Fungi
Journal of
Article
Evaluation of Sex Differences in Murine Diabetic Ketoacidosis
and Neutropenic Models of Invasive Mucormycosis
Teclegiorgis Gebremariam
1
, Sondus Alkhazraji
1
, Abdullah Alqarihi
1
, Nathan P. Wiederhold
2
,
Laura K. Najvar
2,3
, Thomas F. Patterson
2,3
, Scott G. Filler
1,4
and Ashraf S. Ibrahim
1,4,
*
Citation: Gebremariam, T.;
Alkhazraji, S.; Alqarihi, A.;
Wiederhold, N.P.; Najvar, L.K.;
Patterson, T.F.; Filler, S.G.; Ibrahim,
A.S. Evaluation of Sex Differences in
Murine Diabetic Ketoacidosis and
Neutropenic Models of Invasive
Mucormycosis. J. Fungi 2021, 7, 313.
https://doi.org/10.3390/jof7040313
Academic Editor: Michaela Lackner
Received: 8 April 2021
Accepted: 16 April 2021
Published: 18 April 2021
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4.0/).
1
The Division of Infectious Diseases, The Lundquist Institute for Biomedical Innovation at Harbor-University
of California at Los Angeles (UCLA) Medical Center, Torrance, CA 90502, USA;
tghbremariam@lundquist.org (T.G.); salkhazraji@lundquist.org (S.A.); aalqarihi@lundquist.org (A.A.);
sfiller@lundquist.org (S.G.F.)
2
University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA;
wiederholdn@uthscsa.edu (N.P.W.); NAJVAR@uthscsa.edu (L.K.N.); patterson@uthscsa.edu (T.F.P.)
3
South Texas Veterans Health Care System, San Antonio, TX 78229, USA
4
David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA
* Correspondence: ibrahim@lundquist.org; Tel.: +1-310-222-6424
Abstract: There is increased concern that the quality, generalizability and reproducibility of biomed-
ical research can be influenced by the sex of animals used. We studied the differences between
male and female mice in response to invasive pulmonary mucormycosis including susceptibility to
infection, host immune reaction and responses to antifungal therapy. We used diabetic ketoacidotic
(DKA) or neutropenic mice infected with either Rhizopus delemar or Mucor circinelloides. The only
difference detected was that when DKA mice were infected with M. circinelloides, female mice were
more resistant to infection than male mice (median survival time of 5 vs. 2 days for female and male
mice, respectively). However, a 100% lethality was detected among infected animals of both sexes.
Treatment with either liposomal amphotericin B (L-AMB) or posaconazole (POSA) protected mice
from infection and eliminated the difference seen between infected but untreated female and male
mice. Treatment with L-AMB consistently outperformed POSA in prolonging survival and reducing
tissue fungal burden of DKA and neutropenic mice infected with R. delemar or M. circinelloides, in both
mouse sexes. While little difference was detected in cytokine levels among both sexes, mucormycosis
infection in the DKA mouse model induced more inflammatory cytokines/chemokines involved in
neutrophil (CXCL1) and macrophage (CXCL2) recruitment vs. uninfected mice. As expected, this
inflammatory response was reduced in the neutropenic mouse model. Our studies show that there
are few differences between female and male DKA or neutropenic mice infected with mucormycosis
with no effect on the outcome of treatment or host immune response.
Keywords: Rhizopus; Mucor; mucormycosis; murine; sex
1. Introduction
There is a growing concern in the scientific community and lay public about the
reproducibility of biomedical research. Study design elements that are critical to the
reproducibility of results include, but are not limited to blinding, randomization and
sample-size calculations [1,2]. Pre-clinical research with animal models may be difficult
to reproduce, due to differences in the strain of animals that is used, laboratories and
laboratory environments and subtle changes in protocols that may not be effectively
communicated in publications [1,2]. In addition, there is increased recognition that the
quality, generalizability and reproducibility of biomedical research can be influenced by
sex of the experimental animal, and that the over-reliance on a single sex of animals in
pre-clinical research may obscure key sex differences that could guide clinical trials [1].
Thus, the National Institutes of Health (NIH) now recognizes that the failure to account for
J. Fungi 2021, 7, 313. https://doi.org/10.3390/jof7040313 https://www.mdpi.com/journal/jof