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                 Lipogranulomatous Lymphangitis in Canine Intestinal Lymphangiectasia
                   H. J. Van Kruiningen, G. E. Lees, D. W. Hayden, D. J. Meuten and W. A. Rogers
                                               Vet Pathol 1984 21: 377
                                         DOI: 10.1177/030098588402100403

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Vet. Pathol. 21: 377-383 (1984)




      Lipogranulomatous Lymphangitis in Canine Intestinal Lymphangiectasia

                            G.
          H. J. VANKRUININGEN, E. LEES, D. W. HAYDEN, J. MEUTEN,
                                                    D.         and W. A. ROGERS


    Department of Pathobiology, University of Connecticut, Storrs, CT, Department of Veterinary Clinical
     Sciences and Department of Veterinary Pathobiology, College of Veterinary Medicine, University of
    Minnesota, St. Paul MN, Department of Veterinary Pathobiology and Department of Veterinary Clinical
             Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH


   Abstract. Lipogranulomatous lymphangitis of the intestine occurred in four dogs with intestinal lymphangiectasia. All four
presented with chronic diarrhea; three had ascites and two had hypoalbuminemia. Lipogranulomas appeared in lymphatics,
often at the point of mesenteric attachment, of small intestine, ileum, or ileum and colon. Mesenteric lymphatics were
obstructed and villous lacteals were distended. Mesenteric lymph nodes of one dog contained large lipid spaces and that same
animal had a solitary subcapsular lipogranuloma of the liver. This disorder is one of several that result in protein-losing
enteropathy in dogs.


   Lipogranulomas of intestinal lymphatics first were                      analyses were done. After clinical studies, one dog was killed
described, among other lesions, in a case study of nine                    painlessly and necropsied, one required intestinal resection,
dogs with chronic enteric disease and hypoproteinemia                      one died, but only ileum and lymph nodes were available for
                                                                           study, and one was lost to follow-up after exploratory surgery
published in 1973.9 Their case 4, a six-month-old Irish                    and biopsy.
setter, had diarrhea, ascites, and weight loss which                          Tissue samples were fixed in 10% buffered formalin, proc-
terminated in death. Lipid granulomas occurred adja-                       essed, embedded in parafin, sectioned, and stained with
cent to lymphatics along the entire mesenteric attach-                     hematoxylin and eosin (HE). Later the periodic acid-Schiff,
ment to the small intestine. Their case 5 , a five-year-                   oil-red-0, Ziehl-Neelsen, von Kossa's, and Schultz cholesterol
                                                                           techniques were applied. Granulomas from one dog were
old male Labrador retriever with severe ascites, had
                                                                           dissected from the tissues and fixed in 4% glutaraldehyde,
similar white-yellow masses, 1 to 5 mm in diameter                         and ascitic fluid and feces from the same animal were proc-
adjacent to dilated mesenteric lymphatics, and re-                         essed for electron microscopy.'
covered following extensive medical treatment that in-                        In an attempt to demonstrate transmissibility, seven six-
cluded steroids, antibiotics, and diuretics. The granu-                    week-old mongrel puppies were fed chest blood, heart blood,
lomas have been regarded as secondary lesions, i.e., as                    bile, spleen, intestines, and liver (from dog 1) which had been
                                                                           stored by freezing. Three days later a crude emulsion of 30 to
a response to stagnated chyle in the disorder called                       40 granulomas (dog 1) in saline was injected intravenously
intestinal lymphangiecta~ia.~~ abstract from Ber-
                               A brief                                     into four dogs. The animals were fed a commercial dry, cereal
lin documented the occurrence of granulomatous lym-                        base dog food product, examined at intervals for six months,
phangitis with lipid deposits in the muscularis and                        and then necropsied.
subserosa of the small intestine in three of ten dogs with
protein-losing enteropathy.I4 Most recently a four-year-                                               Results
old temer cross with both intestinal lymphangiectasia                       Clinical features and gross lesions
and the granulomas was described, and it was con-                             Dog I: A five-year-old, 6 kg, male Yorkshire temer
cluded that lymphatic hypertension leads to fat leakage                    was presented with bloated abdomen, loose stool,
                                              We
and subsequent granulomatous re~ponse.~ describe                           wheezing, and coughing. Over a four-month period
here the findings in four additional cases and discuss                     clinical signs fluctuated in intensity and included diar-
the pathogenesis and comparative significance.                             rhea, flatulence, ascites, partial anorexia, weight fluc-
                                                                           tuation, normal temperature, and lethargy. A serum
                  Materials and Methods                                    chemistry screen and complete blood count conducted
   Four dogs which presented with diarrhea were examined                   1 1 days after first presentation revealed hypoprotein-
clinically, and complete blood counts and serum chemistry                  emia (3.9 g/dl), hypoalbuminemia (1.3 g/dl), and gran-
                                                                      311

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318                                                    Van Kruiningen e a/.
                                                                      f

 ulocytic shift to the left (white blood cell count 13,805,               were “very thickened and discolored;” accordingly, af-
 segmented neutrophils 57%, band forms 4%, metamye-                       fected ileum, cecum, and a portion of proximal colon
 locytes 16%).When the dog failed to respond to medical                   were resected. The dog made an uneventful recovery.
 treatment euthanasia was elected.                                        A portion of pyloric wall contained no histologic ab-
    At necropsy the abdomen contained translucent as-                     normalities, but the abnormal ileum had focal granu-
 citic fluid, and major portions of the small intestine                   lomatous lymphangitis.
 appeared abnormal. Beginning 35 cm distal to the                            Dog 3: A-six-year-old, 2.3 kg, male Maltese was
 pylorus, the intestinal serosa (subserosa) was studded                   presented with a history of diarrhea and weight loss of
 with approximately 50 scattered soap-white, irregular                    two months duration. Vomiting had occurred during
 to round, raised nodules that varied in size from pin-                   the early part of this period but was no longer a prob-
 point to 4 mm in diameter. These occurred primarily                      lem. The dog was very thin and lethargic, had a dis-
 at the site of mesenteric attachment, but also coursed                   tended abdomen thought to represent ascites, and had
 along lymphatics around the circumference of the gut.                    a thin hair coat and ventral alopecia. The animal was
 They sometimes occurred in clusters. Proximal je-                        afebrile, and had hypoproteinemia (3.2 g/dl), hypoal-
junum was affected most severely over a 14-cm seg-                        buminemia ( 1.4 g/dl), and leukocytosis (26,400 white
 ment. Mid-jejunum was affected focally; distal jejunum                   blood cells with a granulocytic shift to the left [seg-
was diseased over a 30-cm segment, and ileum had few                      mented neutrophils 85%, band forms lo%]). On hos-
 foci. In some affected areas, indiscrete gray stellate                   pital day two, the dog became hypothermic and weak,
 plaques occurred in the mesenteric attachment to the                     and died.
 intestine. These varied from 2 to 6 cm in diameter.                         Only ileum and regional lymph nodes were available
Some affected segments, particularly distal jejunum,                      for examination. The portion of intestines was thick-
had 20 to 25 bright red bands of blood-engorged vessels                   ened, had engorged blood vessels, and was violet in
that extended from (affected) mesenteric attachment                       color. Several soap-white, round to stellate nodules, 3
around the circumference of the gut. Opening of the                       to 8 mm in size occurred along lymphatic vessels at the
intestine revealed prominent white villi (lacteal ectasia)                point of mesenteric attachment to ileum.
throughout. The liver had one similar pinhead-sized,                        Dog 4: A five-year-old, male Yorkshire temer was
soap-white nodule on its surface.                                         presented with a history of bloody diarrhea of several
   Dog 2: A five-year-old, 32 kg, male German shepherd                    weeks duration and declining packed cell volume. Clin-
dog was presented with a history of chronic intermittent                  ical signs included ascites and edema of the limbs and
diarrhea of five months duration. The diarrhea was                        scrotum. At exploratory surgery multiple small white
described as yellowish and watery, without blood, but                     lesions were seen occurring along lymphatic vessels on
sometimes containing mucus. Clinical signs were rather                    the serosal surface of most of the small intestine. (A
unremarkable, including only dry, lusterless coat, and                    more detailed history was not available.)
firm, formed feces. Hemogram, serum chemistry, ra-
diography, proctoscopy, and colon biopsy all were nor-                    Histology
mal, and the dog was discharged with a diagnosis of                         Dogs 1-4: In the intestinal mucosa many of the villi
imtable colon.                                                           had dilated lacteals (fig. l), and lamina propria at the
   The dog was presented for a second time seven                         base of the crypts contained an excessive population of
months later, at six years of age. Intermittent diarrhea                 lymphocytes and plasma cells, and some eosinophils.
continued to be the major clinical sign; formed feces                    Submucosal lymphoid nodules were enlarged; muscu-
always were followed within ten minutes by one or two                    laris mucosa was disrupted in places. Submucosa, mus-
fluid movements. In addition, the dog had begun losing                   cularis, subserosa, and mesentery contained various-
weight (weighed 30 kg), and vomiting occurred when-                      sized granulomas, some of which obviously had been
ever the dog was fed more than eight ounces of canned                    apparent grossly (figs. 2-5). The granulomas were irreg-
dog food at a meal. A serum chemistry screen and                         ular in shape and consisted of amorphous foamy to
complete blood count were normal (serum albumin 2.7                      fibrillar, gray, sometimes eosinophilic, sometimes ba-
g/dl), as were urinalysis and endoparasite checks, but                   sophilic material, surrounded by foamy grayish baso-
radiography suggested persistent narrowing of the py-                    philic macrophages 6 to 15 cells deep (fig. 6). Some
lorus and delayed gastric emptying. A pyloroplasty was                   granulomas had an adjacent associated lymphocyte
done, and at this time the intestines were examined for                  aggregate. Submucosal lymphatics were distended. The
explanation of the chronic diarrhea. The distal 15 cm                    submucosa contained some very large, thick-walled
of ileum, proximal 10 cm of colon, and entire cecum                      vessels (lymphatics) surrounded by granulomas or lym-


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                                               LipogranulomatousLymphangitis                                                 379




   Fig. 1: Severely dilated intestinal lacteals; dog 3. HE.
   Fig. 2: Granulomatous lymphangitis of submucosa and muscularis;dog 4. HE.


phoid nodules. Gray amorphous material similar to                       Oil-red-0 staining of the granulomas revealed floccular
that in the granulomas occurred beneath Peyer’s                         red coloration of the amorphous material and stippled
patches, presumably in lymphatics. Inflammatory lym-                    granular red staining of the macrophages. Periodic acid-
phoid nodules occurred deep in the submucosa, and                       Schiff, Ziehl-Neelsen, von Kossa’s, and Schultz choles-
less frequently in muscularis and subserosa. Neurons                    terol techniques all yielded negative results.
of Meisner’s plexuses appeared prominent and exces-                        Regional lymph nodes were available for study in
sive in number. The larger submucosal granulomas                        dog 1. Peripheral sinuses contained many large lipid
focally distorted submucosa and mucosa. Muscle layers                   spaces and peripheral and medullary sinuses were filled
contained granulomas in apparent association with                       with pink foamy macrophages similar to those seen in
lymphatics. In some sections muscle layers were edem-                   the intestinal granulomas.
atous and fibrotic, muscle cells apparently having been
replaced by fibrocytes. The serosa was thickened fo-
cally. In one dog, small numbers of crystalline spicules,               Other studies
that were birefringent in polarized light, appeared                        Electron microscopy failed to demonstrate virus par-
within the amorphous material at the centers of the                     ticles or bacteria in the granulomas and ascitic fluid of
granulomas. These were not seen in the other cases.                     one dog, and no virus particles were seen in the feces



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380                                                      Van Kruiningen el al.




  Fig. 3: Subserosal granuloma containing amorphous lipid material: dog I. HE.
  Fig. 4: Protruding subserosal granuloma containing lipid vacuoles and amorphous fibrillar material; dog 3. HE.


either. No evidence of illness occurred in the seven        pathology departments at a number of locations in this
experimental dogs over six months, and there were no        country, in Canada, and in Europe.’. I4.l4
lesions at necropsy.                                           Similar lipogranulomas have been described, though
                                                            infrequently, in intestinal lymphangiectasia of man.
                                                            The original description of the human disorder, pub-
                         Discussion                         lished in 1961, shows “serosal lymph vessels occluded
   Our first encounter with the lipogranulomas de- by foamy macrophages” (their fig. 5).27 The authors
scribed occurred in 1971, and mention of them first reported yellow nodules, up to 5 mm in size, along the
was made in the veterinary literature in 1973.9Because course of serosal lymphatics. Subsequently similar le-
the lesions are obvious (fig. 7) it is doubtful that they sions were called lymphangiectatic cysts, some of which
occurred but went unrecognized earlier. All four dogs contained clusters of lipophages (their fig. 4).22The
studied by us had chronic diarrhea (table I), three had cysts appeared as small white or yellow nodules, meas-
ascites, two had hypoalbuminemia, and one had edema uring 0.2 to 1 cm in diameter, they were round to oval,
of the extremities. Clinically these animals had evidence sometimes irregular, and they occurred along the course
of enteric and abdominal weeping of lymphatic con- of small blood vessels, in lymphatics draining into the
tents, i.e., features consistent with a diagnosis of intes- mesentery along the small intestine, especially jejunum
tinal lymphangiectasia.                                     and ileum. The cysts occurred in 60 of 300 consecutive
   The granulomas that we describe are rather special, necropsies and without correlation to disease. In a few
and appear to occur in only a portion of dogs with cysts the material had become inspissated. Histologi-
intestinal lymphangiectasia. They have been recognized cally, the material described by these two groups is
recently at veterinary clinics, teaching hospitals, and identical to that illustrated by us. The cyst contents



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                                                 Lipogranulomatous Lymphangitis                                         38 I




  Fig. 5: Small subserosal granuloma-part of larger protruding nodule. Cuff of macrophages surrounding amorphous
material: dog I . HE.
  Fig. 6: Portion of a subserosal granuloma; cuff of foamy macrophages (M) surrounding amorphous material (A) and few
pyknotic or karyorrhectic nuclei within amorphous material (A). Fatty acid silhouettes in amorphous material at top; dog 2.
HE.




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382                                                           Van Kruiningen el a/.

                                                               matosis of spleen and lymph nodes.”. ‘3.28 Rabbits fed
                                                               liquid petrolatum developed similar lymph nodes.25
                                                                   It is of interest that lipogranulomas never have been
                                                               reported in experimental intestinal lymphatic obstruc-
                                                               tion, even when dogs were used as subjects and the
                                                               course of experimental disease was followed for one
                                                               year.’,8.  17.29 This observation suggests that the granu-

                                                               lomas are evoked by provocative lipid substances which
                                                               are present in the intestinal lymphatics of some dogs,
                                                               but not of others. Perhaps the cause of acquired intes-
                                                               tinal lymphangiectasia is taken orally and absorbed and
   Fig. 7: Gross appearance of intralymphatic subserosal li-   transported with dietary lipids, via lymphatics, subse-
pogranulomas (Rogers, unpublished case material .from Ohio quently producing regional lymphadenitis, lymphangi-
State University College of Veterinary Medicine). Larger nod- tis, or lymphangiectasia-some of which is ultimately
ular lesions are less typical than smaller ones (arrow). Bar = granulomatous.
1 cm.                                                                                                      as
                                                                   In the dog described most re~ently,~ well as our
                                                               dog 1, solitary lipogranulomas identical to those in
                                                               intestinal lymphatics occurred subcapsularly in the
were inspissated and met by granulomatous response liver. It is difficult to explain how stagnated intestinal
in each dog. It is surprising that lymphangiectatic cysts chyle could contribute to such distant granuloma for-
or granulomas have not been reported more frequently mation. The authors have examined one unrelated dog,
in human intestinal lymphangiectasia, even when re- which came to necropsy for dermatitis and had neither
sections and necropsies were                ’*’8*20*23
                                                               diarrhea nor ascites,.-in which similar oval soap-white
   Intestinal lymph stagnation also occurs in Whipple’s nodules appeared subserosally over the intestine, pan-
disease of man.6 Soft nodular elevations, which were creas, liver, and diaphragm, as well as subpleurally. The
white, and up to 1 cm in diameter and 4 to 5 mm in nodules were accompanied by very little granulomatous
height occurred along the mesenteric attachment of a response, and no apparent lymphatic obstruction, and
patient with Whipple’s disease.*’ “Xanthomatous foci” histologically they appeared partially mineralized, like
in the wall of the small intestine, apparently in lym- calcium soaps. The latter case is unexplained.
phatics, are well illustrated (their fig. la). The large lipid    Some dogs with protein-losing enteropathy and in-
vacuoles occurring in the mesenteric lymph nodes of testinal lymphatic lipogranulomas recover.’. l4 People
affected dogs also have been reported in Whipple’s with intestinal lymphangiectasia appear to respond to
disease,” and in what is called idiopathic lipogranulo- cortico~teroids,~. or substitution of medium chain
                                                                                    lo



                                 Table I. Canine intestinal lipogranulomatous lymphangitis
                                                                                                                  HYPO-
                                                                                         Ven- Leu- Neu-           albu-
 Dog                                  Age                      Diar-         As-
                    Breed                                                                tral kocy- tro-           min-     Diseased segment
number                               (Yeas)         Sex        rhea         cites
                                                                                        edema tosis Dhilia        emia

      1    Yorkshire temer             5             M           +            +             -            -    +   1.3     Most of small intestine
      2    German shepherd dog         5             M           +            -             -            -    -   2.7     25 cm of ileum and co-
                                                                                                                            lon
      3    Maltese                     6             M           +            +             -           +     +   1.4     Short segment of ileum
      4    Yorkshire temer             5             M           +            +             +           +                 Most of small intestine
           Basset hounda               1%            M           +            +             -           +     +
           Irish setterb               YZ            M           +            +             +           -     -   1.45    Entire small intestine
           Labrador retrieverb         5             M           -            +            -            -     +   1.9     Small intestine
           Temer mongrelc              4             F           -            +            -            +     +    +      Throughout the small
                                                                                                                            intestine
  a   Meuten (unpublished case material from Texas A & M College of Veterinary Medicine).
      Finco et aL9
      Burns5



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                                                  LipogranulomatousLymphangitis                                                          383

triglyceride diets for those containing long chain tri-                           lymphangiectasia of the intestine. Surg Gynecol Obstet
glycerides.’”” Clinical remission occurred in the dog                             151~391-395, 1980
                                                                            13    LIBER,  A.F.; ROSE,H.G.: Saturated hydrocarbons in fol-
with intestinal lymphangiectasia following similar diet
                                                                                  licular lipidosis of the spleen. Arch Pathol 83: I 16- 122,
therapy. I 5                                                                       I967
                                                                            14                 H.;
                                                                                  LOPPNOW, SCHWARTZ-PORSCHE,                D.: Further study of
                   Acknowledgements                                               protein-losing enteropathy in the dog. Vet Pathol 17: 105,
  Supported in part by funds for Canine Research provided                         1980
by the 1963 Connecticut Legislature and by a grant from the                 l5    OLSON,                      J.F.:
                                                                                            N.C.; ZIMMER, Protein-losing enteropathy
National Foundation for Ileitis and Colitis, Inc.                                 secondary to intestinal lymphangiectasia in a dog. J Am
  The authors thank Drs. C. Moseley and L.M. Siegfried for                        Vet Med Assoc 173:271-274, 1978
case history information, and Ms. Patricia Timmins for man-                 I6               H.;          T.E.;
                                                                                  ORBECK, LARSEN, Hovls, T.: Transient intestinal
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Request reprints from Dr. H.J. Van Kruiningen, Department of Pathobiology, University of Connecticut, Storrs, CT 06268
(USA).



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