Gamna-Gandy Bodies in Surgical Neuropathology Specimens

Transcription

Journal of Neuropathology and Experimental Neurology
Copyright q 2004 by the American Association of Neuropathologists
Vol. 63, No. 2
February, 2004
pp. 106 112
Gamna-Gandy Bodies in Surgical Neuropathology Specimens: Observations and a
Historical Note
B. K. KLEINSCHMIDT-DEMASTERS, MD
Key Words:
noma.
Cavernous angioma; Cholesterol granuloma of bone; Hemosiderin; Pituitary adenoma; Sacral cyst; Schwan-
INTRODUCTION
Stedman’s Medical Dictionary, 27th edition, defines
Gamna-Gandy bodies (synonyms: Gandy-Gamna bodies,
Gamna-Gandy nodules, tobacco flecks, siderotic nodules)
as ‘‘small, firm, spheroidal or irregular foci that are yellow-brown, brown, or rusted color, occurring chiefly in
the spleen in such conditions as congestive splenomegaly
and sickle cell disease, and consisting of relatively dense
fibrous tissue with collagenous fibers impregnated with
iron pigment and calcium salts; probably result from organization and scarring of sites where small perivascular
hemorrhages occurred’’ (1). Still described under this eponymic designation in several general (2–8) and surgical
(9) pathology texts published between 1965 and 1995,
the entity, under this name, has all but disappeared from
several other well-known contemporary general pathology books (10) and surgical pathology texts (11), including more recent editions of the same texts where it was
formerly mentioned (12). In some cases, textbooks have
eliminated the term in their indices and it is only by careful scrutiny of the section on atrial myxomas that one
finds the term ‘‘G-G body’’ inconspicuously hiding in the
middle of a paragraph (13). Few texts provide even black
and white illustrations of the G-G body (2–4), although
a beautiful color photomicrograph of a G-G body in an
atrial myxoma can be found in the C. D. M. Fletcher’s,
Diagnostic Histopathology of Tumors (14).
From Departments of Pathology, Neurology, and Neurosurgery, University of Colorado Health Sciences Center, Denver, Colorado.
Correspondence to: B. K. Kleinschmidt-DeMasters, MD, University
of Colorado Health Sciences Center, 4200 E. Ninth Ave., Denver, CO
80262. E-mail: [email protected]
Whither goest the Gamna-Gandy body? It was still a
viable term taught during my pathology residency training in the early 1980s, but hard to find in textbooks even
then. As noted above, the eponymic designation has now
either been discarded altogether or the description has
been simplified to a more mundane ‘‘multiple brown
scars containing hemosiderin’’ (8). Indeed, even in the
few instances where the term has been retained, the emphasis over the years has shifted away from the collagenous scar aspects of the G-G body (as described in
spleen) to the mineralization of collagenous fibers by
iron, and to a lesser extent, calcium salts (as described in
atrial myxoma). However, going back to Gamna’s original description, and older papers in the literature, this
mineralization, although always present and the essential
component of G-G bodies, was not the histological feature of the nodules that captured the imagination of multiple investigators in the late 1920s and 1930s.
What then did Carlos Gamna, an Italian physician
(1866–1950), describe? Between 1921 and 1927 he published 3 articles (15–17) giving a detailed histological
description of the lesion that bears his name. It should be
acknowledged that others had described and even illustrated similar findings earlier, including the French physician Charles Gandy (1872–1943) in 1902 (18, and again
in 1906 (19), Giovanni Marini in 1902 (20), and Stengel
in 1904 (21). Schuippisser provided a particularly beautiful color drawing of the entity in his 1922 publication
(22) (Fig. 1A). Nevertheless, Gamna gave one of the best
descriptions and was given credit soon after his publications. Gamna described ‘‘disseminated granulomata in
the pulp of the spleen composed of foreign-body giant
cells, hemosiderin deposits, calcium precipitate, hyalinized connective tissue fibers, and curious, straw-colored,
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Abstract. Gamna-Gandy (G-G) bodies are classically defined as spheroidal yellow-brown foci consisting of dense fibrous
tissue and collagenous fibers encrusted with iron pigments and calcium salts. These siderotic nodules were first described in
the spleen early in the twentieth century and for a short time were considered to be caused by fungal infection due to the
presence of unusual ‘‘bamboo-like and articulated’’ fibers in the lesions that vaguely mimicked mycelia forms. This notion
was proven to be incorrect in the 1930s and G-G bodies are now considered to result from organization of small hemorrhages.
Although originally reported in splenomegaly, G-G bodies are well-recognized findings in atrial myxomas where they form
linear arrays of mineral-encrusted fibers, often at the edge of resolving hemorrhages. They rarely have been reported in lymph
nodes, thymoma, thyroid adenoma, and renal cell carcinoma. Curiously, published examples of G-G bodies in central nervous
system (CNS) neoplasms or vascular malformations have not appeared, despite the known tendency for bleeding, even
recurrent episodes of bleeding, in several types of these lesions. Since 1999 I have accrued all the examples of G-G bodies
that I have observed in my practice of surgical neuropathology. These cases are presented here and the historical aspects of
the entity are reviewed.
GAMNA-GANDY BODIES
same year, however, more rigorous scientific studies were
published that proved fungal infection to be incorrect.
Fasiani and Oselladore in 1929 reported being able to
experimentally produce G-G bodies in cats by the injection of alcohol (27). However, it wasn’t until 2 years later,
in 1931, that definitive microbiology studies were published that completely dispelled a fungal causation for GG bodies. Reimann and Kurotchkin studied the spleen in
6 cases of primary and cirrhotic splenomegaly and found
no correlation between whether G-G bodies were present
and whether fungus could be cultured from that spleen
(29). Even after selectively dissecting out the G-G bodies
that they could grossly identify in 1 spleen and spreading
the material directly onto agar slants and 30 agar tubes,
no fungus could be cultured from any of the siderotic
nodules. They even went further and proved that the organisms that they did recover were completely nonpathogenic by inoculating 12 monkeys with the fungus; none
died from fungal infection nor showed splenic abnormalities when they were killed 12 to 18 months later (29).
Reimann and Kurotchkin astutely pointed out that G-G
bodies could be found in several different diseases of the
spleen (tuberculosis, kala-azar, and syphilis), making it
unlikely that there was a single infectious cause for G-G
bodies. They even mentioned briefly that they had seen
G-G bodies in an adenomatous thyroid gland, foreshadowing reports that would appear 40 years later.
With the loss of a possible fungal etiology, the emphasis on the mycelial-like, waxy forms in the lesions
declined and the recognition increased that iron, and to a
lesser extent calcium, encrustation of degenerated tissue
fibers was the essential component of the G-G bodies. As
is often the case with diseases bearing eponymic designations, a gain in the understanding of the etiology parallels a decline in the need for an eponym. Hence, today
a simple descriptor of ‘‘iron encrustation’’ or ‘‘mineral
impregnation of degenerated tissue fibers’’ has replaced
‘‘Gamna-Gandy’’ body and is all that is necessary to recognize this phenomenon. Coupled with the fact that pathologists and physicians in general have advocated decreased usage of eponymic designations, the term
‘‘Gamna-Gandy body’’ seldom appears in our more recent pathology literature or reference tomes.
Interestingly, despite this decline of the use of the term
by pathologists there appears to be renewed interest in
the entity by radiologists. As the resolution of imaging
studies became greater, more radiologists have recognized the characteristic features of these lesions on imaging studies, especially magnetic resonance imaging
(MRI). If the G-G nodules contain a significant amount
of calcium, they can be seen on plain radiographs and
computerized tomographic (CT) images (30). However,
MRI best defines them, and G-G nodules appear as spotlike, low signal intensity lesions on all pulse sequences
(30). They are described as ‘‘best seen on gradient-echo
J Neuropathol Exp Neurol, Vol 63, February, 2004
waxy formation, spheroid, semilunar, or bamboo-shaped,
resembling mycelian structures’’ (quoted by Tedeschi et
al [23]). Gamna termed this lesion that he found in cases
of splenomegaly unassociated with cirrhosis, ‘‘siderotic
splenogranulomatosis,’’ clearly suspecting that the iron
pigment was an important component. What piqued the
interest of him and others, however, were the straw colored, waxy, bamboo-shaped structures noted in the nodules. Years earlier, Marini appears to have considered
these waxy mycelial-like structures to be degenerated
elastic fibers and not infectious agents (20). Nevertheless,
others, including Oberling in 1928 (24) and Jaffe and Hill
in 1928 (25), favored fungal infection as the cause.
Given the fact that the cause was debated, a noncommittal eponymic designation became quickly attached to
these lesions with ‘‘waxy mycelial-like structures’’ and
multinucleated giant cells. Indeed, within only a couple
of years both Oberling (24) in 1928 and Fasiani and Oselladore in 1929 (27) had used the term ‘‘Gandy-Gamna’’
nodules in their publications. Obviously these 2 authors
gave pre-eminence to the even earlier work of Gandy (18,
19), while DeVecchi et al in a 1929 article described
‘‘aree di Gamna’’ in the spleen and ascribed the finding
solely to Gamna (26). However, according to Morehead
the appellation ‘‘Gamna-Gandy body’’ had achieved popularity even earlier, beginning in 1926 (2), and the hyphenated version won out.
In 1929, Hu et al published an observational study of
‘‘Gandi-Gamna’’ bodies (sic, note the permutations the
spelling these gentlemen’s names suffered even 75 years
ago!) They made the point that neither the ‘‘wavy,
branching fibers’’ in siderotic nodules of the spleen (Fig.
1B, left) nor the ‘‘brittle, rod-like fibers’’ (Fig. 1B, middle) resembled the fungi they had recovered by culture
from 3 cases of splenomegaly that they had studied (Fig.
1B, right) (28). Parenthetically, these authors were actually more struck by the similarity between the ‘‘wavy,
branching fibers’’ (Fig. 1B, left) and any possible fungus
and stated that in their opinion the ‘‘brittle, rod-like’’
(waxy, refractile) fibers they found ‘‘were less likely to
be mistaken for mycelium’’ (28). Nevertheless, Hu et al
recognized that neither type of filament found in siderotic
nodules (Fig. 1B, left and center) resembled mycotic hyphae since they looked and stained entirely differently
than the fungi they had recovered from spleens (Fig. 1B,
right). They also noted that on close observation, collagen fibers in G-G bodies could be seen to show a gradation from normal to pigment encrustation, all within
the same fiber.
Then, as now, however, purely morphological studies
failed to convince those who held contrary convictions.
Given the presence of multinucleated giant cells and septated branching fibers in the lesions, it is perhaps somewhat understandable, in retrospect, why some authors believed so strongly in an infectious etiology. Within the
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KLEINSCHMIDT-DEMASTERS
108
GAMNA-GANDY BODIES
cell carcinoma, with a brief report in Archives of Pathology and Laboratory Medicine, signals a resurgence
of interest by pathologists in these forgotten structures
(43). The paper certainly contributes beautiful color pictures of G-G bodies to the contemporary literature.
Probably due to diminished interest in the historical
aspects of the entity, G-G bodies have not been reported
in other organs and tumor types. Certainly other disease
entities provide the hemorrhages, especially recurrent
hemorrhages, which seem to be the requisite substrate on
which G-G bodies occur. After encountering a particularly prominent example of a G-G body in 1999, I have
made a concerted effort to seek out these structures over
the past several years in my surgical neuropathology material.
I have accrued 10 examples in CNS and PNS neoplasms and vascular malformations, most of which have
a well-recognized tendency for spontaneous or repetitive
hemorrhage. The Table provides a listing of the lesions
seen, and I have attempted to place them in descending
order of prominence, based on size and how conspicuous
they were on a given slide and the number of slides involved. Certainly G-G bodies containing waxy, refractile
fibers or a well-developed and focal collagenous scar are
the most eye-catching. However, some cases with copious
iron-encrusted fibers arranged around the edge of large
resolving clots occasionally are also able to get one’s attention! Cases 1 to 10 listed in the Table could be considered ‘‘true’’ G-G bodies in that they were obvious
enough to be found, even if the observer were not specifically searching for them. Cases 1 through 5 were
‘‘case report’’ quality.
However on a much smaller and more focal scale the
identical process happens in some CNS lesions that are
←
Fig. 1. A: Color drawing of Gamna-Gandy body illustrated from the 1922 article by Schuppisser (22) shows the linear blueblack encrusted fibers as well as the waxy septate degenerating collagen fibers that caught the eye of early workers in this field.
B: Black and white drawings from the 1929 article by Hu et al (28) that showed that there was no morphological identity between
the wavy encrusted fibers (left) or the waxy, septate, bamboo-like fibers (center) seen in Gamna-Gandy bodies and the fungi that
could be cultured from spleens (drawn by the authors at right). These authors argued strongly against an infectious fungal etiology
for Gamna-Gandy bodies. C: One type of Gamna-Gandy body, here seen adjacent to a large resolving clot in a metastatic
melanoma contains linear blue-black iron-encrusted fibers that are easily detected on hematoxylin and eosin but are in their full
glory as robin’s egg blue fingers admixed with macrophages on Gomori’s iron stain. This is a nearly identical illustration to that
show in reference 14 as a Gamna-Gandy body in an atrial myxoma. Original magnification: 3200. D, E: The other type of
Gamna-Gandy body, most similar to that described in the spleen, is illustrated in this photomicrograph taken from a cystic
‘‘baseball-sized’’ ulnar nerve schwannoma. Note the numerous multinucleated giant cells (panel D, inset) and linear blue-black
delicate wavy encrusted fibers (seen at higher power in panel E) that overshadow the collagenous background. H&E, original
magnifications: 3100, 3200. F: A similar ‘‘spleen-type’’ Gamna-Gandy body in a pituitary adenoma shows more collagen and
demonstrates thicker, chunkier, encrusted collagen fibers. H&E, original magnification: 3200. G: On higher power, these thicker
encrusted fibers seen in panel F are associated with waxy, refractile, yellow, bamboo-like, ‘‘septate’’ degenerating collagen fibers
and gradations of encrustation along the same fiber can be identified (inset, white arrowhead). Original magnification: 31000.
H: A semilunar waxy, bamboo-like degenerating fiber encircles a small blood vessel in a cavernous angioma (case 6) H&E,
original magnification: 31000. I: Delicate septate encrusted fibers seen focally in a supratentorial primitive neuroectodermal
tumor (PNET) can cause the pathologist to stop and ponder their origin. Original magnification: 3100. J, K: A minute swirl of
encrusted fibers seen near the meninges in an anaplastic meningioma showed strong histochemical reaction with Gomori’s stain
for iron (panel J) and almost no reaction (i.e. black staining) with Von Kossa stain for calcium. Original magnifications: 3200.
T2 sequences, due to the blooming artifact, caused by the
superparamagnetic effects of hemosiderin within those
hemorrhagic remnants ’’ (30). Several CT and MRI reports of G-G bodies in the spleen have recently appeared
(31–35).
MRI has allowed rediscovery of what pathologists already knew 75 years ago, namely that G-G bodies are
very frequent when specifically looked for in spleen. Oberling found G-G bodies in 10% (24 of 200) spleens and
DeVecchi et al in 18% (30 of 169) spleens (quoted by
Tedeschi et al [23]). A more contemporary morphological
study demonstrated that 44% of spleens contained G-G
bodies in cases of portal hypertension (36).
Imaging techniques have also identified G-G bodies in
cardiac myxomas and have verified that they are not rare
in this site either (37, 38). Basso et al found that 10% of
102 cardiac myxomas were heavily calcified (‘‘cardiac
lithomyxoma’’) on x-ray and gross inspection; half of
heavily calcified myxomas showed Gamma-Gandy (sic)
body formation (38). G-G bodies in cardiac myxomas
have been reported several times by pathologists (39–41),
but are obviously seen much more frequently than the
few case reports in the literature would suggest. Indeed
the beautiful example of a G-G body illustrated in the
Fletcher surgical pathology text noted above comes from
a cardiac myxoma (14). The existence of single case reports of G-G nodules in thymoma (23) and follicular adenoma of the thyroid (42) are also likely misleading. Reimann and Kurotchkin noted G-G in adenomatous thyroid
gland and several early authors (Gamna and Schuppisser)
mention finding G-G bodies in retroperitoneal lymph
nodes near cirrhotic livers (quoted by Tedeschi et al [23]).
Perhaps the recent 2003 sighting of G-G bodies in a renal
109
No
Yes, 11 Large clot
No
No
Yes, 1 Moderate clot
Yes, 1 Small focal clot
No
9. Myxopapillary ependymoma, 1
of 2
10. Cavernous angioma, 1 of 1
11. Supratentorial PNET
12. Anaplastic oligodendroglioma
13. Brain abscess with hemorrhage
14. Anaplastic oligodendroglioma
15. Anaplastic meningioma
Yes, 1
Focal process but no
collagen scar
No, focal linear encrusted fibers near meninges
No, focal encrusted degenerating collagen
fibers near vessels
No, focal, minute focus
of linear encrusted fibers
No, focal linear encrusted fibers near meninges
No
No
Yes, 11
Yes, 1
Yes, 1
No
No
Yes, 1
Yes, 11
No
Yes, 111
Yes, 111
No
No
Yes, 111
Yellow,
refractile
‘‘articulated
fibers’’
Yes, 11
Yes,1
No
Yes, 1
No
Yes, 1
No
Yes, 1
No
No
No
No
No
Yes, 11
No
Yes, 111 but most associated with cholesterol clefts
No
No
No
No
No
No
No
Yes, 1
No
No
No
No
Iron-encrusted
fibers adjacent
to macrophages
No
Yes, 111
Multinucleated
giant cells
Key: PNET 5 primitive neuroectodermal tumor; subjective grading of process with 1 5 feature present but not prominent; 11 5 moderate prominence; and
111 5 feature very prominent.
Yes, 11 Large clot
No
7. Benign sacral cyst, 2 of 3
Yes, 111
Yes, 11 Moderate size
clot with numerous
cholesterol clefts
Yes, 111 Large clot
No
No
Yes, 111
Yes, 11 Also numerous
encrusted vessels
No
Yes, 11 Several nodules
Yes, 11
No
Yes, 111
Yes, 111 Large clot
No
G-G body within
focal
hyalinized nodule
4. Benign sacral cyst, 2 of 12
5. Pituitary adenoma, 2 of 3
1. Metastatic melanoma, 3 of 3
2. Schwannoma of ulnar nerve, 1
of 7
3. Cholesterol granuloma of temporal bone, 1 of 12
Tumor type, number of
slides involved
Linear, iron-encrusted
fibers adjacent to
resolving clot
TABLE
110
GAMNA-GANDY BODIES
too could find areas where single degenerated waxy collagen fibers showed gradations to full blue-black mineral
encrustation (Fig. 1G, inset).
In this series, the first type of G-G body (subacute,
‘‘atrial myxoma-like’’) was prominent around large areas
of resolving hemorrhage in a metastatic melanoma (case
1), 2 congenital, non-neoplastic sacral cysts (cases 4 and
7), and a cholesterol granuloma of the temporal bone
(case 3). Cases with a nodular, densely collagenous scar,
linear or mycelial iron-encrusted fibers, waxy bamboolike yellow refractile material, but no clot were the most
focal type of G-G body (remote, ‘‘spleen-like’’). Examples included a cystic, baseball-sized schwannoma of the
ulnar nerve (case 2), a mixed growth hormone-prolactin
secreting pituitary adenoma (case 5), and all 3 cavernous
angiomas (cases 6, 8, and 10). A myxopapillary ependymoma (case 9) also showed a focal dense collagen deposit and linear iron-encrusted fibers, but lacked the
waxy, refractile, bamboo-like degenerative collagen material. A brain abscess that manifested hemorrhage and
thickened, collagenous blood vessels with mineralization
and waxy refractile fibers qualified as a ‘‘miniature version’’ of the same process (case 13) due to its limited
nature. More focal linear iron-encrusted fibers unassociated with waxy degenerated collagen fibers of collagen
deposition were also seen in several CNS tumors that lack
a collagenous background or abundant thick-walled collagenized blood vessels. These ‘‘miniature’’ examples included the supratentorial PNET (case 11, Fig. 1I). This
case showed beautiful septate linear encrusted fibers (Fig.
1I) that might make the pathologist pause and ponder
their origin. Given the limited amount of collagen in a
supratentorial PNET, it is not surprising that these were
seen adjacent to blood vessels also containing organismlike wavy linear encrustations. Wavy linear encrusted fibers were also focally present in 2 anaplastic oligodendrogliomas (cases 12 and 14) and an anaplastic
meningioma (case 15). In cases where sufficient tissue on
deeper levels allowed for multiple stains to be performed,
the iron stain (Gomori’s iron stain) (Fig. 1J) showed considerably stronger histochemical reaction than the Von
Kossa stain for calcium (Fig. 1K, note absence of black
staining) in these linear encrustations.
Clearly, what is described and illustrated in this review
of my surgical neuropathology material is hardly unique.
Virtually every reader can probably cite even better examples from their own surgical or autopsy neuropathology case files. The likely—and indeed the desired—response to the examples shown in this paper might be
‘‘I’ve seen that many times before but never knew it had
a name’’ (or maybe even thought it deserved a name!)
To set the record straight, G-G bodies in surgical neuropathology probably don’t deserve a special designation
generally devoid of collagenous substrate for mineralization, save for the meninges or the hyalinized walls of
blood vessels. Cases 11 to 15 are examples of this very
focal and ‘‘miniature versions’’ of the same thing. Admittedly, the limited nature of the process barely deserved mention in the microscopic description of the corresponding surgical pathology report, and in most
instances I found them solely because I was hunting for
them. But, in this regard, the supratentorial primitive neuroectodermal tumor (PNET) (Case 11) contained enough
of the segmented, septate, ‘‘fungal-like’’ encrustations
that they caught the eye of the referring pathologist who
submitted the case. These miniature versions really do
not deserve the appellation of ‘‘Gamna-Gandy body’’ but
do serve to underscore the fact that the same encrustation
of degenerated collagen fibers can occur in CNS tumors,
albeit to a very limited degree. Clearly, the amount of
collagen available in the CNS for scarring is limited to
select areas around blood vessels or in meninges, and one
would not expect the process to be as well-developed in
the CNS than in PNS or non-nervous system sites.
Basically, G-G bodies in the CNS and PNS (and I suspect elsewhere) fall into 2 groups. The first type of G-G
body represents a subacute phase of the lesion and is
characterized by linear iron-encrusted fibers at the edge
of a resolving clot, and is identical to what is usually
illustrated in cardiac myxomas (14). The fibers are blueblack and readily detectable on hematoxylin and eosin
stain, although iron stains allow full appreciation of the
phenomenon (Fig. 1C). No multinucleated giant cells,
waxy refractile ‘‘mycelial-like’’ fibers, or collagen scar
are evident in this type of G-G body. Often the ironencrusted fibers are immediately juxtaposed to collections
of macrophages.
The second type of G-G body represents the remote
phase of the lesion and is characterized by focal nodular
collagenous scars (Fig. 1D) containing linear wavy aggregates of iron-encrusted fibers without associated clot
(Fig. 1E). This second type is what is classically described in the spleen of individuals with chronic portal
hypertension and best fits the Stedman’s Dictionary definition of the entity. The most prominent example (Case
2, a cystic, ‘‘baseball-sized’’ schwannoma of the ulnar
nerve) also contained numerous multinucleated giant
cells (Fig. 1D, inset). In several cases the collagen predominated and the encrusted fibers were thicker and
chunkier (Fig. 1F, case 5, a mixed growth hormone-prolactin secreting pituitary tumor is illustrated). Several cases contained prominent waxy, yellow, refractile ‘‘bamboo-like’’ segmented degenerated collagen fibers within
the dense, nodular collagenous scar (Fig. 1G), or in semilunar orientation around blood vessels (Fig. 1H), identical
to those described by Gamna and illustrated so beautifully by Schuppiser (Fig. 1A). Just like Hu et al (28), I
111
112
or warrant guest appearances as case reports. But the historical aspects of Gamna-Gandy bodies are worth knowing about, specifically the people involved and the beauty
of their morphological descriptions, now nearly 100 years
ago. When we see G-G bodies in our practices of neuropathology they now can serve as reminders of ‘‘what’s
in a name.’’
ACKNOWLEDGMENTS
The author thanks Dr. Robert H. Shikes, Professor of Pathology and
Medical History, for his helpful insights and critical review of the manuscript, Dr. Roberto Gianani for his translation from the Italian of the
article by Marini, Mr. Andrew Rex for skillful manuscript preparation,
and Ms. Lisa Litzenberger for photographic expertise.
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Gamna-Gandy Bodies in Surgical Neuropathology Specimens

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