Nephrol Dial Transplant (2009) 24: 3876–3881
doi: 10.1093/ndt/gfp503
Advance Access publication 25 September 2009
Historical Note
The juxtaglomerular apparatus of Norbert Goormaghtigh—a critical
appraisal
Garabed Eknoyan1 , Robert Rubens2 and Norbert Lameire3
1
Renal Section, Department of Medicine, Baylor College of Medicine, Houston, TX, USA, 2 Division of Endocrinology and 3 Renal
Division, Department of Medicine, University Hospital Gent, Gent, Belgium
Correspondence and offprint requests to: Garabed Eknoyan; E-mail: [email protected]
Keywords: afferent arterioles; Goormaghtigh cells; juxtaglomerular
apparatus; macula densa; renin
The discovery of the unique structural relationships between the early distal tubule of the nephron and the vascular pole of its originating glomerulus and the subsequent
demonstration of the functional and clinical import of this
remarkable complex—the juxtaglomerular apparatus—is
one of the principal achievements of nephrology. Of the
several investigators who made this possible, an immeasurable debt is owed to Norbert Goormaghtigh (1890–1960),
who was not only one of its first observers but the only
one to persevere in its investigation, to recognize and define the critical relationship of the complex he named the
juxtaglomerular apparatus, and in what were clearly prescient insights to foresee correctly many of its functions
that were to be documented in the ensuing decades. His
discovery, description and deductions of the juxtaglomerular apparatus and its roles are a landmark in the history of
medicine. Regrettably, his key part in characterizing and
elucidating this distinct apparatus has been confused, often misrepresented, frequently misunderstood and generally
forgotten.
Historical background
In order to appropriately evaluate the credit that Goormaghtigh deserves in the discovery of the juxtaglomerular apparatus, it is important to consider his work in the
context of the state of the medical sciences, the knowledge
of kidney function and the socio-political setting in which
he conducted his studies. In the medical sciences, it was
the closing years of the era of endocrinology launched in
1856 by Charles-Edouard Brown-Sequard (1817–94), when
he published his studies on the adrenal gland based on the
concept of internal secretions developed and pursued by his
immediate predecessor at the Collège de France, Claude
Bernard (1813–78) [1]. This was the stimulus for one of
the first studies on the kidney as an endocrine organ by
Robert Tigerstedt (1853–1923), Professor of Physiology at
the Karolinska Institute. In 1898, Tigerstedt reported that
rabbit renal cortical, but not medullary, tissue pulverized in
alcohol, desiccated and solubilized in saline when injected
into other rabbits caused an increase in blood pressure. He
proposed the name renin for the pressor factor [2]. The
work of these two investigators was of direct relevance to
the career of Goormaghtigh, who started his investigative
career with studies of endocrine function in general and
of the adrenal gland in particular, an experience that was
to prove important in his postulation of an endocrine function of the juxtaglomerular apparatus, and his later proposal
of renin as the potential pressor substance released by the
juxtaglomerular cells [3–5].
This was also the period that experimental physiology
was on its ascendancy, as new tools to measure function
were being developed, but structural studies remained very
much in vogue and provided a basis for the undertaking
of functional studies. In fact, a term then used and one of
the categories in which abstracts were classified was ‘histophysiologie’ (histo-physiology), a word that Goormaghtigh
often used in the text and title of his papers. This is also
evident in the name of the medical journals on microscopic
anatomy being launched at the time, notable amongst which
is ‘Bulletin d’histologie appliqué à la physiologie’ (Bulletin
of Histology Applied to Physiology), in which one of the
earliest papers on the afferent arteriolar changes of the juxtaglomerular complex was published [6]. As such, that a
pathologist like Goormaghtigh would venture into functional studies of clinical relevance was not unexpected.
As for the state of knowledge of the kidneys, the anatomical basis of their function was established in 1842, when
William Bowman (1816–92) described his eponymous capsule of the glomerular capillary tuft and demonstrated its
continuity with that of the basement membrane of the
connecting tubule [7]. The subsequent intense debate that
followed between proponents of the glomerulus as a secretory structure championed by Rudolph Heidenhain (1834–
1891) or a simple filter championed by Carl Ludwig (1816–
95) was nearing resolution in favour of the latter from
the direct glomerular micromanipulator-guided studies of
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The juxtaglomerular apparatus of Norbert Goormaghtigh
Alfred N. Richards (1826–1966) in the early 1920s [8].
In his studies, Richards used frogs because of the accessibility of the ventral surface of their kidneys to direct visualization. Relevant to the work of Goormaghtigh is the
early observation and report by Richards and his associates
of the intermittency of glomerular function [9]. In clinical studies of the kidneys, the notion of hypertension as a
cause of kidney disease, rather than just a result of kidney
disease, was being differentiated by the work of Franz
Volhard (1872–1950) and Theodor Fahr (1877–1914), who
in 1914 provided their classification of Bright’s disease and
characterized the arteriosclerotic (nephrosclerotic) kidney
[10]. Thus, by the opening decades of the 20th century,
when Goormaghtigh began his studies, it was generally
considered that whereas the diseased kidney could cause
hypertension, the more common form of elevated blood
pressure was a primary form of ‘essential’ hypertension,
in which renal involvement was secondary to the hypertension. The cause of elevated blood pressure and the role of
the kidney in either form of hypertension remained uncertain and debatable. This was another area directly relevant
to the research of Goormaghtigh, who studied the vasculature in hypertension and was the first to propose a link of
hypertension to the juxtaglomerular apparatus.
3877
Table 1. Temporal breakdown of the publications of Norbert Goormaghtigh broken down by the subject they address
Period
Subject
Single
Number author Adrenal HBP Renal
1914–20
1921–25
1926–30
1931–35
1936–40
1941–45
1946–50
1951–55
1955–60
Total
5
17
16
19
28
8
7
10
3
113
5
13
11
14
12
7
7
6
2
77
3
6
3
3
1
1
2
1
6
1
2
18
10
4 (1)
8 (6)
7 (5)
4 (4)
6 (4)
1 (1)
31 (21)
Cancer Other
2
2
4
3
1
2
1
15
2
8
9
7
10
1
1
1
39
In the column labelled renal, the numbers in parenthesis indicate publications about the juxtaglomerular apparatus.
Norbert Goormaghtigh—biography and
scholarship
It is on this background in the state of the medical sciences that Goormaghtigh made his major contributions on
the juxtaglomerular apparatus in the period between the
two world wars, both of which to some extent influenced
and shaped his personal life. Born on 14 February 1890
in the North Sea port city of Ostend, in West Flanders,
Goormaghtigh graduated in medicine from the University
of Gent in 1913. Drafted into service at the break of the
First World War (WWI), he served as a surgical pathologist
in an English Field Hospital in Hoogstade. It is there that
he met and married an English nurse, Mabel Lawrence, in
1917. The Second World War (WWII) was equally defining
in his life, when his favoured son was accused and imprisoned in Daschau in 1943. The following year, the Gestapo
incarcerated him also, albeit for only a short period. The
toll of WWII on his work and productivity is reflected
in the diminishing number of his publications (Table 1).
His subsequent administrative responsibilities as a rector
(1947–1950) of the University of Gent (Figure 1), during a
particularly difficult period in its history, further hampered
and practically ended his investigative career. Following a
series of progressively severe and incapacitating cardiac attacks beginning in November 1957, he died on 2 January
1960 [3–5].
After WWI, Goormaghtigh returned to the University
of Gent, where under the tutelage of the professor of microscopic anatomy, Omer van der Stricht (1862–1925), he
completed his thesis on the adrenal glands, demonstrating that the zona fasciculata of the adrenal cortex was the
source of corticosteroids while its medulla was adrenergic.
The following year, in 1922, he was appointed to the chair
Fig. 1. Norbert Goormaghtigh (1890–1960). Formal picture as Rector of
the University of Gent (1947–1950).
of Pathology at the University of Gent [3–5]. It is then that
he embarked on a productive career of research and training in experimental pathology (Figure 2, Table 1). He was
a prolific author and a meticulous experimenter, who was
himself directly involved in the work of published studies.
He is the single author of 68% of his 113 publications. The
rest of his papers, except for two of them, are two authored
only, reflecting the fact that he was also an admired teacher
and role model who trained and supervised the work of an
increasing number of graduates (the second authors of 36
of his multi-authored publications) in the period preceding
WWII.
The principal areas of his studies were endocrinology in
general and the adrenal glands in particular, carcinogenesis,
hypertension and the kidney (Table 1). Of the 39 publications listed under other in Table 1 almost all are on endocrine
glands (thyroid, parathyroid, ovaries, insulin). Excluding
this category of others, it is evident that most of his publications (27% or 31 articles) were on the kidney and two-thirds
3878
of these (21 out of 31) were on the juxtaglomerular apparatus (Table 1). His first renal publication in 1924 is about
horseshoe kidneys and not directly relevant to our topic
[11]. What is relevant, however, from this early period is his
work on hypertension, beginning in the mid-1920s. This
work, which had begun on the relationship of hypertension
with the adrenal glands [12], then extended to studies of the
effect of hypertension on the renal vasculature [13,14]. For
his initial studies, he used an experimental model of hypertension induced by the stimulation of the carotid sinus developed in collaboration with the Professor of Pharmacology and Therapeutics at the University of Gent, Corneille
Heymans (1892–1968), the 1938 Nobel laureate in Physiology or Medicine for his discovery of chemoreceptors
in the carotid sinus and aortic arch. Later, after Harry
Goldblatt (1891–1977) described a reproducible ischaemic
model of hypertension in 1934 [15], Goormaghtigh used
Goldblatt kidneys to study the sequential changes of the
renal vasculature and the juxtaglomerular complex as
renovascular hypertension sets in and evolves [16,17].
His first paper on the juxtaglomerular apparatus was
written in French, [18], as were three-quarters of his publications (76%, or 86 out of 113). Despite its location in
the Flemish northern part of Belgium, the official teaching
language of the University was French until 1930, when
the changeover to Dutch begun. This is also about the time
that the dominant language of the medical sciences began
to change to English. This is reflected in the publications of
Goormaghtigh (Figure 2). His first paper in English, published in 1934, was on the thyroid gland [19]. The majority
(10 out of 13) of his English papers were published during the decade between 1936 and 1945, and most of them
(8 out of 10) were on the juxtaglomerular apparatus.
Norbert Goormaghtigh—the juxtaglomerular
apparatus
It is with this background of considerable experience in
the morphology of endocrine glands and the vascular effects of hypertension that Goormaghtigh published his first
manuscript on the juxtaglomerular apparatus in 1932 [18].
In this first report, Goormaghtigh acknowledges the work
of two of his predecessors in the field. Essentially, in 1925,
J. H. C. Ruyter was the first to call attention to the structural
peculiarities of unique cells lining the afferent arteriole as it
approaches the glomerulus [20]. Ruyter described in mice
the changes in the smooth muscles of the juxtaglomerular
afferent arterioles, which begin to lose their fibrils and are
replaced by one or more layers of larger granular cells with
prominent oval nuclei. He characterized them as epithelioid
cells, which are variably present in different afferent arterioles, being most abundant in those supplying the cortical
glomeruli. He suggested that by swelling these cells could
occlude the lumen of the afferent arterioles and thereby
regulate blood flow to the glomerular capillaries. He reported observing similar cells in rat kidneys, but explicitly denied their presence in dogs, monkeys, guinea pigs,
cats, rabbits and man. Two years later, and independent
of Ruyter, Charles Oberling (1895–1960), then working in
G. Eknoyan et al.
Fig. 2. Graphic presentation of the publications of Norbert Goormaghtigh.
For each of the depicted 5-year period, the dotted bars represent total
number of publications, crosshatched bars single authored publications,
solid bars publications on the kidney and shaded bars those in English.
Strasbourg, reported the presence of similar cells in human kidneys in a brief two-page report published in 1927
[21]. He highlighted their features as identical to the subcutaneous digital glomi described by his then mentor Paul
Mason (1880–1959).
In his inaugural paper on the subject [18], Goormaghtigh
described in detail the afibrillar cells of the juxtaglomerular arterioles, principally in an 8-year-old girl who had died
of scarlet fever. He characterized them as afibrillar granular cells and identified them with those lining the afferent
arteriole described by Ruyter. In addition, he identified a
second population of smaller, also afibrillar but agranular,
spindle-shaped cells in the vascular pole, and highlighted
the rich enervation of the entire area. The second type of
cells he described were subsequently termed lacis cells because of their interlacing processes separated by basement
membrane. Like Oberling, he mentioned the similarity of
his findings to the subcutaneous glomi of Masson [22].
Masson had used the term glomus (from the Latin for ball
of thread) to describe the subcutaneous plexus of arteriovenous anastomoses (anastamoses artérioveneuse) rolled
upon itself and embedded in fibrous tissue that blends into
the surrounding dermis. The analogy made was not only
to shape but also the appearance of the cells lining the
glomic arterioles and the abundance of neural fibres supplying these neuro-muscular cells (cellules neuromusculaires)
described by Masson, hence the title of Goormaghtigh’s
first manuscript ‘Les segments neuro-myo-artériel juxtaglomerulaires des reins’ [18].
Relevant to this background are two other reports by Karl
W. Zimmermann (1861–1935) of the University of Berne.
In 1929, Zimmermann had mentioned briefly the changes
in the epithelial cells of the distal tubule returning to the
region of its originating glomerulus, where it makes contact
with the afferent arteriole [23]. In this paper he states, ‘In all
mammals that I have studied, there is at the junction of the
ascending branch of the loop of Henle with the afferent arteriole an increase in the number of epithelial cell nuclei of
that side of the tubule. For some time now, in my lectures I
The juxtaglomerular apparatus of Norbert Goormaghtigh
have called this structure the macula densa’. The juxtaposition of the distal tubule to the vascular pole of its originating
glomerulus had been described in 1889 by Camillo Golgi
(1843–1926) [24], the 1906 Nobel laureate in Physiology or
Medicine, and confirmed in the early 1900s in the elegant
reconstructive models of the nephron developed by Karl Peter (1870–1955), who also noted the distal tubular epithelial
cell changes but failed to name them [25]. In a subsequent
extensive paper [26], Zimmermann provides further details
on the macula densa and the adjacent cells in that location.
What Zimmermann described in 1933 was that as the afferent arteriole approaches the glomerulus, the medial cells
begin to multiply irregularly, expanding into a vascular
sleeve that fills the space between the afferent and efferent vessels and extends into the glomerulus. These are the
external mesangial cells, as they have since been identified
and as we know them today. Because of their appearance
as a cushion supporting the vascular pole of the glomerulus, Zimmermann called them polkissen, i.e. polar cushion
or pad. Zimmermann does not mention the ‘epithelioid’
cells of Ruyter or the ‘leiomyeloid’ granular cells of Goormagtigh. In fact, he specifically states that he was unable
to detect any noteworthy irregularities in the arrangement
of the smooth muscular cells of the afferent arteriole. Unfortunately, in the literature that followed, Zimmermann’s
polkissen cells came to be equated with the granular cells of
Goormaghtigh, and the term polkissen cell was used to refer to the epithelioid, myeloepithelioid, afibrillar, lacis and
granular cells described in the same region by different investigators. To complicate matters further, various authors
came to refer interchangeably and variably to the granular cells lining the afferent arteriole, the agranular lacis
cells and the collective polkissen cells as Goormaghtigh
cells [27–29]. Goormaghtigh had indeed described them,
but from the outset he was clear in his differentiation of
the granular cells lining the afferent arteriolar wall from the
agranular ones filling the space in the vascular pole of the
glomerulus.
Regrettably, the story as recounted generally by morphologists follows this chronological order giving priority
to Ruyter, and then using the confusing terminology that
followed the introduction of the term polkissen, fails to differentiate and credit appropriately the subsequent studies
of Goormaghtigh. Ruyter, who was a technician in the laboratory of Martin W. Woerdeman (1892–1990), professor
of pathology at the University of Amsterdam, was studying various mitochondrial stains on kidney tissue when he
made his observations on the afferent arterioles. He never
pursued the subject or published another paper on it. Neither did Oberling at the time, although he did return to the
subject more than a decade later at which time he felt compelled to write literally a harangue defending the priority,
importance, and acuity of his initial observations in 1927
and their contrast to the subsequent errors of Goormaghtigh
[30]. Zimmermann retired the year following his polkissen
paper and died 2 years later. He never wrote another paper
on the kidneys.
What may have helped Ruyter’s cause was his suggestion
that the afferent cells he had described could by swelling
cause afferent arterial obstruction. This was espoused by
A. N. Richards, whose studies in frogs had shown intermit-
3879
tency of glomerular function [8]. The demonstration of similar granular cells in frogs by Harald Okkels (1898–1970) of
Copenhagen provided the species-specific evidence needed
by Richards [6,31]. In one of the first American textbooks
on the kidney authored by ‘eminent authorities’ and published in 1935, Richards states that ‘a sphincter-like structure at the origin of the glomerular capillaries from the
afferent arteriole’ regulates glomerular function because
‘. . . Okkels having confirmed the observation of Ruyter
that the muscular wall of the afferent arteriole exhibits a
specialized thickening close to the glomerulus found that
mechanical stimulation at that point produced constriction.’
[32]. He makes no mention of Goormaghtigh.
Unlike the other early workers mentioned so far, Goormaghtigh continued to work on the subject for the next
15 years during which he provided a solid founding for the
important functions of the juxtaglomerular apparatus. His
insights, aptitudes and clarity of conclusions are evident
in his very first 1932 manuscript on the juxtaglomerular
apparatus [18]. It begins by providing the background (hypertension, endocrinology) from which he approached the
subject; makes a link to the physiologic studies of glomerular function of Richards and the clinico-pathological studies of Volhard; closes the discussion by posing a series of
questions that need to be addressed in future experimental
studies; and in the final statement of the conclusion refers
to the neuro-myo-arterial juxtaglomerular segment he described as a vaso-sensitive organ that protects and regulates
the glomerular capillary flow. This is the classic model of
hypothesis generating experimental medicine promulgated
by Claude Bernard, and it is in the very tradition of Bernard
that Goormaghtigh went on to study and elucidate the functions of the organ, which he named the juxtaglomerular
apparatus [33–37]. In a series of subsequent experimental
studies, he went on to propose that the afferent arteriole is
an endocrine organ, secreting a vasomotor hormone important not only in the control of renal circulation, but also in
the pathogenesis of hypertension. He is said to have used
the term ‘enartrine’ for the vasoactive substance [4], but
in his published articles proposes that it is renin. Further,
after the description of anuric acute renal failure in traumatic crush injury in WWII [38], he studied and reported
the vascular changes of the juxtaglomerular apparatus in
anuric crush syndrome, including those in preserved specimens he had studied in WWI, when stationed in Hoogstade
[39,40].
A good example of his analytical and perceptive aptitudes is his paper about the macula densa [33]. In
his report, Zimmermann never refers to any functional
significance of the structure he named. In contrast, in
concluding his observations on the intimate structural relationships of the juxtaglomerular apparatus’ structural components Goormaghtigh states, ‘The anatomic relationships
described above allows eventually for the glomerular circulation to be informed of the changes in its corresponding
tubule. In this case then, the epithelial cells (macula densa)
would act as a sensory plaque placed at a most important position of the nephron; hence, the possibility of an automatic
regulation of the glomerular circulation controlled either
by changes in volume or the physico-chemical composition of the urine (tubular fluid) flowing passed the plaque’.
3880
G. Eknoyan et al.
students [28], who began unravelling the line of documentations of the functions of the juxtaglomerular apparatus of
Goormaghtigh that continues to the present [44,45]. As
shown in Figure 3, following the lull in the period after
the war there was an exponential increase in the number of
publications on the juxtaglomerular apparatus beginning in
the 1960s that peaked in the 1970s and continues at a steady
pace to the present. The accrued information from this work
on the juxtaglomerular apparatus has had far reaching consequences that have not only expanded our understanding
of renal structure, function, pathophysiology and therapeutics but also affected that of the care of patients with acute
and chronic kidney disease.
450
400
350
300
250
200
150
100
50
0
51-4 51-9 60-4 65-9 70-4 75-9 80-4 85-9 90-4 95-9 00-4
Fig. 3. Number of publications per 5-year period listed in PubMed under
the search word ‘juxtaglomerular apparatus’ for the period 1951–2004.
This is as succinct and clear a statement as could be made
about tubuloglomerular feedback, as we understand it now.
To have been formulated in 1937 at a time that the giants
of nephrology of the day considered the juxtaglomerular
apparatus mere structural changes due to mechanical stress
[41,42] only indicates the considerable insights that Goormaghtigh brought to his power of morphologic observations. His ability to foresee structural–functional correlates
and correctly formulate them is stunning, to say the least,
and these were far ahead of their time. It was decades later
that they were documented and elucidated.
Essentially then, Goormaghtigh literally single-handedly
recognized and documented the significance of the critical structural relationship of the juxtaglomerular apparatus and foretold the many roles of his apparatus that were
fully documented after WWII. At the time, however, his
prescient conclusions were based on histological observations, without any bioassay or biochemical confirmation.
As such, they could be influenced, to some extent, by subjective impressions. This reservation is magnified by the
fact that the figures illustrating his papers were drawings or
camera lucida renderings of his microscopic observations.
Goormaghtigh acknowledges this shortcoming in a 1951
manuscript in which for the first time he presents a single
photomicrograph in support of his drawings [37]. And with
the appropriate humbleness of an experimentalist he questions his own conclusions about renin as being indirect and
inferential.
These self-acknowledged limitations notwithstanding,
what is most striking in his work is that literally everyone of his sagacious deductions has been and continues
to be substantiated and documented. Unfortunately, the
promise of the important functions of the juxtaglomerular
apparatus that Goormaghtigh had promoted became moribund during WWII, as did his own investigative work not
only during the war but thereafter as well when he became rector of the University from 1947 to 1950. His last
paper on the subject, published in 1956, is on the renal
circulation in chronic glomerulonephritis [43]. That is just
about the time that the entire subject was being resurrected
by the meticulous studies of Phyllis M. Hartroft and her
An apologia
The delay in work on the juxtaglomerular apparatus and
the confusion in appropriate attribution of its discovery
are perhaps best reflected in the magnum opus of Homer
Smith, who in his 1950 classic book ‘The Kidney. Structure
and Function in Health and Disease’ devotes barely one
page to the subject [41]. The section is titled ‘Polkissen
or Juxtaglomerular Apparatus’, which reservedly mentions
Goormaghtigh’s findings only to dismiss them by referring
to Jean R. Oliver (1889–1976) who ‘finds no suggestion of
endocrine nature for the polkissen cells and thinks that they
represent structural modifications resulting from the mechanical stresses where the thin-walled arteriole enters the
glomerulus. This view is consonant with their hyperplasia
in degenerative renal disease!’.
This was not the first time that Homer Smith was wrong.
He had long resisted the countercurrent mechanism in
generating concentrated urine. In that error he lived long
enough to see its documentation and wrote a humorous
piece in 1959 about an imaginary encounter with Saint
Peter at the Gates of Heaven where he admits his error and
attempts to justify why he had insisted for so long on drawing the tubule straight [46]. Unfortunately, Smith did not
live long enough to write a similar apologetic piece on the
juxtaglomerular apparatus. Nevertheless, and in the same
general vein, one can imagine a similar scene where Saint
Peter inquires of Smith: ‘You were intimately familiar with
the early work on the granular cells of Goormaghtigh and
summarized it in your 1940 Harvey Lecture [47]. Why did
you confuse it by equating it all with the frivolous polkissen
term in your book?’ To which Smith answers, ‘I was misled
by the two people I admired most, Richards who espoused
the mechanical description of Ruyter and by Oliver who denied any endocrine function of the apparatus [41,42], and
attributed intermittency of glomerular function to the shunting of afferent flow through the arterioles of Carl Ludwig,
“the discoverer of glomerular filtration” [48]. How could I
deny the opinion of these three giants of nephrology? In my
defence though I must submit the only coloured illustration
of my book, its frontispiece to which I refer in the section on
the polkissen as “a normal glomerulus, where the structure
of the afferent arteriole is clearly visible”. Please note the
granular cells of Goormaghtigh I failed to mention in the
text. Mea culpa. Mea maxima culpa’.
The juxtaglomerular apparatus of Norbert Goormaghtigh
Conclusion
The unique structural and functional features of the juxtaglomerular apparatus were recognized, examined, described, characterized and studied by Goormaghtigh, whose
name deserves to be associated with it. Bowman and
Malphigi earned their eponymous attributions for much
less work than what Goormaghtigh did to unravel that of
his remarkable juxtaglomerular apparatus. As for terms
like polkissen and lacis, or descriptors such as epithelioid or myelopithelioid cells, the sooner they are forgotten
and omitted from future textbooks the clearer the story of
Goormaghtigh’s juxtaglomerular apparatus will become.
Conflict of interest statement. None declared.
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Received for publication: 28.8.09; Accepted in revised form: 28.8.09