PBPrimate BiologyPBPrimate Biol.2363-4715Copernicus GmbHGöttingen, Germany10.5194/pb-2-57-2015From the working group “Experimental Pathology” to the department
“Pathology Unit” – historical development in retrospectKaupF.-J.fkaup@gwdg.deGerman Primate Center, Pathology Unit, Kellnerweg 4, 37077 Göttingen, GermanyF.-J. Kaup (fkaup@gwdg.de)14August201521576311June201530July20154August2015This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://pb.copernicus.org/articles/2/57/2015/pb-2-57-2015.htmlThe full text article is available as a PDF file from https://pb.copernicus.org/articles/2/57/2015/pb-2-57-2015.pdf
The Pathology Unit of the German Primate Center started as the working group
of Experimental Pathology in 1992. This small group with one veterinary
pathologist and a technician was founded based on an idea of Prof. Dr. Kuhn,
who wanted to strengthen the pathology research activities and to establish a
centralized electron microscopy laboratory. Later on, experimental pathology,
veterinary services and primate husbandry were integrated as the Department
of Veterinary Medicine and Primate Husbandry but subsequently again
separated. Prof. Dr. Franz-Josef Kaup, the head of the previously integrated
department, remained in his capacity as the leader of the different units.
Over the years, the research activities have changed from SIV-associated
pathology to other infectious diseases. Today, the main research focus is on
the pathogenesis of orthopoxvirus infection, primate pathology, neglected
tropical diseases and nonhuman primates as models for chronic respiratory
diseases. This paper gives an overview of the historical development and
aspects of research activities.
Introduction
Following its establishment in the early 1980s, the initial divisional
structure of the German Primate Center reorganized its scientific focus
towards the end of this decade. In this context, establishment of a new
Morphology and Systematics Department was considered, for which acquisition
of a transmission electron microscope was planned. In the financial year of
1990, a budget of DM 750 000 was set aside for a transmission electron
microscope. Establishment of an electron microscopic device was also
supported by the German Council of Science during evaluation of the German
Primate Center in January 1990. At the same time, the head of the German
Primate Center, Professor Kuhn, considered setting up an independent
scientific working group for experimental pathology in addition to the
existing Pathology Department headed by Dr. Manfred Brack.
Establishment of the working group “Experimental Pathology”:
1992–1996
In the subsequent meetings of the Scientific Advisory Council and the
Supervisory Board, establishment of three working groups was decided on in June
1991: Electron Microscopy, Behavior Research, and Experimental Pathology
(Supervisory Board Meeting on 4 June 1991). Since an eligible
candidate for the head of the Electron Microscopy group could not be found,
supervision of the electron microscope as part of the central service
facility was assigned to the new Experimental Pathology group.
At the same time, Dr. Franz-Josef Kaup, who at the time was a research
assistant in the electron microscopy division of the Institute of Pathology,
University of Veterinary Medicine Hanover, was invited to give a talk at the
German Primate Center. On 30 January 1992 Dr. Kaup gave a presentation titled
“Morphologic Methods of Viral Detection with Special Reference to
Immunoelectron Microscopy” at the German Primate Center. After discussion in
the Scientific Advisory Council, Dr. Kaup was endorsed as head for the new
Experimental Pathology working group. Thus, two recommendations of the German
Council of Science (establishment of a unit Electron Microscopy and a unit
Experimental Pathology) could be realized by a single occupancy.
After granting of the Venia legendi for “General Pathology and
Pathologic Anatomy of Domestic Animals`” by the University of Veterinary
Medicine in Hanover, PD Dr. Kaup took up employment at the German Primate
Center on 1 August 1992.
From the working group Experimental Pathology to the Department of
Veterinary Medicine and Primate Husbandry: 1992–2002
Transmission electron micrograph on the cover page of the
program 5th German AIDS congress in Hanover, 1994. The micrograph presents
an intracytoplasmic vacuole containing SIV particles. The structure was
found in an SIV-induced giant cell from an infected rhesus monkey (Macaca mulatta). Photo
taken by Kaup, Experimental Pathology, German Primate Center.
Cryptosporidiosis in an SIV-infected rhesus macaque.
Enterocytes (Nu – nucleus) with adjacent parasites. The parasitophorous vacuoles (PV) are probably formed by the microvilli (MV) of the affected
enterocytes. The ultrastructure of the vacuoles argue for the morphology of
schizonts containing merozoites. Cryptosporidiosis is a typical
opportunistic infection in SIV-infected macaques. Transmission electron
microscopy.
Scanning electron micrograph showing a hemispherical intestinal dome
area bulging into the gut lumen and surrounded by intestinal villi. The domes
are covered by enterocytes and M cells (M – cytoplasm, Nu – nucleus). Transmission electron microscopy demonstrates the
close contact of an M cell with intraepithelial lymphocytes (IEL). Ileum,
rhesus monkey (Macaca mulatta).
Gross pathology of a hepatic echinococcosis. The parasites
invade the liver tissue with multiple cystic transformation. Echinococcus multilocularis infection of a
rhesus monkey of the German Primate Center.
Macroscopic findings in a cynomolgus macaque (Macaca fascicularis) from a
diagnostic necropsy. Abundant amounts of encysted parasitic larvae in the
abdominal viscera. In this case of a pentastomiasis PCR was done. The
sequence matched 98 % that of Armillifer agkistrodontis.
Skin lesions due to a calpox infection in a marmoset
(Callithrix jacchus). Apart from inflammatory signs calpox lesions are characterized by so-called Guarnieri bodies (arrow) within the cytoplasm of epithelial cells.
Transmission electron microscopy of the Guarnieri bodies presents orthopoxvirus particles (inset).
Transmission electron micrograph of a ciliated cell (Ci) originating from the tracheal
respiratory epithelium of a newborn marmoset (Callithrix jacchus). In the airway
lumen numerous cross-sectioned cilia present normal axonemes consisting of a central pair
of filaments surrounded by nine other pairs. In addition to normal cilia an atypical
cilium (CC) is demonstrated. This malformation belongs to compound cilia of
bulging type which contains loosely and randomly embedded axonemes.
During the first few years, the newly formed working group focused on the
pathogenesis of gastrointestinal and respiratory infections, while related
ultrastructural studies contributed to the establishment of a central
electron microscopy division (Kaup et al., 1994, 1998, 2005; Kuhn and Kaup,
1996). In this process, the Department of Virology and Immunology proved to
be a valuable partner, as both experimental SIV infections in rhesus macaques
(Fig. 1) and associated opportunistic infections opened new research fields
for the working group (Figs. 2 and 3). At the beginning of 1994, Dr. Kerstin
Mätz-Rensing joined the working group as the first research assistant,
and spontaneous nonhuman primate disease increasingly became the subject of
research.
Special emphasis was laid on the establishment of immunohistochemical markers
for nonhuman primate tissue, which were used in different studies on the
pathogenesis of the intestinal SIV infection, but also for tumor
differentiation and classification in nonhuman primates (Kuhn et al., 1999;
Didier et al., 1999; Mätz-Rensing et al., 1999b; Kaup et al., 2001; Kahnt
et al., 2002). Beside pathomorphological methods, new in vivo
experimental techniques were also implemented. Endoscopic techniques were
introduced at the German Primate Center during a study on SIV passage via the
intestinal barrier (Kewenig et al., 1999; Schäfer et al., 2002). Since
then, endoscopy has been an essential tool that is widely used to this day to
obtain gastrointestinal biopsies in experimental infections, for example,
with Helicobacter pylori. Dr. Kaup, who was meanwhile appointed as
an exceptional professor by the University of Veterinary Medicine Hanover,
succeeded Professor Kuhn as the animal welfare officer of the German Primate
Center in February 1996.
After an evaluation in 1996, the Department of Veterinary Medicine and
Primate Husbandry headed by Professor Dr. Franz-Josef Kaup was established by
merging the Experimental Pathology and the Primate Husbandry working groups
(headed by Dr. W. Kaumanns). In addition, the functional Veterinary Care unit
(led by Dr. T. Gatesman) separated from the Department of Pathology and was
integrated into the new department. The functional division of the
pathological diagnostics, along with the necropsy hall, bacteriology lab and
parasitology lab remained connected to the Department of Pathology headed by
Dr. Brack. The new department consisted of the Functional Pathology,
Veterinary Medicine/Primate Husbandry, and Biology of Primate Keeping working
groups. The certified biologist Uwe Schönmann became colony manager and
head of the Primate Husbandry working group in 1998.
With the retirement of Dr. Manfred Brack in 1999, a longstanding era at the
German Primate Center ended. The Department of Pathology was disbanded, and
the staff and diagnostic divisions of histology, bacteriology, and
parasitology, as well as the operation of the necropsy hall were assigned to
the Department of Veterinary Medicine and Primate Husbandry.
Henceforward, the Department of Veterinary Medicine and Primate Husbandry was
the central service unit of the German Primate Center. It provided veterinary
care with dispensary, veterinary diagnostics (pathology, histology,
bacteriology, and parasitology), primate husbandry with animal and sample
supply, transmission electron microscopy, and animal welfare. This broad
service spectrum was intensively used by many internal and external
scientists. On 1 December 2000, Professor Dr. Kaup was appointed university
professor for laboratory animal
pathology at the University of Veterinary Medicine Hanover, which was
connected to his position as the head of the Department of Veterinary
Medicine and Primate Husbandry at the German Primate Center.
New trends of research
During this time, the scientific spectrum of the department also expanded. In
2001, Dr. Uwe Hahmann and Professor Walter Bodemer established a new working
group named Spongiform Encephalopathies, which focused on the pathogenesis of
prion diseases and was notably funded by the EU during the BSE crisis
(Krasemann et al., 2010; Kiesel et al., 2012a, b). The SIV/SHIV macaque model
was continuously serviced pathomorphologically for the Department of Virology
and Immunology (headed by Professor Dr. Hunsmann) and later on the
Department of Infection Models (Dr. Stahl-Hennig). Dr. Mätz-Rensing
succeeded to establish a macaque model for experimental Helicobacter pylori infections (Mätz-Rensing et al., 1999a; Mätz-Rensing et al.,
2001) as well as detection systems for alveolar echinococcosis (Tappe et al.,
2007), a tapeworm infection that has been increasingly diagnosed in the
breeding colonies of the German Primate Center (Fig. 4).
From the “Department of Veterinary Medicine and Primate Husbandry” to the
department “Pathology Unit”: 2002–2015
History of the Pathology Unit at the German Primate Center
(1992–2015)
Date1 August 1992Working group ExperimentalPathology Head: Dr. KaupDivision Pathology andVeterinary Services Head: Dr. BrackBreeding and Husbandry Head: Dr. Kaumanns1 January 1997Dept. Veterinary Medicine and Primate Husbandry (Functional Pathology, Breeding and Husbandry, Veterinary Services) Head: Prof. Dr. KaupDept. Pathology Head: Dr. Brack1 December 1999Dept. Veterinary Medicine and Primate Husbandry (Primate Pathology, PrimateHusbandry with VeterinaryServices) Head: Prof. Dr. Kaup1 January 2003Pathology Unit Head: Prof. Dr. KaupCost Center Primate Husbandry (with Veterinary Services) Head: Prof. Dr. Kaup Manager: Uwe Schönmann1 April 2010Pathology Unit Head: Prof. Dr. Kaup with Airway Immunology (Satellitestation of Fraunhofer ITEMHanover): actual head:Dr. F. DahlmannCost Center Primate Facilities (with Veterinary Services) Head: Prof. Dr. Kaup Manager: Uwe Schönmann
With the appointment of Professor Dr. Treue as the new scientific director,
the six existing departments and three working groups were reorganized. The
Department of Veterinary Medicine and Primate Husbandry were separated and a
new Pathology Unit (which was also part of the new Infection Research
Section) was established. The Primate Husbandry and Veterinary Medicine
groups were renamed into Cost Center Primate Husbandry. As both facilities
were headed by Professor Kaup, the duties and responsibilities of this group
remained unchanged (Table 1).
In 2004, the Pathology Unit set up two new working groups. The
Dermatopathology group, headed by Dr. Bärbel Löblich-Beardi, worked
on alopecia in rhesus macaques (Beardi et al., 2007; Steinmetz et al., 2005,
2006) and the herpesvirus group, headed by Dr. Dieter Jentsch. Following the
retirement of Professor Bodemer, Dr. Jentsch, and Dr. Löblich-Beardi,
research activities became more focused within the Pathology Unit.
The Primate Pathology group concentrated on spontaneous diseases in nonhuman
primates for many years (Mätz-Rensing et al., 2012a) (Fig. 5). The group,
led by Dr. Mätz-Rensing, established a new orthopoxvirus model in
marmosets based on a diagnostic case of an orthopoxvirus infection in New
World monkeys (Fig. 6). This model was used to investigate the clinical and
pathological changes of this novel infection and enabled translational
evaluation of vaccine efficacy.
This orthopoxvirus model was developed in response to a disease outbreak in a
private primate husbandry in 2002. Several New World monkeys, among them
common marmosets (Callithrix jacchus), died within a very short
period of time. Necropsy of some animals with subsequent histological and
electron microscopic examinations at the German Primate Center revealed an
orthopoxvirus infection. In collaboration with the Robert Koch
Institute (RKI), a cow pox virus was isolated. Sequence analyses and
phylogenetic investigations showed that it was a novel cow pox virus, which
was named calpox virus after its host species (“Callithrix”)
(Mätz-Rensing et al., 2006, 2012b; Kramski et al., 2010; Schmitt et al.,
2014).
The virus was cultured from different organs, and a virus stock was
generated by means of a permanent cell line. Meanwhile, different studies
were conducted to determine the infectious dose and the optimal inoculation
route for experimental infection and to characterize the pathogenesis and
the spread of the virus to different organs. Vaccination studies with
intranasal virus challenge (8.3 × 103 PFU of calpox virus) showed that
the old vaccine, which had many adverse effects (vaccinia virus Elstree VACV
LE-BN), provided adequate protection in comparison to subsequently developed
vaccines (MVA: modified vaccinia virus Ankara; MVTT: modified vaccinia virus
Tiantan), which did not induce reliable immunization.
In April 2010, a cooperation was established with a working group of the
Fraunhofer Institute for Toxicology and experimental Medicine (ITEM) Hanover
(today headed by Dr. Franziska Dahlmann), which works on primate models for
COPD and asthma (Seehase et al., 2011, 2012). This group is supported by a
working group of the Pathology Unit named Anatomy/Pathology of the
respiratory tract headed by Dr. Martina Bleyer (Hoffmann et al., 2013, 2014)
(Fig. 7). Furthermore, a new research group studies neglected tropical
diseases in particular Treponema infection in baboons. This group
(head Dr. Sascha Knauf) combines laboratory investigations in infectious
diseases with field studies in free-living nonhuman primates (Knauf et al.,
2012, 2015).
Outlook
Over the past few decades, the German Primate Center has continuously focused
on nonhuman primate pathology. Results of the research activities are
documented in more than 200 publications and 41 veterinary medical
dissertations. In addition to its great contribution to research, the
pathological diagnostics with associated etiological examinations and
extensive sample supply represent important services offered by the German
Primate Center that have been used extensively by external scientists and
vets. At the German Primate Center, seven veterinarians have completed their
five-year training to become veterinary specialists in pathology. The
research activities and the diagnostic services of the Pathology Unit are of
special value to the Infection Research Section because of the profound
expertise in primate diseases and pathology, which is essential for a primate
center.Edited by: E. Fuchs Reviewed by: two anonymous referees
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