onset of cardiac failure was variable who diagnosed Case 2 and referred the patient to
and presumably depended on the size of the shunt and me.
the amount of cardiac reserve. It may come on as
early as a week after the operation or be delayed for REFERENCES
some years. In a number of cases the onset of cardiac BURCHELL, H. B. (1954), Circulation, 10, 577.
failure was the first sign that an arteriovenous fistula DE BAKEY,M. E., COOLEY, D. A., MORRIS,G. C., and
had resulted from the disk operation. COLLINS, H. (1958), Ann. Surg., 147, 646.
FORTUNE, C. (1956), Med. J. Aust., I, 660.
TREATMFiNT GLASS,A. B., and ILGENFRITZ, H. C. (1954), Ann. Surg.,
140, 122.
Operations directed to treatment of the fistula HARBISON, P. S. (1954), Ibid., 140, 342.
have been done at varying times, but the 2 cases HOLSCHER, E. C. (1948),J. BoneJt Surg., 30A, 968.
described here are the earliest (7 days) and latest LEAVENS, M. E., and BRADFORD, F. K. (1953), J . Neurosurg.,
(7 years) after a disk operation that have been 10, 544.
recorded. LINTON,R. R., and WHITE,P. D. (1945), Arch. Surg.,
The onset of cardiac failure is a clear indication Chicago, 50, 6.
that closure of the fistula is an urgent necessity. MACK,J. R. (1956), Amer. Surg., 22, 752.
One patient died during investigation and 4 were MIXTER, W. J., and BARR,J. S. (1934), New Eng1.J. Med.,
treated by ligature operations to exclude the fistula. 21 I . 210.
SEELEY; S. F., HUGHES, C. V., and JAHNKE, E. J. (I954),
There is no doubt that ligature of the common iliac Surgery, 35, 421.
artery above and below a fistula will result in little SMITH,V. M., HUGHES, C. W., SAW,O., JOY, R. J. T.,
impairment of circulation to the corresponding foot and MATTINGLY, T. W. (1957), Arch. intern. Med., 100,
as the collateral circulation is excellent, and in all the 833.

PRIMARY MALIGNANT LYMPHOID TUMOURS OF

THE INTESTINAL TRACT
REPORT OF 37 CASES WITH A STUDY OF FACTORS
INFLUENCING PROGNOSIS
BY I. M . P. DAWSON, J. S. CORNES, AND B. C. MORSON
FROM THE PATHOLOGY DEPARTMENTS OF WESTMINSTER HOSPITAL, ST. MARK’S HOSPITAL AND THE GORDON HOSPITAL

tumours of lymphoid tissue affecting the

MALIGNANT important symptoms were referable to the bowel or
alimentary tract have been recognized for more than because the intestinal lesions appeared larger and
a hundred years, and well over 600 cases involving more important than the other lesions found at
the small and large intestine are now on record. laparotomy or necropsy. The possibility that such
Unfortunately, many of these cases are poorly docu- intestinal lesions might in fact have been part of a
mented, and are of little help to anyone making a more generalized disorder was not often mentioned,
critical study of these tumours. and very few papers stated the criteria used in making
Firstly, at least a third of the recorded cases are the diagnosis of a malignant lymphoma primarily
not certainly primary neoplasms of the intestinal situated in the intestinal tract.
tract, although they are often listed as such in the Secondly, the term ‘lymphosarcoma’ has been
titles of the papers because the earliest and most used by many writers to indicate any or all of the
 MALIGNANT LYMPHOID TUMOURS OF INTESTINE 81
varieties of malignant tumours of lymphoid tissue, in 1947. The tumours were considered clinically
and the finer distinctions of giant follicular lymphoma, to be primary in the intestine on the following
Hodgkin’s disease, and reticulum-cell sarcoma have grounds :-
been ignored. I . When the patients were first seen there was
Thirdly, before 1950, benign lymphoid polyps of no palpable superficial lymphadenopathy.
the rectum were not generally recognized as such 2. Chest radiographs showed no obvious enlarge-
and were often called ‘lymphosarcomas’. Some of ment of the mediastinal lymph-nodes.
these cases have been included in published series 3. The white-blood cell-counts, total and differ-
of malignant lymphomas of the gastro-intestinal ential, were within normal limits.
tract, which explains some of the long-term survivals 4. At laparotomy the bowel lesion predominated,
recorded in the literature (Helwig and Hansen, the only lymph-nodes obviously affected being those
1951). in its immediate neighbourhood.
Fourthly, many of the large series of cases 5. The liver and spleen appeared free of tumour
reported in the literature give little individual case in every case.
data, simply summarizing the main findings in Some cases were found in which the retro-
general tables. Because these tables are usually peritoneal lymph-nodes were affected as well as the
unrelated, it is virtually impossible to trace a par- mesenteric lymph-nodes and bowel. We excluded
ticular case from one table to another. The subject all these cases from our study since the primary
is further confused by some cases being published lesion might well have been in the abdominal lymph-
several times in different journals, or by being re- nodes rather than in the bowel.
published in ever-enlarging series from the same Adequate follow-up data were obtained in 34
medical centre. of the 37 cases. In 33 cases operation specimens
Lymphoid tumours have been reported more fre- were available for study, and in 7 necropsy speci-
quently in the stomach than in the intestinal tract. mens were also available. In the 4 remaining cases
Friedman (1959), for example, has reported a series the diagnoses were based on the results of sig-
of 75 gastric cases from the Mount Sinai Hospital, moidoscopies, barium enemas, rectal biopsies, lymph-
New York, and similar large series have been pub- node biopsies, and the findings at laparotomy.
lished by Madding and Walters (1940), 47 cases; Material for histological study was fixed in 10 per
Allen, Donaldson, Sniffen, and Goodale (1954), cent formol saline and embedded in paraffin. Sec-
44 cases; Thorbjarnarson, Pearse, and Beal (I959), tions were stained using Erhlich’s haematoxylin and
37 cases; Snoddy (1952), 34 cases; Warren and 0 2 5 per cent alcoholic eosin, and Gordon and
Littlefield (1955)~30 cases; Wolferth, Brady, Enter- Sweets’s (1936) silver impregnation technique was
line, and Blakemore (1959), 26 cases; and by others. used to demonstrate reticulin. The cases were then
Very few large series of malignant intestinal lymphoid classified into giant follicular lymphoma, lympho-
tumours have been published. Faulkner and Dockerty sarcoma, Hodgkin’s disease and Hodgkin’s sarcoma,
(1952) described 33 cases seen at the Mayo Clinic, reticulum-cell sarcoma, as described by Harrison
and similar series have been published by Allen and (1953).
others (1954)~34 cases; Raiford (I933), 32 cases; In excluding benign rectal lymphomas from this
Warren (1959)~24 cases; Marcuse and Stout (I950), series we required that such tumours should be
13 cases; and by others. There are very few cases entirely within the mucosa and submucosa, that there
recorded in the British literature. Skrimshire (1955) should be no invasion of the underlying muscle coats,
described 14 cases from St. Thomas’s Hospital, and that there should be at least two discrete germinal
London; Irvine and Johnstone (1955) 17 cases seen follicles present. If the rectal biopsies failed to
at the Western Infirmary, Glasgow; Ogilvie and include the muscle coats, and no germinal follicle
Shaw (1955) 5 cases seen at the Essex County was seen, the biopsies were regarded as inconclusive.
Hospital, Colchester; and Azzopardi and Menzies The diagnosis of a primary malignant rectal lymphoma
(1960) 10 cases from the Postgraduate Medical was only made when the muscle coats were clearly
School, London. invaded by a tumour mass, and in none of these
No one centre can hope to see enough primary cases was any follicular pattern seen. The principal
intestinal cases to be able to lay down any generally findings in 87 cases of benign rectal lymphoma seen
useful prognostic criteria, or to arrive at any definite at St. Mark’s Hospital have been summarized by
conclusions about the best methods of treatment. Morson (1959).
Only through the publication of essential individual A detailed study of cases reported in the litera-
case data is it possible for one centre to share its ture has been made, and 142 intestinal cases have
results with others. For these reasons we wish to been found where there was sufficient individual
set on record the essential data from a series of case data to indicate that one was dealing with a
37 cases of primary malignant lymphoid tumours primary bowel lesion. Only those cases stating the
of the intestinal tract from three major centres, to age and sex of the patient, the site and cell type of
review well-documented primary cases recorded in the tumour, the type of treatment given, and sufficient
the literature, and to consider some of the factors clinical data for the diagnosis of a primary lesion
which appear to influence prognosis. and for provisional follow-up were chosen. For
comparison, I 17 primary malignant lymphomas of
MATERIALS AND METHODS the stomach, similarly recorded in the literature, have
The 37 cases to be described were found during also been studied.
a search through the pathology reports of St. Mark’s Our 37 intestinal cases, together with the 142
and Westminster Hospitals for the past twenty-five intestinal cases and the 117 gastric cases collected
years, and the Gordon Hospital since its re-opening from the literature, form the basis of this report.
6
82 THE BRITISH JOURNAL OF SURGERY
RESULTS habits, and growth was often visible on proctoscopy

intestinal traitare given in' Table-Z. -The age given

is the age at onset of the disease when this could be

FIG. 92.-Ileum, ccecum, and ascending colon. Bulky protu- FIG. g4.--Ileum, czcum, and ascending colon. Aneurysmal
berant growth (reticulum-cell sarcoma) of ccecum. (Care 17.) ileal growth (reticulum-cell sarcoma). (Case 9.)

determined, and if not, the age at diagnosis. The of malaise until the sudden onset of obstruction
length of survival recorded is the duration from the ( I I cases) or perforation (2 cases) necessitated surgical
date of resection or commencing radiotherapy, or intervention.
from the time of diagnosis when no specific treatment Macroscopical Appearances.-In 33 of the 37 cases
was given. the tumours were discrete. In 27 of these the tumours
Symptoms and Signs.-The chief presenting symp- were single, and in 6 cases two or more tumours were
toms and signs are summarized in Table ZZ. The present. Macroscopically, the discrete tumours

FIG. g3.-Descending colon, sigmoid colon, and rectum. FIG. gS.-Transverse, descending, and sigmoid colon.
Two separate annular growths (lymphosarcomas) in recto- Multiple lymphomatous polyposis (giant follicular lymphoma
sigmoid region. Note smooth appearance of colon due to pattern). (Case 34.)
quiescent ulcerative colitis. (Case 21.)

small intestinal tumours most commonly presented appeared to be of three types: 11 were bulky pro-
with nausea, vomiting, and other signs suggesting tuberant growths (Fig. 92); 21 were annular or
intestinal obstruction, and a mass was often palpable plaque-like thickenings of the bowel wall (Fig. 93);
in the abdomen. Growths in the colon and rectum and I presented as an aneurysmal dilatation of the
most often presented with bleeding and altered bowel terminal ileum (Fig. 94). In the 4 remaining cases
 MALIGNANT LYMPHOID TUMOURS OF INTESTINE 83
the tumours presented as a multiple lymphomatous lymphosarcomas penetrating the muscle coats, with
polyposis affecting long segments of the intestinal the sigmoid growth extending outwards into the
tract (Fig. 95). Further details of these 4 cases have pericolic fat (Fig. 93). A more detailed description of
been published elsewhere (Cornes, 19.61). There this case is available elsewhere (Cornes, Smith, and
was no tendency for any one histological type of Southwood, 1961).
tumour to be associated with any particular macro- One case (No. 26) had a large lymphocytic
scopical appearance, to produce multiple tumours or lymphosarcoma of the rectum with a small

1 1 1
REGIONAL OUTCOMB
NUMBERCELL
kyB
Im*.
SEX AGE LOCATION LYMPH- SURGICAL RADIO- Survival
TYPE NODES REMOVAL
INVOLVED
THERAPY -
Systemic Patient
Rek%ce Disease
fl. Dead
---
--- -
---
- -- ----
I
2
M.
M.
89
62
J
J and I
S
M
LS
LS
0
?
++ 0
0
A
D
I I0
0
3
4
M.
M.
48
47
J and I
J and I
M
M
LS
LS
++ ++ ++ D
A
16
6
4
1
5 M. 41 I S RS ? + 0 D 3 0
+++ +++
6 M. 49 I S LS 0 D 3 6
7 M. 52 I S LS ? D 2 0
8 F.
M.
50
58 1
I S
S
RS
RS
+? ++ ++
D
D 2
I
9
10 M. 41 I S RS + 0 0 A I1
11
12
F.
F.
56
24
I
I
S
S
HD
RS
?
1
++ 0
+ 0
?
+
?
D
? I"8
13 M.
M.
54
59
IC
IC
S
S
RS
LS
++ ++ 0
++
0
+ 0
0
D
A 4 2
14
15
16
M.
M.
18
60
IC
C
S
S
RS
HD 0
? ++ 0
0
?
0
?
A
?
I 5
?
17
18
M.
F.
52
71
C
C
S
S
RS
RS
0
0
++ 0
+ 0
0
0
+? A
D
2
1
1
4
19 M.
M.
29
60
C
Cand R
S
M
HD
LS
?
0
++ 0
0
?
0 0 A
?
IS
?
o
20
21 F. 42 Cand R M
S
LS
RS
0
?
+0 0 + 0
+ A
D
I 2
I0
M. 44 R 0 0
22
23 F. 57 R S LS 0 ++ 0
+
0 0 A 1s 3
++
F. 65 R S RS 0 + D 7
24
25 F. 61 R S
S
RS
LS
++ 0
+ 0 0 D
D 1
0
0
26 M. 57 R 0 0 0
27
28
M. 65 R S
S
LS
LS 0
+ 0
++ 0
+ A
A 3
4
2
M. R
29 F.
54
36 R S
S
LS
RS
++ 0
0
+ A
D
17 6
I0
F. 35 R
+++
30
F. 66 R S LS 0 0 A 2 6
31
32 F. 53 R S
M
HD
LS
++ 0
++ A
D
1 9
F. 54 R 1 5
33
34 M. 75 D-R MP
MP
GF
LS
+ 0
+ + A
D
I
2
I0
6
F. 44 D-R 0
35
36 M.
M.
51
50
J-1
C-R
MP
MP
HD
LS
+0 0
+ 0
+
D 2
37 A 1, 3 1 3
I l l I I I

C, Colon' D Duodenum; I, Ileum; IC, Ileocecal; J, Jejunum; 5, Rectum; S, Single tumour; M, Multiple tumours; MP, Lympho-
matou; poiyposis; GF, Giant follicular lymphoma; HD, Hodglun's disease; LS, Lymphosarcoma; RS, Reticulum-cell sarcoma.

diffuse polyposis, or to show a predilection for any Table I I . - h b j o ~ PRESENTINGSYMPTOMS

AND SIGNS IN
one site. 37 CASESOF PRIMARY MALIGNANTINTESTINAL
Lymph-nodes.-The finding of enlarged mesenteric LYMPHOMAS
lymph-nodes at operation did not necessarily indi-
cate involvement by tumour or that the intestinal
growths were inoperable. In 4 cases surgeons re-
ported enlarged lymph-nodes at operation, but no
tumour was found when the lymph-nodes were sec-
tioned and examined histologically. In 5 cases no Bleeding per
enlarged lymph-nodes were seen at operation, and Severe rectum I 8 2 XI
abdo-
none were found when the specimens were examined minal pain,
in the laboratory, yet tumour was found histologically nausea,
vomiting
and
8 I 0 9
in each case. In only 8 cases was the finding of Malaise, vague
pains, etc.
enlarged lymph-nodes at operation actually associated Symptoms 5 7 2 I4
not
with their involvement by growth. stated I 2 0 3
Associated Disorders.-One case (No. 21) compli- Visible growth
in rectum 0 12 3 IS
cated a chronic ulcerative colitis. This patient gave Palpable abdo-
minal mass
a fifteen years' history of intermittent diarrhea and Signs 5 2 I 8
of ob-
bleeding. At laparotomy two tumours were found, suuct ion 8 2 I 11
one in the sigmoid colon and one in the rectum. Signs of per-
foration 2 0 0 2
Sections showed a chronic, quiescent ulcerative Signs not stated 2 2 0 4
colitis affecting the whole colon, and two lymphocytic
84 THE BRITISH JOURNAL OF SURGERY

mucus-secreting adenocarcinoma immediately below S t u d y of Primary Cases recorded in the

it at the anorectal junction. In a second case (No. 7) Literature.-
resection of a lymphocytic lymphosarcoma of the Survival Studies.-We have attempted to extend
terminal ileum was followed one year later by the our observations by a study of similar cases recorded
development of an adenocarcinoma of the sigmoid in the literature. Table I I I gives the follow-up data
colon. I n a third case (No. 17) resection of a on 176 intestinal cases and 117 gastric cases. The
reticulum-cell sarcoma of the ascending colon was 176 intestinal cases include 34 cases from our present
followed eighteen months later by the development study and 142 cases collected from the literature.
of five separate carcinomas of the rectum and sig- The table shows that about half of the recorded
moid colon. Further details of these three cases intestinal cases have been followed for less than
have been given elsewhere (Cornes, 1960). A fourth I year, and that very few cases have been followed

case (No. 3 ) died sixteen years after the resection of for 10 years. Most of the recorded deaths were in
multiple lymphocytic lymphosarcomas of the jejunum the first year. None of the deaths occurring after
and ileum. At necropsy there was a carcinoma of the 10 years were due to the original disease, and there
upper lobe of the left lung, but no evidence of any is no record of any of these patients surviving more
lymphosarcoma. than 10 years with evidence of recurrent disease.
Follow-up Studies.-Of 34 cases with follow-up Several patients who survived 5 years had clinical
data available, 17 are dead. Three deaths were due evidence of either a local recurrence or a systemic
to post-operative complications, 3 were due to other spread of their disease, and some of the recorded
Table I V.-UNCORRECTED
5-YEAR AND 10-YEAR SURVIVAL Table V.-INFLUENCE OF AGEON LENGTH
OF SURVIVAL
FIGURES
OF RECORDED
CASES OF PRIMARY MALIGNANT IN CASES OF PRIMARYMALIGNANT
INTESTINAL
T VWDU~XAA T . ~ . ~ T ~ T \ ~ Z A O

deal IS in the 5-10-year period were due to the

causes, and I I deaths were directly due to the disease. orig ial disease.
Of 17 survivors, 7 have either a local recurrence or 'able IV gives the uncorrected 5-year and 10-year
are suffering from generalized disease, and 10 patients survival figures for the cases listed in Table 111.
are alive, well, and apparently free from recurrent These percentages are based simply on the total
disease. Taking all the available results into con- number of cases studied, the number of patients
sideration it would appear that not more than one- surviving the 5-year and ro-year periods, and the
quarter of all cases will survive ten years from the total number of deaths. They do not include the
time of diagnosis. patients who are alive, but who have not been
 MALIGNANT LYMPHOID TUMOURS OF INTESTINE 85
followed for the 5-year and 10-year periods. These Multiple Turnours.-The gastro-intestinal tract is
figures therefore give a gloomier picture of these often secondarily involved in generalized malignant
disorders than corrected survival figures would lymphomatosis, and in such cases the tumour
give. deposits are usually multiple, and may be fairly
Age and Sex.-Age at onset did not appear to widespread. These cases are usually associated with
have any significant influence upon the site of a bad prognosis. Multiple primary growths other
intestinal lesions. Thirty-two of the 176 intestinal than lymphomatous polyposis also occur and were
cases under review occurred in patients under the
over the age of 40 years. These cases are compared
in Table V, where it will be seen that the overall
prognosis is slightly better in the under-zo group,
and if the cases surviving more than one year are AUTHORS ~URGICAI
-
age of 20 years, and 116 cases occurred in patients Table VZI.-DATA FROM g RECORDED
MALIGNANTCBCALLYMPHOMAS

EMO OVAL
CASES OF PRIMARY

ALIVE SURVIVAL
OR ~

DEAD yr. (mth.

Table VI.-DATA FROM 8 RECORDED CASES OF PRIMARY
MALIGNANTDUODENAL LYMPHOMAS
Jackson and
I I
Parker + 0 -
Erbes and
Stehlin
D’Alonzo
++ + 0
-~ Warren and
0 0

Kaplan, Tyler, and

Canale + 0 0
Lulenski
Portmann,
+ ? +
Case, Ribando, and Dunne, and
Halstead
Jackson and Parker
+
0
0
0
?
3
Hazard
Pattison
++ +0 ++
Skrimshire 3 Warren and
Marcuse and Stout
Skrimshire
0
0
0
0

++
0 5
I0
Lulenski
Bresnihan
++ 0
0
0
0
Marcuse and Stout 0 I3 Azzopardi and
Marcuse and Stout 0 + 44 Menzies + + 0

considered the outlook appears even more favourable. found in 18 of the intestinal cases under review.
The majority of the tumours found in young people Five of these cases survived 5 years, and 3 survived
were lymphosarcomas; 26 of the 32 cases were of for 10 years or more. When strict criteria are used
this type, 5 were reticulum-cell sarcomas, and I was for the diagnosis of primary malignant intestinal
a giant follicular lymphoma (Marcuse and Stout, lymphomas, there is no good evidence that these
1950). There was no case of primary Hodgkin’s multiple tumours have a worse prognosis than the
disease or Hodgkin’s sarcoma in the under-zo age- solitary neoplasms.
group, and none of the primary reticulum-cell Lymph-nodes.-The influence of regional lymph-
sarcomas occurred in children under the age of node involvement on prognosis was difficult to assess.
10 years. Thirty-four of the gastric and intestinal cases under
Primary malignant intestinal lymphomas are review survived for 10years. In 8 cases the histology
approximately twice as common in men as in women. of the regional lymph-nodes was not recorded, in
One hundred and fifteen cases occurred in males, 18 cases the nodes were said to be free from involve-
and 61 in females. Under the age of 20 years, males ment, and in 8 cases the nodes were said to be
outnumbered females by more than three to one, involved. Regional lymph-node involvement does
25 cases occurring in males, and 7 in females. No not therefore preclude the chance of a long survival.
other significant relationship could be found between Treatment.-Of I 3 intestinal cases surviving 10
sex, site of tumour, cell type, or length of survival. years, 4 were treated by surgery alone, and 9 by
Site and Cell Type of Lesion.-Tables IZI, ZV surgery and radiotherapy. We could find no well-
suggest that lesions in the stomach have a better documented record of any primary intestinal case
prognosis than intestinal lesions. Lesions in the treated solely by radiotherapy surviving for 10years.
duodenum have a poor prognosis compared with Too few cases have been recorded to assess the
similar lesions in other parts of the intestinal tract. influence of radiotherapy, but from the data available
Eight well-documented primary duodenal cases it was not obvious that radiotherapy significantly
recorded in the literature are summarized in Table VZ. lengthened a patient’s chance of survival. It did,
In the second case in the table the patient was however, produce a remarkable clinical improvement
reported to have survived the immediate post- in a number of cases, and there were several reports
operative period, but no further follow-up details of the striking reduction in size of abdominal
were given. The remaining cases were all dead. masses, alleviation of obstructive symptoms, and
Apart from the duodenum, the situation of lesions improvement in the patient’s sense of well-
in other parts of the intestinal tract did not appear being.
to have any significant influence upon prognosis,
and there was no good evidence to suggest that DISCUSSION
czcal lesions necessarily had any better prognosis Selection of Cases.-Since malignant tumours
than similar lesions elsewhere (see Table VZI) (Usher of lymphoid tissue often originate in the retro-
and Dixon, 1943). Giant follicular lymphomas and peritoneal lymph-nodes it is not surprising that
lymphosarcomas appear to have a better prognosis gastro-intestinal tract involvement is seen in at least
than Hodgkin’s disease, Hodgkin’s sarcoma, or 10-20 per cent of all cases of malignant lymphoid
reticulum-cell sarcoma. tumour (Gall and Mallory, 1942). Willis (1953)
86 THE BRITISH JOURNAL OF SURGERY

found that nearly two-thirds of his cases of lympho- in other parts of the intestinal tract does not appear
sarcoma appeared to originate in the abdominal to influence the patient’s length of survival after
lymph-nodes. These findings probably account for treatment. Usher and Dixon (I943), Marshall and
the many hundreds of cases of malignant lymphoid Meissner (1950) , Lockwood (1952), and Azzopardi
tumour affecting the gastro-intestinal tract recorded and Menzies (1960)have all suggested that caecal
in the literature. Unfortunately, very few papers lesions have a better prognosis than similar lesions
have stated the criteria used in making this diagnosis in other parts of the intestinal tract, whilst Allen and
and it is therefore difficult to recognize which cases others (1954)and Warren and Littlefield (1955)have
are primary lesions and which are not. Because suggested that they have a worse prognosis. These
several well-known reviews of the literature include differences of opinion are probably due to the small
a number of cases which are not apparently primary number of cases studied. Our study includes 9 caecal
bowel tumours, their discussions of the factors which tumours, and we could find no significant evidence
appear to influence the prognosis of primary bowel that these tumours behaved any differently from
lesions are of questionable value. similar lesions in other parts of the large intestine,
Only primary lesions of the stomach and intestines jejunum, or ileum.
have been referred to in this study, and where there Multiple Turnours.-It is often suggested that
was any doubt about a recorded case it has not been multiple primary tumours have a worse prognosis
included. We have not used the large series recorded than single tumours. Many reviews include tumours
by Balfour and McCann (IS~O), Madding and which are not primary bowel lesions: when strict
Walters (1940),Usher and Dixon (I943),McSwain criteria are used in the diagnosis of a primary bowel
and Beal(1944), Spellberg and Zivin (1949)~ Marshall lesion there is no good evidence that multiple lesions
and Meissner (I~so), Faulkner and Dockerty (1952)~do have a worse prognosis. Faulkner and Dockerty
Crile, Hazard, and Allen (I952), Burman and van (1952)found that multiple primary growths had a
Wyk (1955)~ Hunt, Broders, and Hightower (1958), better prognosis after resection than single growths,
Thorbjarnarson and others (1959)~ Jackson and Coady and in our own series multiple lesions had a similar
(1959)~ or Warren (1959)because these papers give prognosis to the single ones.
only general information, and do not provide indi- Multiple lymphomatous polyposis is an unusual
vidual case data. We have not used the cases reported condition in which sessile or pedunculated polyps
by Raiford (1933),or by Patterson, Callow, and composed of varying types of lymphoid tissue involve
Ettinger (1958),because of our uncertainty about considerable segments of the gastro-intestinal tract.
the cell types described. We have not used the In the majority of cases the polyps extend from the
Lahey Clinic series reported by Warren and Littlefield pyloric end of the stomach to the anorectal junction.
(1955)because the age and sex of the patients were Because of the extensive gastro-intestinal tract
not given, and because they included a group of involvement radical surgery is impossible, and such
‘unclassified lymphomas ’ which had a surprisingly cases have therefore got a bad prognosis. In a recent
good prognosis. In our experience ‘unclassified study of 27 cases (Cornes, 1961)the majority of 7
lymphomas’ have a very bad prognosis because they patients were dead within 2-3 years from the time
are usually anaplastic sarcomas which we find difficult of diagnosis, and the longest recorded survival was
to classify as Hodgkin’s sarcoma, reticulum-cell only 4 years (Swenson, 1943).
sarcoma, or lymphoblastic lymphosarcoma (see also Lymph-node Involvement. - It is perhaps
Lumb, 1954). Inevitably some cases have been over- understandable that most surgeons should equate
looked and the selection of cases for publication may enlarged mesenteric lymph-nodes in these cases with
not fully reflect the general behaviour of these secondary tumour involvement. Yet many of the
tumours since some were published simply to enlarged nodes show only follicular hyperplasia and
illustrate cases of long survival and others to sinus reaction. If the bowel lesion is considered to
illustrate features of small-bowel tumours. Despite be a large inoperable carcinoma and a biopsy is taken
these and other limitations, however, certain features only from a mesenteric lymph-node the true nature
emerge which appear to have some significance. of the bowel lesion may be missed. The surgeon
Influence of Site.-Primary malignant lym- may then be denied the benefit of second thoughts
phomas of the gastro-intestinal tract are found most about the operability of the lesion, the only treat-
frequently in the stomach. In the intestines these ment which holds out any real hope of cure for the
tumours are found most frequently in the ileum. patient, and the patient may be denied the benefits
Apart from the caecum, large-intestinal lesions are of radiotherapy. Regional lymph-node involvement
uncommon. The large number of cases affecting was found in 52 per cent of our 37 cases, and it did
the rectum and sigmoid colon in our series of 37 cases not appear to have any significant effect upon prog-
simply reflects the specialized work of St. Mark’s nosis. This surprising finding has been noted by
Hospital and the Gordon Hospital in the field of others, e.g., Marshall and Meissner (1950)~ Marcuse
colonic and rectal surgery, and the large number of and Stout (1950), Allen and others (1954),and
cases referred to these centres from different parts Azzopardi and Menzies (1960).
of the world. Influence of Cell Type.-We were unable to
Gastric lesions appear to have a better prognosis find any record of benign Hodgkin’s disease (para-
than similar lesions in the intestines, probably because granuloma) affecting the gastro-intestinal tract, nor
they give rise to symptoms earlier, are easier to any record of a primary giant follicular lymphoma
diagnose, and are more amenable to surgery. Duo- of the stomach. Nearly all the tumours in young
denal lesions appear to have a bad prognosis because children were lymphosarcomas, and reticulum-cell
of their special situation, and the technical diffi- sarcoma, Hodgkin’s disease, and Hodgkin’s sarcoma
culties of surgical removal. The situation of lesions were all found in an older age-group.
 MALIGNANT LYMPHOID TUMOURS OF INTESTINE 87
Some writers have found that in cases of primary feature of some of these lesions is their large size,
malignant lymphoid tumours of the gastro-intestinal and this alone should not deter a surgeon from
tract there appeared to be no significant relationship attempting a surgical removal. There are several
between cell type and survival (Warren and Lulenski, reports of cases at first thought to have been inoper-
1942; Usher and Dixon, 1943 ;Faulkner and Dockerty, able because of the size of the bowel lesion, which
1952; and Irvine and Johnstone, 1955). Marcuse survived for many years after operation. The triad
and Stout (1950), Skrimshire (1955), and Azzopardi of a large tumour of the bowel with a short clinical
and Menzies (1960) have noticed that primary giant history, and a striking lack of emaciation, should
follicular lymphomas have a better prognosis than suggest the diagnosis of malignant lymphoid tumour
the other primary malignant lymphomas. Allen and rather than carcinoma. Large carcinomas are usually
others (1954) noticed that primary reticulum-cell necrotic, and are often associated with severe emacia-
sarcoma, lymphoblastic lymphosarcoma, and Hodg- tion, toxic symptoms, metastases, and a bad prognosis.
kin’s sarcoma appeared to have a worse prognosis A few cases similar to the third case in our series
than primary giant follicular lymphoma, lymphocytic have been described in which the tunours were
lymphosarcoma, and Hodgkin’s disease. Raiford multiple, or involved fairly long segments of the
(1932) and Spellberg and Zivin (1949) noticed that bowel, and prevented their complete surgical removal.
primary reticulum-cell sarcomas had a poorer prog- Despite incomplete removal, some of these intestinal
nosis than the primary lymphosarcomas. Until more cases survived several years, some with and some
primary cases surviving the 5-year and 10-year without post-operative radiotherapy (Allen and others,
periods are on record it will not be possible to come 1954). Similar results have been reported in the
to any definite conclusion, but our survey tends to gastric cases (Pattison, 1934; Stout, 1953; Thorb-
suggest that there is a relationship between cell type jarnarson and others, 1959).
and length of survival. Giant follicular lymphomas There is general agreement that radiotherapy
appear to have the best prognosis, and lympho- should be used in inoperable cases, in cases with
sarcomas appear to have a better prognosis than regional lymph-node involvement, and in those cases
reticulum-cell sarcomas, Hodgkin’s disease, and in which tumour is found at the resected end of an
Hodgkin’s sarcoma. operation specimen. The value of post-operative
Associated Diseases.-Primary malignant lym- radiotherapy in cases in which the bowel lesions
phomas of the colon are uncommon and the finding have been completely removed and the regional
of malignant lymphomas complicating 7 cases of lymph-nodes are not involved is still a matter for
chronic ulcerative colitis (Cornes, Smith, and South- dispute. Several cases surviving the 10-year period
wood, 1961) may have some significance; a.relation- have been treated by surgery alone, so post-operative
ship between these two disorders cannot be excluded. radiotherapy is not essential for a long survival. We
Too few cases have been reported to assess the could find no compelling data for or against radio-
influence of ulcerative colitis on length of survival. therapy in such cases. In those cases shown to be
However, of the 7 cases recorded, 4 died within 18 associated with a bad prognosis (lymphoblastic
months, z were alive and had local recurrences within lymphosarcoma, reticulum-cell sarcoma, Hodgkin’s
9 months of surgical resections, and only I patient disease, and Hodgkin’s sarcoma), a prophylactic,
was reported alive and well I year after operation. post-operative course of radiotherapy would appear
Four of our 37 intestinal cases were associated to be a wise procedure.
with carcinomas, 3 of which were primary carcinomas A striking feature of all reported series of malig-
in the colon or rectum. Very few cases of this type nant lymphoid tumours of the intestinal tract is the
have been described (Cornes, 1960). These unusual high percentage of deaths occurring in the fmt two
findings underline the importance of an adequate years from the time of diagnosis or treatment. This
clinical follow-up on all cases, and urge caution is partly accounted for by post-operative deaths, and
against assuming that a second growth in the intestinal partly by the fact that quite a number of the recorded
tract is necessarily a recurrence or a metastasis from cases may not have been primary bowel tumours.
the original primary tumour. In some cases it is possible that the bowel lesions
Treatment.-Some authors regard 5-year sur- were only the earliest manifestation of a generalized
vivals after treatment as cures or apparent cures. disease, and were noticed before the more distant
But there are several reports of patients developing a lesions became obvious.
local recurrence or a generalized spread of their In any study of malignant lymphoid tumours
disease, and dying in the 5-10-year period. We have there are always 2-3 per cent of the cases which
found no report of any patient with a primary show a long survival irrespective of the extent of
intestinal lesion surviving more than 10 years with lymph-node involvement, or of treatment (Stout,
evidence of recurrent disease, and none of the deaths 1942). We have already drawn attention to the
in patients who lived for 10 years or more after records of long survivals after the incomplete removal
operation were related to their original disease. For of some malignant intestinal lymphomas. The fact
these reasons we think it wise to regard only 10-year that some patients have been complaining of symp-
survivals as apparent cures. toms for four or five years before they were first seen
All the patients with a primary intestinal lesion further suggests that some tumours can remain
who lived for 10 years from the time of diagnosis localized for long periods of time before spreading
had been treated by surgery, or by a combination to other parts of the body. Why some tumours
of surgery and radiotherapy, and there is general remain localized for such long periods of time has
agreement that a wide surgical removal of the never been fully explained, and there is still much
intestinal lesion together with the neighbouring to be learnt about the behaviour of these tumours
lymph-nodes is the treatment of choice. A striking and the best methods of treating them.
88 THE BRITISH JOURNAL OF SURGERY
SUMMARY BIBLIOGRAPHY
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