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Primate Biol., 4, 93–100, 2017
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doi:10.5194/pb-4-93-2017
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Research article
Feasibility of intravitreal injections and ophthalmic safety
assessment in marmoset (Callithrix jacchus) monkeys
Birgit Korbmacher1, Jenny Atorf2, Stephanie Fridrichs-Gromoll1, Marilyn Hill3, Sven Korte1,
Jan Kremers2, Keith Mansfield3, Lars Mecklenburg1, Andrew Pilling3, and Andreas Wiederhold1
1Covance Preclinical Services GmbH, Kesselfeld 29, 48163 Münster, Germany
2Department of Ophthalmology, University Hospital Erlangen, Maximiliansplatz 2, 91054 Erlangen, Germany
3Novartis Pharma AG, Basel, Klybeckstraße, 4002 Basel, Switzerland
Correspondence to: Birgit Korbmacher (birgit.korbmacher@covance.com, birgit.niggemann@covance.com)
Received: 16 November 2016 – Revised: 4 April 2017 – Accepted: 4 April 2017 – Published: 28 April 2017
Abstract. To safeguard patients, regulatory authorities require that new drugs that are to be given by the intrav-
itreal (IVT) route are assessed for their safety in a laboratory species using the same route of administration. Due
to the high similarity of ocular morphology and physiology between humans and nonhuman primates (NHPs) and
due to the species specificity of many biotherapeutics, the monkey is often the only appropriate model. To this
end, intravitreal administration and assessment of ocular toxicity are well established in cynomolgus monkeys
(Macaca fascicularis). In contrast, the common marmoset monkey (Callithrix jacchus) is not a standard model
for ocular toxicity studies due to its general sensitivity to laboratory investigations and small eye size. It was the
purpose of the present work to study whether the marmoset is a useful alternative to the cynomolgus monkey
for use in intravitreal toxicological studies. Six marmoset monkeys received repeated (every 2 weeks for a total
of four doses) intravitreal injections of 10 or 20 µL of a placebo. The animals were assessed for measurements
of intraocular pressure (IOP), standard ophthalmological investigations and electroretinography (ERG). At the
end of the dosing period, the animals were sacrificed and the eyes were evaluated histologically. ERG revealed
similar results when comparing predose to end-of-study data, and there was no difference between the two dose
volumes. A transient increase in the IOP was seen immediately after dosing, which was more pronounced after
dosing of 20 µL compared to 10 µL. Ophthalmologic and microscopic observations did not show any signifi-
cant changes. Therefore, it can be concluded that 10 µL as well as 20 µL intravitreal injections of a placebo are
well tolerated in the marmoset. These results demonstrate that the common marmoset is an alternative to the
cynomolgus monkey for intravitreal toxicity testing.
1 Introduction
To support clinical trials of new drugs to be given by the in-
travitreal (IVT) route, it is required to assess the safety after
IVT administration to a laboratory species. Due to the high
similarity of ocular morphology and physiology between hu-
mans and nonhuman primates (NHPs) and given the species
specificity of many biotherapeutics, the monkey often is the
only appropriate species for preclinical safety testing. To this
end, intravitreal administration procedures and assessments
of ocular toxicity in cynomolgus monkeys (Macaca fasci-
cularis) are well established (Niggemann et al., 2006). In
contrast, the common marmoset monkey (Callithrix jacchus;
Fig. 1) is not a standard model for ocular toxicity studies
due to its general sensitivity to laboratory investigations and
small eye size.
However, apart from a polymorphism in red–green color
vision (Mollon et al., 1984 and Travis et al., 1988), only mi-
nor structural and functional differences in the retina were
described in comparison to macaques. In addition, recordings
from single neurons in the lateral geniculate nucleus showed
that the functional properties of visually responsive cells in
marmosets are very similar to those in the macaque (Kremers
et al., 1999). It was the purpose of the present work to study
whether the marmoset is a useful alternative to the cynomol-
Published by Copernicus Publications on behalf of the Deutsches Primatenzentrum GmbH (DPZ).
94 B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment
Figure 1. Common marmoset monkey (Callithrix jacchus).
gus monkey for use in intravitreal toxicological studies and
whether injecting a volume of 10 or even 20µL would be
tolerated.
2 Materials and methods
2.1 Pre-study test
To determine various weight and anatomical measurements,
seven eyes from four adult common marmosets, that were
sacrificed for reasons unrelated to this study, were obtained
at necropsy, and following removal of periorbital muscle
and fat, the eyes were snap-frozen at −70 ◦C. Eyes were
thawed and weighed. Transverse and sagittal measurements
were performed. Volumetric measurements were made by
recording fluid displacement in a 10.0 mL graduated cylin-
der. The eye was then dissected and similar measurements
were recorded for the vitreous and lens.
2.2 Housing, ethical and regulatory guideline
considerations
During the development of a specific biotechnology-derived
compound, it was shown that the marmoset was the only
pharmacologically relevant species for nonclinical safety
testing. Due to the very limited experience with IVT adminis-
tration in marmosets (Ivanova et al., 2010; Melo et al., 2012;
Neitz et al., 2013), this feasibility study was conducted in or-
der to prepare for a good laboratory practice (GLP) toxicity
study with this specific compound.
The test facility Covance Preclinical Services GmbH (Ger-
many) is fully accredited by AAALAC International. All pro-
cedures in this study were in compliance with the German
Animal Welfare Act and were approved by the local Institu-
tional Animal Care and Use Committee (IACUC). Further-
more, the procedures were performed in consideration of the
Directive 2010/63/EU of the European Parliament and of the
Council of 22 September 2010 on the protection of animals
used for scientific purposes.
The standard social housing for marmosets at Covance,
Münster (Germany), is according to the “Commission Rec-
ommendation 2007/526/EC on guidelines for the accommo-
dation and care of animals used for experimental and other
scientific purposes (Appendix A of Convention ETS 123)”.
The standard cage allows three-dimensional movements by
this highly agile primate species in groups of two or three
individuals.
The animals received a variety of food, which was pre-
pared freshly each day and given twice a day according to a
meal plan. The room temperature was between 22 and 28 ◦C,
with a relative humidity between 40 and 70 %, and artifi-
cial lighting was in 12 h dark/light cycle. The cages were en-
riched with sleeping boxes, wooden chips, plastic balls and
wooden bars.
2.3 Feasibility study
The animals were 1 to 10 years old and weighed between
349 and 501 g. One group of three male marmoset monkeys
received repeated bilateral intravitreal injections of 10µL of
a placebo (70 mM mannitol, 20 mM histidine pH 6.5, and
0.04 % polysorbate) every second week (days 1, 15, 29,
and 43). The second group of three male animals received
20 µL of a placebo on the same days. Ophthalmic exami-
nations and intraocular pressure (IOP) measurements were
performed once before there start of dosing (predose), on
days 1 (directly after dosing), 3, 15 (directly after dosing), 17,
29 (directly after dosing), 31, 43 (directly after dosing) and
45 (before the animals were sacrificed as scheduled). Elec-
troretinography (ERG) was performed twice before the start
of dosing and at week 6 of the study (after the last adminis-
tration of the placebo).
2.3.1 Intravitreal dosing
The animals were fasted before they were anesthetized by
intramuscular injection of ketamine and medetomidine. My-
driasis was induced by using 1 % tropicamide eye drops, and
an antiseptic (povidone-iodine 5 %) solution was instilled in
the area of the injection. A local ophthalmic anesthetic was
instilled into both eyes prior to insertion of a lid speculum. A
microscope was used for dose administration with the aim to
observe any reflux (see Fig. 2). The distance from the corneal
limbus was measured (approx. 1.5 to 2.0 mm) and marked
on the conjunctiva. The needle was inserted approximately
3 mm into the vitreous body in the direction to the posterior
pole. The needle stayed in that position for 3–5 s after dos-
ing so that the vehicle could distribute in the vitreous body.
Before the needle was removed it was clasped with a Col-
ibri forceps to avoid reflux. Reflux could not be completely
avoided but was only seen on few occasions.
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B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment 95
Figure 2. Intravitreal administration in the Marmoset eye.
Ointment containing dexpanthenol was instilled onto each
eye following the dosing, and atipamezole was used as an
anesthetic antidote at the end of the procedure (intramuscular
injection).
2.3.2 Ophthalmic examinations
Ophthalmic examinations were conducted following seda-
tion using ketamine. Mydriasis was induced by using 1 %
tropicamide eye drops. The eye and the connecting tissues
were evaluated during the macroscopic investigations. The
ocular fundus with the macula lutea, papilla, ocular vessels
and retina was assessed funduscopically. Slit lamp examina-
tions including fluorescein staining were performed to evalu-
ate the anterior and medium segment of the eye with conjunc-
tiva, cornea, anterior chamber, iris, lens and vitreous body. In
addition, the intraocular pressure was determined using the
TonoVet®tonometer.
2.3.3 Electroretinography
The animals were dark adapted for at least 30 min prior to
anesthesia using ketamine and medetomidine. The pupils
were dilated with 1 % tropicamide eye drops and 0.5 % at-
ropine eye drops. Further preparation of the animals was per-
formed under dimmed red light to ensure that rod sensitivity
was preserved.
For the first measurement, ERGs were only measured in
the right eyes using DTL (Dawson–Trick–Litzkow) elec-
trodes that were placed over the lower conjunctiva of each
eye, serving as active electrodes. The eyes were covered by
methylcellulose and a custom-made contact lens (radius of
curvature: 3.5 mm; 5 mm diameter; 0 diopter; Cantor & Nis-
sel, UK) to avoid desiccation of the eye. During the second
measurement and the dosing phase, the left and right eyes
were measured simultaneously and the DTL electrodes and
contact lenses were replaced by contact lens electrodes (same
properties as above; Mayo Corporation, Japan). The contact
lens electrodes were easier to handle and gave nearly iden-
tical results as the DTL electrodes. The data obtained with
both techniques were considered comparable. Needle elec-
trodes that were placed subcutaneously at the base of the ip-
silateral ears served as references. Ground needle electrodes
were placed at the base of the tail. The animals were placed
on a platform that could be slid into the full-field stimulator.
Each recording lasted approximately 30 min.
The animals underwent ERG measurements to the follow-
ing five stimulus protocols:
1. Scotopic flash ERGs were recorded with a dark back-
ground. The responses to six flash strengths (0.0095,
0.03, 0.095, 0.3, 0.95 and 3.0 cd·s m−2) were recorded.
The flash frequency was 0.3 Hz. The recordings to six
flashes were averaged. The a-waves were measured
only at the highest flash strength (i.e., 3.0 cd m−2) from
baseline to the trough of the a-wave. The b-waves were
measured at all flash strengths. The amplitudes were de-
fined as the voltage difference between the trough of the
a-wave to the peak of the b-wave.
2. Oscillatory potentials (OPs) were measured for four
flashes on a dark background at a rate of 0.1 Hz. The
flash strength was 3.0 cd·s m−2. Representative for all
OPs, the OP amplitude between the peak of OP2 and
the following trough was measured. The latency was de-
fined as the time to the trough following OP2.
3. Photopic flicker ERGs were recorded for a train of
3.0 cd·s m−2flashes on a 100 cd m−2background at a
rate of 30.1 Hz. The responses to 50 flashes were mea-
sured and averaged. The measurements were performed
directly after the background was switched on and were
repeated after 10 min of adaptation. A general increase
in the ERG responses was observed during this time.
Therefore, only the second measurement was used for
further analysis. The response amplitude was defined as
a trough-to-peak amplitude.
4. The responses to red flashes on a 100 cd m−2white
background were recorded. Two flash strengths were
used: 0.3 and 0.95 cd·s m−2. The flash rate was 1.5 Hz
and the responses to 30 flashes were averaged. White
backgrounds were chosen instead of blue backgrounds
to be able to compare the data with previous data ob-
tained from cynomolgus monkeys. The white back-
grounds were photopic and thus sufficiently suppressed
rod-driven signals. The b-wave amplitudes and implicit
times were measured.
5. The photopic flashes were repeated with white flashes.
The responses to 20 flashes of 3.0 cd·s m−2strength
were averaged. The flash rate was 1.5 Hz. The a- and
b-wave amplitudes and latencies were measured.
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96 B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment
Table 1. Ocular weight and linear and volumetric measurements from adult common marmoset eyes.
Animal 1 Animal 2 Animal 2 Animal 3 Animal 3 Animal 4 Animal 4 Mean SD
Eye 1 Eye 1 Eye 2 Eye 1 Eye 2 Eye 1 Eye 2
Eye weight (g) 0.59 0.749 0.7412 0.6489 0.6618 0.7472 0.7366 0.70 0.058
Lens weight (g) 0.019 0.027 0.026 0.030 0.041 0.026 0.051 0.03 0.010
Lens wt / eye wt 0.03 0.04 0.03 0.03 0.07 0.03 0.07 0.04 0.017
Circumference (A) 3.3 3.8 3.8 3.4 3.4 3.9 3.9 3.6 0.244
Transverse (cm)
Circumference (B) 3.5 3.9 3.9 3.6 3.5 3.8 3.8 3.7 0.164
Sagittal (cm)
Lens volume (mL) n/a 0.03 0.03 0.03 0.04 0.01 0.025 0.03 0.009
Vitreous weight (g) n/a 0.558 0.552 0.424 0.487 0.483 0.587 0.52 0.056
Vitreal wt / total eye wt n/a 0.74 0.74 0.65 0.8 0.65 0.80 0.73 0.062
Vitreous volume (mL) 0.4 0.6 0.6 0.6 0.6 0.5 0.5 0.54 0.073
Total volume (mL) 0.6 0.8 0.8 0.8 0.8 0.7 0.8 0.76 0.073
Vitreal vol / total vol 0.67 0.75 0.75 0.71 0.63 0.71 0.63 0.69 0.049
2.3.4 Necropsy and histopathology of the eye
Animals were sedated by intramuscular injection of ketamine
followed by an intravenous sodium pentobarbitone overdose
prior to exsanguination. Both eyes including the optic nerve
were fixed in Davidson’s fluid. The eye was bisected in a hor-
izontal plane, just below the equator, and embedded in paraf-
fin wax. Sections were prepared at a nominal thickness of
5 µm. Three serial sections were taken through each block at
1 mm spacing, yielding a total of six sagittal sections per eye
(Fig. 3). These sections included the optic disc and the fovea.
Sections were stained with hematoxylin and eosin (H&E).
3 Results
3.1 Pre-study test
Weights and linear and volumetric measurements are pro-
vided in Table 1. Total mean vitreal volume was determined
at 0.54 mL and mean vitreal weight at 0.52 g. The mean vit-
real wt / total eye weight ratio was 0.73 and is comparable to
the ratio of 0.65 reported for cynomolgus monkey eyes using
a frozen dissection method (Struble et al., 2014).
3.2 Feasibility study
3.2.1 ERGs
Representative for all ERG parameters, Fig. 4a and b show
the b-wave amplitudes and latencies of the scotopic elec-
troretinograms, respectively, of the right eyes of both treated
groups measured twice before injections (predose 1 and 2)
and 6 weeks after injections. The ERG assessment revealed
similar results when comparing predose to end-of-study data,
and there was no difference between the two dose volumes.
Figure 3. Trimming and sectioning of the eye.
None of the measured parameters showed any difference
between data obtained from the left and right eyes. The vari-
ability in the data was satisfactory (see Fig. 4). We averaged
all amplitude and latency data for each stimulus condition
(i.e., obtained from the two eyes, from the three experimental
sessions and from all animals in the two groups). The sco-
topic b-wave amplitudes deviated from the averages up to
about 30 % from these averages for low-intensity flashes. At
high intensities the deviation was maximally 15 %. The de-
viation in all other parameters was generally less than 10 %,
except for the OP amplitudes and the b-wave amplitude ob-
tained with the dimmer (0.3 cd·s m−2) red flash, where the
deviations could be larger probably due to the smaller ampli-
tudes and thus less favorable signal-to-noise ratio (similar to
the scotopic b-wave amplitude at low flash strengths).
In agreement with macaque and human data, the ampli-
tudes increase with increasing flash strength. Furthermore,
the implicit times decrease with increasing stimulus strength.
The absolute values of the scotopic a- and b-wave amplitudes
measured with 3 cd·s m−2flashes agree with those measured
in humans at the same conditions (Hamilton et al., 2015).
The implicit time of the a-wave at the same flash strength
was also similar to those measured in human subjects. The la-
tency of the b-wave was, however, shorter (35 ms) than those
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B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment 97
Figure 4. (a) Scotopic b-wave amplitudes. (b) Scotopic b-wave latencies.
Table 2. ERG reference data from 46 cynomolgus monkeys (right eye) in comparison to the mean of the three marmosets (right eye) from
group 1 before dosing.
Standard response Species b-wave b-wave peak a-wave a-wave peak Flash Adaptation
amplitude latency amplitude latency intensity status
(µV) (ms) (µV) (ms) (mcds m−2)
rod response cyno 119 [29] 50 [4] – – 95 dark
marmoset 78 [23] 41 [3] (30 min)
maximal response cyno 194 [41] 38 [2] 95 [24] 17 [2] 3000 dark
marmoset 244 [62] 34 [3] 123 [9] 15 [0.4]
oscillatory potential cyno 18 [6] 25 [1] – – 3000 dark
marmoset 16 [11] 24 [1] – –
30 Hz flicker cyno 77 [20] 57 [0.9] – – 3000 light
marmoset 145 [5] 58 [0.5] – – (10 min)
red flash cone response cyno 41 [13] 24 [2] – – 950 light
marmoset 116 [5] 22 [0.5]
white flash cone response cyno 88 [25] 24 [0.8] 16 [3] 14 [0.9] 3000 light
marmoset 177 [17] 26 [0.7] 48 [10] 15 [0.4]
[ ] =standard deviation.
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98 B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment
Figure 5. (a) Intraocular pressure of group 1 (10 µLeye−1). (b) Intraocular pressure of group 2 (20µLeye−1).
measured by Hamilton et al. (2015) in human subjects (about
50 ms).
In general, the responses to the different flash intensities
are comparable to those measured in cynomolgus monkeys
(Table 2). However, the cone-driven response appears to be
stronger than in cynomolgus monkeys. This is likely to be re-
lated to the higher cone density found in marmosets in com-
parison with macaques (Goodchild et al., 1996).
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B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment 99
3.2.2 Ophthalmic examinations
Slit lamp examination and funduscopy did not show any
changes in ocular structures which could be due to manip-
ulation.
3.2.3 Intraocular pressure
A transient increase in the intraocular pressure was seen im-
mediately after dosing which was more pronounced after
dosing of 20 µL compared to 10 µL (see Fig. 5a and b) in-
dicating the influence of the volume to the intraocular pres-
sure immediately following dosing. Pressure increase indi-
cates that 20 µL is about the maximum volume injectable
without damage to the intraocular structures.
3.2.4 Histology
Microscopic findings were limited to the site of injection
(Fig. 6a) and were characterized by minimal focal disorga-
nization of stromal layers mainly affecting the muscle of
the ciliary body (Fig. 6b) and a subepithelial infiltrate of in-
flammatory cells of the conjunctiva at the corneoscleral lim-
bus. The cell infiltrate was composed of neutrophils and/or
mononuclear cells, was minimal in magnitude, and was focal
or multifocal in distribution. Disorganization of stromal lay-
ers and inflammatory cell infiltrates occurred to the same ex-
tent in animals from the 10 and the 20 µL dose volume group.
There was no difference in magnitude between the groups, no
morphological evidence of occlusion of the iridocorneal an-
gle, and no evidence of optic nerve or retinal damage from
increased intraocular pressure (Fig. 6c).
4 Discussion
During pretest evaluation of marmoset eyes, the volume of
the vitreous body was determined at 0.54 mL. In cynomol-
gus monkeys the volume was determined at 2mL (Struble at
al., 2014) using the same technique. Since the standard injec-
tion volume in cynomolgus monkey is 50µL per eye, the vol-
ume of 10 and 20 µL was selected for this study. It could be
shown that this is a feasible volume for injection into the vit-
reous body of the eye from a marmoset. A transient effect to
the intraocular pressure immediately after dosing was seen at
10 and 20 µL doses. However, this increased intraocular pres-
sure did not result in any changes in the morphology of the
eye that was evaluated microscopically. Therefore, both vol-
umes could be used for future study. The electroretinogram
showed that there were no changes during the study due to
the intravitreal dosing of a placebo. In addition, a comparison
to reference data from the cynomolgus monkeys (Table 2)
shows that the cone-driven response appears to be stronger
than in cynomolgus monkeys, which is likely to be related to
the higher cone density found in marmosets.
Figure 6. (a) H&E-stained section from the eye of a marmoset
monkey treated intravitreally (10 µL). The image shows the ciliary
body and portions of the iris, sclera and lens. Note the needle track
lesion in the sclera (arrow) and the disorganization of collagen fibers
in the pars plana of the ciliary body, accompanied by few inflam-
matory cell infiltrates. (b) H&E-stained section from the eye of a
marmoset monkey treated intravitreally (10 µL). This picture shows
the disorganization of the stromal layers and minimal inflammatory
cell infiltrates. (c) H&E-stained section from the eye of a marmoset
monkey treated intravitreally (20 µL). This picture shows the nor-
mally structured papilla of the optic nerve with no microscopical
changes induced by transiently increased intraocular pressure.
5 Conclusion
It is concluded that, based on IOP measurements, ERG
recording, and ophthalmologic and microscopic observa-
tions, up to 20 µL intravitreal injections of a placebo were
well tolerated in the marmoset. Therefore, the common mar-
moset provides a potential alternative to the cynomolgus
monkey for ocular toxicity testing.
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100 B. Korbmacher et al.: Feasibility of intravitreal injections and ophthalmic safety assessment
Data availability. All measured ERG results are available in the
Supplement.
The Supplement related to this article is available online
at doi:10.5194/pb-4-93-2017-supplement.
Author contributions. B. Korbmacher wrote this paper as the
first author. J. Atorf and J. Kremers were responsible for estab-
lishing and analyzing the electroretinograms. S. Friderichs-Gromoll
performed the pathology and A. Pilling reviewed the slides and the
pathology evaluation. K. Mansfield supplied the pre-study data re-
garding the weight and volume of the marmoset eyes. A. Wieder-
hold performed the ophthalmic examinations. M. Hill planned this
project and was responsible for the design together with S. Korte.
L. Mecklenburg reviewed the manuscript.
Competing interests. The authors declare that they have no con-
flict of interest.
Acknowledgements. The authors would like to thank the
operational and administrative staff for their support.
Edited by: G. Weinbauer
Reviewed by: A. Wegener and one anonymous referee
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